Translational Gene Regulation in Plants: A Green New Deal

Ricardo A Urquidi-Camacho; Ansul Lokdarshi; Albrecht G von Arnim

doi:10.1002/wrna.1597

. Author manuscript; available in PMC: 2022 Jul 6.

Published in final edited form as: Wiley Interdiscip Rev RNA. 2020 May 4;11(6):e1597. doi: 10.1002/wrna.1597

Translational Gene Regulation in Plants: A Green New Deal

Ricardo A Urquidi-Camacho ¹, Ansul Lokdarshi ², Albrecht G von Arnim ³

PMCID: PMC9258721 NIHMSID: NIHMS1820551 PMID: 32367681

Abstract

The molecular machinery for protein synthesis is profoundly similar between plants and other eukaryotes. Mechanisms of translational gene regulation are embedded into the broader network of RNA-level processes including RNA quality control and RNA turnover. However, over eons of their separate history, plants acquired new components, dropped others, and generally evolved an alternate way of making the parts list of protein synthesis work. Research over the past five years has unveiled how plants utilize translational control to defend themselves against viruses, regulate translation in response to metabolites, and reversibly adjust translation to a wide variety of environmental parameters. Moreover, during seed and pollen development plants make use of RNA granules and other translational controls to underpin developmental transitions between quiescent and metabolically active stages. The economics of resource allocation over the daily light-dark cycle also include controls over cellular protein synthesis. Important new insights into translational control on cytosolic ribosomes continue to emerge from studies of translational control mechanisms in viruses. Finally, sketches of coherent signaling pathways that connect external stimuli with a translational response are emerging, anchored in part around TOR and GCN2 kinase signaling networks. These again reveal some mechanisms that are familiar and others that are different from other eukaryotes, motivating deeper studies on translational control in plants.

Graphical Abstract

graphic file with name nihms-1820551-f0001.jpg

Recent advances in our understanding of translational gene regulation in plants include genome-wide control phenomena, mechanistic insights into the translation apparatus, and emerging signal transduction pathways.

1. INTRODUCTION

The protein synthesis machinery has remained highly conserved throughout the evolutionary history of life on earth. In plants, the structure and function of the ribosome, the mRNA, and the charging of tRNAs largely resemble those of other eukaryotes. However, the unique lifestyle of plants has resulted in certain adaptations in the translation apparatus. For example, as compared to animals, plant viruses and the innate plant immune system interact differently with the plant translation apparatus.

This review interrelates recent discoveries on translational gene regulation of cytosolic mRNAs in seed plants, building on previous excellent reviews on the same topic (Browning and Bailey-Serres, 2015; Merchante et al., 2017; Goldenkova-Pavlova et al., 2018; Mazzoni-Putman and Stepanova, 2018). We begin at the level of cellular ‘systems’ physiology emphasizing, in order, metabolic control of global protein synthesis, genome-wide studies of translational control in response to environmental perturbations and the role of ribonucleoprotein granules. We then briefly introduce the cytosolic translation apparatus, the ribosome and the roles of the translation factors. The following section summarizes the current status of translational control in plants along two axes; translation factors and RNA sequence features. Topics such as small RNAs, covalent RNA modifications, non-coding RNAs, RNA quality control, and concepts discovered in viruses are covered, while translational control in mitochondria and chloroplasts is not (Zoschke and Bock, 2018). Detailed coverage is reserved for discoveries within the last three to five years. Over this period, we have finally seen the outlines of complete signaling pathways that connect a regulatory stimulus with a specific translational response. The final section summarizes the current status of these still emerging studies. In a sincere but ultimately futile attempt at brevity, this review rarely compares plants with animals or fungi, but deliberately focuses on what is known from plants.

2. GLOBAL REGULATION OF TRANSLATION THREE WAYS

2.1. Metabolic Control of Bulk Protein Synthesis

Protein synthesis is the predominant sink for assimilated nitrogen and sulfur, and it is the destination for much of the inorganic phosphate in the form of ribosomal RNAs. Protein synthesis also expends a significant portion of the cell’s energy. Different from other eukaryotes, as photoautotrophic organisms, plants mine all of these resources from their inorganic environment. Because supplies are typically limiting for growth, it is to be expected that protein synthesis is regulated by light and darkness and by the metabolic status of carbon, nitrogen, and sulfur assimilation. In addition, protein synthesis is regulated by the environmental factors that constrain the uptake of CO₂ and nutrients, such as high temperature and water potential.

Over the past decade, researchers have gained deep quantitative insights into the global control of protein synthesis over the day-night cycle. Key experimental techniques include proteome-wide measurements of mRNA and protein levels, measurements of ribosome numbers, mRNA ribosome loading, protein turnover rates, and metabolic flux analysis of inorganic C and N into amino acids and proteins. Data primarily from vegetative rosettes of Arabidopsis have revealed that ribosome numbers per cell are generally stable, coherent with the long half-life of ribosomal proteins (Piques et al., 2009; Ishihara et al., 2017; Li et al., 2017a). The fraction of ribosomes found in polyribosomes, i.e. actively translating, fluctuates slightly around 60±20% with a peak during the day (Pal et al., 2013; Missra et al., 2015). Levels of most amino acids cycle with a low peak after dusk in a light and circadian clock-dependent manner (Ishihara et al., 2015; Flis et al., 2019). The protein synthesis rate however, cycles with a larger (~3-fold) amplitude (Ishihara et al., 2015), which leads to the hypothesis that ribosomes may initiate and elongate more slowly at night, especially at cooler temperature (Pyl et al., 2012). Nitrogen assimilation into amino acids occurs preferentially during the day, implying that amino acids used for protein synthesis at night must come predominantly from stored pools (Pal et al., 2013; O’Leary et al., 2017). An influential finding is that the Arabidopsis circadian clock adjusts the rate of starch degradation at night to the seasonal length of the dark period (photoperiod), presumably to not deplete its most fungible source of energy prior to dawn (Gibon et al., 2009; Scialdone et al., 2013; Sulpice et al., 2014; Flis et al., 2019). As amino acid levels are similarly stable (Gibon et al., 2009), this feature in turn allows protein synthesis to operate during the entire night period. Instead, protein synthesis is correlated with sucrose content, more so than with any other carbohydrate (Pal et al., 2013).

According to diel proteomics data most protein levels fluctuate little over the course of the day, with exceptions, despite robust cycles in their mRNA levels (Baerenfaller et al., 2012; Seaton et al., 2018). This result has now become better understood. First, different proteins are turned over with a wide range of degradation rates, but because the average half-life is 3.1–3.5 days (Ishihara et al., 2015; Li et al., 2017a), cycles in the protein synthesis rate are expected to cause only small fluctuations in the level of most proteins. Second, the density of ribosomes per mRNA also fluctuates over the day-night cycle. While for some mRNAs ribosome loading or protein synthesis rate are in phase with the transcript level (‘translational coincidence’), this is not always the case (Missra et al., 2015; Seaton et al., 2018). Thus, phase delays between cycles of mRNA abundance and cycles of ribosome loading allow the cycle of protein synthesis rates to adopt different waveforms.

When ribosome loading data are used as proxy for the protein synthesis rate, it is under the assumption that all ribosomes elongate at the same speed regardless of mRNA sequence and environmental conditions. Our understanding of the balance sheet of protein synthesis would greatly benefit from protein-specific protein synthesis rates, which has been a tough nut to crack in plants (Li et al., 2012b; Lewandowska et al., 2013; Ishihara et al., 2015; Glenn et al., 2017). This is relevant because the ratio between new protein synthesis and protein turnover may be a major factor determining growth rate, as suggested by comparisons between different Arabidopsis strains (Ishihara et al., 2017).

2.2. Control of the Translatome by Environmental Perturbation

The environment in which translation takes place varies with regards to numerous factors, many of which influence translational efficiency. Among these factors, changes in abiotic conditions such as temperature, water potential, and light cause dramatic shifts in translation rates over short periods of time, hours or minutes. Some developmental transitions are nearly as rapid, specifically hydration of seeds or pollen, as are responses to microbial infection. Metabolic changes in agents such as sugars and oxygen also have profound effects even though they are more difficult to control in planta. The effect of genetic manipulations on translation is also of interest. However, in this case, differences in translation rates are the result of complex cellular events that have played out over days or weeks, making it more difficult to attribute a specific difference in translation to the specific genetic perturbation. A recent trend that may gather momentum is to combine genetic and environmental treatments (Merchante et al., 2015; Missra et al., 2015; Zhang et al., 2017; Cho et al., 2019; Lokdarshi et al., 2020a). Multi-omics studies also hold potential to unravel how translational control is integrated with upstream events such as transcription and the cellular signaling infrastructure (Bazin et al., 2017; Hafidh et al., 2018; Lee and Bailey-Serres, 2019).

Abiotic factors that affect the energy charge of the cell such as light, darkness and oxygen availability affect translation in profound ways as has been documented by polysome profiling, TRAP-Seq and ribosome footprinting experiments (see Glossary). The effects of light on the translatome have been explored by shifting etiolated seedlings from dark to light (Liu et al., 2012; Liu et al., 2013), by exposing plants to darkness in the middle of the day (Juntawong and Bailey-Serres, 2012) and by comparing translation over the daily light-dark cycle in wild-type and clock-deficient strains (Missra et al., 2015). Plant translatomes have also been examined in response to hypoxia and reoxygenation (Branco-Price et al., 2008; Juntawong et al., 2014; Cho et al., 2019; Lee and Bailey-Serres, 2019) and heat stress (Yanguez et al., 2013; Lukoszek et al., 2016; Merret et al., 2017; Zhang et al., 2017; Su et al., 2018). Hypoxia and heat stress were the first major conditions that have allowed cross-species comparisons, demonstrating that fundamental features of the translatome response are in fact similar (Mustroph et al., 2010; Park et al., 2012; Ueda et al., 2012). Translation efficiencies were also collected for drought (Kawaguchi and Bailey-Serres, 2005; Lei et al., 2015), herbicide (Lokdarshi et al., 2020a); phosphate starvation (Bazin et al., 2017), cold (Juntawong et al., 2013), and the heavy metal, cadmium (Sormani et al., 2011). Translatome-wide responses have also been analyzed in response to metabolic signals, specifically sucrose (Nicolai et al., 2006; Gamm et al., 2014) and the hormone ethylene (Merchante et al., 2015). What has remained unclear is whether the major reorganization of the translatome that occurs in each case is essentially one and the same global response in every case, or whether each variable triggers its own characteristic response. This question has been difficult to resolve because of different experimental platforms and plant growth conditions, but is of great interest in order to attribute how various cellular signaling pathways cooperate to regulate translation. However, certain functionally defined groups of mRNAs behave as translational regulons in that they are translationally co-regulated across multiple conditions, for example ribosomal protein mRNAs (Branco-Price et al., 2008; Juntawong and Bailey-Serres, 2012; Missra et al., 2015.

Genetic perturbation, specifically, loss of function mutations in eIF4 isoforms (see Figure 1 and below), the h subunit of eIF3 and the ribosomal protein, RPL24, had profound effects on the translatome (Kim et al., 2007; Martinez-Silva et al., 2012; Tiruneh et al., 2013; Cho et al., 2019), while others, such as those in eIF3k and the poly(A)-binding proteins had surprisingly subtle consequences (Tiruneh et al., 2013) unless PABP gene dosage was severely curtailed (Zhao et al., 2019). Genetic perturbations have been particularly informative when paired with short-term environmental treatments (Merchante et al., 2015; Zhang et al., 2017; Cho et al., 2019; Lokdarshi et al., 2020a). For example, a deficiency in the initiation factor eIF5B, the protein responsible for ribosomal subunit joining, caused a delay in the recovery of ribosome loading after heat shock (Zhang et al., 2017).

What global translational control occurs during the response of plants to pathogens? Given that bacteria and fungi seek to draw on the host’s amino acids, and viruses additionally rely on the host’s translation apparatus, translational control should be a battleground in pattern-triggered and effector-triggered immunity. However, our understanding is at an early stage. Upon activation of a bacterial pattern triggered immune response with a flagellin peptide, poly(A) binding proteins (PABPs) mediated a global shift in translational efficiency that affected preferentially mRNAs with (GA)_n motifs in their 5’ leader (Xu et al., 2017a). Likewise, still in the absence of pathogen, two groups examined the global translational response during effector-triggered immunity, after spontaneous activation of the resistance proteins RPM1 (Meteignier et al., 2017) and RPS2 (Yoo et al., 2019). For comparison, in the presence of pathogen, infections with turnip mosaic virus in Arabidopsis and the fungus Blumeria graminis in barley also caused global shifts in translational efficiencies (Moeller et al., 2012), also see (Reynoso et al., 2012). Finally, in a model system of infection with a DNA virus, signaling through the cell surface receptor, NIK1, all but eliminated the transcripts of ribosome biogenesis genes, a response mediated by a moonlighting activity of the ribosomal protein RPL10 (Brustolini et al., 2015; Zorzatto et al., 2015). The underlying molecular trigger remains to be confirmed, but strikingly, virus-induced DNA and RNAs could elicit this pathway (Teixeira et al., 2019). In summary, we are witnessing that plant pathogens and the host immune response interfere with translation at two levels, translational efficiency in the narrow sense, as well as synthesis of the translation apparatus. Interactions of viruses with the plant translation apparatus will be explored in more detail below.

To what degree is translational efficiency cell type specific? This question has been addressed by cell type-specific ribosome isolation (TRAP-Seq) (Reynoso et al., 2015) in the root (Mustroph et al., 2009), phloem upon virus infection (Collum and Culver, 2017; Collum et al., 2019), leaf bundle sheath (Aubry et al., 2014), pollen tubes (Lin et al., 2014), and the shoot apex (Tian et al., 2019) including the inflorescence meristem (Jiao and Meyerowitz, 2010). While these experiments give unprecedented insights into the spectrum of ribosome loaded mRNAs in individual cell types, it is more challenging to infer cell type specific translational efficiencies because this requires normalization with total mRNA levels from the same cell preparation. Normalization can be achieved by comparing ribosome footprints and whole transcripts from manually dissected tissue, e.g. in the Arabidopsis root (Hsu et al., 2016; Bazin et al., 2017).

While most examples of translational control were discovered in response to changing environments, there are cases during development, e.g. (Yamasaki et al., 2015), such as seed development from late embryo maturation, over dormancy, to seed germination (Oracz and Stawska, 2016; Basbouss-Serhal et al., 2015; Galland et al., 2017; Shamimuzzaman and Vodkin, 2018; Sajeev et al., 2019). Comparison of two stages, seed germination and pollen germination, is particularly instructive (Figure 2). During the four stages of seed germination, two stages experience abundant translational control, seed hydration (stage I) and germination proper (III), which is marked by the root tip protruding from the seed coat. In contrast, stage II, rupture of the seed coat, and stage IV, seedling emergence and greening, have fewer examples of mRNAs changing their ribosome loading (Bai et al., 2017; Bai et al., 2020). Likewise, during early germination in maize, mRNAs for ribosomal proteins are translationally stimulated (Jimenez-Lopez et al., 2011). For comparison, tobacco pollen development and germination also involve a period of dehydration that is followed by rapid changes in protein expression (Ischebeck et al., 2014). Similar to seeds, during pollen tube growth mRNAs are also partitioned into different classes for staged translation (Hafidh et al., 2018). Pollen also contains an unusual and novel type of non-translating monosome (EDTA/puromycin-resistant particle, EPP). Besides mRNA, EPPs contain elongation factor EF-1A, suggesting that they are awaiting the developmental signal for jumpstarting full translation of their sequestered transcripts (Hafidh et al., 2018). The molecular signals that drive these translational shifts should be a fascinating area for future research. As a preview of plausible signaling events, eIF4G, eIF4B and eIF5B become dephosphorylated immediately after pollen germination (Fila et al., 2016).

Figure 2: — Yellow boxes indicate translation state, abundance of polysome or monosomes and cellular RNP complexes; blue (pink) boxes indicate functional gene ontology terms that are translationally active (repressed); green boxes indicate examples of translationally repressed mRNAs corresponding to a specific developmental stage.

**(A) Pollen.** The vertical timeline covers (pre-)meiotic (sporophytic, diploid) followed by postmeiotic (gametophytic, haploid) stages of tobacco pollen. Early stage proteomes are characterized by abundant heat shock protein chaperones (HSPs), RNA binding proteins (RBPs), cell wall loosening enzymes and protein degradation, while the later gametophytic stage is rich in glycolytic and fermentation enzymes and late embryo abundant (LEA) proteins. LEA proteins are linked to ABA signaling, cell wall synthesis and the maintenance of ROS balance. Mature, desiccated pollen grains contain a high amount of monosomes in the form of special structures called EDTA/Puromycin resistant Particles (EPPs), which are translationally inactive. EPPs contain stalled monosomes on transcripts maintained in a translationally quiescent state, to be released for translation towards the maturation phase of pollen germination. The EPP proteome contains ribosomal 60S proteins and translation initiation and elongation factors. Examples of the mature pollen EPP transcriptome include pollen-specific cell wall glycoprotein (*NTP303* ortholog *ATSKU5*) and pollen-specific LIM domain containing protein (*WLIM2B*). After Hafidh et al., 2018 and Ischebeck et al., 2014. **(B) Seed germination** begins with a dry seed (top=early) and involves two distinct translational shifts, coincident with seed hydration and root protrusion (‘germination’ proper). During the hydration shift (0–6 h after imbibition) transcripts found abundant in the last stages of seed maturation become polysome loaded and actively translated (e.g. PM1 is translated during this phase and suppresses the translation of a glycine-rich protein). The second translational shift (26–48 h) occurs between testa rupture and root protrusion. At this stage, abundant polysomes contain transcripts related to RNA processing and modification and lipid metabolism. After Bai et al., 2017, Bai et al., 2020.

2.3. Translational Control through mRNP Granules

Like other eukaryotes, plants respond to a variety of abiotic stresses by sequestering cellular mRNAs into two types of mRNA ribonucleoprotein (mRNP) complexes, stress granules and processing bodies (P-bodies). Stress granules (SG) were first observed in response to heat stress and also occur during hypoxia, darkness, salt, and other conditions (Weber et al., 2008; Sorenson and Bailey-Serres, 2014; Yan et al., 2014; Gutierrez-Beltran et al., 2015; Lokdarshi et al., 2016). Stress granules are probably of diverse types, distinguishable by characteristic protein components. P-bodies are sites of mRNA decapping, nonsense-mediated decay (NMD), and thus fating for mRNA degradation. However, under certain circumstances P-bodies harbor mRNAs for translational repression, for instance in etiolated seedlings (Merchante et al., 2015; Jang et al., 2019).

When stress granules form, polysome loading declines and sometimes collapses dramatically. However, upon release of the stress, stress granules quickly disappear and mRNAs return to the polysomal pool (Branco-Price et al., 2008; Sorenson and Bailey-Serres, 2014). Stress granules exchange mRNAs with P-bodies (processing bodies), and SGs are associated with P-bodies (Hamada et al., 2018). Thus, stress granules lie at the nexus of two post-transcriptional processes, translation and mRNA turnover (Chantarachot and Bailey-Serres, 2018).

In Arabidopsis, numerous proteins associate with stress granules (Chantarachot and Bailey-Serres, 2018; Kosmacz et al., 2019). Aside from translation initiation factors and PABP, the oligouridylate binding proteins (UBPs) and the RNA binding protein RBP45/47 are the proteins most closely related to a driver of stress granule in animals, the TIA-1-related proteins. UBPs and RBP45/47 are markers for stress granules, as they are absent from P-bodies (Weber et al., 2008; Sorenson and Bailey-Serres, 2014; Nguyen et al., 2016; Nguyen et al., 2017).

The complex mechanisms that drive mRNAs from polysomes into stress granules are gradually becoming better understood. In response to heat stress, there is at first some evidence for ribosome pausing, possibly because heat shock proteins such as HSP70 cannot keep up with demand as they assist with nascent protein folding (Merret et al., 2015). This is followed by global polysome collapse, while specific mRNAs are retained on polysomes (Yanguez et al., 2013; Lukoszek et al., 2016; Zhang et al., 2017), and other mRNAs such as ribosomal protein mRNAs are sequestered in heat stress granules. Translation factors eIF4A and eEF1B are bound by and potentially protected by small heat shock proteins, which localize to stress granule-like foci (McLoughlin et al., 2016). mRNAs can return to the translated pool when temperatures drop, a process assisted by HSP101 (Merret et al., 2017). Extended heat results in RNA degradation (Merret et al., 2017; Su et al., 2018).

Concerning mechanisms of stress granule formation in the hypoxia response, UBP1C binds oligouridine tracts of mRNAs under control conditions but associates with mRNAs targeted to stress granules during hypoxia (Sorenson and Bailey-Serres, 2014). Meanwhile, the calcium sensor CML38 associates reversibly with stress granules (Lokdarshi et al., 2016). In mammalian cells, formation of stress granules is sometimes dependent on signaling through the eIF2α kinases such as GCN2, although this is not uniform (Farny et al., 2009; Emara et al., 2012; Anderson et al., 2015; Arimoto-Matsuzaki et al., 2016). In plants, few of the signals that trigger eIF2α-phosphorylation are known to trigger stress granules and vice versa (Lageix et al., 2008; Zhang et al., 2008; Lokdarshi et al., 2020a). Specifically, treatments that cause stress granules in Arabidopsis (heat, darkness, hypoxia) do not trigger eIF2α-P. On the contrary, heat and darkness reduce preexisting eIF2α-P (Lokdarshi et al., 2020a). Therefore, it appears that stress granules form through an alternate pathway, possibly involving binding of 2’,3’-cAMP to RBP47 (Kosmacz et al., 2018), but the mechanisms remain poorly understood.

Recently, a signaling event during the defense response triggered by bacterial flagellin has revealed a possible mechanism for stress granule/P-body directed translational control under pathogen infection. TZF9, a member of the twin zinc finger protein family, is found in both stress granules and P-bodies. The loss-of-function tzf9 mutant had elevated ribosome loading of flagellin-responsive mRNAs (Tabassum et al., 2020). Additionally, phosphorylation of TZF9 by MAP kinase supports the idea of translational control of gene expression under pathogen stress (Xu et al., 2017), and suggests that TZF9 may function by modulating the balance between active translation and mRNA sequestration in the context of mRNP granules (Tabassum et al., 2020).

3. THE PLANT TRANSLATION APPARATUS

3.1. The Ribosome

The structure of a plant 80S ribosome has been deduced for wheat by cryoelectron microscopy (Armache et al., 2010). The four ribosomal RNAs (25S, 5.8S and 5S in the 60S subunit and 18S in the 40S) are accompanied by 81 different ribosomal proteins (RPs). Of these, all except the plant-specific P3 protein in the acidic stalk of the 60S are orthologous to metazoan proteins. The genetic architecture of the RPs opens many opportunities to understand the evolution of a large ribonucleoprotein complex. Each Arabidopsis RP is encoded by 2–7 highly similar paralogs (Browning and Bailey-Serres, 2015; Hummel et al., 2015). With at most a few exceptions, all the 81 RPs have at least two paralogs expressed, as judged by proteomics or ribosome footprinting, and at least 80% of the 239 RP genes are expressed into proteins, while 13 are considered pseudogenes (Hummel et al., 2015). The DNA sequences of certain paralogous pairs evolve in a concerted manner, possibly by gene conversion events between related paralogs, which is reminiscent of the concerted evolution of the duplicated rRNA genes (Devis et al., 2015).

While many paralogous pairs of RPs are expressed with similar tissue specificity, differences in the absolute mRNA level are common (Browning and Bailey-Serres, 2015). When one compares the RP mRNA expression levels across maize germplasms, the levels of several RP mRNAs are anti-correlated with leaf size. This is surprising because RP expression is generally positively correlated with plant growth, and it suggests that frugal expression of RPs may boost growth (Baute et al., 2016). The ribosome loading of the paralogous RP mRNAs can differ substantially (Tiruneh et al., 2013). While a few of the paralogs have unusual, environmentally sensitive mRNA expression patterns (Browning and Bailey-Serres, 2015), the translation states of most of the RP mRNAs are co-regulated, forming a tight translational regulon in Arabidopsis (Kim et al., 2007; Branco-Price et al., 2008; Juntawong and Bailey-Serres, 2012; Tiruneh et al., 2013). The RP mRNAs possess characteristic sequence features including a short 3’UTR and a high GC content in their short 5’UTRs and are enriched for the telo-box sequence motif (Branco-Price et al., 2005; Juntawong and Bailey-Serres, 2012), which may or may not predispose these mRNAs for joint regulation.

Because of the duplication of RP genes, null mutants of a single gene are typically viable, yet display a characteristic pointed- and serrated-leaf phenotype (Zheng et al., 2016). In turn, double mutants that eliminate the two prominently expressed paralogs typically cause gametophytic or embryo lethality (Casanova-Saez et al., 2014; Zsogon et al., 2014; Kim et al., 2015; Yan et al., 2016). It is not uncommon that bona fide null alleles of two RP paralogs have slightly different phenotypes. This observation raises the hypothesis that the two paralogs have different functions. These functions could either be differential extraribosomal activities, e.g. (Ferreyra et al., 2010). Alternatively, the two paralogs may impart slightly different properties on the ribosome, leading to the notion of functionally ‘specialized ribosomes’. Granted, according to the rules of combinatorial mathematics no two plant ribosomes should be exactly alike, and some RP paralogs are expressed differently (Hummel et al., 2012; Moin et al., 2017). However, the ‘specialized ribosome’ hypothesis faces challenges. First, in most cases it is difficult to rule out that the difference in mutant phenotype is due to a difference in the expression patterns of the paralogs (Horiguchi et al., 2012; Zsogon et al., 2014; Devis et al., 2015), or is due to residual activities of the mutated alleles, e.g. (Creff et al., 2010). Other questions immediately arise: What is the specialized biochemical role of the specialized ribosome? And how might a specialized ribosome be matched with its designated client mRNA or sorted to its designated site of action in the cell? Nonetheless, the prospect of specialized ribosomes will continue to intrigue the translation community.

It is not often that a specific biochemical function is ascribed to a ribosomal protein in a plant. uL23/RPL23a is a recent case; for RP nomenclature see (Ban et al., 2014). When a protein that is to be targeted to the chloroplast outer envelope is being translated, uL23/RPL23a responds to the targeting signal still lodged in the ribosome exit tunnel by attracting the AKR2A targeting receptor to the ribosome, such that when the targeting signal emerges from the exit tunnel it is effectively recognized by the targeting receptor (Kim et al., 2015).

Aside from differences in amino acid composition between paralogs, ribosomal proteins and associated translation factors become structurally diversified by numerous posttranslational modifications, first and foremost phosphorylation. Phosphorylation of several RPs and eIFs is stimulated by light and carbon dioxide and declines in darkness in a diel manner (Boex-Fontvieille et al., 2013; Choudhary et al., 2015; Nukarinen et al., 2016). About four different patterns of phosphorylation can be clearly distinguished, stimulation by light and CO2 (eS6/RPS6, uS11/RPS14, eIF4B), stimulation by darkness (eIF4A, eIF4G), stimulation by high CO2 and darkness (eIF4B and eIF3b), or no change (many proteins) (Boex-Fontvieille et al., 2013). Among these, phosphorylation of the 40S subunit has been studied in most detail for eS6/RPS6, located at the foot of the small subunit and phosphorylated by the S6 kinase as one output of the TOR kinase signaling pathway. eS6-P occurs in response to light, auxin, photoassimilates, and photomorphogenetic signals and is repressed by stresses such as heat and hypoxia (Dobrenel et al., 2016b; Chen et al., 2018; Enganti et al., 2018). Peculiar in the field of circadian biology, eS6 phosphorylation is controlled in an incoherent (opposing) manner by light and the circadian clock (Enganti et al., 2018). In summary, the patterns of phosphorylation often suggest hypotheses concerning their functions because they are correlated with growth-promoting or energy starvation conditions. However, the biochemical significance of phosphorylation at the level of translation and its physiological significance for plant growth remain to be resolved in most cases.

3.2. The Translation Factors

3.2.1. Initiation

Translation of mRNA is divided into three phases, initiation, elongation, and termination. Of these, initiation is the most highly regulated and involves the largest number of factors (Figure 1) (Browning and Bailey-Serres, 2015). In brief, the 5’ cap of an mRNA is recognized by the heterodimer between the cap binding protein eIF4E and a scaffold protein, eIF4G, which together are called eIF4F. Plants possess an abundant, alternate isoform of the cap binding complex, named eIFiso4F, consisting of eIFiso4E and a small isoform of eIF4G, eIFiso4G. The eIF4E isoforms bind the cap with a range of affinities (Kropiwnicka et al., 2015; Khan and Goss, 2018). The multiple eIFs also service different mRNAs with different efficiencies (Mayberry et al., 2009; Gallie, 2016), and they play key roles in the defense against viruses. The third protein in the eIF4 group is the helicase eIF4A, which unfolds the 5’ end of the mRNA. Finally, eIF4B is structurally less conserved among eukaryotes than most other factors and functions in part to stimulate eIF4A helicase activity, e.g. (Mayberry et al., 2009; Zhao et al., 2017; Liu and Goss, 2018).

The 40S subunit of the ribosome is prepared for initiation by the trimeric GTPase eIF2 whose alpha subunit is the target of a pan-eukaryotic regulatory phosphorylation event to be discussed in more detail below. eIF2 delivers the initiator methionyl-tRNA (Met-tRNAi) to the peptidyl (P)- site of the 40S. By far the largest of the eIFs is eIF3, a complex of twelve subunits and a loosely associated j subunit (Raabe et al., 2019). eIF3 functions as an organizing scaffold for eIF1, 1A, 2 and 5, and all together form a multifactor complex (Dennis et al., 2009).

The 40S subunit loaded with its initiation factors is known as the 43S preinitiation complex. Bringing the 43S preinitiation complex into contact with the mRNA and its cap-binding complex is attributed to binding between eIF3 and eIF(iso)4G (Browning and Bailey-Serres, 2015). Once brought to the 5’ end of the mRNA, the 43S scans down the 5’ leader of the mRNA until the Met-tRNAi basepairs with an AUG start codon. Start codon recognition is highly regulated. As in other eukaryotes, the scanning ribosome recognizes the AUG start codon better when it appears in a specific ‘Kozak’-sequence context, which in eudicot plants is AANAUGGC and in monocotyledenous plants is GCNAUGGC (Sugio et al., 2010; Gupta et al., 2016; Merchante et al., 2017). The small proteins eIF1A and eIF1 assist in start codon recognition. At this time, eIF5 stimulates GTP hydrolysis by eIF2. Next, the eIFs leave their positions on the 40S, and the large eIF5B GTPase mediates recruitment and binding of a 60S subunit, concluding the initiation phase. Among the remaining eIFs, eIF2B is hypothesized to function as the guanine nucleotide exchange factor for eIF2, although its necessity in this capacity has been questioned (Browning and Bailey-Serres, 2015). eIF5A is no longer considered to be an initiation factor, but an elongation factor whose yeast homolog functions to suppress ribosome stalling on oligo-proline stretches (Gutierrez et al., 2013; Shin et al., 2017). eIF6 is a small, lightly characterized protein (Guo et al., 2011) that binds the large subunit and is thought to assist in subunit separation and/or joining as well as in ribosome biogenesis (Missbach et al., 2013).

Start codon context is a nexus for translational regulation in several contexts. Start codon context affects the choice between alternative start codons that exist in the open reading frames (ORFs) of certain proteins with alternative subcellular targeting sequences. Here the choice of start codon determines the amino-terminal targeting sequence of the protein (Wamboldt et al., 2009; Kasaras and Kunze, 2017). Initiation at non-AUG start codons is non-negligible, occurs routinely on specific mRNAs, influences the inhibitory potential of upstream open reading frames and generally diversifies the spectrum of translated ORFs, especially on 5’ leader sequences (Vaughn et al., 2012; von Arnim et al., 2014; Laing et al., 2015; Hsu et al., 2016; van der Horst et al., 2020). The regulatory potential of Kozak context was brought into focus in the context of the eIF5 mimic proteins, which assist eIF1A in enforcing the Kozak rule by counteracting eIF5. Very interestingly across the eukaryotes, including plants, eIF5 mimic proteins are translated from a start codon in a poor Kozak context (UUUAUGA), which suggests that this protein suppresses start codon recognition, and its level is autoregulated (Loughran et al., 2018). In non-plants this is also the case for eIF1 (Ivanov et al., 2010).

3.2.2. Translation Initiation Factors as Agents of Antiviral Resistance

Potyviruses utilize a viral 5’ linked (VPg) protein as a cap analog to engage host cap binding proteins for efficient translation initiation (Figure 3A). Wild type eIF4E has an even higher affinity to VPg than to the 5’ cap (Miyoshi et al., 2006; Coutinho de Oliveira et al., 2019), whereas certain mutated eIF4E/iso4E alleles interact less well with VPg (Gallois et al., 2010; Mazier et al., 2011). The translation factors of the eIF4 complex were identified as determinants of recessive resistance against viruses from several families, with potyviruses as a particularly well studied example (Sanfaçon, 2015). The mutations affect eIF4E and eIFiso4E (Ruffel et al., 2002), eIF4G (Lee et al., 2010; Macovei et al., 2018), eIFiso4G (Albar et al., 2006; Rubio et al., 2019) and the 4E Homologous Protein 4EHP (Gomez et al., 2019).

Figure 3. — The main protein-coding ORFs of the viral mRNA are represented by a single red box. **(A)** The viral genome-linked protein Vpg substitutes for a 5’ cap in certain RNA viruses by attracting eIF4E and the cap binding complex to the 5’ end of the viral RNA. **(B)** Shunting (upper) and reinitiation (lower schematic) of ribosomes on the long 5’ leader of pararetroviruses. For details see text. **(C)** An internal ribosome entry site in triticum mosaic virus relies on a critical hairpin loop and associated polypyrimidine sequence to attract eIF4G and the ribosome. **(D)** 3’ cap-independent translational enhancers come in a wide variety of forms. The schematic is not drawn to scale and illustrates shared concepts rather than one specific example. Common elements include 3’ hairpin structures that attract elements of the cap-binding and preinitiation complexes and interact with the 5’ leader of the viral RNA through kissing-loop basepairing interactions. For details see text.

The fact that loss of function alleles of genes belonging to small gene families confer resistance may suggest that the potyviruses have evolved to prefer one paralog of cap binding protein over all the others. In contrast, the plant host can utilize multiple paralogs, in keeping with the finding that more than one eIF4F gene must be lost before mutants suffer serious detrimental phenotypes (Callot and Gallois, 2014; Gallie, 2016; Gauffier et al., 2016; Li et al., 2017b; Patrick et al., 2018; Lellis et al., 2019). Virus resistance can evolve when the paralog serving the virus mutates to a loss-of-function allele. In this way, the plant can stay one step ahead of the virus even though its rate of sequence change and the rate with which new alleles spread through the population is far slower than that of the virus. In favor of this hypothesis, the allelic diversity of eIF4E genes explains different degrees of resistance durability in tobacco (Michel et al., 2019). Specifically, a resistance breaking strain of potato virus Y with a mutation in its VPg switched its preference from the eIF4E1 paralog towards an eIFiso4E paralog in its tobacco host (Takakura et al., 2018).

Mutations in eIF4 genes confer agronomically relevant virus resistance. Surprisingly, eIF4E variant alleles with amino acid substitutions sometimes confer broader and more durable resistance than alleles engineered to be downregulated or null-alleles (Gauffier et al., 2016). Substitution alleles discovered as natural variants in one species (Ibiza et al., 2010) can provide virus resistance when engineered into another species, sometimes without suppressing crop yield (Bastet et al., 2018). Alleles of different eIF4E isoforms have also been combined by ‘pyramiding’ to broaden the spectrum of resistance. For example, introducing a mutation in eIF4E discovered in pea into Arabidopsis conferred resistance to potyviruses, and combining this new allele with a mutation in eIFiso4E extended the resistance to include a luteovirus (Bastet et al., 2018). eIF4 complex alleles that confer virus resistance are also among the first examples of Cas9-mediated genome editing, not only in experimental model species (Pyott et al., 2016; Bastet et al., 2019), but even in crops, with examples in cucumber and cassava against potyviruses and in rice against rice tungro spherical virus (Chandrasekaran et al., 2016; Macovei et al., 2018; Gomez et al., 2019).

3.2.3. Elongation, Termination and Recycling

During translation elongation, charged tRNA is recruited into the empty aminoacyl (A)-site of the ribosome, the peptidyltransferase activity of the large ribosomal RNA catalyzes peptide bond formation, the mRNA-tRNA hybrid translocates one codon at a time, followed by the discharge of the uncharged tRNA through the exit (E)-site (Figure 1). tRNAs are delivered by the GTP binding elongation factor eEF1A, which is reconstituted by its guanine nucleotide exchange factor, eEF1B. The ribosome is moved forward by one codon by a second GTPase, eEF2. It is worth noting that slowing or accelerating translation elongation should have no lasting effects on the protein synthesis rate unless it blocks initiation, or elongation stalls completely. Slowing elongation by two-fold will necessarily increase the ribosome density by two-fold, but the rate at which protein synthesis will finish remains the same. Slowing the elongation rate globally will however, reduce the pool of free ribosomes, which may inhibit bulk initiation.

Once the ribosome reaches a stop codon, the release factor eRF1 is delivered to the empty A-site with the help of the GTPase eRF3 and releases the nascent polypeptide (Figure 1). A role for eRF1 was confirmed in rice, where amino acid substitutions in the eRF1 homolog ESP1 reduced the expression of a subset of prolamine seed storage proteins. Of note, prolamines or a luciferase reporter terminating with UAA or UAG stop codons were compromised in the esp1 mutants while mRNAs terminating with UGA were unaffected (Elakhdar et al., 2019) suggesting that the three stops are serviced with different efficiencies in the esp1 mutants. Next, the ATP binding cassette protein ABCE1 (AtRLI in Arabidopsis) then separates the 40S and 60S ribosomal subunits, a process called recycling (Navarro-Quiles et al., 2018). A mutation in one of the Cardamine hirsuta ABCE1 paralogs, SIMPLE LEAF3, suppressed the characteristic lobed leaf shape in this species (Kougioumoutzi et al., 2013). The opposite of termination, namely stop codon readthrough, is rare compared to proper termination, based on Ribo-Seq experiments (Merchante et al., 2015; Hsu et al., 2016), but was elegantly exploited to regulate the expression of eRF1 itself (see below) (Nyiko et al., 2017; Elakhdar et al., 2019). Readthrough at levels as high as 30%, as compared to less than 1% normally, takes place commonly in viruses via specific RNA sequence elements, e.g. (Firth et al., 2011; Kuhlmann et al., 2016; Xu et al., 2018).

The poly(A) binding proteins (PABPs) are considered core translation factors. In Arabidopsis PAB2, PAB4 and PAB8 are jointly expressed in the diploid phase of the life cycle and are partially functionally redundant (Gallie, 2017; Zhao et al., 2019). The extent of PABP binding to mRNAs correlates with translational efficiency, although the spectrum of mRNAs affected depends on the experimental conditions (Tiruneh et al., 2013; Gallie, 2017; Zhao et al., 2019).

Plant mRNAs are thought to conform to the closed-loop model, where PABP forms a physical bridge via eIF4G and eIF4E between the 5’ and 3’ ends of the mRNA (Browning and Bailey-Serres, 2015; Gallie, 2018). The closed-loop model is often invoked when elements in the 3’ region of a transcript influence translation initiation. As described below, plant RNA viruses have developed their own version of the closed-loop by virtue of kissing loops, RNA hairpins in the 5’ and 3’ untranslated regions that can basepair with each other (Figure 3D) (Truniger et al., 2017; Liu and Goss, 2018; Kraft et al., 2019), and PABP also interacts with viral cap binding proteins (Khan and Goss, 2019). However, there is no direct evidence that a ribosome having terminated at a stop codon will be redirected to the 5’ cap of the same mRNA molecule (Vicens et al., 2018).

3.2.4. Translation Reinitiation

When a ribosome that has just terminated translation on a stop codon fails to dislodge from the mRNA, immediately resumes scanning on the same mRNA, and initiates translation at another AUG codon farther downstream the ribosome has undergone reinitiation (Figure 4A, B). The mechanism of reinitiation is not fully understood in any organism (Gunisova et al., 2018), but it is clear that spontaneous reinitiation is common only after short ORFs, typically upstream open reading frames (uORFs) in the 5’ leader (von Arnim et al., 2014). In the exceptional case of cauliflower mosaic virus, reinitiation after long coding sequences is boosted by the viral transactivator protein, TAV, a scaffold that coordinates with initiation factors such as eIF3 and eIF4B, other host proteins, and the ribosome (Pooggin and Ryabova, 2018). Extensive work on the 5’ leader of cauliflower mosaic virus (CaMV) and related pararetroviruses has suggested that the reinitiating 40S has different properties from a cap-dependent 40S. For example, even in the absence of TAV, the reinitiating 40S is capable of ‘shunting’ past a 500nt secondary structure in the CaMV 5’ leader (Figure 3B), and its ability to distinguish authentic from near-cognate start codons may be reduced (Pooggin and Ryabova, 2018).

Figure 4. — **(A)** Structure of an mRNA with one *main ORF* (mORF, yellow) and three uORFs (blue), one of which overlaps the mORF. Start codons are highlighted with bent arrows.

**(B)** Reporter gene translation assay designed to quantify leaky scanning *versus* reinitiation on an mRNA with a single uORF. As compared to the wild-type allele (I), in allele (II) the start codon of the uORF has been mutated to prevent initiation. In allele (III), the stop codon of the uORF has been mutated so as to extend the uORF into the main ORF, which precludes reinitiation at the Reporter AUG. Additional mutations may be needed to remove any downstream in-frame stops in the 5’ leader and to ensure that the uORF is out of frame with the main ORF. The rates of leaky scanning past the uORF initiation codon (LS), of initiation at the uAUG (I), of initiation-reinitiation (I/R) and of failure to reinitiate (I/NR) are calculated from the empirical reporter gene expression activities A_I, A_II and A_III as shown in the table. Numbers shown are for illustration only.

**(C) uORF-mediated metabolic control on the GGP (GDP-galactose phosphorylase) mRNA** (after Laing et al., 2015). At a high ascorbate level, the non-canonical start codon (ACG) of the uORF is recognized and the encoded conserved peptide disallows reinitiation thus switching translation of the main ORF off. At low ascorbate the ACG codon is thought to be skipped by leaky scanning.

**(D) uORF-mediated metabolic control on the AdoMetDC (adenosyl-methionine decarboxylase) mRNA** (after Hanfrey et al., 2005 and Uchiyama-Kadokura et al., 2014). At a low polyamine level, ribosomes initiate on uORF1, thus bypass the start of uORF2, and reinitiate on the main ORF. At a high polyamine level, uORF1 is skipped and uORF2 is translated. uORF2 codes for a conserved peptide and is not conducive to reinitiation, thus inhibiting translation of AdoMetDC by negative feedback.

Which of the canonical initiation factors are required for successful reinitiation remains unknown, first and foremost how the 40S acquires a fresh Met-tRNAi. Studies in diverse organisms suggest that certain translation initiation factors can remain associated with the translating ribosome across short uORFs, thus preserving the competence of the ribosome to reinitiate (Gunisova et al., 2018; Pooggin and Ryabova, 2018). eIF3 is clearly central for reinitiation on viral RNAs (Pooggin and Ryabova, 2018) and cellular RNAs (Roy et al., 2010; Schepetilnikov et al., 2013; Zhou et al., 2014), reviewed in (Merchante et al., 2017; Raabe et al., 2019). The mechanics of reinitiation are of interest because it determines the portfolio of synthesized proteins across the entire transcriptome.

3.3. RNA Quality Control and Turnover in Plant Translation

When a ribosome encounters an mRNA that prohibits regular completion of the translation process, the ‘aberrant’ mRNA is fated for degradation by XRN4 and SKI2 exonuclease pathways (Szadeczky-Kardoss et al., 2018a). Of the handful of molecular quality control processes known in animals or fungi most are just beginning to be characterized in plants. Ribosomes stuck at the 3’ end of an RNA, e.g. because of miRNA-directed slicer activity, trigger Non-Stop Decay (Szadeczky-Kardoss et al., 2018b), which utilizes homologs to the yeast proteins Hbs1 (related to eRF3) and Dom34 (related to eRF1). These proteins are also invoked under No-Go Decay, i.e. when a ribosome stalls on the poly-lysine encoded by the poly(A) tail, other stalling peptides, or strong RNA secondary structure (Szadeczky-Kardoss et al., 2018a).

The best studied quality control mechanism in plants is nonsense-mediated decay (NMD), a complex process that is triggered on mRNAs with premature termination (stop) codons, splice junctions located over 50 nt downstream of a stop codon, uORFs, and long 3’ UTRs. NMD allows the plant to identify and destroy mRNAs that would otherwise give rise to partial proteins, which may possess maladaptive activities. The NMD mechanism requires three Upf proteins (UPF1 to UPF3), SMG1 and SMG7, and a helicase distantly related to eIF4A, eIF4A III (Ohtani and Wachter, 2019; Poidevin et al., 2019). NMD is further stimulated by other accessory proteins such as the helicase DDX6 (RH12) (Sulkowska et al., 2019).

NMD plays an important role in plant posttranscriptional control. uORFs create premature termination codons, and some but not all uORF-containing mRNAs are NMD substrates (Nyiko et al., 2009). Very interestingly, the expression of the termination factor eRF1 is regulated by an autoregulatory negative feedback loop that involves NMD and degradation of the mRNA when eRF1 levels are sufficient, as compared to stop codon readthrough and suppression of NMD when eRF1 levels are limiting (Figure 5) (Nyiko et al., 2017). Finally, RNA viruses contain multiple coding sequences in their mRNA, whose upstream termination codons can trigger NMD of the entire RNA. Viral sequence elements that stimulate stop codon read-through serve as suppressors of NMD, and unstructured regions downstream of a stop codon can suppress NMD as well (May et al., 2018). In the pararetrovirus cauliflower mosaic virus the multifunctional transactivator protein (TAV) also suppresses NMD on the polycistronic mRNA by interacting with the cofactor for decapping, VARICOSE, in P-bodies (Lukhovitskaya and Ryabova, 2019). In summary, NMD and related RNA quality control processes make the translation machinery robust and able to effectively deal with errors in the upstream steps of gene expression.

Figure 5. — **(A) Structure of the eRF1 mRNA.** After splicing of an intron from the 3’UTR, the 3’UTR is believed to be marked by an exon junction complex. The canonical eRF1 CDS terminates with a stop codon that is prone to translational readthrough (weak stop), which is followed by a regular in-frame stop codon downstream of the exon-exon junction.

**(B) Alternate outcomes during the first round of translation.** When the eRF1 level is high, the canonical termination codon is recognized by eRF1. The exon junction complex remains and triggers degradation of the mRNA by NMD. When the eRF1 level is low, the weak, canonical termination codon is not recognized, translation readthrough occurs and translation stops at the downstream stop. In the process, the exon junction complex is removed thus keeping the mRNA stable and the rate of eRF1 synthesis high. After (Nyiko et al., 2017).

NMD proteins are cellular markers for P-bodies (Processing Bodies), cytoplasmic mRNP granules where mRNAs are decapped. P-bodies also contain ribonucleases for RNA degradation. However, several recent studies have shown that mRNAs are also degraded co-translationally where the 5’−3’ exoribonuclease XRN4 follows a ribosome, whether it is actively translating or stalled (Merret et al., 2015; Yu et al., 2016; Ueno et al., 2018; Ueno et al., 2019). The evidence? The 5’ ends of these in-vivo degraded mRNAs display the triplet periodicity that identifies them as ribosome protected fragments (Hou et al., 2016; Yu et al., 2016). Decay with co-translational characteristics occurs during heat stress (Merret et al., 2013) and, extremely rapidly, during recovery from excess light (Crisp et al., 2017) and thus complements P-body mediated degradation. From the extent of periodicity in the 5’ ends, Yu and coworkers (Yu et al., 2016) deduced a ‘cotranslational decay index’ describing the fraction of co-translational decay versus other modes of decay of each mRNA. This was broken down further by Crisp and coworkers (Crisp et al., 2017) to distinguish decay behind a moving ribosome and a paused ribosome. In summary, these analyses clearly indicate that significant RNA turnover occurs on ribosome-loaded and presumably actively translated RNAs.

3.4. Translational control by accessory translation factors

In recent years it has emerged that the core translation initiation factors partner with a variety of accessory proteins that influence their activity (Figure 6). In general, the evidence for their involvement in translational control rests primarily on their physical interaction with eIFs, whereas their role in translational control will require additional investigation. In mammals, the eIF4E binding proteins (4E-BPs) repress translation by competing with the 5’ cap for binding to eIF4E; they are active when growth is slow and are inhibited by mTOR signaling. While clear homologs for 4E-BPs are missing in plant genomes, several other proteins interact with cap binding proteins. CONSERVED BINDING OF eIF4E 1 (CBE1) interacts both in vitro and in vivo with eIF4E/iso4E in the context of cap binding complex (Patrick et al., 2018). CBE1 bears hallmarks of TOR signaling, given that its phosphorylation is induced by sucrose and rapidly reduced by the TOR inhibitor AZD-8055 (Van Leene et al., 2019). Moreover, CBE1 attenuates expression of cell cycle genes (Patrick et al., 2018).

Figure 6. — CBE1 is an eIF4E binding protein that is phosphorylated in a TOR-dependent manner (Patrick et al., 2018). CERES likewise forms cap-binding complexes with eIF4E/iso4E, which lack eIF4G/iso4G (Toribio et al., 2019).

Activity of the RNA helicase eIF4A is stimulated by MRF proteins, likely through phosphorylation through the TOR kinase pathway (based on Lee et al., 2017). In contrast, phosphorylation of eIF4A by cyclin-dependent kinase may inhibit eIF4A (after Hutchins et al., 2004 and Bush et al., 2016). The RNA binding protein SOAR1 inhibits translation initiation, likely by disrupting the interaction between eIF4G and poly(A) binding proteins. SOAR1 can also bind directly to mRNAs such as the one for ABI5, an abscisic acid-signaling transcription factor (after Mei et al., 2014 and Bi et al., 2019). The jasmonic acid inducible protein JIP60 in barley undergoes proteolytic cleavage upon methyl-jasmonate (MeJA) treatment, which liberates a domain resembling *ribosome inactivating protein* (RIP30) and an eIF4E-like domain. Uncleaved JIP60 also induces the dissociation of the 80S subunit by an unknown mechanism (after Rustgi et al., 2014). MRF: MA3-containing translation regulatory factor; CDKA: Cyclin-dependent kinase A; eIF: Eukaryotic initiation factor; SOAR1: Suppressor of the ABA Receptor-overexpressor 1; JIP: Jasmonate-induced protein; RIP: Ribosome inactivating protein. Some of the findings presented in this figure are correlative or based on circumstantial evidence.

While the effect of CBE1 and other proposed eIF4E binding proteins on translation remains open (Wu et al., 2017), CERES is a plant-specific eIF4E/iso4E-binding protein with a leucine-rich repeat domain (Toribio et al., 2019). CERES is part of actively translating initiation complexes, including eIF3 and PABP, with the peculiarity that eIF4G/iso4G is absent when CERES is present. CERES positively supports translation during the day, specifically promoting translation of light- and carbohydrate-related mRNAs.

Finally, the pentatricopeptide repeat protein SOAR1 inhibits translation by binding to eIFiso4G and thus competing out eIFiso4E and PABP (Bi et al., 2019). While SOAR1 appears to antagonize eIFiso4G biochemically, loss of function mutations in SOAR1 and eIFiso4Gs suggest an agonistic relationship because mutations in either render plants hypersensitive to abscisic acid (ABA) while overexpression of SOAR1 has the opposite effect. SOAR1 also regulates the translation of mRNAs in the ABA signaling pathway, binding of which may explain the complex functional relationship between SOAR1 and eIFiso4G (Bi et al., 2019).

Ribosome inactivating proteins (RIPs) represent a rather unusual mode of translational control. RIPs are glycosidases that depurinate viral RNAs as well as 25S rRNA in its functionally critical sarcin/ricin loop. They are encoded widely in plant genomes and have antimicrobial and antiviral activities (Di and Tumer, 2015; Zhu et al., 2018a). The RIP pokeweed antiviral protein (PAP) deadenylates rRNA and viral mRNAs. Recent work explains that PAP preferentially targets viral RNA because PAP prefers to bind the complex between uncapped viral RNA and eIFiso4F (Domashevskiy et al., 2017). A second class of RIPs discovered in barley functions in translational control by inducibly releasing a carboxy-terminal domain that resembles eIF4E, which in turn regulates translation while the mature RIP domain depurinates the ribosome (Rustgi et al., 2014; Przydacz et al., 2020). Finally, in a third line of research, a putative RIP was discovered to underlie hybrid sterility in rice (Yu et al., 2018), which complicates rice breeding. Hybrid sterility arises from a toxic RIP-like protein that functions in the maternal sporophyte and prohibits the development of male or female gametophytes unless the gametophyte carries the requisite antitoxin gene, which is genetically linked to the toxin. In summary, these potentially extremely toxic proteins have been roped into diverse functions in plant cell biology and defense.

A variety of kinase pathways impart information from the environment onto translation initiation factors in the form of phosphorylation (Table 1) (Dennis et al., 2009; Boex-Fontvieille et al., 2013; Fila et al., 2016; Nukarinen et al., 2016; Van Leene et al., 2019). Focusing on recent advances, in proliferating cells, cyclin-dependent protein kinase A (CDKA) interacts with eIF4A during S, G2 and M phases (Figure 6). Phospho-null and phosphomimetic mutations in its RNA binding domain suggest that phosphorylation by CDKA inhibits eIF4A activity (Bush et al., 2016). Meanwhile, under dark and glucose withdrawal conditions, four paralogous MRF proteins (MA3-domain containing translation regulatory factors) are transcriptionally induced, bind eIF4A, and stimulate translation (Figure 6). The MRF accessory translation factors are a target of phosphorylation most likely through the TOR-S6K pathway (Lee et al., 2017).

Table 1.

Phosphorylation of translation initiation factors.

Initiation factor	Kinase	System	Stimulus	Outcome	Reference
eIF2- subunit α	GCN2	Arabidopsis, tobacco	Herbicide, stress		Lageix et al., 2008; Zhang et al., 2008
eIF2- subunit β	TOR	Arabidopsis Cell Culture	Sucrose		van Leene et al., 2019
eIF2B- subunit δ	TOR	Arabidopsis, Arabidopsis Cell Culture	Sucrose		Boex-Fontvieille et al., 2013; van Leene et al., 2019
eIF3- subunit b		Arabidopsis	Darkness, high CO2		Boex-Fontvieille et al., 2013; Choudhary et al., 2015
eIF3- subunit c	CK2	In vitro, Arabidopsis			Dennis & Browning, 2009; Boex-Fontvieille et al., 2013; Choudhary et al., 2015
eIF3- subunit d		Arabidopsis			Boex-Fontvieille et al., 2013
eIF3- subunit h	TOR-S6K1	Arabidopsis	Auxin	increased translation of uORF containing transcripts	Schepetilnikov et al., 2013
eIF3- subunit i	BRI1	in-vitro		unknown	Ehsan et al., 2005
eIF4A	CDKA	In vitro	Darkness	inactive eIF4A In vitro/ unknown In vivo	Bush et al., 2016; Boex-Fontvieille et al., 2013
eIF4B	CK2, TOR	In vitro, Arabidopsis Cell Culture	Sucrose High CO2		Gallie et al., 1997; Dennis & Browning, 2009; van Leene et al., 2019; Choudhary et al., 2015 Boex-Fontvieille et al., 2013;
eIF4E	SnRK1	In vitro			Bruns et al., 2019
eIF4G	TOR	Arabidopsis Cell Culture	Sucrose Darkness		van Leene et al., 2019; Boex-Fontvieille et al., 2013
eIFiso4E	SnRK1	In vitro			Bruns et al., 2019
eIFiso4G	SnRK1	Maize	Hypoxia	Regulation of core hypoxia gene expression	Cho et al., 2019; Choudhary et al., 2015
eIF5	CK2	In vitro, Arabidopsis			Dennis & Browning, 2009; Boex-Fontvieille et al., 2013; Choudhary et al., 2015
eIF6	TOR	Arabidopsis Cell Culture	Sucrose		van Leene et al., 2019

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The table emphasizes events with a known stimulus, outcome or kinase.

Multiple phosphorylation events occur on eIF4F/iso4F. Wheat eIFiso4E is phosphorylated on Ser207; while the responsible kinase is unknown in this case, phosphorylation reduced the energy barrier for binding to two cap analogs (ant-m7GTP and m7GpppC) (Khan and Goss, 2018). eIF4E is also phosphorylated by the energy sensing kinase SnRK1 (sucrose non-fermenting related kinase 1) in vivo in both yeast and transformed Nicotiana benthamiana, leading to translation repression (Figure 7). A drop in polysomes is seen in a T67D phosphomimic mutant and lost in the corresponding phospho-null allele, suggesting a negative effect on eIF4E activity (Bruns et al., 2019). SnRK1 also phosphorylates eIFiso4G on multiple sites during hypoxia stress alongside other translation factors (Boex-Fontvieille et al., 2013; Cho et al., 2016). Phosphorylation of eIFiso4G under low-energy conditions supports the ribosome loading of specific mRNAs including 14 core hypoxia-inducible transcripts (Cho et al., 2019). Of note, the examples from this and earlier sections demonstrate that it is common for a given translation factor to be targeted by multiple kinases at multiple sites, potentially orchestrating an intricate fine tuning of translation factor activities in response to energy status, metabolism, defense, and growth cues.

Figure 7. — The Snf1 related kinases SnRK1 and SnRK2 are activated during energy deprivation and ABA signaling. Phosphorylation by SnRK1 of eIFiso4G contributes to the repression of translation under hypoxia in maize (note color coding). Phosphorylation of eIF4E and eIFiso4E by SnRK1 is observed *in vitro*. Both SnRK1 and SnRK2 also lead to phosphorylation of Raptor in the TOR complex, which may contribute to TOR inhibition during energy deprivation and ABA stress signaling. Some of the findings presented here are correlative or based on circumstantial evidence. ADH: Alcohol dehydrogenase, LBD: LOB domain-containing protein, NIP: Nodulin-26 like intrinsic protein. For details see text.

4. RNA FEATURES

4.1. Covalent Modification of mRNAs

In the mRNA, its primary sequence elements, secondary structure and covalent modifications all potentially contribute to translational control. The canonical 5’ cap and 3’ poly(A) tail both are required for mRNA stability, as decapping, deadenylation and endonucleolytic cleavage all fate the mRNA for degradation. In recent years, three other covalent modifications have attracted interest. First, methylation at the N⁶ position of the adenine ring (m⁶A) is regulated dynamically, preferentially in 3’ regions of mRNAs (Luo et al., 2014; Ruzicka et al., 2017). m⁶A is expected to alter the potential of adenine to form Watson-Crick basepairs or Hogsteen-type hydrogen bonding, which would affect tRNA decoding, secondary structure and small RNA binding. Analogous to epigenetic marks in DNA, m⁶A is recognized by reader proteins (Scutenaire et al., 2018), reviewed in (Reichel et al., 2019). Second, methylation of cytosine (m⁵C) is also observed in mRNAs and noncoding RNAs (David et al., 2017). Third, substitution of the canonical m⁷G cap with an NAD⁺ dinucleotide occurs in up to 5% of a gene’s transcripts (Zhang et al., 2019). The NAD⁺-capped mRNAs are polyadenylated, spliced and found in polysomes (Wang et al., 2019). Proteins responsible for removing NAD⁺ are also encoded in plant genomes, but may not function in this capacity (Kwasnik et al., 2019; Pan et al., 2019). For all these covalent mRNA modifications, their immediate impact on translation is not well defined but m⁶A is known to lower or boost mRNA stability (Shen et al., 2016; Anderson et al., 2018).

An unusual mechanism for a virus to acquire a 5’ cap is manifested by the ‘cap-snatching’ viruses, of which tomato spotted wilt virus is one of the few known examples in plants. In an unconventional twist on ‘covalent mRNA modification’, these viruses cleave the 5’ end, including the cap, from host mRNAs, and utilize it as a primer for mRNA transcription of their genome. Cap snatching is apparently more easily achieved with mRNAs targeted for degradation in P-bodies. In support of this, a dcp2 decapping mutant is more susceptible to infection by this virus (Ma et al., 2019) likely because mRNAs linger for longer in P-bodies before being degraded. This case represents an intriguing strategy of a virus subverting the host mRNA degradation machinery to its own needs.

4.2. Secondary Structure

Secondary structure of mRNAs is largely driven by Watson-Crick basepairing forming stem-loops in the RNA, and tertiary structures can be augmented by Hogsteen-type hydrogen bonding over the remaining solvent exposed face of the nucleobase. Measuring secondary structure is complicated because in vivo, ex vivo, and in vitro conditions often yield different results. Predicting secondary structure is challenging because all but the shortest RNAs potentially fold into alternative structures with similar thermodynamic stability and because helicase activities disturb equilibrium conditions in vivo. Nonetheless, secondary structure has been estimated transcriptome-wide at nucleotide resolution using a variety of chemical structure-probing reagents (Li et al., 2012a; Ding et al., 2014; Vandivier et al., 2016; Mitchell et al., 2019). Correlations between secondary structure and translational efficiency are fairly sparse, but the regions around start and stop codons are depleted in secondary structure. Moreover, the mRNA’s chemical reactivity with structure probing reagents varies across certain mRNAs in a way suggesting that globular enzyme domains are translated from unstructured mRNA regions, i.e. faster, while interdomain regions are more structured, i.e. translated more slowly. This pattern may promote the proper folding of the globular domain before the next nascent domain emerges from the ribosome (Tang et al., 2016). Finally, because RNA folding is temperature dependent, RNAs may function as cellular thermometers. A rise in temperature is a minimally invasive method to thermodynamically unfold an RNA in vivo. However, unfolding of RNAs upon 3h of heat shock, as measured by transcriptome-wide mapping of mRNA structure, did not predict increases in translation but rather predicted RNA degradation (Su et al., 2018). If we had hypothesized that RNA secondary structure substantively constrains ribosome loading, this result would seem to tip the scales against this hypothesis. In fact, secondary structures that are thermodynamically stable enough to resist the helicase activity of the ribosome (Desai et al., 2019) are fairly uncommon; most known cases are from viruses and 3’ UTRs. Recently, the G-quadruplex has emerged as a stable RNA-fold. Although widespread, especially in G-rich monocot genomes, there are few examples for a G-quadruplex in a 5’ leader sequence repressing translation (Kwok et al., 2015; Griffin and Bass, 2018; Kopec and Karlowski, 2019).

Another translationally relevant secondary structure is found in the 5’ leader of the pararetroviruses such as cauliflower mosaic virus. Here, an elaborate hairpin structure (ΔG ~−200kcal/mol) contains a sequence motif that attracts the viral coat protein to initiate capsid assembly. To leave the motif undisturbed, the 40S ribosome is able to bypass the hairpin through a nonlinear scanning mechanism referred to as shunting (Figure 3B). Interestingly, in nearly every virus examined, the capacity to shunt requires a short uORF right upstream of the shunt take-off site. Apparently, some property specific to the post-termination (40S) ribosome makes it permissive to skip past the hairpin structure, possibly because the prior translation event stripped helicase activities from the 40S subunit (Pooggin and Ryabova, 2018).

Variations on a theme by Kozak are orchestrated by many plant RNA viruses. Besides the 5’ terminal VPg proteins, the 3’ UTRs of many RNA viruses harbor cap-independent translational enhancers (3’ CITEs), RNA sequences that interact with the 5’ end through basepairing and protein-protein interactions by bound translation factors (Figure 3D). 3’CITEs extend the closed-loop model from cellular to viral RNAs. They typically interact with cognate 5’ sequence elements through basepairing between RNA secondary structures referred to as kissing loops. Analogous to PABPs connecting with eIF4G, the 3’ CITEs commonly attract the initiation factors of the eIF4 complex including eIF4E/iso4E, eIF4G/iso4G, eIF4A or eIF4B as well as PABP and eventually the 40S, e.g. (Du et al., 2017; Liu and Goss, 2018; Kraft et al., 2019). Because the wealth of literature on viral 3’ CITEs cannot be done justice in this general review we refer readers to thorough reviews by (Sanfaçon et al., 2015; Truniger et al., 2017). As a variation on 3’ CITEs, stable tRNA-like structures (Le et al., 2017) form on certain viral 3’ UTRs and boost translation, by binding to 60S, 80S or 40S subunits (Gao et al., 2012), interacting with 5’ ends through kissing loops, and increasing the fraction of mRNAs available for translation (Gao et al., 2018).

The rich panoply of 3’ CITEs raises the question whether plants also make use of classical internal ribosome entry sites (IRESs), RNA sequence elements in 5’ UTRs that, by virtue of their secondary structure and factor binding properties, attract the 40S or 80S ribosome in a cap-independent manner (Figure 3C). Reports of IRESs in nuclear encoded plant mRNAs are small in number, e.g. (Dinkova et al., 2005; Mardanova et al., 2008). The stem-cell regulator WUSCHEL is translated from an mRNA with a bona fide IRES in its 5’UTR, stimulated by the RNA binding protein La (Cui et al., 2015). IRESs are common in animal viruses but appear less common in plants (Roberts et al., 2015; May et al., 2017). However, in the potyvirus triticum mosaic virus, a long 5’UTR that is riddled with upstream AUGs contains a complex secondary structure with a critical 8bp hairpin-loop. The structure passes as an IRES by fulfilling several accepted criteria. It drives cap-independent bicistronic translation in vitro and in vivo. It is resistant to a stable hairpin at the 5’ end of the RNA, expected to block scanning ribosomes. It recruits eIF4G/iso4G with higher affinity than eIF4E/iso4E (Roberts et al., 2017). Moreover, a polypyrimidine stretch upstream of the actual translation start codon may basepair with the 18S rRNA (Jaramillo-Mesa et al., 2019), another typical feature of animal IRESs. Taken together, while 3’ CITEs and 5’ IRESs are characteristic for plant and animal viruses respectively, it now appears that both paradigms occur in both kingdoms.

4.3. Small RNAs

Small RNAs that function as guide RNAs for Argonaute-based RNA-induced silencing complexes (RISCs) typically mediate cleavage of their target mRNAs, which can occur cotranslationally as well as in non-translating RNP granules such as P-bodies (Yu et al., 2017; Chantarachot and Bailey-Serres, 2018). However, small RNAs, mainly miRNAs but in exceptional cases also siRNAs, may also inhibit translation directly as demonstrated in vitro (Iwakawa and Tomari, 2013). Certain miRNA-mRNA pairs are subject to translational inhibition, which occurs preferentially on membrane bound ribosomes (Li et al., 2013). Whether a miRNA preferentially inhibits translation or cleaves its mRNA target can be cell type specific (Brosnan et al., 2019).

Although several proteins that mediate translational inhibition by miRNA were identified early on, the molecular mechanisms that determine the choice between translational inhibition and RNA degradation largely remain to be resolved (Brodersen et al., 2008; Yang et al., 2012; Li et al., 2013; Ma et al., 2020). This question has been difficult to unravel, because, first, even miRNAs that are known to inhibit translation typically also degrade their target (Yu et al., 2017), and second because even RISC-mediated RNA turnover often occurs on polyribosomes (Li et al., 2013; Yu et al., 2016). In vivo, many miRNAs and even chromatin-modifying 24nt siRNAs are found in polysomes, along with AGO1 (Lanet et al., 2009; Marchais et al., 2019). Strikingly, the production of phased siRNAs from noncoding RNAs not only occurs on membrane-bound polyribosomes, but requires the translation of a previously unrecognized open reading frame on the RNA substrate (Bazin et al., 2017). This finding exemplifies a core concept of RNA-level regulation: processes that lend themselves to neat conceptual separation in the text book are often tightly commingled inside the cell.

4.4. tRNAs

tRNAs and their corresponding aminoacyl-tRNA-synthetases (aaRSs) are often regarded merely as bulk biochemical reagents for protein synthesis. However, the molecular biology of tRNAs also has regulatory significance. The 61 codons are serviced by tRNAs transcribed and processed from nearly 600 tRNA genes and charged by about 45 aminoacyl-tRNA synthetase enzymes (Cognat et al., 2017; Park and Kim, 2018). The relative abundance of tRNAs affects the fidelity of decoding as well as the speed of translation elongation, which in turn influences mRNA turnover.

tRNA biogenesis is regulated in coordination with other translational events as an output of the TOR kinase pathway (Ahn et al., 2019). When activated, TOR phosphorylates and inhibits MAF1, a general repressor of RNA Pol III, thus enhancing Pol III-dependent transcription of tRNAs, 5S rRNA and other small RNAs and promoting cell growth. Accordingly, maf1 mutations in Arabidopsis cause hypersensitivity to diverse stresses, such as oxidative stress and DNA damage (Ahn et al., 2019). Given that maf1 mutants look normal under favorable conditions, MAF1 appears to regulate tRNA biogenesis in response to environmental perturbations that require translation regulation. MAF1 must be important because certain pathogens such as Xanthomonas citri release a pathogenicity effector molecule that targets MAF1 in an apparent effort to boost protein synthesis (Soprano et al., 2018).

In response to stresses such as salt, drought, oxidative stress and phosphorous deficiency, tRNAs are broken down into defined tRNA fragments (tRFs) (Thompson et al., 2008; Megel et al., 2019), reviewed in (Park and Kim, 2018). These fragments arise via Dicer-dependent and RNAse T2-dependent pathways (Alves et al., 2017; Martinez et al., 2017; Megel et al., 2019). While some tRFs are tRNA halves clipped at the anticodon, others are smaller and appear in AGO-containing RISCs (Trolet et al., 2019), where they may potentially affect translation (Zhang et al., 2009), as recently demonstrated in vitro (Lalonde et al., 2020). Interestingly, tRFs arise not only from cytosolic, but also from plastidic and mitochondrial precursors (Cognat et al., 2017). Discovered in phloem sap, they may function as long-distance signaling molecules (Zhang et al., 2009). However, our understanding of how tRFs mediate responses to environmental stress is still at an early stage (Alves et al., 2017; Park and Kim, 2018). Taken together, tRNA biology illustrates that environmental perturbations regulate translation not only through the phosphorylation status of translation factors and inhibiting the ribosome loading of mRNAs but also via tRNA biogenesis and potentially the appearance of tRNA fragments.

4.5. Upstream Open Reading Frames

The most widely distributed translationally active RNA sequence element is the upstream open reading frame (uORF). An uORF is defined as a coding sequence of any length that typically begins with an AUG in the 5’ leader sequence (also called the 5’ untranslated region) of an mRNA (Figure 4A). About 30%−40% of plant genes give rise to an mRNA that contains an uORF. Unless skipped by ‘leaky scanning’ (Sugio et al., 2010), uORFs repress the translation of the main ORF by engaging the scanning ribosome and diverting it from the main AUG (von Arnim et al., 2014; Srivastava et al., 2018). uORFs that extend into the main coding sequence are most inhibitory. Ribosome footprinting has yielded direct evidence that many uORFs are actively translated (Liu et al., 2013; Juntawong et al., 2014; Hsu et al., 2016; Bazin et al., 2017; Kurihara et al., 2020; Wu et al., 2019). Because an uORF termination codon is a premature stop codon that triggers NMD, the fate of the mRNA depends on the capacity of the ribosome to reinitiate translation, which is inversely related to uORF length.

Aside from uORF length and AUG sequence context, an uORF will be less inhibitory if the uAUG lies within another uORF, if the uORF begins with a non-AUG start codon, and if the uAUG is occasionally removed by alternative splicing or skipped because of alternative transcription initiation downstream in the 5’ leader (Roy et al., 2010; Zhou et al., 2014; Kurihara et al., 2018) (Figure 4B). For example, translation of the phytochrome interacting factor PIF3 is inhibited by retention of an uORF-containing intron in the 5’ leader, whose retention is stimulated by light (Dong et al., 2020).

uORFs are the basis for translational regulation by environmental conditions, as illustrated by two genome-wide studies. First, blue light stimulates the translation of >100 uORFs in Arabidopsis, which in turn attenuates the translation of the downstream main ORF (Kurihara et al., 2020). Second, phosphate starvation alters the ratio of ribosome loading between uORF and mORF on at least 8 mRNAs, including several that may influence root architecture for phosphate uptake (Bazin et al., 2017).

uORFs that induce ribosomal arrest via their encoded peptide sequence (Hayashi et al., 2017; van der Horst et al., 2019) are more likely to also inhibit translation. The over 100 uORFs that encode conserved peptides (CPuORFs) in Arabidopsis are a small minority of uORFs but underpin a very interesting regulatory paradigm of metabolic control of translation. In some of these, the inhibitory potential of the uORF is regulated by the concentration of a specific cellular metabolite, such as sucrose (Rahmani et al., 2009), phosphocholine (Alatorre-Cobos et al., 2012), galactinol (Zhu et al., 2012), boron (Tanaka et al., 2016; Aibara et al., 2018), thermospermine (Ishitsuka et al., 2019) or other small molecules. Recently a case of an uORF regulated by photosynthesis has shown that uORFs can render translation tissue-specific (Ribone et al., 2017). Evidently, although metabolic control by uORFs also occurs in fungi and animals, this paradigm appears to have evolved a larger spectrum of applications in plants.

The enzyme GDP-l-galactose phosphorylase (GGP) in the ascorbate biosynthesis pathway exemplifies this uORF-mediated metabolic control (Figure 4C). Translation begins at a non-AUG uORF in the 5’UTR (ACG instead of AUG), which encodes a 60–65 amino acid peptide. By an unknown mechanism, the non-AUG start codon is recognized more readily under high ascorbate levels, thereby downregulating the GGP protein when the end product is abundant (Laing et al., 2015). This uORF is conserved from green algae to angiosperms.

The uORFs in the 5’ leader of an mRNA represent a binary decision tree for the ribosome. Each AUG start codon serves as a node that force the scanning ribosome to decide whether to initiate or not, and the length of the uORF determines which sections of the 5’ leader are being scanned. The 5’ leader can be compared to the board game of ‘snakes (chutes) and ladders’, where each AUG is analogous to the start of a ladder, because it allows the ribosome to skip other AUGs, while each stop codon is a ‘terminal snake’ because it puts the ribosome at risk of being ejected from the 5’ leader by virtue of failing to reinitiate. This principle is illustrated by the clustered uORFs in the mRNA for S-adenosylmethionine decarboxylase (AdoMetDC or SAMDC), which is rate limiting for polyamine synthesis (Figure 4D). The 5’ leader harbors a CPuORF whose AUG is overlapped and thus masked by a second uORF, aptly termed the “tiny” uORF because it is only 3 codons long (Hanfrey et al., 2005). Under low polyamine levels, the tiny uORF is translated thus masking the inhibitory CPuORF but allowing reinitiation at the AdoMetDC main ORF and boosting polyamine synthesis. In contrast, under elevated polyamine levels the tiny uORF is skipped and hence the CPuORF translated. Subsequent ribosome stalling on the CPuORF peptide feedback-inhibits the synthesis of the AdoMetDC enzyme (Hanfrey et al., 2005; Uchiyama-Kadokura et al., 2014; Takamatsu et al., 2020).

Some uORFs are evolutionarily conserved by their position in the 5’ leader, but not their sequence (Vaughn et al., 2012; Bazin et al., 2017). Even uORFs that are not noticeably conserved at the peptide level can mediate translational responses to the environment. At least two different mRNAs are translationally repressed by boron by uORF-mediated mechanisms. For the boron uptake channel NIP5;1 the uORF is an AUG-Stop (Tanaka et al., 2016), whereas in the boron transporter BOR1 repression by boron is mediated by a group of three uORFs. uORFs are present in BOR1 mRNAs of different species but are not conserved at the peptide level. Here, an AUG-Stop uORF contributes to the regulation, but the most important uORF is a longer one (Aibara et al., 2018). Thus, the vast majority of uORFs that are not conserved at the peptide level should at least be considered to have regulatory potential (Vaughn et al., 2012).

In summary, with the uORF, nature has evolved an elegant regulatory principle because, first, uORFs can evolve rapidly in a digital manner by single nucleotide substitutions that form or remove AUG triplets and, second, uORFs allow for translational control by the ribosome itself despite its structure-flattening helicase activity. With the development of precise gene editing tools, we can expect that uORFs will be incorporated into strategies to manipulate protein synthesis and plant phenotype under specific conditions (Xu et al., 2017b; Zhang et al., 2018; Si et al., 2020).

5. EMERGENT SIGNAL-RESPONSE PATHWAYS IN TRANSLATION

Until approximately ten years ago we knew of upstream signals that regulate translation in indirect ways, and we were aware of downstream mechanisms of translational control that were not yet connected to the mechanistic signaling pathways. Over the past ten years these two domains have become linked in several cases, an exciting advance in the field of plant translational control. In this last section, we highlight a few of these case studies.

5.1. Translational control of bZIP transcription factor mRNAs by the sucrose-dependent peptoswitch

Among more than 40 distinct CPuORF homology groups (Jorgensen and Dorantes-Acosta, 2012; Vaughn et al., 2012; Ebina et al., 2015; van der Horst et al., 2019) those that have been tested typically suppress translation of their main ORF in a peptide sequence-dependent manner, and the peptide causes ribosome arrest at or upstream of the uORF stop codon. In a study examining the 5’ ends of mRNAs in the process of degradation it was noted that multiple ribosomes may pile up behind the arrested ribosome (Hou et al., 2016). Of note, similar ribosome pile-up was also observed in an unusual case of peptide-mediated ribosome arrest on the main ORF of a canonical mRNA (Yamashita et al., 2014). In any event, a stalled ribosome precludes translation reinitiation if it does not already trigger RNA degradation (Ebina et al., 2015; Hayashi et al., 2017).

In the case of one subclass of basic leucine zipper (bZIP) transcription factors, a long CPuORF in the 5’ leader represses translation in response to sucrose, the abundant transport form of photoassimilated carbohydrates. Given that translational arrest can be recapitulated in vitro, it was hypothesized that the ribosome exit tunnel in the 60S subunit and the CPuORF-encoded peptide create a specific metabolite binding pocket for sucrose, which is proposed to allosterically affect the peptidyl transfer reaction and/or peptide release (peptoswitch model) (Yamashita et al., 2017; van der Horst et al., 2020).

When bZIPs are overexpressed by removing said sucrose-induced repression of translation, both the sugar signaling compound, trehalose-6-phosphate, and several amino acids overaccumulate in the plant. This supports the role of the CPuORF in the regulation of general carbon/nitrogen metabolism (Hanson et al., 2008; Ma et al., 2011; Weiste et al., 2017). It is intriguing that the sucrose-induced translational repression feeds back into carbon (sugar) and nitrogen (amino acid) metabolism, which in and of itself globally regulate translation through the SnRK and TOR pathways, as will be described below.

Whether all CPuORFs function in a similar manner by sensing metabolites to regulate ribosome stalling remains an open question. Also, what are the critical structural features of the CPuORF’s nascent peptide that allow metabolite induced ribosome stalling? And should there not also be cases of metabolites unstalling a naturally stalled ribosome? After all, a stalled ribosome would offer a longer time window for successful recruitment of the correct metabolite than an actively translating ribosome. These intriguing questions have biotechnological implications, given the current boom in devising precise ways for regulating gene expression directly at the level of mRNA translation (Xu et al., 2017b; Li et al., 2019; Mauger et al., 2019; Si et al., 2020).

In principle, the binding of a specific metabolite to a translating ribosome is a eukaryotic analog to the bacterial riboswitch (van der Horst et al., 2020). However, instead of a metabolite binding to an RNA tertiary structure, according to the sucrose ‘peptoswitch’ model, the metabolite binds to a translating ribosome harboring a characteristic nascent peptide as its specificity determinant. In this fashion plants have adapted the riboswitch concept although their 5’ leader sequences are prevented from adopting stable secondary structures by the scanning 40S ribosome.

5.2. TOR kinase signaling

The TARGET OF RAPAMYCIN (TOR) kinase plays a vital role in integrating multiple external cues (e.g., light, nutrient availability and energy status, hormones, stress) to stimulate cellular processes underlying cell growth and development. Specifically, TOR kinase affects the levels of numerous transcripts, including those for plastid ribosomes (Dobrenel et al., 2016b), and stimulates the cell cycle (Xiong and Sheen, 2013; Pfeiffer et al., 2016) and translation (Shi et al., 2018). Overall, core elements of the eukaryotic TOR pathway are conserved in plants, including TOR’s antagonistic relationship with the energy-sensing SnRKs, TOR’s dependence on the partner proteins RAPTOR and LST8, its activation under energy replete conditions, and its signaling through the kinases S6 kinase (S6K) and YAK1 (Barrada et al., 2019; Forzani et al., 2019), and the potentiation of TOR signals by the inhibitory subunit Tap46 of protein phosphatase 2A (Ahn et al., 2011; Ahn et al., 2015). Phosphorylation of S6K and of the ribosomal protein eS6 are diagnostic markers of TOR activity across eukaryotes, including in plants (Dobrenel et al., 2016a; Chen et al., 2018).

Because many recent reviews have summarized the status of plant TOR signaling in detail (Sesma et al., 2017; Schepetilnikov and Ryabova, 2018; Shi et al., 2018; Ahmad et al., 2019; Caldana et al., 2019; Forzani and Meyer, 2019; Rodriguez et al., 2019) this section will focus on effects of TOR on the translation apparatus, building on the early observation that silencing of TOR inhibits mRNA-ribosome loading (Deprost et al., 2007). The translational activation of specific mRNAs by the plant hormone auxin is one of the best characterized translational functions of the TOR kinase signaling pathway (Schepetilnikov et al., 2013; Schepetilnikov et al., 2017) (Figure 8). Auxin was first shown to promote the phosphorylation of S6K and its target, eS6 (RPS6) in cell suspension cultures (Turck et al., 2004). In the plant shoot, light promotes auxin biosynthesis, which then triggers binding of the GTP-bound Rho-like small G protein (ROP2) to the N-terminus of TOR (Li et al., 2017c; Schepetilnikov et al., 2017). Once activated, TOR phosphorylates the S6K, which leads to the phosphorylation of the h subunit of eIF3, a protein implicated in translation reinitiation on uORF-containing mRNAs (Roy et al., 2010). mRNAs encoding auxin response transcription factors (ARFs) contain uORFs and require translation reinitiation (Nishimura et al., 2005; Zhou et al., 2014; Chen et al., 2019), as do the mRNAs for the sucrose-repressed S-class bZip transcription factors (Wiese et al., 2004; Rahmani et al., 2009; Roy et al., 2010). Accodingly, TOR kinase activation by auxin stimulates the gene specific translation of transcription factors with developmental (ARFs) and metabolic (S-class bZips) functions.

Figure 8: — **(Left)** Four TOR outputs. (i) TOR triggers phosphorylation of the h subunit of eIF3 through the S6 kinase. This event supports the role of eIF3h in reinitiation after uORF translation. It is triggered by light stimulated synthesis of auxin and subsequent activation of TOR by the Rho-like small G protein (ROP2). (ii) Phosphorylation of the RNA polymerase III repressor protein, Maf1, boosts synthesis of tRNAs and rRNAs. (iii) TOR induces the phosphorylation of ribosomal protein eS6 through the S6 kinase, although the biochemical significance of this event remains unknown. (iv) TOR phosphorylation of MRF proteins through S6 kinase triggers MRF1 association with eIF4A and activates translation. (v) Sulfur deficiency depletes TOR activity, possibly via low glucose and SnRK signaling.

**(Middle)** Interaction of SnRKs and TOR. (i) Under conditions of low energy, active SnRK1 may phosphorylate Raptor1B, which may trigger disassembly of the active TOR complex and translational inhibition. High energy signals such as trehalose-6-phosphate, glucose −6 or −1-phosphate inhibit repression of SnRK1 on TOR complex. (ii) ABA also activates SnRK1 via its negative regulator, protein phosphatase 2C (PP2C). (iii) SnRK2 is activated by ABA under abiotic stress conditions and may likewise lead to Raptor phosphorylation. SnAK is the SnRK activating kinase whose binding to SnRK is inhibited by T6P. Other phosphorylation targets of SnRK are listed in Table 1.

**(Right)** GCN2 kinase is co-activated by GCN1 and uncharged tRNA. GCN2 phosphorylates the α subunit of the GTPase eIF2. GCN2 is activated by multiple abiotic and biotic stressors, some of which may deplete amino acids and increase deacylated tRNAs. Depletion of O-acetyl serine, a precursor of cysteine, stimulates GCN2. Reactive oxygen species (ROS) arise from the photosynthetic apparatus under excess light and activate GCN2. ROS also accompany many of the other triggers known to activate GCN2 such as herbicide and cold.

Black arrows and red T-bars represent activation or inhibition, respectively. Dashed lines indicate indirect or hypothetical connections. Based on Schepetilnikov et al., 2013 and 2017, Rodrigues et al., 2013; Nukarinen, 2016; Lee and Pai, 2017; Izquierdo et al., 2018; Ahn and Pai, 2019; Van Leene et al., 2019, Wang et al., 2018, Rodriguez et al., 2019, Dong et al., 2017, Lageix et al., 2008, Wang et al., 2018, Lokdarshi et al., 2020a, Lokdarshi et al., 2020b.

TOR kinase additionally signals to a variety of translation-relevant proteins including MRFs, which are partners of eIF4A helicase, the ribosomal protein eS6, and the inhibitor of Pol III, MAF1 (Bush et al., 2016; Lee et al., 2017; Ahn et al., 2019). Together with global and gene-specific effects on polysome loading and rRNA transcription (Deprost et al., 2007; Ren et al., 2011; Dobrenel et al., 2016b), it appears that the TOR pathway signals to the translation apparatus in multifarious ways (Figure 8). There is a general correlation between (i) the signals known to stimulate the TOR pathway, such as light, glucose and sucrose, (ii) the absence of abiotic stressors that signal through the ABA pathway, (iii) TOR activity as scored by phosphorylation of S6K and eS6 (Xiong and Sheen, 2013; Dobrenel et al., 2016b; Pfeiffer et al., 2016; Chen et al., 2018) and active translation. For example, eS6-P is found on polysomes within 2 hours of light exposure (Enganti et al., 2018).

Evidence points to a critical role for the energy sensing SnRKs (Margalha et al., 2019). Trehalose-6 phosphate (T6P) is synthesized from UDP-glucose and glucose-6-phosphate and is considered a proxy for sucrose in plants (Figueroa and Lunn, 2016; Rodriguez et al., 2019), but also feeds back to repress sucrose levels and promotes nitrogen assimilation and amino acid synthesis (Yadav et al., 2014; Figueroa et al., 2016). T6P can bind SnRK1 directly and inhibits it in vitro by disrupting the interaction between SnRK1 and its upstream activating kinase, SnAK (Zhai et al., 2018). SnRK1 in turn can bind and phosphorylate RAPTOR1 (Nukarinen et al., 2016; Van Leene et al., 2019), a biochemical link between SnRK and TOR of intriguing but speculative significance (Figure 8). In contrast, under stress conditions (e.g., drought, cold), ABA activates SnRK2, which also leads to phosphorylation of RAPTOR (Wang et al., 2018), potentially contributing to the suppression of global translation that occurs under diverse ABA-mediated stresses. ABA also activates the SnRK1 signaling pathway by inhibiting type 2C protein phosphatases (PP2C) that are negative regulators of SnRK1 (Rodrigues et al., 2013). Vice versa, under favorable growth conditions, phosphorylation of the ABA receptor PYL by the TOR kinase prevents ABA binding and thus attenuates stress signaling (Wang et al., 2018). Although the actual impact on translation of these stress and energy signals through SnRKs and TOR kinase remains to be defined more fully, potential mechanisms to convey the signals are emerging.

While SnRK1 may exert some of its activities through TOR, it affects translation even more directly. SnRK1 phosphorylates eIFiso4G1 under submergence stress (low O₂ or hypoxia) (Cho et al., 2016; Cho et al., 2019). This results in the selective translation of hypoxia-induced mRNAs that mediate submergence tolerance without affecting general translation (Figure 7). Moreover, SnRK1 phosphorylates the mRNA cap binding proteins eIF4E and eIFiso4E resulting in translational suppression (Bruns et al., 2019) (Figure 7). These emerging targets of SnRK1 depict a more direct role in regulating translation beyond the TOR signaling pathway.

Metabolite profiling after TOR inactivation has revealed a profound reorganization of the metabolome affecting sugars and organic acids, and characteristic increases in most amino acids (Moreau et al., 2012; Mubeen et al., 2018; Caldana et al., 2019). Outside the plant kingdom TOR is an amino acid sensor, but in plants the corresponding evidence is sparse if not absent. Instead, TOR stimulates nitrate reduction but represses both nitrogen uptake and amino acid accumulation in Arabidopsis and Chlamydomonas (Ahn et al., 2011; Moreau et al., 2012; Mubeen et al., 2018). These roles may seem at odds with TOR’s role in boosting translation. However, they appear more coherent when considering that high amino acid levels in Arabidopsis are a hallmark of carbon starvation conditions (Gibon et al., 2009) and that TOR is also a suppressor of autophagy.

While little is clear about TOR sensing nitrogen, TOR has been linked to sensing sulfur. Cysteine is synthesized from serine and sulfite in three enzymatic steps, starting with sulfite reductase (SiR) reducing sulfite to sulfide. The sir1 mutant strain has low levels of S6K phosphorylation, ribosomal RNA, transcripts encoding ribosomal proteins as well as general translation (Dong et al., 2017). These phenotypes of the sir1 mutant can be explained by low TOR activity, because glucose feeding, which boosts TOR activity, ameliorates the retarded growth phenotype of sir1. Flux of reduced sulfur into glutathione competes with flux into cysteine; accordingly a cad2 mutation, which restricts glutathione synthesis, suppresses the sir1 phenotype and even rescues TOR activity (Speiser et al., 2018). These findings suggest that cysteine or a cysteine precursor can stimulate TOR activity, thus linking sulfur or amino acid status to translation.

5.3. The GCN2 kinase

The phosphorylation of eIF2α is one of the most widely studied translational control events across all eukaryotes. In animals and fungi, eIF2α is phosphorylated on a conserved serine residue (Ser51) by the GCN2 kinase (General Control Nonderepressible 2) as part of the integrated stress response, which represses translation globally (Wek, 2018). GCN2 kinase is activated upon binding of uncharged tRNA, a consequence of amino acid depletion, to the GCN2 C-terminal histidyl-tRNA synthetase (HisRS)-like regulatory domain (Dong et al., 2000; Garriz et al., 2009; Lageix et al., 2015). In animals and yeast, phosphorylation of eIF2α represses translation by inhibiting the guanine nucleotide exchange factor for eIF2, eIF2B (Figure 8). While eIF2B is highly conserved in plants and forms a physical complex, whether eIF2B functions in this manner, and to what degree P-eIF2α represses translation remains unknown (Browning and Bailey-Serres, 2015; McWhite et al., 2020).

In animals and yeast, the GCN2 kinase is further activated by cofactors, including the P-stalk of the ribosome, the HEAT repeat protein GCN1, and the ABC transporter-like protein GCN20 (Garcia-Barrio et al., 2000; Inglis et al., 2019). The Arabidopsis homologs of GCN1 (ILITHYIA/ILA) and GCN20 are likewise required for GCN2-dependent eIF2α phosphorylation (Wang et al., 2017; Faus et al., 2018; Izquierdo et al., 2018). This suggests that certain elements of the GCN2 signaling architecture are conserved in plants.

While translation is repressed globally when levels of active eIF2 are low, specific mRNAs such as GCN4 in yeast and ATF4 in mammals are translationally induced by virtue of a specific pattern of uORFs in their 5’ leader region (Wek, 2018). Attempts to identify GCN2-resistant targets of translational control led to the Arabidopsis transcription factor TBF1/HsfB1, which functions in the response to pathogens (Pajerowska-Mukhtar et al., 2012; Liu et al., 2019); coincidentally, its CPuORF confers translational repression in response to galactinol, a precursor of the trisaccharide raffinose (Zhu et al., 2018b).

A series of observations is consistent with the notion that the plant GCN2-eIF2α module is also a sensor of amino acid depletion. Although there is no direct in planta evidence that GCN2 is activated by uncharged tRNA, GCN2 is activated by herbicides that inhibit amino acid synthesis. GCN2 phosphorylates eIF2α on the canonical, conserved serine residue (Ser56) (Zhang et al., 2008; Faus et al., 2015; Izquierdo et al., 2018; Zhao et al., 2018), and this event is sometimes accompanied by global translational repression (Lageix et al., 2008; Lokdarshi et al., 2020a). Genetic depletion of O-acetyl serine, the precursor for cysteine, depletes amino acid levels and triggers eIF2α-P (Dong et al., 2017). The signaling molecule β-aminobutyric acid (BABA) inhibits aspartyl-tRNA synthetase activity, which may well lead to accumulation of uncharged tRNAs; and the inhibition of plant growth caused by BABA is indeed GCN2-dependent (Luna et al., 2014). Moreover, overexpression of GCN2 kinase deregulates free amino acid levels in wheat (Byrne et al., 2012).

However, other evidence indicates a broader role for GCN2 in plant translational control beyond amino acid sensing. First, plant GCN2 is activated by several abiotic stresses, pathogens, and defense-related signaling molecules (Lageix et al., 2008; Sormani et al., 2011; Wang et al., 2017; Liu et al., 2019; Llabata et al., 2019; Lokdarshi et al., 2020a). Upon infection with Pseudomonas syringae, the GCN2-eIF2α module is involved in the regulation of genes encoding ABA receptors, ABA biosynthetic enzymes and ABA related transcription factors (Liu et al., 2019). These studies indicate specific adjustments to gene expression via the GCN2-eIF2α module. More recently, conditions that elevated reactive oxygen species (excess light, herbicides, cold and salt) rapidly triggered eIF2 phosphorylation by GCN2 in a manner dependent on light and photosynthetic electron transport (Lokdarshi et al., 2020a; Lokdarshi et al., 2020b). To date, the ROS hydrogen peroxide is the only signal shown to activate GCN2 in darkness. These findings implicate the GCN2-eIF2α module in a retrograde signaling event that allows the chloroplast to regulate translation in the cytosol.

In summary, in conjunction with TOR, the GCN2 kinase appears to mediate responses to numerous metabolic and environmental signals. Both kinases are part of a metabolic signaling network that aligns protein synthesis with nitrogen, sulfur, carbon, energy, and amino acid availability. The precise mechanisms by which these two kinases support plant translation appears to be quite different from animals and fungi and remains to be explored in more detail.

Conclusion

Mechanistic studies are revealing numerous mechanisms whereby environmental parameters can influence the general translation apparatus in plants. Of particular interest are recent discoveries of various accessory translation factors not known from other organisms. Although we know that different mRNAs respond in a gene specific manner to these parameters, the underlying mechanism is clear in only a few cases. The TOR and GCN2 kinases anchor two major signaling pathways that impact translation. How exactly these and other translational control pathways become sensitized to upstream signals remains an open question, as is the question of cell type specific translational control. It can be expected that protein synthesis be tightly regulated in response to the nitrogen and amino acid supply, but ‘whether’ and ‘how’ also remains to be better understood. Thus, despite accelerating progress over the past years, there is a bewildering number of open questions. It is tempting to resort to the better understood paradigms from yeast and animals, but experience has shown that these may apply to plants only in part or not at all.

Global transcriptome-wide studies continue to yield ever deeper insights into the factors that control translational efficiency, with ribosome footprinting experiments yielding particularly exciting data on ribosome positions on mRNAs. These experiments have focused on the RNA level. However, inferences of actual protein synthesis rates from ribosome loading data would only be reliable if ribosome elongation speed was invariant, which is unknown. The prospect of measuring protein synthesis rates directly remains tantalizing but technically challenging. Likewise, experimental and computational methods for integrating translation data with other omics data are most valuable for a more holistic understanding of the entire gene expression pipeline. Translational efficiency of mRNAs is an evolving trait. How DNA sequence variation within populations and between species contributes to translational control may help to explain agricultural productivity and plant evolution. Finally, although much remains to be understood about the fundamentals of translation in plants, translational control holds great promise for synthetic biology applications when the goal is to fine tune gene expression.

Acknowledgments

We thank Anwesha Dasgupta for discussion during the conceptualization of the article. We apologize to authors whose articles relating to translational control were not included due to space constraints and our focus on more recent publications.

Funding Information

This work was supported by grants from the National Science Foundation (IOS-1456988 and MCB 1546402) and the National Institutes of Health (NIH R15 GM129672) to AGvA.

Glossary of Key Concepts

CITE: Cap-independent translational enhancers are RNA-sequence elements that enhance translation initiation by the 40S ribosome independent of the 5’ cap. CITEs are common in RNA viruses and typically reside within the 3’UTR. They fold into characteristic hairpin structures, which attract some or all of the canonical translation initiation factors that are part of the cap binding or 43S preinitiation complexes. 3’CITEs often basepair with RNA elements in the 5’ leader, forming a kissing loop.
Closed loop model: Because the poly(A) binding proteins bound to the poly(A) tail of an mRNA have the capacity to interact with subunits of the cap binding complex, foremost eIF4G or eIFiso4G, the 3’ end of the mRNA may come to be juxtaposed to its 5’ end.
Codon usage bias: The phenomenon that the 2–6 synonymous codons coding for a given amino acid are not found at the proportions expected by random chance alone. The degree of codon usage bias can be measured as a property of an entire genome, an amino acid, an individual gene, a portion of a gene, or a reading frame.
CPuORF: A conserved-peptide upstream open reading frame is an uORF whose encoded peptide is evolutionarily conserved. Where known, CPuORF peptides often function by stalling the elongating ribosome.
Eudicot: The clade of the flowering plants characterized by having a pair of embryonic leaves. Eudicots include most crop species. The sister clade, the monocotyledonous plants (monocots), includes grasses, cereal crops, lilies, orchids, palms and various other families.
G-quadruplex: A secondary structure formed by four triplets of guanines (GGG) in RNA or DNA. The guanines form three stacked rectangles of 4 guanines each, that are stabilized by Hogsteen-type hydrogen bonding and base stacking.
GCN2: Named General Control Nonderepressible 2 in budding yeast, this protein kinase phosphorylates the initiation factor eIF2α in response to environmental and metabolic cues, typically causing global translational repression. The name stems from the observation that the yeast gcn2 mutant is unable to induce a set of genes responsible for amino acid uptake and synthesis.
IRES: An internal ribosome entry site is an RNA sequence element located in the 5’ untranslated region of an RNA that can attract a 40S ribosome to initiate translation with minimal scanning and independent of the 5’ cap of the mRNA.
Kissing loop: A hairpin loop in an RNA that basepairs with another hairpin loop.
5’ leader: The section of mRNA from the 5’ end to the AUG of the main coding sequence (CDS). Typically called the 5’ untranslated region (5’ UTR), this section often contains upstream open reading frames that are translated. Therefore we sometimes substitute the term 5’ leader for 5’ UTR.
Main ORF: The main protein coding sequence of an mRNA that is conventionally annotated as the coding sequence (CDS) is referred to as the main ORF to distinguish it from upstream ORFs in the 5’ leader or downstream ORFs in the 3’UTR.
NMD: Nonsense-mediated decay is an mRNA quality control process that degrades mRNAs with unusual characteristics such as long 3’ UTRs, spliced introns downstream of a stop codon and premature stop codons.
Nuclear Cap Binding Protein: consists of CBP20 and CBP80 subunits. It is thought to function during the first ‘pioneer’ round of translation and thus affects RNA quality control events such as NMD and cotranslational decay. CBP20/80 also functions in alternative splicing and miRNA biogenesis in the nucleus. CBP20 is distinct from the ‘novel cap binding protein’ (nCBP) better known as 4EHP.
P-body: Short for processing body, a cytosolic RNP granule containing mRNAs and, typically, decapping enzymes, Argonautes, NMD components, and ribonucleases. P-bodies often serve to turn over mRNAs as a form of RNA quality control.
Polycistronic RNA: An mRNAs that possesses multiple, independently translated coding regions. The most common cases are mRNAs with uORFs and viral RNAs with multiple coding sequences.
Polysome profiling: A biochemical technique first adopted in the 1960s that separates different ribonucleoprotein complexes by centrifugation across a density gradient, usually made with sucrose. Distinguish from ‘ribosome profiling’.
Recycling: After translation termination, the process in which the small and large ribosomal subunits are split apart from each other and detached from the mRNA.
Reinitiation: After translation termination, the process in which a small ribosomal subunit remains attached to the mRNA, migrates towards the 3’ end, and proceeds to initiate translation on a second protein coding region of the same mRNA.
Ribosome loading: The extent to which an mRNA is loaded with ribosomes. Ribosome loading can be expressed as the fraction of a gene’s mRNA molecules that are associated with ribosomes, or as the average number of ribosomes per mRNA or other measures. Ribosome loading can be measured using polysome profiling or ribosome footprinting.
Ribosome footprinting: Also known as Ribo-Seq and ribosome profiling, a biochemical technique in which polysomes are isolated, the exposed sections of the mRNA are digested with ribonuclease, and the remaining ribosome-protected mRNA fragments (footprints) are analyzed, usually by deep sequencing.
RIP: A ribosome inactivating protein is an enzyme, typically a glycosidase, that depurinates the sarcin/ricin loop of the 25S rRNA, a motif important for binding of elongation factors to the ribosome.
RISC: The RNA-induced silencing complex contains at the minimum an Argonaute protein and a small guide RNA. Plant RISC complexes typically cleave their target mRNA, but some small RNA-mRNA pairs are translationally repressed.
RNP granule: Ribonucleoproteins (RNPs) can assemble reversibly in defined cytosolic regions by a process that has been compared to liquid phase separation. Stress granules and P-bodies are common types of RNP granules.
SnRK: The plant homolog of Snf1-related protein kinase. SnRK1 is structurally and functionally related to AMP-activated kinases, is activated under energy starvation conditions, but is known to not bind AMP directly. SnRK2 is structurally related to SnRK1 and functions in the abscisic acid signaling pathway.
Stress granule: A cytosolic RNP granule containing mRNAs, certain translation factors, and RNA chaperones. Stress granules sequester intact mRNAs away from the 80S ribosome. Stress granules are transient structures. Thus, localization of an mRNA to stress granules is often reversible.
TOR: Target of rapamycin kinase is the plant ortholog of mammalian mTOR. Plant TOR kinase forms a complex akin to TORC1 with the partner proteins RAPTOR and LST8. A TOR complex equivalent to TORC2 has not been detected in plants.
Translation efficiency: The efficiency with which an mRNA is translated is a measure of the protein synthesis rate from the mRNA. Translation efficiency is measured by normalizing ribosome loading data (from ribosome footprinting, polysome profiles, or TRAP-Seq) by the mRNA transcript level from the same sample.
Translational regulon: A group of mRNAs whose translation efficiency (ribosome loading) is affected in a concerted manner by experimental perturbation.
Translatome: The sum of all ribosome-associated mRNAs in a biological sample, as opposed to the transcriptome, which comprises all transcribed RNAs.
TRAP-Seq: For tagged ribosome affinity purification and RNA sequencing the ribosome is tagged with a genetically encoded affinity handle, such as the FLAG epitope, and expressed in a tissue-specific manner as directed by a given promoter. Tagged ribosomes are isolated from a cell extract and the attached mRNAs are identified by deep sequencing.
uORF: An upstream open reading frame is a coding region, usually short, that initiates with a start codon in the otherwise untranslated 5’ leader sequence of an mRNA, upstream of the main coding sequence (CDS or mainORF) of the mRNA. uORFs typically inhibit translation of the main ORF. An uORF may or may not overlap the main ORF.

Footnotes

Conflict of Interest Statement

The authors have no conflicts of interest to declare.

Contributor Information

Ricardo A. Urquidi-Camacho, UT-ORNL Graduate School of Genome Science and Technology, The University of Tennessee, Knoxville, TN 37996.

Ansul Lokdarshi, Department of Biochemistry & Cellular and Molecular Biology, University of Tennessee, Knoxville, TN 37996.

Albrecht G von Arnim, Department of Biochemistry & Cellular and Molecular Biology and UT-ORNL Graduate School of Genome Science and Technology, University of Tennessee, Knoxville, TN 37996.

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PERMALINK

Translational Gene Regulation in Plants: A Green New Deal

Ricardo A Urquidi-Camacho

Ansul Lokdarshi

Albrecht G von Arnim

Abstract

Graphical Abstract

1. INTRODUCTION

2. GLOBAL REGULATION OF TRANSLATION THREE WAYS

2.1. Metabolic Control of Bulk Protein Synthesis

2.2. Control of the Translatome by Environmental Perturbation

Figure 1. General overview of cytosolic mRNA translation.

Figure 2: Regulation of translatomes in pollen development and seed germination.

2.3. Translational Control through mRNP Granules

3. THE PLANT TRANSLATION APPARATUS

3.1. The Ribosome

3.2. The Translation Factors

3.2.1. Initiation

3.2.2. Translation Initiation Factors as Agents of Antiviral Resistance

Figure 3. Noncanonical mechanisms of translational enhancement in plant viruses.

3.2.3. Elongation, Termination and Recycling

3.2.4. Translation Reinitiation

Figure 4. uORFs can control translation in response to metabolites.

3.3. RNA Quality Control and Turnover in Plant Translation

Figure 5. The expression of termination factor eRF1 is regulated by negative feedback.

3.4. Translational control by accessory translation factors

Figure 6. Translational control by proteins associated with the eIF4 cap-binding complex.

Table 1.

Figure 7. Effects of SnRK signaling on translation.

4. RNA FEATURES

4.1. Covalent Modification of mRNAs

4.2. Secondary Structure

4.3. Small RNAs

4.4. tRNAs

4.5. Upstream Open Reading Frames

5. EMERGENT SIGNAL-RESPONSE PATHWAYS IN TRANSLATION

5.1. Translational control of bZIP transcription factor mRNAs by the sucrose-dependent peptoswitch

5.2. TOR kinase signaling

Figure 8: Overview of the cytosolic translation regulatory network anchored on three major protein kinases, TOR, SnRKs and GCN2.

5.3. The GCN2 kinase

Conclusion

Acknowledgments

Funding Information

Glossary of Key Concepts

Footnotes

Contributor Information

References

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