In plants, perception of invading pathogens involves cell-surface immune receptor kinases. Here, we report that the Arabidopsis SITE-1 PROTEASE (S1P) cleaves endogenous RAPID ALKALINIZATION FACTOR (RALF) propeptides to inhibit plant immunity. This inhibition is mediated by the malectin-like receptor kinase FERONIA (FER), which otherwise facilitates the ligand-induced complex formation of the immune receptor kinases EF-TU RECEPTOR (EFR) and FLAGELLIN-SENSING 2 (FLS2) with their co-receptor BRASSINOSTEROID INSENSITIVE 1–ASSOCIATED KINASE 1 (BAK1) to initiate immune signaling. We show that FER acts as a RALF-regulated scaffold that modulates receptor kinase complex assembly. A similar scaffolding mechanism may underlie FER function in other signaling pathways.

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The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling

Receptor-like kinases (RLKs) and Receptor-like proteins (RLPs) play crucial roles in plant immunity, growth, and development. Plants deploy a large number of RLKs and RLPs as pattern recognition receptors (PRRs) that detect microbe- and host-derived molecular patterns as the first layer of inducible defense. Recent advances have uncovered novel PRRs, their corresponding ligands, and mechanisms underlying PRR activation and signaling. In general, PRRs associate with other RLKs and function as part of multiprotein immune complexes at the cell surface. Innovative strategies have emerged for the rapid identification of microbial patterns and their cognate PRRs. Successful pathogens can evade or block host recognition by secreting effector proteins to “hide” microbial patterns or inhibit PRR-mediated signaling. Furthermore, newly identified pathogen effectors have been shown to manipulate RLKs controlling growth and development by mimicking peptide hormones of host plants. The ongoing studies illustrate the importance of diverse plant RLKs in plant disease resistance and microbial pathogenesis.

Receptor Kinases in Plant-Pathogen Interactions: More Than Pattern Recognition.

Plants have evolved a repertoire of monitoring systems to sense plant morphogenesis and to face environmental changes and threats caused by different attackers. These systems integrate different signals into overreaching triggering pathways which coordinate developmental and defence-associated responses. The plant cell wall, a dynamic and complex structure surrounding every plant cell, has emerged recently as an essential component of plant monitoring systems, thus expanding its function as a passive defensive barrier. Plants have a dedicated mechanism for maintaining cell wall integrity (CWI) which comprises a diverse set of plasma membrane-resident sensors and pattern recognition receptors (PRRs). The PRRs perceive plant-derived ligands, such as peptides or wall glycans, known as damage-associated molecular patterns (DAMPs). These DAMPs function as 'danger' alert signals activating DAMP-triggered immunity (DTI), which shares signalling components and responses with the immune pathways triggered by non-self microbe-associated molecular patterns that mediate disease resistance. Alteration of CWI by impairment of the expression or activity of proteins involved in cell wall biosynthesis and/or remodelling, as occurs in some plant cell wall mutants, or by wall damage due to colonization by pathogens/pests, activates specific defensive and growth responses. Our current understanding of how these alterations of CWI are perceived by the wall monitoring systems is scarce and few plant sensors/PRRs and DAMPs have been characterized. The identification of these CWI sensors and PRR-DAMP pairs will help us to understand the immune functions of the wall monitoring system, and might allow the breeding of crop varieties and the design of agricultural strategies that would enhance crop disease resistance.

https://onlinelibrary.wiley.com/doi/pdf/10.1111/tpj.13807

Plant cell wall-mediated immunity: cell wall changes trigger disease resistance responses

Plants solely rely on innate immunity of each individual cell to deal with a diversity of microbes in the environment. Extracellular recognition of microbe- and host damage-associated molecular patterns leads to the first layer of inducible defenses, termed pattern-triggered immunity (PTI). In plants, pattern recognition receptors (PRRs) described to date are all membrane-associated receptor-like kinases or receptor-like proteins, reflecting the prevalence of apoplastic colonization of plant-infecting microbes. An increasing inventory of elicitor-active patterns and PRRs indicates that a large number of them are limited to a certain range of plant groups/species, pointing to dynamic and convergent evolution of pattern recognition specificities. In addition to common molecular principles of PRR signaling, recent studies have revealed substantial diversification between PRRs in their functions and regulatory mechanisms. This serves to confer robustness and plasticity to the whole PTI system in natural infections, wherein different PRRs are simultaneously engaged and faced with microbial assaults. We review the functional significance and molecular basis of PRR-mediated pathogen recognition and disease resistance, and also an emerging role for PRRs in homeostatic association with beneficial or commensal microbes.

https://onlinelibrary.wiley.com/doi/pdf/10.1111/tpj.13808

Pattern recognition receptors and signaling in plant-microbe interactions.

Plants actively perceive and respond to perturbations in their cell walls which arise during growth, biotic and abiotic stresses However, few components involved in plant cell wall integrity sensing have been described to date Using a reverse-genetic approach, we identified the Arabidopsis thaliana leucine-rich repeat receptor kinase MIK2 as an important regulator of cell wall damage responses triggered upon cellulose biosynthesis inhibition Indeed, loss-of-function mik2 alleles are strongly affected in immune marker gene expression, jasmonic acid production and lignin deposition MIK2 has both overlapping and distinct functions with THE1, a malectin-like receptor kinase previously proposed as cell wall integrity sensor In addition, mik2 mutant plants exhibit enhanced leftward root skewing when grown on vertical plates Notably, natural variation in MIK2 (also named LRR-KISS) has been correlated recently to mild salt stress tolerance, which we could confirm using our insertional alleles Strikingly, both the increased root skewing and salt stress sensitivity phenotypes observed in the mik2 mutant are dependent on THE1 Finally, we found that MIK2 is required for resistance to the fungal root pathogen Fusarium oxysporum Together, our data identify MIK2 as a novel component in cell wall integrity sensing and suggest that MIK2 is a nexus linking cell wall integrity sensing to growth and environmental cues

/pdf/the-arabidopsis-leucine-rich-repeat-receptor-kinase-mik2-lrr-42gbxsaqkj.pdf

The Arabidopsis leucine-rich repeat receptor kinase MIK2/LRR-KISS connects cell wall integrity sensing, root growth and response to abiotic and biotic stresses.

Plant infections caused by fungi are often associated with an increase in the pH of the surrounding host tissue1. Extracellular alkalinization is thought to contribute to fungal pathogenesis, but the underlying mechanisms are poorly understood. Here, we show that the root-infecting fungus Fusarium oxysporum uses a functional homologue of the plant regulatory peptide RALF (rapid alkalinization factor)2,3 to induce alkalinization and cause disease in plants. An upshift in extracellular pH promotes infectious growth of Fusarium by stimulating phosphorylation of a conserved mitogen-activated protein kinase essential for pathogenicity4,5. Fungal mutants lacking a functional Fusarium (F)-RALF peptide failed to induce host alkalinization and showed markedly reduced virulence in tomato plants, while eliciting a strong host immune response. Arabidopsis plants lacking the receptor-like kinase FERONIA, which mediates the RALF-triggered alkalinization response6, displayed enhanced resistance against Fusarium. RALF homologues are found across a number of phylogenetically distant groups of fungi, many of which infect plants. We propose that fungal pathogens use functional homologues of alkalinizing peptides found in their host plants to increase their infectious potential and suppress host immunity. The fungal pathogen Fusarium oxysporum is shown to use a functional homologue of the plant regulatory peptide RALF (rapid alkalinization factor) to induce alkalinization and cause disease in plants.

A fungal pathogen secretes plant alkalinizing peptides to increase infection.

Nature Microbiology 1, 16043 (2016); published 11 April 2016; corrected 9 May 2016. Following discussions regarding the details of the early experiments carried out for this Letter, it became clear that an additional author, Manuel S. Lopez-Berges, should have been included. All versions of the Letter have now been updated to rectify this omission.

/pdf/corrigendum-a-fungal-pathogen-secretes-plant-alkalinizing-4b6e9m1inn.pdf

Mercedes Leon-Ruiz

Papers

A fungal pathogen secretes plant alkalinizing peptides to increase infection.

Corrigendum: A fungal pathogen secretes plant alkalinizing peptides to increase infection