Focus Issue Editorial: Biotic Stress

Devastating diseases caused by pathogens and pests have threatened crop production, human health, and the stability of global economies. Extensive efforts to more fully understand the mechanisms of plant immune responses and pathogen virulence have yielded new insights that may aid in maintaining or enhancing yields and nutritional quality, as plant pathogen ranges fluctuate in response to climate change and consumer preferences also evolve. Progress in our understanding has been both rapid and significant, warranting this “Focus Issue on Biotic Stress,” which includes four diverse Update Reviews on recent advances in the field, 12 primary Research Articles covering various research areas on plant host interactions with pathogens and pests, and one Breakthrough Technologies.

Regulation of phytohormone biosynthesis and signaling is a key component of plant–biotic stress interactions. Defense suppression and developmental reprogramming via alterations to phytohormone biosynthesis and signaling pathways are critical mechanisms used by pests and pathogens to thrive and cause disease. In their Update, Gheysen and Mitchum (2019) describe how plant-parasitic cyst and root-knot nematodes alter defense and developmental programs by manipulating plant hormone pathways to establish specialized feeding sites within host roots. The authors also highlight how these nematodes have evolved to secrete a variety of plant peptide hormones that mimic endogenous plant-growth–regulating peptides and hijack developmental programs to establish effective feeding sites. At invasion sites, plants attempt to defend themselves by reinforcing the cell wall against insect and pathogen attack, producing defensive compounds such as callose. In maize (Zea mays), benzoxazinoids are known to enhance callose deposition and promote resistance to phloem feeding sap-sucking aphids. In this issue, Varsani et al. (2019) demonstrate that maize inbred line Mp708 utilizes a newly elucidated defense mechanism via 12-oxo-phytodienoic acid, independent of the jasmonic acid pathway, as a key regulator of enhanced callose deposition to limit colonization by corn leaf aphid (Rhopalosiphum maidis). Using the Arabidopsis (Arabidopsis thaliana)–two-spotted spider mite (Tetranychus urticae) plant herbivore model system, Santamaría et al. (2019) identified a role for the Toll-interleukin receptor–lectin domain protein Phloem Protein2 (PP2)-A5 in resistance against two-spotted spider mites. PP2-A5–overexpressing plants showed enhanced resistance to mite herbivory, whereas loss-of-function mutants exhibited much more extensive leaf damage. Metabolite profiling revealed that altered hormonal signaling, rather than changes in indole glucosinolates, underpin PP2-A5–mediated resistance to provide new insight into the plant–spider mite interaction. Ali et al. (2019) describe the identification and characterization of a RING-type E3 ubiquitin ligase, JASMONATE-ASSOCIATED VQ-MOTIF GENE1 (JAV1)-ASSOCIATED UBIQUITIN LIGASE1 (JUL1), which ubiquitinates JASMONATE-ASSOCIATED VQ-MOTIF GENE1 (JAV1/VQ22), a repressor of jasmonate-mediated defense responses. The JAV1/JUL1 functional module was discovered to act as a specific coordinator of plant defense responses against the generalist herbivore Spodoptera litura.

Nutrient acquisition from host cells is a key necessity for plant-attacking pests and microbial intruders. Whereas insects and nematodes can use physical devices, such as stylets, to gain access to nutrient-rich plant phloem sap or to establish specialized feeding sites, the challenging barrier afforded by plant cell walls is harder to address for microbes. In the case of biotrophic and hemibiotrophic pathogens, dedicated structures such as haustoria or infection hyphae facilitate the establishment of an interface to plant host cells. In their Update, Judelson and Ah-Fong (2019) describe how mutual exchange of biomolecules at the oomycete-plant interface impact disease outcomes. The authors not only elaborate on the task of the interface as a trading place for nutrients, but also highlight its role as a battleground enabling plant defense and microbial counterdefense. Carbohydrates are key nutrients absorbed by pathogenic microbes and required to maintain infection. In an elegant study using a fluorescence resonance energy transfer-based biosensor to trace Glc distribution in fungal cells, Sosso et al. (2019) studied carbohydrate partitioning in the interaction between maize and its biotrophic fungal pathogen, Ustilago maydis, causing smut disease. The authors discovered comprehensive alterations in carbohydrate allocation during infection, which happens alongside changes in expression levels of maize genes encoding sugar transporters of the SWEET family. Additionally, they found a steep Glc gradient in fungal hyphae, with highest Glc levels in the hyphal tips. Whereas sugar transporters thus seem essential for carbohydrate delivery to microbial intruders, they rather surprisingly can also play a role in conferring disease resistance. The wheat (Triticum aestivum) Lr67 gene encodes a high-affinity Glc-proton symporter that transports Glc from the apoplastic space to the cytosol. A particular mutation in the gene, resulting in a single amino acid substitution within a transmembrane domain, leads to dominantly inherited resistance to multiple fungal pathogens (rusts and powdery mildew). Milne et al. (2019) have now demonstrated that the orthologous barley transporter, HvSTP13, has similar transport characteristics to wheat Lr67. The authors further revealed that the multipathogen resistance phenotype could be recapitulated in barley (Hordeum vulgare) by transgenic expression of the resistance-conferring allele of wheat Lr67, demonstrating conservation of the underlying resistance mechanism between grasses.

Communication between plants and microbes is essential during pathogen infection. Rybak and Robatzek (2019) provided an excellent overview in their “Update” on the important roles of extracellular vesicles in secretion and exchange of protein, RNA, lipid, and metabolites in interacting hosts and microbes. Both microbial- and plant-derived extracellular vesicles, their contents and functions in pathogenesis and plant immune responses, were discussed. Soluble n-ethylmaleimide-sensitive factor attachment protein receptor proteins are key components of vesicle trafficking in plants and eukaryotic pathogens. Cao et al. (2019) identified a rice Qa-Soluble n-ethylmaleimide-sensitive factor attachment protein receptor protein, syntaxin121, which accumulates at fungal penetration sites and contributes to rice resistance against Magnaporthe oryzae infection. This study reinforces the importance of vesicle trafficking for host resistance against fungal pathogens. Han et al. (2019) characterized an extracellular chitinase, MoChi1 from the rice blast fungus M. oryzae, which suppresses chitin-induced reactive oxygen species responses. They identified an interacting protein of MoChi1 from rice, a jacalin-related Mannose-Binding Lectin (OsMBL1). OsMBL1 is induced by M. oryzae infection and positively regulates rice immune responses. Isolation of apoplast extracts is a critical step for secretion and vesicle trafficking studies, which is especially challenging in monocots. Gentzel et al. (2019) developed a simple method to collect apoplast contents in maize, and established an easy protocol to measure apoplast hydration. They demonstrate applicability of the procedure by the efficient recovery of a bacterial maize pathogen (Pantoea stewartii ssp stewartii) residing in the apoplastic space.

Cytoplasmic sensor proteins composed of an amino-terminal coiled-coil or Toll-interleukin receptor domain, a central nucleotide-binding domain, and carboxyl-terminal Leucine-rich repeats represent the canonical versions of plant NLR-type resistance proteins. These typically confer isolate-specific resistance against a given pathogen by direct or indirect perception of a pathogen effector protein or directly act on a host target protein(s). This type of immunity is usually referred to as effector-triggered immunity (ETI). A recently emerged variation of this canonical scheme is the integration of other protein domains (integrated domains, IDs) into plant NLR proteins. These IDs are presumed to mimic authentic host targets of pathogen effectors to serve as decoys to attract effector proteins and trigger a boosted immune response. In an Update article, Grund et al. (2019) provide a nice overview about the current state-of-the-art regarding NLRs with IDs. The authors describe their distribution, illustrate experimentally validated examples, and discuss potential mechanisms for effector recognition by NLRs with IDs. During ETI, oxidants generate a largely unexplored shift in intracellular redox potential. In their Breakthrough Technology article, McConnell et al. (2019) report a novel method, comprising an enrichment procedure coupled to mass spectrometry-based quantification, to study the plant redoxome (i.e. proteome-wide oxidative modifications of proteins caused by oxidants) during ETI. The authors demonstrate the usefulness of the new technology by comparing the redoxome of wild-type and oligopeptidase mutant plants defective in ETI. Dracatos et al. (2019) also took advantage of a comparatively new method, “MutChromSeq,” to clone a leaf rust resistance gene (Rph1) in a grass species (barley) with a large and highly complex genome. The procedure rests on sequencing of flow-sorted chromosomes from multiple individual mutants and comparative analysis to identify candidate genes. By this approach, the authors recognized a single candidate gene for Rph1, which encodes an NLR protein and represents the first leaf rust resistance gene cloned from cultivated barley. Notably, Rph1 is closely related to the Arabidopsis antibacterial resistance gene RPM1.

MAPK cascades are important signaling components in plant immunity. Li et al. (2019) identified a group D MAPK gene from rice (Oryza sativa), OsMAPK20-5, which negatively regulates ethylene and nitric oxide pathways. Silencing of OsMAPK20-5 confers broad resistance to the two most destructive pests of rice, adult brown planthopper (Nilaparvata lugens) and white-backed planthopper (Sogatella furcifera).

Epigenetic regulation has been recently recognized as an important molecular mechanism for gene regulation during plant–pathogen interactions. Chromatin modification was implicated in regulating the production of volatile organic compounds (VOCs) and secondary metabolites in filamentous fungi. Estrada-Rivera et al. (2019) have elucidated the function of a histone deacetylase HDA-2 in chromatin modification of Trichoderma atroviride, a beneficial fungus that promotes plant growth. HAD-2 regulates not only the levels of VOCs, but also the profiles of the VOCs, impacting plant growth. Nuclear lamina is a key structure that provides docking sites for chromatin, critical for gene regulation and maintaining proper nuclear function and morphology. Choi et al. (2019) identified a family of candidate nuclear lamina proteins in Arabidopsis, Crowded Nuclei (CRWN), which impact plant development and defense responses. Loss-of-function of CRWN proteins induces salicylic acid biosynthesis, expression of immune-responsive genes, spontaneous defense responses, and cell death. CRWN genes are essential, because knocking out all four family members is lethal.

These Updates and Research Articles elucidate how interactions between plants and pathogens/pests lead to beneficial or detrimental outcomes. We look forward to future advancements based on our understanding of plant biotic stress responses aimed at developing innovative and eco-friendly control strategies for plant protection.