Plant‐parasitic nematode secreted peptides hijack a plant secretory pathway

Frey, Nicolas Frei dit; Favery, Bruno

doi:10.1111/nph.16842

Cited by 9 publications

(4 citation statements)

References 16 publications

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“…Robust identification of the comprehensive effector repertoire of a given plant pathogen is foundational to understanding its pathology, and hence, can inform the development of resistance to crop diseases (Lovelace et al 2023). Plant pathogen effectors are also important as a means for investigating fundamental host processes, and as promising targets for biotechnological application (Bedell et al 2012;Frei Dit Frey and Favery 2021). Taken together, results from this work provide an overview of cyst nematode parasitism which can form the basis of further functional studies of the effectorome, and demonstrate the utility of gland-cell transcriptomics as a method for effector discovery.…”

Section: Introductionmentioning

confidence: 75%

The origin, deployment, and evolution of a plant-parasitic nematode effectorome

Molloy,

Shin,

Long

et al. 2024

Preprint

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Plant-parasitic nematodes constrain global food security. During parasitism, they secrete effectors into the host plant from two types of pharyngeal gland cells. These effectors elicit profound changes in host biology to suppress immunity and establish a unique feeding organ from which the nematode draws nutrition. Despite the importance of effectors in nematode parasitism, there has been no comprehensive identification and characterisation of the effector repertoire of any plant-parasitic nematode.To address this, we advance techniques for gland cell isolation and transcriptional analysis to define a stringent annotation of putative effectors for the cyst nematodeHeterodera schachtiiat three key life-stages. We define 659 effector gene loci: 293 “known” high-confidence homologs of plant-parasitic nematode effectors, and 366 “novel” effectors with high gland cell expression. In doing so we define a comprehensive “effectorome” of a plant-parasitic nematode.Using this effector definition, we provide the first systems-level understanding of the origin, deployment and evolution of a plant-parasitic nematode effectorome. The robust identification of the comprehensive effector repertoire of a plant-parasitic nematode will underpin our understanding of nematode pathology, and hence, inform strategies for crop protection.

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Section: Introductionmentioning

confidence: 75%

The origin, deployment, and evolution of a plant-parasitic nematode effectorome

Molloy,

Shin,

Long

et al. 2024

Preprint

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“…In this scenario, the common ancestral receptors could have recognised a PAMP, with the peptide sequence of this PAMP possibly converted to serve as a phytocytokine to regulate plant developmental processes. Multiple phytocytokines, such as PSK, PSY, SCOOPs, and CLE peptides, are present in plant pathogens and pests [71][72][73][74][75] . Whether the perception of phytocytokines evolved from the perception of PAMPs, or pathogens developed phytocytokine-mimics to repress immune responses remains an open question.…”

Section: Discussionmentioning

confidence: 99%

Evolutionary trajectory of pattern recognition receptors in plants

Ngou,

Wyler,

Schmid

et al. 2024

Nat Commun

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Cell-surface receptors play pivotal roles in many biological processes, including immunity, development, and reproduction, across diverse organisms. How cell-surface receptors evolve to become specialised in different biological processes remains elusive. To shed light on the immune-specificity of cell-surface receptors, we analyzed more than 200,000 genes encoding cell-surface receptors from 350 genomes and traced the evolutionary origin of immune-specific leucine-rich repeat receptor-like proteins (LRR-RLPs) in plants. Surprisingly, we discovered that the motifs crucial for co-receptor interaction in LRR-RLPs are closely related to those of the LRR-receptor-like kinase (RLK) subgroup Xb, which perceives phytohormones and primarily governs growth and development. Functional characterisation further reveals that LRR-RLPs initiate immune responses through their juxtamembrane and transmembrane regions, while LRR-RLK-Xb members regulate development through their cytosolic kinase domains. Our data suggest that the cell-surface receptors involved in immunity and development share a common origin. After diversification, their ectodomains, juxtamembrane, transmembrane, and cytosolic regions have either diversified or stabilised to recognise diverse ligands and activate differential downstream responses. Our work reveals a mechanism by which plants evolve to perceive diverse signals to activate the appropriate responses in a rapidly changing environment.

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“…For example, genetic analysis in legumes has revealed a central role for CLE in the shoot-root circuit that regulates the number of nitrogen-fixing nodules able to be induced by rhizobacteria [36,37]. Furthermore, plant parasitic nematodes are also known to encode CLE-like peptides [38] and have impacts on parasitism such that Lotus japonicas carrying hyper-nodulating alleles of har-1, which is an ortholog of the canonical Arabidopsis CLE receptor clv1, exhibits a significantly higher infection with nematodes (Lohar and Bird, 2003) compared to wild-type plants. Beyond legumes, natural sequence polymorphisms at an orthologous locus in tomato correlate with RKN host range [39].…”

Section: Discussionmentioning

confidence: 99%

Root-Knot-Nematode-Encoded CEPs Increase Nitrogen Assimilation

Mishra,

Hu,

DiGennaro

2023

Life

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C-terminally encoded peptides (CEPs) are plant developmental signals that regulate growth and adaptive responses to nitrogen stress conditions. These small signal peptides are common to all vascular plants, and intriguingly have been characterized in some plant parasitic nematodes. Here, we sought to discover the breadth of root-knot nematode (RKN)-encoded CEP-like peptides and define the potential roles of these signals in the plant–nematode interaction, focusing on peptide activity altering plant root phenotypes and nitrogen uptake and assimilation. A comprehensive bioinformatic screen identified 61 CEP-like sequences encoded within the genomes of six root-knot nematode (RKN; Meloidogyne spp.) species. Exogenous application of an RKN CEP-like peptide altered A. thaliana and M. truncatula root phenotypes including reduced lateral root number in M. truncatula and inhibited primary root length in A. thaliana. To define the role of RKN CEP-like peptides, we applied exogenous RKN CEP and demonstrated increases in plant nitrogen uptake through the upregulation of nitrate transporter gene expression in roots and increased 15N/14N in nematode-formed root galls. Further, we also identified enhanced nematode metabolic processes following CEP application. These results support a model of parasite-induced changes in host metabolism and inform endogenous pathways to regulate plant nitrogen assimilation.

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Plant‐parasitic nematode secreted peptides hijack a plant secretory pathway

Abstract: This article is a Commentary on Wang et al. (2021), 229: 563–574.

Cited by 9 publications

References 16 publications

The origin, deployment, and evolution of a plant-parasitic nematode effectorome

The origin, deployment, and evolution of a plant-parasitic nematode effectorome

Evolutionary trajectory of pattern recognition receptors in plants

Root-Knot-Nematode-Encoded CEPs Increase Nitrogen Assimilation

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