Focus on epigenetics

Epigenetics delves into the intricate changes and regulations of biological traits without altering DNA sequences. It is pivotal to various aspects related to plant development and responses to the environment. Consequently, knowledge of the plant epigenetic regulation network, encompassing both upstream signals and downstream targets, is imperative for crop improvements, thereby ensuring food security amidst shifting climates. With this objective in mind, the Plant Physiology Editorial Team has curated this Focus Issue on plant epigenetics, containing a compilation of research articles alongside timely reviews. The topics cover diverse types of plant epigenetic modifications, including DNA methylation; histone modifications; noncoding RNAs; and chromatin accessibility, primarily focusing on their role in regulating crop agronomic traits.

Advancements in high-throughput sequencing technologies have greatly enhanced the resolution and scale of DNA methylation profiling. In 1 Update of this Focus Issue, Liu and Zhong (2024) discussed the features and performances of the most recent DNA methylation sequencing technologies. The authors also summarized the current knowledge concerning DNA methylation plasticity, as well as its role in mediating plant–environment interactions.

While a wealth of knowledge on DNA methylation has been obtained from studies using the model plant Arabidopsis, the effects caused by defective DNA methylation in crop species are still largely unknown. In this issue, Xu et al. (2023) discovered through a rice genetic screen that mutations in components of the rice RNA-directed DNA Methylation (RdDM) pathway led to an impaired transgene silencing, pleiotropic developmental defects, and increased disease resistance. Furthermore, Meijer et al. (2023) discovered a role for RdDM in intergenerational acquired resistance (IAR) in progeny from rice plants infected by the parasitic nematode Meloidogyne graminicola. Knock-down mutants in the 24-nt siRNA biogenesis gene DCL3a were affected in IAR, which was associated with a defect in IAR-related changes in the inducibility of jasmonic acid/ethylene-controlled defense genes.

Another commonly observed developmental defect in crop RdDM mutants is reduced seed production. This effect prompted Dew-Budd et al. (2023) to explore whether RdDM is critical in mediating subgenome dominance in polyploid crops. Alternatively, RdDM may play a vital role in proper endosperm development by balancing maternal-to-paternal genome dosage. These hypotheses were tested in 3 Brassicaceae species using mutants crippled in RdDM components. While seed set reduction was observed in RdDM mutants of all 3 species, the obligate outcrosser Capsella grandiflora exhibited the most pronounced defects, suggesting mating type-dependent effects of RdDM in seed production.

DNA methylation not only functions in silencing transposons and maintaining genome integrity but also regulates plant metabolic traits. Danshen (Salvia miltiorrhiza), a valuable Chinese herbal medicine, synthesizes bioactive compounds, such as tanshinones and phenolic acids, in its roots. He et al. (2023) observed dynamic expression changes of key metabolic genes during Danshen root development, which are accompanied by alterations in DNA methylation. Cao et al. (2023) discovered in peaches that the transcription factor, PpNAC1, and DNA demethylase1 (PpDML1) form a positive feedback loop to regulate ethylene synthesis during peach fruit ripening synergistically. This result is consistent with previous studies in tomato (Gao et al. 2022), and they together indicate a conserved regulatory circuit involving DNA methylation in climacteric fruit ripening.

Both DNA methylation and N6-methyladenosine (m⁶A) in mRNA are nucleic acid-based epigenetic modifications, invoking questions regarding the genetic and functional interplay between them. The tomato RNA demethylase, SlALKBH2, has previously been shown to bind the transcripts of the DNA demethylase, SlDML2, modulating SlDML2 transcript stability and fruit ripening (Zhou et al. 2019). In this Focus Issue, Luo et al. (2023) identified a novel crosstalk mode between these 2 epigenetic processes by showing that the maize mRNA adenosine methylase (ZmMTA) physically interacts with Decrease in DNA methylation 1 (ZmDDM1), and that m⁶A modification facilitates the recruitment of ZmDDM1 to its target genomic loci. This interplay is critical for maize embryogenesis and endosperm development.

Noncoding RNAs, including both small RNAs and long noncoding RNAs (lncRNAs), represent another layer of epigenetic regulation governing essential crop traits. In this Focus Issue, Lian et al. (2023) investigated the microRNA-target pair, OsmiR397 and OsLACCASE-15, in modulating flowering traits in rice. Converging evidence points to the role of peroxisome-localized OsLACCASE-15 in regulating photorespiration. Yeqing et al. (2023) discovered that the rose lncRNA, lncWD83, physically interacts with PLANT U-BOX PROTEIN 11 (RcPUB11), a U-box-containing E3 ubiquitin ligase, promoting RcPUB11-mediated proteasomal degradation of the floral repressor MYC2 LIKE (RcMYC2L). As RcMYC2L directly targets the RcFT promoter and negatively regulates RcFT gene expression, knocking down the expression of either lncWD83 or RcPUB11 delays rose flowering.

In addition to the regulation of flowering traits, lncRNAs also mediate plant responses to diverse environmental cues, as summarized by Traubenik et al. (2024) in this Focus Issue. Their discussion raises intriguing questions about how short-term responses of lncRNAs are channeled through epigenetic modifications to equip plants with long-term memory in coping with recurring stress conditions, even across generations. Successfully unraveling the underlying epigenetic mechanisms will enable us to better harness lncRNAs as tools to breed crops that can adeptly adapt to changing environments.

Histone acetylation constitutes a major class of epigenetic modifications typically associated with transcriptionally active genes. Histone deacetylases (HDACs) remove acetyl groups from histone tails, promoting tighter DNA wrapping and subsequent repression of associated genes. To investigate the role of HISTONE DEACETYLASE 19 (HDA19) in gynecium organ formation, Manrique et al. (2023) employed cell-type-specific labeling with fluorescence-activated cell sorting. They demonstrated that downregulation of SHOOT MERISTEMLESS (STM) by HDA19 in the carpel margin meristem is crucial for meristem cell differentiation and gynecium organogenesis. Additionally, exploring how enzymatic activities of HDAC themselves are regulated raises another intriguing question. Liu et al. (2023) discovered that phosphorylation at serine 193 of HISTONE DEACETYLASE 9 (HDA9) is essential for its function. The importance and conservation of phosphorylation at the serine residue were also confirmed using amino acid-substituted human HDAC3.

This Focus Issue also includes a study of SET DOMAIN GROUP 711 (OsSDG711), the rice Enhancer of zeste [E(z)] component of the PRC2 complex (Lu et al. 2023). The authors discovered that OsSDG711 directly modulates the expression of cytokinin oxidase/dehydrogenases (OsCKXs) through H3K27me3 deposition, affecting organ size in rice. Histone modifications play a pivotal role in regulating plant development in response to both internal and external cues. In a timely Update, Cheng et al. (2023) summarized how histone modifiers are recruited to specific genomic loci and how their activities are adjusted in response to diverse developmental and environmental stimuli, including plant age, hormones, temperature, light, and nutrients. In a related review, Chen et al. (2023) summarized the historical studies illuminating the mechanistic links between histone acetylation and gene expression, and discussed about the complex causal relationship between them. This article also focuses on the role of histone acetylation in plant seed development, and its application in plant breeding was also discussed.

Among environmental factors, temperature changes, both short-term fluctuations and seasonal dynamics, have a profound impact on plant development. Therefore, plants have to deploy elegant epigenetic circuits to memorize the cold and heat exposure to ensure optimal survival. Using the Arabidopsis FLOWERING LOCUS C (FLC) as an example, Gao and He (2023) discussed how histone modifications switch from active to repressive states during vernalization and how they are reset during embryo development. Nishio et al. (2023) discussed epigenetic mechanisms associated with plant responses to distinct types of heat stress, including priming and reoccurring heat stresses, both systemically and in local tissues.

Similar to temperature, light is also a key environmental factor in determining plant traits, especially for crops that are sensitive to photoperiod, such as soybean. Through the characterization of differentially accessible chromatin regions between light and dark treatments, Huang et al. (2023) identified soybean light-responsive enhancers. Such strategies could be applied to other crop species to identify enhancer motifs responsive to various environmental stimuli. For a comprehensive overview of plant chromatin accessibility, including its regulatory role and interaction with various types of epigenetic modifications, we recommend the Update by Candela-Ferre et al. (2024). This Update can also serve as a framework to guide students and educators in learning about the categorization and key features of various epigenetic modifications.

Fossdal et al. (2024) reviewed the role epigenetic mechanisms in long-term stress adaptation of gymnosperms. Although some epigenetic mechanisms are profoundly different in gymnosperms compared to model angiosperms, there are many striking examples of long-lasting stress memory in gymnosperms that increase the phenotypic plasticity and climatic adaptation of these long-living species. For instance, epigenetic memory of photoperiod and temperature during embryogenesis and seed development of Norway spruce influences bud phenology and frost tolerance in the progeny, which can persist for over 20 yr. The review by Fossdal et al. (2024) highlights various additional examples of memory in gymnosperms to both biotic and abiotic stresses and reviews the emerging evidence for regulation at the levels of DNA methylation, noncoding RNA, and histone modifications/variants.

Collectively, studies presented in this Focus Issue further strengthen the viewpoint that epigenetic modifications play a key role in regulating diverse plant biological processes, which underscores their significance in crop improvements under climate change. In addition, we hope that this Focus Issue brings you a clear view of the significant goals and challenges we are striving to achieve and overcome. As epigenetic regulators typically have genome-wide targets and pleiotropic effects, understanding how the regulatory complex assembles and how target specificity is determined in response to diverse internal and external stimuli is crucial for developing tools and strategies for efficient and precise epigenetic engineering to aid crop improvements. Moreover, it is increasingly recognized that tissue and cell heterogeneity pose a major obstacle to the precise dissection of the regulatory mechanisms of epigenetic modifications. Therefore, advancements in technologies that can effectively resolve epigenetic modifications at single-cell resolution are highly desirable and will undoubtedly elevate our understanding of epigenetic regulation to the next level.

Data availability

No new data were generated or analysed in support of this research.

Dive Curated Terms

The following phenotypic, genotypic, and functional terms are of significance to the work described in this paper:

• HDA9 Gramene: AT3G44680

• HDA9 Araport: AT3G44680

• HDA19 Gramene: AT4G38130

• HDA19 Araport: AT4G38130

• FLC Gramene: AT5G10140

• FLC Araport: AT5G10140

• HDAC3 Gramene: O15379

• HDAC3 Araport: O15379