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Favery, B.

Publications and source records attributed to Favery, B..

7 recordsLinked to original sources

The root knot nematode effector MiEFF186 interacts with a splicing factor to reshape plant transcriptome

The root-knot nematode Meloidogyne incognita secretes specific effectors to manipulate root cells and induce their redifferentiation into multinucleate feeding giant cells, which are essential for its development. A dedicated screen identified the M. incognita MiEFF186a effector as a regulator of alternative splicing, a crucial mechanism of transcriptional gene regulation whereby a single gene can produce multiple mature mRNA variants, in plants. EFF186 is expressed in the esophageal glands of nematode juveniles, and in planta, it localizes to the nucleus and accumulates in the nucleolus. A yeast two-hybrid approach identified the nucleolar G-patch protein GDP1/CIS2 as a MiEFF186a target in tomato and Arabidopsis. Transcriptomic analyses of Arabidopsis roots ectopically expressing MiEFF186a or impaired in GDP1/CIS2 function revealed changes in both gene expression and alternative splicing, with partially overlapping responses. Finally, alteration of GDP1/CIS2 expression by virus-induced gene silencing in Solanaceae or in Arabidopsis gdp1 mutants affects susceptibility to M. incognita. Together, these results identify GDP1/CIS2 as a host target of MiEFF186a and support a role for these proteins in the modulation of host RNA metabolism during nematode parasitism.

plant biology↗

A conserved root-knot nematode effector targets plant kinesin light chain related proteins to promote parasitism

Root-knot nematodes (RKNs) are obligate plant parasites that establish biotrophic interactions with a wide range of host plants, causing major crop losses worldwide. During infection, RKNs secrete effector proteins from their esophageal glands into root tissues via a stylet. These effectors target specific subcellular compartments and manipulate host cell functions to induce the formation of hypertrophied and multinucleated giant cells, which serve as feeding sites essential for nematode development. Here we describe a new RKN-specific effector, EFFECTOR17 (EFF17), conserved in the five most damaging RKN species: Meloidogyne incognita, M. enterolobii, M. arenaria, M. javanica, and M. hapla. In situ hybridization showed that EFF17 genes are specifically expressed in the esophageal glands of various RKN species. Silencing EFF17 in M. incognita reduced its reproduction on Nicotiana benthamiana, demonstrating a key role in parasitism. Yeast two-hybrid and split luciferase assays revealed that tomato and Arabidopsis KINESIN LIGHT CHAIN RELATED (KLCR)/CELLULOSE-MICROUBULE UNCOUPLING (CMU) proteins are host targets of MiEFF17. Arabidopsis klcr mutants developed significantly fewer galls and egg masses. Our findings propose that EFF17 manipulates KLCR function to promote parasitism.

plant biology↗

Plant-parasitic nematode microRNAs hijack plant AGO1 to induce host-cell reprogramming

Cross-kingdom RNA interference (ckRNAi) is emerging as a mode of inter-organismal gene regulation, yet mechanistic examples in plant-metazoan interactions remain limited. Here, we demonstrate miRNA-driven ckRNAi in the nematode-plant pathosystem. Root-knot nematodes are among the most destructive plant pathogens, reprogramming root tissues to develop into galls containing multinucleated, hypermetabolic giant feeding cells essential for parasitism. AGO1-associated small-RNA immunoprecipitation (AGO1-RIP) from tomato galls revealed the selective in planta loading of 10 M. incognita miRNAs into host AGO1. Integrating degradome profiling, target prediction, and dual-luciferase reporter assays, we validated miRNA-directed silencing of nine tomato transcripts by four secreted nematode miRNAs. These targets map to major pathway classes involved in immune signaling, metabolic regulation, and cellular reprogramming linked to feeding-site establishment. Functional analyses further show that the nematode-secreted miR-2b is enhances giant feeding cell development. Comparative AGO1-RIP in Arabidopsis thaliana identified a conserved subset of AGO1-loaded nematode miRNAs, including miR-2b and miR-100, consistent with shared small-RNA effectors across hosts. Finally, the overlap between AGO1-loaded miRNA families and helminth secreted small-RNA repertoires supports evolutionary convergence on RNA-based virulence strategies. Collectively, our findings establish miRNA-mediated ckRNAi as a mechanistic component of plant-root-knot nematode interactions and provide a framework for leveraging RNA-based vulnerabilities for nematode control.

plant biology↗

Transcriptional responses of Solanum lycopersicum to three distinct parasites reveal host hubs and networks underlying parasitic successes

Crops face attacks from a wide range of pathogens and pests that deploy various parasitic strategies. All aggressors must manipulate major plant functions, such as immune signaling, hormone pathways, metabolism, and development, to successfully establish themselves and complete their life cycle. Here, we compared the tomato plant's response to three evolutionary distant pathogens (nematodes, aphids and oomycetes) during compatible interactions using a transcriptomic approach. We identified differentially expressed genes and biological processes, and highlighted potential key host hubs associated with successful parasitism. By integrating recent published datasets, we refined our understanding of the global and tissue-specific mechanisms targeted during compatible interactions and, through co-expression analysis, identified clusters showing shared dysregulation patterns enriched in specific GO terms. Finally, model-to-crop translational analysis using the Arabidopsis interactome network, repositioned tomato candidates within larger interaction networks and emphasized the key positions occupied by some of them. Identifying these pivotal tomato targets is crucial to decipher processes underlying parasitism and, consequently, offers new opportunities to develop sustainable multi-pathogen control strategies.

plant biology↗

miR167-ARF8, an auxin-responsive module involved in the formation of root-knot nematode-induced galls in tomato

O_LIRoot-knot nematodes (RKN) from genus Meloidogyne induce the dedifferentiation of root vascular cells into giant multinucleate feeding cells. These feeding cells result from an extensive reprogramming of gene expression in targeted root cells, as shown by transcriptomic analyses of galls or giant cells from various plant species. C_LIO_LISmall non-coding RNAs, and messenger RNAs from tomato (Solanum lycopersicum) galls and uninfected roots were sequenced. De novo microRNA prediction in the tomato genome identified microRNAs expressed in galls and uninfected roots. Statistical analyses identified 174 miRNA genes differentially expressed in galls at 7 and/or 14 days post infection (dpi). C_LIO_LIIntegrative analyses combining small non-coding RNA and transcriptome datasets with the specific sequencing of cleaved transcripts identified miRNA targets in tomato galls. Functional analyses of promoter-GUS fusions and CRISPR-Cas9 mutants highlighted the role of the miR167-regulated transcription factor AUXIN RESPONSE FACTOR 8 (ARF8) in giant cell formation. C_LI

plant biology↗

Chromatin landscape dynamics in development of the plant parasitic nematode Meloidogyne incognita

In model organisms, epigenome dynamics underlies a plethora of biological processes. The role of epigenetic modifications in development and parasitism in nematode pests remains unknown. The root-knot nematode Meloidogyne incognita adapts rapidly to unfavorable conditions, despite its asexual reproduction. However, the mechanisms underlying this remarkable plasticity and their potential impact on gene expression remain unknown. This study provides the first insight into contribution of epigenetic mechanisms to this plasticity, by studying histone modifications in M. incognita. The distribution of five histone modifications revealed the existence of strong epigenetic signatures, similar to those found in the model nematode Caenorhabditis elegans. We investigated their impact on chromatin structure and their distribution relative to transposable elements (TE) loci. We assessed the influence of the chromatin landscape on gene expression at two developmental stages: eggs, and pre-parasitic juveniles. H3K4me3 histone modification was strongly correlated with high levels of expression for protein-coding genes implicated in stage-specific processes during M. incognita development. We provided new insights in the dynamic regulation of parasitism genes kept under histone modifications silencing. In this pioneering study, we establish a comprehensive framework for the importance of epigenetic mechanisms in the regulation of the genome expression and its stability in plant-parasitic nematodes. Author summaryThe nematode Meloidogyne incognita is one of the most destructive plant parasites worldwide. Its ability to infect a wide range of hosts and its high adaptability contribute to its parasitic success. We investigated the role of epigenetic mechanisms -- specifically post-translational histone modifications -- in the parasitic life cycle. We showed these modifications are linked to gene expression regulation and likely contribute to nematode development and pathogenicity.

genomics↗

Silencing SmD1 in Solanaceae alters susceptibility to root-knot nematodes

Root-knot nematodes (RKNs) are among the most damaging pests of agricultural crops. Indeed, Meloidogyne is an extremely polyphagous genus of nematodes that can infect thousands of plant species. A few genes for resistance (R-genes) to RKNs suitable for use in crop breeding have been identified, and new virulent strains and species of nematode emerge rendering these R-genes ineffective. Effective parasitism is dependent on the secretion, by the RKN, of effectors targeting plant functions, which mediate the reprogramming of root cells into specialised feeding cells. These cells, the giant cells, are essential for RKN development and reproduction. The EFFECTOR 18 protein (EFF18) from M. incognita interacts with the spliceosomal protein SmD1 in Arabidopsis, disrupting its function in alternative splicing regulation and modulating the giant cell transcriptome. We show here that EFF18 is a conserved RKN-specific effector. We also show here that EFF18 effectors also target SmD1 in Nicotiana benthamiana and Solanum lycopersicum. The alteration of SmD1 expression by virus-induced gene silencing (VIGS) in Solanaceae affects giant cell formation and nematode development. Thus, SmD1 is a susceptibility gene and a promising target for the development of broad resistance, especially in Solanaceae, for the control of Meloidogyne spp.

plant biology↗