bioRxiv Science⌕ Search

Biology subjects

Jaubert, S.

Publications and source records attributed to Jaubert, S..

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↗

A knowledge graph and topological data analysis framework to disentangle the tomato-multi pathogens complex gene regulatory network

Global population is rapidly increasing, representing a major challenge for food supply, exacerbated by climate change and environmental degradation. Despite the pivotal role of agriculture, plant health and survival are threatened by various biotic stressors. Although how plants respond to each of these individual stresses is well studied, little is known about how they respond to a combination of many of these bio-aggressors occurring together. To tackle this question, first, we built TomTom, a knowledge graph gathering molecular interactions from nine publicly available databases, including transcription factors- or microRNAs-targets, protein-protein interactions, and functional terms. Then, we selected transcriptomics data of tomato subjected to six distinct pathogens and performed an integrative analysis. We found 5561 candidate genes involved in the multi-stress response of tomato. To study how the response is orchestrated, we mapped those genes in TomTom and extracted a comprehensive gene regulatory network (GRN) composed of 71 transcription factors (TF) and 1786 target genes. By estimating the TF activity, we identified 43 TFs responding either specifically to one or multiple bio-aggressors. GRN analyses with a topological data analysis approach allowed to identify 18 clusters of TFs with similar properties, yielding four main configurations localized in specific regions of the GRN. Finally, we found one NAC and four ERF hubs which cooperatively coordinate the tomato response to multiple pathogens. Our findings allowed to study the complex molecular reprogramming in tomato upon interaction with different biotic agents, providing tools scalable to other questions involving tomato molecular interactions and beyond.

systems 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↗

Copper microRNAs govern the formation of giant feeding cells induced by the root knot nematode Meloidogyne incognita in Arabidopsis thaliana

miR408 and miR398 are two conserved microRNAs which expression is activated by the SPL7 transcription factor in response to copper starvation. We identified these two microRNAs families as upregulated in Arabidopsis thaliana and Solanum lycopersicum roots infected by root-knot nematodes. These endoparasites induce the dedifferentiation of a few root cells and the reprogramming of their gene expression to generate giant feeding cells. By combining functional approaches, we deciphered the signaling cascade involving these microRNAs, their regulator and their targets. MIR408 expression was located within nematode-induced feeding cells in which it co-localised with SPL7 expression and was regulated by copper. Moreover, infection assays with mir408 and spl7 KO mutants or lines expressing targets rendered resistant to cleavage by miR398 demonstrated the essential role of the SPL7/MIR408/MIR398 module in the formation of giant feeding cells. Our findings reveals how perturbation of plant copper homeostasis, via the SPL7/MIR408/MIR398 module, governs the formation of nematode-induced feeding cells.

plant biology↗