Publications by authors named "Pierre Abad"

69 Publications

A Meloidogyne incognita C-type lectin effector targets plant catalases to promote parasitism.

New Phytol 2021 Aug 27. Epub 2021 Aug 27.

Institute of Vegetables and Flowers, Chinese Academy of Agricultural Science, Beijing, 100081, China.

Root-knot nematodes (RKNs), Meloidogyne spp., secrete effectors to modulate plant immune responses and establish a parasitic relationship with host plants. However, the functions and plant targets of C-type lectin-like effectors of M. incognita remain unknown. Here, we characterised a CTL-like effector of M. incognita, MiCTL1a, and identified its target and role in nematode parasitism. In situ hybridisation demonstrated the expression of MiCTL1 in the subventral glands, and in planta, immunolocalisation showed its secretion during M. incognita parasitism. Virus-induced gene silencing of the MiCTL1 reduced the infection ability of M. incognita in Nicotiana benthamiana. The ectopic expression in Arabidopsis not only increased susceptibility to M. incognita but also promoted root growth. Yeast two-hybrid and co-immunoprecipitation assays revealed that MiCTL1a interacts with Arabidopsis catalases, which play essential roles in H O homeostasis. Knockout or overexpression of catalases showed either increased or reduced susceptibility to M. incognita, respectively. Moreover, MiCTL1a not only reduced catalase activity in vitro and in planta but also modulated stress-related gene expressions in Arabidopsis. Our data suggest that MiCTL1a interacts with plant catalases and interferes with catalase activity, allowing M. incognita to establish a parasitic relationship with its host by fine-tuning ROS-mediated responses.
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http://dx.doi.org/10.1111/nph.17690DOI Listing
August 2021

The Nuclear Effector MiEFF1 Interacts With Cytosolic Glyceraldehyde-3-Phosphate Dehydrogenases to Promote Parasitism.

Front Plant Sci 2021 9;12:641480. Epub 2021 Apr 9.

Institut Sophia Agrobiotech, INRAE, CNRS, Université Côte d'Azur, Sophia Antipolis, France.

Root-knot nematodes are obligate endoparasites that maintain a biotrophic relationship with their hosts over a period of several weeks. They induce the differentiation of root cells into specialized multinucleate hypertrophied feeding cells known as giant cells. Nematode effectors synthesized in the esophageal glands and injected into the plant tissue through the syringe-like stylet play a key role in giant cell ontogenesis. The MiEFF1 is one of the rare effectors of phytopathogenic nematodes to have been located in feeding cells. This effector specifically targets the giant cell nuclei. We investigated the functions modulated by this effector, by using a yeast two-hybrid approach to identify its host targets. We characterized a universal stress protein (USP) and cytosolic glyceraldehyde-3-phosphate dehydrogenases (GAPCs) as the targets of MiEFF1. We validated the interaction of MiEFF1 with these host targets in the plant cell nucleus, by bimolecular fluorescence complementation (BiFC). A functional analysis with GUS reporter lines and knockout mutant lines showed that GAPCs were induced in giant cells and that their non-metabolic functions were required for root-knot nematode infection. These susceptibility factors are potentially interesting targets for the development of new root-knot nematode control strategies.
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http://dx.doi.org/10.3389/fpls.2021.641480DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8062903PMC
April 2021

Toward genetic modification of plant-parasitic nematodes: delivery of macromolecules to adults and expression of exogenous mRNA in second stage juveniles.

G3 (Bethesda) 2021 02;11(2)

Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, UK.

Plant-parasitic nematodes are a continuing threat to food security, causing an estimated 100 billion USD in crop losses each year. The most problematic are the obligate sedentary endoparasites (primarily root knot nematodes and cyst nematodes). Progress in understanding their biology is held back by a lack of tools for functional genetics: forward genetics is largely restricted to studies of natural variation in populations and reverse genetics is entirely reliant on RNA interference. There is an expectation that the development of functional genetic tools would accelerate the progress of research on plant-parasitic nematodes, and hence the development of novel control solutions. Here, we develop some of the foundational biology required to deliver a functional genetic tool kit in plant-parasitic nematodes. We characterize the gonads of male Heterodera schachtii and Meloidogyne hapla in the context of spermatogenesis. We test and optimize various methods for the delivery, expression, and/or detection of exogenous nucleic acids in plant-parasitic nematodes. We demonstrate that delivery of macromolecules to cyst and root knot nematode male germlines is difficult, but possible. Similarly, we demonstrate the delivery of oligonucleotides to root knot nematode gametes. Finally, we develop a transient expression system in plant-parasitic nematodes by demonstrating the delivery and expression of exogenous mRNA encoding various reporter genes throughout the body of H. schachtii juveniles using lipofectamine-based transfection. We anticipate these developments to be independently useful, will expedite the development of genetic modification tools for plant-parasitic nematodes, and ultimately catalyze research on a group of nematodes that threaten global food security.
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http://dx.doi.org/10.1093/g3journal/jkaa058DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8022973PMC
February 2021

The root-knot nematode effector MiEFF18 interacts with the plant core spliceosomal protein SmD1 required for giant cell formation.

New Phytol 2021 03 9;229(6):3408-3423. Epub 2020 Dec 9.

INRAE, Université Côte d'Azur, CNRS, ISA, Sophia Antipolis, F-06903, France.

The root-knot nematode Meloidogyne incognita secretes specific effectors (MiEFF) and induces the redifferentiation of plant root cells into enlarged multinucleate feeding 'giant cells' essential for nematode development. Immunolocalizations revealed the presence of the MiEFF18 protein in the salivary glands of M. incognita juveniles. In planta, MiEFF18 localizes to the nuclei of giant cells demonstrating its secretion during plant-nematode interactions. A yeast two-hybrid approach identified the nuclear ribonucleoprotein SmD1 as a MiEFF18 partner in tomato and Arabidopsis. SmD1 is an essential component of the spliceosome, a complex involved in pre-mRNA splicing and alternative splicing. RNA-seq analyses of Arabidopsis roots ectopically expressing MiEFF18 or partially impaired in SmD1 function (smd1b mutant) revealed the contribution of the effector and its target to alternative splicing and proteome diversity. The comparison with Arabidopsis galls data showed that MiEFF18 modifies the expression of genes important for giant cell ontogenesis, indicating that MiEFF18 modulates SmD1 functions to facilitate giant cell formation. Finally, Arabidopsis smd1b mutants exhibited less susceptibility to M. incognita infection, and the giant cells formed on these mutants displayed developmental defects, suggesting that SmD1 plays an important role in the formation of giant cells and is required for successful nematode infection.
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http://dx.doi.org/10.1111/nph.17089DOI Listing
March 2021

Gall-Inducing Parasites: Convergent and Conserved Strategies of Plant Manipulation by Insects and Nematodes.

Annu Rev Phytopathol 2020 08;58:1-22

INRAE, CNRS, Université Côte d'Azur, ISA, F-06600 Sophia-Antipolis, France; email:

Gall-inducing insects and nematodes engage in sophisticated interactions with their host plants. These parasites can induce major morphological and physiological changes in host roots, leaves, and other tissues. Sedentary endoparasitic nematodes, root-knot and cyst nematodes in particular, as well as gall-inducing and leaf-mining insects, manipulate plant development to form unique organs that provide them with food from feeding cells. Sometimes, infected tissues may undergo a developmental switch resulting in the formation of aberrant and spectacular structures (clubs or galls). We describe here the complex interactions between these plant-reprogramming sedentary endoparasites and their infected hosts, focusing on similarities between strategies of plant manipulation. We highlight progress in our understanding of the host plant response to infection and focus on the nematode and insect molecules secreted in planta. We suggest thatlooking at similarities may identify convergent and conserved strategies and shed light on the promise they hold for the development of new management strategies in agriculture and forestry.
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http://dx.doi.org/10.1146/annurev-phyto-010820-012722DOI Listing
August 2020

The root-knot nematode effector MiPDI1 targets a stress-associated protein (SAP) to establish disease in Solanaceae and Arabidopsis.

New Phytol 2020 11 18;228(4):1417-1430. Epub 2020 Jul 18.

Department of Plant Pathology and Key Laboratory of Pest Monitoring and Green Management of the Ministry of Agriculture, China Agricultural University, Beijing, 100193, China.

Large amounts of effectors are secreted by the oesophageal glands of plant-parasitic nematodes, but their molecular mode of action remains largely unknown. We characterized a Meloidogyne incognita protein disulphide isomerase (PDI)-like effector protein (MiPDI1) that facilitates nematode parasitism. In situ hybridization showed that MiPDI1 was expressed specifically in the subventral glands of M. incognita. It was significantly upregulated during parasitic stages. Immunolocalization demonstrated MiPDI1 secretion in planta during nematode migration and within the feeding cells. Host-induced silencing of the MiPDI1 gene affected the ability of the nematode to infect the host, whereas MiPDI1 expression in Arabidopsis increased susceptibility to M. incognita, providing evidence for a key role of MiPDI1 in M. incognita parasitism. Yeast two-hybrid, bimolecular fluorescence complementation and coimmunoprecipitation assays showed that MiPDI1 interacted with a tomato stress-associated protein (SlSAP12) orthologous to the redox-regulated AtSAP12, which plays an important role in plant responses to abiotic and biotic stresses. SAP12 silencing or knocking out in Nicotiana benthamiana and Arabidopsis increased susceptibility to M. incognita. Our results suggest that MiPDI1 acts as a pathogenicity factor promoting disease by fine-tuning SAP-mediated responses at the interface of redox signalling, defence and stress acclimation in Solanaceae and Arabidopsis.
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http://dx.doi.org/10.1111/nph.16745DOI Listing
November 2020

Plant Proteins and Processes Targeted by Parasitic Nematode Effectors.

Front Plant Sci 2019 30;10:970. Epub 2019 Jul 30.

Centre National de la Recherche Scientifique, Institut National de la Recherche Agronomique, Institut Sophia Agrobiotech, Université Côte d'Azur, Sophia Antipolis, France.

Sedentary endoparasitic nematodes, such as root-knot nematodes (RKN; spp.) and cyst nematodes (CN; spp. and spp.) cause considerable damage to agricultural crops. RKN and CN spend most of their life cycle in plant roots, in which they induce the formation of multinucleate hypertrophied feeding cells, called "giant cells" and "syncytia," respectively. The giant cells result from nuclear divisions of vascular cells without cytokinesis. They are surrounded by small dividing cells and they form a new organ within the root known as a root knot or gall. CN infection leads to the fusion of several root cells into a unique syncytium. These dramatically modified host cells act as metabolic sinks from which the nematode withdraws nutrients throughout its life, and they are thus essential for nematode development. Both RKN and CN secrete effector proteins that are synthesized in the oesophageal glands and delivered to the appropriate cell in the host plant via a syringe-like stylet, triggering the ontogenesis of the feeding structures. Within the plant cell or in the apoplast, effectors associate with specific host proteins, enabling them to hijack important processes for cell morphogenesis and physiology or immunity. Here, we review recent findings on the identification and functional characterization of plant targets of RKN and CN effectors. A better understanding of the molecular determinants of these biotrophic relationships would enable us to improve the yields of crops infected with parasitic nematodes and to expand our comprehension of root development.
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http://dx.doi.org/10.3389/fpls.2019.00970DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6682612PMC
July 2019

A MIF-like effector suppresses plant immunity and facilitates nematode parasitism by interacting with plant annexins.

J Exp Bot 2019 10;70(20):5943-5958

Department of Plant Pathology and Key Laboratory of Pest Monitoring and Green Management of the Ministry of Agriculture, China Agricultural University, Beijing, China.

Plant-parasitic nematodes secrete numerous effectors to facilitate parasitism, but detailed functions of nematode effectors and their plant targets remain largely unknown. Here, we characterized four macrophage migration inhibitory factors (MIFs) in Meloidogyne incognita resembling the MIFs secreted by human and animal parasites. Transcriptional data showed MiMIFs are up-regulated in parasitism. Immunolocalization provided evidence that MiMIF proteins are secreted from the nematode hypodermis to the parasite surface, detected in plant tissues and giant cells. In planta MiMIFs RNA interference in Arabidopsis decreased infection and nematode reproduction. Transient expression of MiMIF-2 could suppress Bax- and RBP1/Gpa2-induced cell death. MiMIF-2 ectopic expression led to higher levels of Arabidopsis susceptibility, suppressed immune responses triggered by flg22, and impaired [Ca2+]cyt influx induced by H2O2. The immunoprecipitation of MiMIF-2-interacting proteins, followed by co-immunoprecipitation and bimolecular fluorescence complementation validations, revealed specific interactions between MiMIF-2 and two Arabidopsis annexins, AnnAt1 and AnnAt4, involved in the transport of calcium ions, stress responses, and signal transduction. Suppression of expression or overexpression of these annexins modified nematode infection. Our results provide functional evidence that nematode effectors secreted from hypodermis to the parasite cuticle surface target host proteins and M. incognita uses MiMIFs to promote parasitism by interfering with the annexin-mediated plant immune responses.
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http://dx.doi.org/10.1093/jxb/erz348DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6812717PMC
October 2019

Gene copy number variations as signatures of adaptive evolution in the parthenogenetic, plant-parasitic nematode Meloidogyne incognita.

Mol Ecol 2019 05 29;28(10):2559-2572. Epub 2019 Apr 29.

INRA, Université Côte d'Azur, CNRS, ISA, Sophia Antipolis, France.

Adaptation to changing environmental conditions represents a challenge to parthenogenetic organisms, and until now, how phenotypic variants are generated in clones in response to the selection pressure of their environment remains poorly known. The obligatory parthenogenetic root-knot nematode species Meloidogyne incognita has a worldwide distribution and is the most devastating plant-parasitic nematode. Despite its asexual reproduction, this species exhibits an unexpected capacity of adaptation to environmental constraints, for example, resistant hosts. Here, we used a genomewide comparative hybridization strategy to evaluate variations in gene copy numbers between genotypes of M. incognita resulting from two parallel experimental evolution assays on a susceptible vs. resistant host plant. We detected gene copy number variations (CNVs) associated with the ability of the nematodes to overcome resistance of the host plant, and this genetic variation may reflect an adaptive response to host resistance in this parthenogenetic species. The CNV distribution throughout the nematode genome is not random and suggests the occurrence of genomic regions more prone to undergo duplications and losses in response to the selection pressure of the host resistance. Furthermore, our analysis revealed an outstanding level of gene loss events in nematode genotypes that have overcome the resistance. Overall, our results support the view that gene loss could be a common class of adaptive genetic mechanism in response to a challenging new biotic environment in clonal animals.
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http://dx.doi.org/10.1111/mec.15095DOI Listing
May 2019

Characterization of siRNAs clusters in Arabidopsis thaliana galls induced by the root-knot nematode Meloidogyne incognita.

BMC Genomics 2018 Dec 18;19(1):943. Epub 2018 Dec 18.

INRA, Université Côte d'Azur, CNRS, ISA, Paris, France.

Background: Root-knot nematodes (RKN), genus Meloidogyne, are plant parasitic worms that have the ability to transform root vascular cylinder cells into hypertrophied, multinucleate and metabolically over-active feeding cells. Redifferentiation into feeding cells is the result of a massive transcriptional reprogramming of root cells targeted by RKN. Since RKN are able to induce similar feeding cells in roots of thousands of plant species, these worms are thought to manipulate essential and conserved plant molecular pathways.

Results: Small non-coding RNAs of uninfected roots and infected root galls induced by M. incognita from Arabidopsis thaliana were sequenced by high throughput sequencing. SiRNA populations were analysed by using the Shortstack algorithm. We identified siRNA clusters that are differentially expressed in infected roots and evidenced an over-representation of the 23-24 nt siRNAs in infected tissue. This size corresponds to heterochromatic siRNAs (hc-siRNAs) which are known to regulate expression of transposons and genes at the transcriptional level, mainly by inducing DNA methylation.

Conclusions: Correlation of siRNA clusters expression profile with transcriptomic data identified several protein coding genes that are candidates to be regulated by siRNAs at the transcriptional level by RNA directed DNA methylation (RdDM) pathway either directly or indirectly via silencing of neighbouring transposable elements.
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http://dx.doi.org/10.1186/s12864-018-5296-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6297998PMC
December 2018

Genome-wide expert annotation of the epigenetic machinery of the plant-parasitic nematodes Meloidogyne spp., with a focus on the asexually reproducing species.

BMC Genomics 2018 May 3;19(1):321. Epub 2018 May 3.

Université Côte d'Azur, INRA, ISA, Sophia Antipolis, France.

Background: The renewed interest in epigenetics has led to the understanding that both the environment and individual lifestyle can directly interact with the epigenome to influence its dynamics. Epigenetic phenomena are mediated by DNA methylation, stable chromatin modifications and non-coding RNA-associated gene silencing involving specific proteins called epigenetic factors. Multiple organisms, ranging from plants to yeast and mammals, have been used as model systems to study epigenetics. The interactions between parasites and their hosts are models of choice to study these mechanisms because the selective pressures are strong and the evolution is fast. The asexually reproducing root-knot nematodes (RKN) offer different advantages to study the processes and mechanisms involved in epigenetic regulation. RKN genomes sequencing and annotation have identified numerous genes, however, which of those are involved in the adaption to an environment and potentially relevant to the evolution of plant-parasitism is yet to be discovered.

Results: Here, we used a functional comparative annotation strategy combining orthology data, mining of curated genomics as well as protein domain databases and phylogenetic reconstructions. Overall, we show that (i) neither RKN, nor the model nematode Caenorhabditis elegans possess any DNA methyltransferases (DNMT) (ii) RKN do not possess the complete machinery for DNA methylation on the 6th position of adenine (6mA) (iii) histone (de)acetylation and (de)methylation pathways are conserved between C. elegans and RKN, and the corresponding genes are amplified in asexually reproducing RKN (iv) some specific non-coding RNA families found in plant-parasitic nematodes are dissimilar from those in C. elegans. In the asexually reproducing RKN Meloidogyne incognita, expression data from various developmental stages supported the putative role of these proteins in epigenetic regulations.

Conclusions: Our results refine previous predictions on the epigenetic machinery of model species and constitute the most comprehensive description of epigenetic factors relevant to the plant-parasitic lifestyle and/or asexual mode of reproduction of RKN. Providing an atlas of epigenetic factors in RKN is an informative resource that will enable researchers to explore their potential role in adaptation of these parasites to their environment.
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http://dx.doi.org/10.1186/s12864-018-4686-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5934874PMC
May 2018

A root-knot nematode small glycine and cysteine-rich secreted effector, MiSGCR1, is involved in plant parasitism.

New Phytol 2018 01 16;217(2):687-699. Epub 2017 Oct 16.

INRA, Université Côte d'Azur, CNRS, ISA, 400 route des Chappes, 06903, Cedex Sophia-Antipolis, France.

Root-knot nematodes, Meloidogyne spp., are obligate endoparasites that maintain a biotrophic relationship with their hosts. They infect roots as microscopic vermiform second-stage juveniles, and establish specialized feeding structures called 'giant-cells', from which they withdraw water and nutrients. The nematode effector proteins secreted in planta are key elements in the molecular dialogue of parasitism. Here, we compared Illumina RNA-seq transcriptomes for M. incognita obtained at various points in the lifecycle, and identified 31 genes more strongly expressed in parasitic stages than in preparasitic juveniles. We then selected candidate effectors for functional characterization. Quantitative real-time PCR and in situ hybridizations showed that the validated differentially expressed genes are predominantly specifically expressed in oesophageal glands of the nematode. We also soaked the nematodes in siRNA to silence these genes and to determine their role in pathogenicity. The silencing of the dorsal gland specific-Minc18876 and its paralogues resulted in a significant, reproducible decrease in the number of mature females with egg masses, demonstrating a potentially important role for the small glycine- and cysteine-rich effector MiSGCR1 in early stages of plant-nematode interaction. Finally, we report that MiSGCR1 suppresses plant cell death induced by bacterial or oomycete triggers of plant defense.
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http://dx.doi.org/10.1111/nph.14837DOI Listing
January 2018

Characterization of microRNAs from Arabidopsis galls highlights a role for miR159 in the plant response to the root-knot nematode Meloidogyne incognita.

New Phytol 2017 Nov 14;216(3):882-896. Epub 2017 Sep 14.

INRA, Université Côte d'Azur, CNRS, ISA, 400 route des Chappes, BP167, 06903, Sophia Antipolis, France.

Root knot nematodes (RKN) are root parasites that induce the genetic reprogramming of vascular cells into giant feeding cells and the development of root galls. MicroRNAs (miRNAs) regulate gene expression during development and plant responses to various stresses. Disruption of post-transcriptional gene silencing in Arabidopsis ago1 or ago2 mutants decrease the infection rate of RKN suggesting a role for this mechanism in the plant-nematode interaction. By sequencing small RNAs from uninfected Arabidopsis roots and from galls 7 and 14 d post infection with Meloidogyne incognita, we identified 24 miRNAs differentially expressed in gall as putative regulators of gall development. Moreover, strong activity within galls was detected for five miRNA promoters. Analyses of nematode development in an Arabidopsis miR159abc mutant had a lower susceptibility to RKN, suggesting a role for the miR159 family in the plant response to M. incognita. Localization of mature miR159 within the giant and surrounding cells suggested a role in giant cell and gall. Finally, overexpression of miR159 in galls at 14 d post inoculation was associated with the repression of the miR159 target MYB33 which expression is restricted to the early stages of infection. Overall, these results implicate the miR159 in plant responses to RKN.
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http://dx.doi.org/10.1111/nph.14717DOI Listing
November 2017

Hybridization and polyploidy enable genomic plasticity without sex in the most devastating plant-parasitic nematodes.

PLoS Genet 2017 06 8;13(6):e1006777. Epub 2017 Jun 8.

INRA, Université Côte d'Azur, CNRS, ISA, France.

Root-knot nematodes (genus Meloidogyne) exhibit a diversity of reproductive modes ranging from obligatory sexual to fully asexual reproduction. Intriguingly, the most widespread and devastating species to global agriculture are those that reproduce asexually, without meiosis. To disentangle this surprising parasitic success despite the absence of sex and genetic exchanges, we have sequenced and assembled the genomes of three obligatory ameiotic and asexual Meloidogyne. We have compared them to those of relatives able to perform meiosis and sexual reproduction. We show that the genomes of ameiotic asexual Meloidogyne are large, polyploid and made of duplicated regions with a high within-species average nucleotide divergence of ~8%. Phylogenomic analysis of the genes present in these duplicated regions suggests that they originated from multiple hybridization events and are thus homoeologs. We found that up to 22% of homoeologous gene pairs were under positive selection and these genes covered a wide spectrum of predicted functional categories. To biologically assess functional divergence, we compared expression patterns of homoeologous gene pairs across developmental life stages using an RNAseq approach in the most economically important asexually-reproducing nematode. We showed that >60% of homoeologous gene pairs display diverged expression patterns. These results suggest a substantial functional impact of the genome structure. Contrasting with high within-species nuclear genome divergence, mitochondrial genome divergence between the three ameiotic asexuals was very low, signifying that these putative hybrids share a recent common maternal ancestor. Transposable elements (TE) cover a ~1.7 times higher proportion of the genomes of the ameiotic asexual Meloidogyne compared to the sexual relative and might also participate in their plasticity. The intriguing parasitic success of asexually-reproducing Meloidogyne species could be partly explained by their TE-rich composite genomes, resulting from allopolyploidization events, and promoting plasticity and functional divergence between gene copies in the absence of sex and meiosis.
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http://dx.doi.org/10.1371/journal.pgen.1006777DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5465968PMC
June 2017

Resistance to root-knot nematodes Meloidogyne spp. in woody plants.

New Phytol 2016 07 29;211(1):41-56. Epub 2016 Apr 29.

INRA, UMR 1355, Institut Sophia Agrobiotech, 06903, Sophia Antipolis, France.

I. 42 II. 43 III. 44 IV. 47 V. 49 VI. 50 VII. 50 VIII. 50 IX. 52 52 References 52 SUMMARY: Root-knot nematodes (RKNs) Meloidogyne spp. cause major damage to cultivated woody plants. Among them, Prunus, grapevine and coffee are the crops most infested by worldwide polyphagous species and species with a more limited distribution and/or narrower host range. The identification and characterization of natural sources of resistance are important steps to develop RKN control strategies. In woody crops, resistant rootstocks genetically different from the scion of agronomical interest may be engineered. We describe herein the interactions between RKNs and different woody crops, and highlight the plant species in which resistance and corresponding resistance (R) genes have been discovered. Even though grapevine and, to a lesser extent, coffee have a history of rootstock selection for RKN resistance, few cases of resistance have been documented. By contrast, in Prunus, R genes with different spectra have been mapped in plums, peach and almond and can be pyramided for durable resistance in interspecific rootstocks. We particularly discuss here the Ma Toll/interleukin-1 receptor-like-nucleotide binding-leucine-rich repeat gene from Myrobalan plum, one of the longest plant R genes cloned to date, due to its unique biological and structural properties. RKN R genes in Prunus will enable us to carry out molecular studies aimed at improving our knowledge of plant immunity in woody plants.
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http://dx.doi.org/10.1111/nph.13933DOI Listing
July 2016

The Arabidopsis microtubule-associated protein MAP65-3 supports infection by filamentous biotrophic pathogens by down-regulating salicylic acid-dependent defenses.

J Exp Bot 2016 Mar 21;67(6):1731-43. Epub 2016 Jan 21.

INRA, Université de Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France

The oomycete Hyaloperonospora arabidopsidis and the ascomycete Erysiphe cruciferarum are obligate biotrophic pathogens causing downy mildew and powdery mildew, respectively, on Arabidopsis. Upon infection, the filamentous pathogens induce the formation of intracellular bulbous structures called haustoria, which are required for the biotrophic lifestyle. We previously showed that the microtubule-associated protein AtMAP65-3 plays a critical role in organizing cytoskeleton microtubule arrays during mitosis and cytokinesis. This renders the protein essential for the development of giant cells, which are the feeding sites induced by root knot nematodes. Here, we show that AtMAP65-3 expression is also induced in leaves upon infection by the downy mildew oomycete and the powdery mildew fungus. Loss of AtMAP65-3 function in the map65-3 mutant dramatically reduced infection by both pathogens, predominantly at the stages of leaf penetration. Whole-transcriptome analysis showed an over-represented, constitutive activation of genes involved in salicylic acid (SA) biosynthesis, signaling, and defense execution in map65-3, whereas jasmonic acid (JA)-mediated signaling was down-regulated. Preventing SA synthesis and accumulation in map65-3 rescued plant susceptibility to pathogens, but not the developmental phenotype caused by cytoskeleton defaults. AtMAP65-3 thus has a dual role. It positively regulates cytokinesis, thus plant growth and development, and negatively interferes with plant defense against filamentous biotrophs. Our data suggest that downy mildew and powdery mildew stimulate AtMAP65-3 expression to down-regulate SA signaling for infection.
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http://dx.doi.org/10.1093/jxb/erv564DOI Listing
March 2016

Evolutionarily distant pathogens require the Arabidopsis phytosulfokine signalling pathway to establish disease.

Plant Cell Environ 2016 07 9;39(7):1396-407. Epub 2015 Nov 9.

INRA, Univ. Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900, Sophia Antipolis, France.

Secreted peptides and their specific receptors frequently orchestrate cell-to-cell communication in plants. Phytosulfokines (PSKs) are secreted tyrosine-sulphated peptide hormones, which trigger cellular dedifferentiation and redifferentiation upon binding to their membrane receptor. Biotrophic plant pathogens frequently trigger the differentiation of host cells into specialized feeding structures, which are essential for successful infection. We found that oomycete and nematode infections were characterized by the tissue-specific transcriptional regulation of genes encoding Arabidopsis PSKs and the PSK receptor 1 (PSKR1). Subcellular analysis of PSKR1 distribution showed that the plasma membrane-bound receptor internalizes after binding of PSK-α. Arabidopsis pskr1 knockout mutants were impaired in their susceptibility to downy mildew infection. Impaired disease susceptibility depends on functional salicylic acid (SA) signalling, but not on the massive up-regulation of SA-associated defence-related genes. Knockout pskr1 mutants also displayed a major impairment of root-knot nematode reproduction. In the absence of functional PSKR1, giant cells arrested their development and failed to fully differentiate. Our findings indicate that the observed restriction of PSK signalling to cells surrounding giant cells contributes to the isotropic growth and maturation of nematode feeding sites. Taken together, our data suggest that PSK signalling in Arabidopsis promotes the differentiation of host cells into specialized feeding cells.
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http://dx.doi.org/10.1111/pce.12627DOI Listing
July 2016

Gall-forming root-knot nematodes hijack key plant cellular functions to induce multinucleate and hypertrophied feeding cells.

J Insect Physiol 2016 Jan 26;84:60-69. Epub 2015 Jul 26.

INRA, UMR 1355 Institut Sophia Agrobiotech, 06900 Sophia-Antipolis, France; Univ. Nice Sophia Antipolis, UMR 7254 Institut Sophia Agrobiotech, 06900 Sophia-Antipolis, France; CNRS, UMR 7254 Institut Sophia Agrobiotech, 06900 Sophia-Antipolis, France. Electronic address:

Among plant-parasitic nematodes, the root-knot nematodes (RKNs) of the Meloidogyne spp. are the most economically important genus. RKN are root parasitic worms able to infect nearly all crop species and have a wide geographic distribution. During infection, RKNs establish and maintain an intimate relationship with the host plant. This includes the creation of a specialized nutritional structure composed of multinucleate and hypertrophied giant cells, which result from the redifferentiation of vascular root cells. Giant cells constitute the sole source of nutrients for the nematode and are essential for growth and reproduction. Hyperplasia of surrounding root cells leads to the formation of the gall or root-knot, an easily recognized symptom of plant infection by RKNs. Secreted effectors produced in nematode salivary glands and injected into plant cells through a specialized feeding structure called the stylet play a critical role in the formation of giant cells. Here, we describe the complex interactions between RKNs and their host plants. We highlight progress in understanding host plant responses, focusing on how RKNs manipulate key plant processes and functions, including cell cycle, defence, hormones, cellular scaffold, metabolism and transport.
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http://dx.doi.org/10.1016/j.jinsphys.2015.07.013DOI Listing
January 2016

Three BUB1 and BUBR1/MAD3-related spindle assembly checkpoint proteins are required for accurate mitosis in Arabidopsis.

New Phytol 2015 Jan 29;205(1):202-15. Epub 2014 Sep 29.

UMR 1355, Institut Sophia Agrobiotech, INRA, 400 route des Chappes, F-06903, Sophia-Antipolis, France; UMR 7254, CNRS, 400 route des Chappes, F-06903, Sophia-Antipolis, France; UMR 1355, Université de Nice Sophia-Antipolis, 400 route des Chappes, F-06903, Sophia-Antipolis, France.

The spindle assembly checkpoint (SAC) is a refined surveillance mechanism which ensures that chromosomes undergoing mitosis do not segregate until they are properly attached to the spindle microtubules (MT). The SAC has been extensively studied in metazoans and yeast, but little is known about its role in plants. We identified proteins interacting with a MT-associated protein MAP65-3, which plays a critical role in organising mitotic MT arrays, and carried out a functional analysis of previously and newly identified SAC components. We show that Arabidopsis SAC proteins BUB3.1, MAD2, BUBR1/MAD3s and BRK1 interact with each other and with MAP65-3. We found that two BUBR1/MAD3s interacted specifically at centromeres. When stably expressed in Arabidopsis, BRK1 localised to the kinetochores during all stages of the mitotic cell cycle. Early in mitosis, BUB3.1 and BUBR1/MAD3.1 localise to the mitotic spindle, where MAP65-3 organises spindle MTs. A double-knockout mad3.1 mad3.2 mutant presented spindle MT abnormalities, chromosome misalignments on the metaphase plate and the production of lagging chromosomes and micronuclei during mitosis. We conclude that BRK1 and BUBR1/MAD3-related proteins play a key role in ensuring faithful chromosome segregation during mitosis and that their interaction with MAP65-3 may be important for the regulation of MT-chromosome attachment.
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http://dx.doi.org/10.1111/nph.13073DOI Listing
January 2015

The Cyclin-Dependent Kinase Inhibitor KRP6 Induces Mitosis and Impairs Cytokinesis in Giant Cells Induced by Plant-Parasitic Nematodes in Arabidopsis.

Plant Cell 2014 Jun 24;26(6):2633-2647. Epub 2014 Jun 24.

Institut National de la Recherche Agronomique, UMR 1355 ISA/Centre National de la Recherche Scientifique, UMR 7254 ISA/Université de Nice-Sophia Antipolis, UMR ISA, 400 route des Chappes, 06903 Sophia-Antipolis, France

In Arabidopsis thaliana, seven cyclin-dependent kinase (CDK) inhibitors have been identified, designated interactors of CDKs or Kip-related proteins (KRPs). Here, the function of KRP6 was investigated during cell cycle progression in roots infected by plant-parasitic root-knot nematodes. Contrary to expectations, analysis of Meloidogyne incognita-induced galls of KRP6-overexpressing lines revealed a role for this particular KRP as an activator of the mitotic cell cycle. In accordance, KRP6-overexpressing suspension cultures displayed accelerated entry into mitosis, but delayed mitotic progression. Likewise, phenotypic analysis of cultured cells and nematode-induced giant cells revealed a failure in mitotic exit, with the appearance of multinucleated cells as a consequence. Strong KRP6 expression upon nematode infection and the phenotypic resemblance between KRP6 overexpression cell cultures and root-knot morphology point toward the involvement of KRP6 in the multinucleate and acytokinetic state of giant cells. Along these lines, the parasite might have evolved to manipulate plant KRP6 transcription to the benefit of gall establishment.
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http://dx.doi.org/10.1105/tpc.114.126425DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4114956PMC
June 2014

Elucidating the molecular bases of epigenetic inheritance in non-model invertebrates: the case of the root-knot nematode Meloidogyne incognita.

Front Physiol 2014 6;5:211. Epub 2014 Jun 6.

INRA, Institut Sophia Agrobiotech, UMR 1355 ISA Sophia-Antipolis, France ; CNRS, Institut Sophia Agrobiotech, UMR 7254 ISA Sophia-Antipolis, France ; Institut Sophia Agrobiotech, Université de Nice Sophia-Antipolis, UMR ISA Sophia-Antipolis, France.

Root-knot nematodes of the genus Meloidogyne are biotrophic plant parasites that exhibit different life cycles and reproduction modes, ranging from classical amphimixis to obligatory mitotic parthenogenesis (apomixis), depending on the species. Meloidogyne incognita, an apomictic species, exhibits a worldwide distribution and a wide host range affecting more than 3000 plant species. Furthermore, evidences suggest that apomixis does not prevent M. incognita from adapting to its environment in contrast to what is expected from mitotic parthenogenesis that should theoretically produce clonal progenies. This raises questions about mechanisms of genome plasticity leading to genetic variation and adaptive evolution in apomictic animals. We reasoned that epigenetic mechanisms might in part be responsible for the generation of phenotypic variants that provide potential for rapid adaptation. We established therefore a pipeline to investigate the principal carriers of epigenetic information, DNA methylation and post-translational histone modifications. Even if M. incognita possesses the epigenetic machinery i.e., chromatin modifying enzymes, 5-methyl-cytosine and 5-hydroxy-methyl-cytosine content is absent or very weak. In contrast, we demonstrated that the canonical histone modifications are present and chromatin shows typical nucleosome structure. This work is the first characterization of carriers of epigenetic information in M. incognita and constitutes a preamble to further investigate if M. incognita development and its adaptation to plant hosts are under epigenetic control. Our pipeline should allow performing similar types of studies in any non-model organism.
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http://dx.doi.org/10.3389/fphys.2014.00211DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4047830PMC
June 2014

Pyramiding, alternating or mixing: comparative performances of deployment strategies of nematode resistance genes to promote plant resistance efficiency and durability.

BMC Plant Biol 2014 Feb 22;14:53. Epub 2014 Feb 22.

INRA, UMR1355 INRA/UNSA/CNRS, Institut Sophia Agrobiotech, BP167, Sophia Antipolis F-06903, France.

Background: Resistant cultivars are key elements for pathogen control and pesticide reduction, but their repeated use may lead to the emergence of virulent pathogen populations, able to overcome the resistance. Increased research efforts, mainly based on theoretical studies, explore spatio-temporal deployment strategies of resistance genes in order to maximize their durability. We evaluated experimentally three of these strategies to control root-knot nematodes: cultivar mixtures, alternating and pyramiding resistance genes, under controlled and field conditions over a 3-years period, assessing the efficiency and the durability of resistance in a protected crop rotation system with pepper as summer crop and lettuce as winter crop.

Results: The choice of the resistance gene and the genetic background in which it is introgressed, affected the frequency of resistance breakdown. The pyramiding of two different resistance genes in one genotype suppressed the emergence of virulent isolates. Alternating different resistance genes in rotation was also efficient to decrease virulent populations in fields due to the specificity of the virulence and the trapping effect of resistant plants. Mixing resistant cultivars together appeared as a less efficient strategy to control nematodes.

Conclusions: This work provides experimental evidence that, in a cropping system with seasonal sequences of vegetable species, pyramiding or alternating resistance genes benefit yields in the long-term by increasing the durability of resistant cultivars and improving the long-term control of a soil-borne pest. To our knowledge, this result is the first one obtained for a plant-nematode interaction, which helps demonstrate the general applicability of such strategies for breeding and sustainable management of resistant cultivars against pathogens.
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http://dx.doi.org/10.1186/1471-2229-14-53DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3944934PMC
February 2014

Identification of novel target genes for safer and more specific control of root-knot nematodes from a pan-genome mining.

PLoS Pathog 2013 Oct 31;9(10):e1003745. Epub 2013 Oct 31.

INRA, UMR 1355 ISA, Institut Sophia Agrobiotech, Sophia-Antipolis, France ; CNRS, UMR 7254 ISA, Institut Sophia Agrobiotech, Sophia-Antipolis, France ; Université de Nice Sophia-Antipolis, UMR ISA, Institut Sophia Agrobiotech, Sophia-Antipolis, France.

Root-knot nematodes are globally the most aggressive and damaging plant-parasitic nematodes. Chemical nematicides have so far constituted the most efficient control measures against these agricultural pests. Because of their toxicity for the environment and danger for human health, these nematicides have now been banned from use. Consequently, new and more specific control means, safe for the environment and human health, are urgently needed to avoid worldwide proliferation of these devastating plant-parasites. Mining the genomes of root-knot nematodes through an evolutionary and comparative genomics approach, we identified and analyzed 15,952 nematode genes conserved in genomes of plant-damaging species but absent from non target genomes of chordates, plants, annelids, insect pollinators and mollusks. Functional annotation of the corresponding proteins revealed a relative abundance of putative transcription factors in this parasite-specific set compared to whole proteomes of root-knot nematodes. This may point to important and specific regulators of genes involved in parasitism. Because these nematodes are known to secrete effector proteins in planta, essential for parasitism, we searched and identified 993 such effector-like proteins absent from non-target species. Aiming at identifying novel targets for the development of future control methods, we biologically tested the effect of inactivation of the corresponding genes through RNA interference. A total of 15 novel effector-like proteins and one putative transcription factor compatible with the design of siRNAs were present as non-redundant genes and had transcriptional support in the model root-knot nematode Meloidogyne incognita. Infestation assays with siRNA-treated M. incognita on tomato plants showed significant and reproducible reduction of the infestation for 12 of the 16 tested genes compared to control nematodes. These 12 novel genes, showing efficient reduction of parasitism when silenced, constitute promising targets for the development of more specific and safer control means.
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http://dx.doi.org/10.1371/journal.ppat.1003745DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3814813PMC
October 2013

Conserved DNA Motifs, Including the CENP-B Box-like, Are Possible Promoters of Satellite DNA Array Rearrangements in Nematodes.

PLoS One 2013 27;8(6):e67328. Epub 2013 Jun 27.

Department of Molecular Biology, Rudjer Bošković Institute, Zagreb, Croatia.

Tandemly arrayed non-coding sequences or satellite DNAs (satDNAs) are rapidly evolving segments of eukaryotic genomes, including the centromere, and may raise a genetic barrier that leads to speciation. However, determinants and mechanisms of satDNA sequence dynamics are only partially understood. Sequence analyses of a library of five satDNAs common to the root-knot nematodes Meloidogyne chitwoodi and M. fallax together with a satDNA, which is specific for M. chitwoodi only revealed low sequence identity (32-64%) among them. However, despite sequence differences, two conserved motifs were recovered. One of them turned out to be highly similar to the CENP-B box of human alpha satDNA, identical in 10-12 out of 17 nucleotides. In addition, organization of nematode satDNAs was comparable to that found in alpha satDNA of human and primates, characterized by monomers concurrently arranged in simple and higher-order repeat (HOR) arrays. In contrast to alpha satDNA, phylogenetic clustering of nematode satDNA monomers extracted either from simple or from HOR array indicated frequent shuffling between these two organizational forms. Comparison of homogeneous simple arrays and complex HORs composed of different satDNAs, enabled, for the first time, the identification of conserved motifs as obligatory components of monomer junctions. This observation highlights the role of short motifs in rearrangements, even among highly divergent sequences. Two mechanisms are proposed to be involved in this process, i.e., putative transposition-related cut-and-paste insertions and/or illegitimate recombination. Possibility for involvement of the nematode CENP-B box-like sequence in the transposition-related mechanism and together with previously established similarity of the human CENP-B protein and pogo-like transposases implicate a novel role of the CENP-B box and related sequence motifs in addition to the known function in centromere protein binding.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0067328PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3694981PMC
October 2017

Diversity and evolution of root-knot nematodes, genus Meloidogyne: new insights from the genomic era.

Annu Rev Phytopathol 2013 13;51:203-20. Epub 2013 May 13.

INRA, UMR1355 Institut Sophia Agrobiotech, F-06903 Sophia Antipolis, France.

Root-knot nematodes (RKNs) (Meloidogyne spp.) are obligate endoparasites of major worldwide economic importance. They exhibit a wide continuum of variation in their reproductive strategies, ranging from amphimixis to obligatory mitotic parthenogenesis. Molecular phylogenetic studies have highlighted divergence between mitotic and meiotic parthenogenetic RKN species and probable interspecific hybridization as critical steps in their speciation and diversification process. The recent completion of the genomes of two RKNs, Meloidogyne hapla and Meloidogyne incognita, that exhibit striking differences in their mode of reproduction (with and without sex, respectively), their geographic distribution, and their host range has opened the way for deciphering the evolutionary significance of (a)sexual reproduction in these parasites. Accumulating evidence suggests that whole-genome duplication (in M. incognita) and horizontal gene transfers (HGTs) represent major forces that have shaped the genome of current RKN species and may account for the extreme adaptive capacities and parasitic success of these nematodes.
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http://dx.doi.org/10.1146/annurev-phyto-082712-102300DOI Listing
December 2013

Ectopic expression of Kip-related proteins restrains root-knot nematode-feeding site expansion.

New Phytol 2013 Jul 10;199(2):505-519. Epub 2013 Apr 10.

Institut National de la Recherche Agronomique, UMR 1355 ISA/Centre National de la Recherche Scientifique, UMR 7254 ISA/Université de Nice-Sophia Antipolis, UMR ISA, 400 route des Chappes, Sophia-Antipolis, France.

The development of nematode feeding sites induced by root-knot nematodes involves the synchronized activation of cell cycle processes such as acytokinetic mitoses and DNA amplification. A number of key cell cycle genes are reported to be critical for nematode feeding site development. However, it remains unknown whether plant cyclin-dependent kinase (CDK) inhibitors such as the Arabidopsis interactor/inhibitor of CDK (ICK)/Kip-related protein (KRP) family are involved in nematode feeding site development. This study demonstrates the involvement of Arabidopsis ICK2/KRP2 and ICK1/KRP1 in the control of mitosis to endoreduplication in galls induced by the root-knot nematode Meloidogyne incognita. Using ICK/KRP promoter-GUS fusions and mRNA in situ hybridizations, we showed that ICK2/KRP2, ICK3/KRP5 and ICK4/KRP6 are expressed in galls after nematode infection. Loss-of-function mutants have minor effects on gall development and nematode reproduction. Conversely, overexpression of both ICK1/KRP1 and ICK2/KRP2 impaired mitosis in giant cells and blocked neighboring cell proliferation, resulting in a drastic reduction of gall size. Studying the dynamics of protein expression demonstrated that protein levels of ICK2/KRP2 are tightly regulated during giant cell development and reliant on the presence of the nematode. This work demonstrates that impeding cell cycle progression by means of ICK1/KRP1 and ICK2/KRP2 overexpression severely restricts gall development, leading to a marked limitation of root-knot nematode development and reduced numbers of offspring.
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http://dx.doi.org/10.1111/nph.12255DOI Listing
July 2013

Plant parasitic nematode effectors target host defense and nuclear functions to establish feeding cells.

Front Plant Sci 2013 13;4:53. Epub 2013 Mar 13.

Institut Sophia Agrobiotech, UMR INRA 1355 - Université Nice-Sophia Antipolis - CNRS 7254 Sophia Antipolis, France.

Plant parasitic nematodes are microscopic worms, the most damaging species of which have adopted a sedentary lifestyle within their hosts. These obligate endoparasites have a biotrophic relationship with plants, in which they induce the differentiation of root cells into hypertrophied, multinucleate feeding cells (FCs). Effectors synthesized in the esophageal glands of the nematode are injected into the plant cells via the syringe-like stylet and play a key role in manipulating the host machinery. The establishment of specialized FCs requires these effectors to modulate many aspects of plant cell morphogenesis and physiology, including defense responses. This cell reprogramming requires changes to host nuclear processes. Some proteins encoded by parasitism genes target host nuclei. Several of these proteins were immunolocalized within FC nuclei or shown to interact with host nuclear proteins. Comparative genomics and functional analyses are gradually revealing the roles of nematode effectors. We describe here these effectors and their hypothesized roles in the unique feeding behavior of these pests.
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http://dx.doi.org/10.3389/fpls.2013.00053DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3595553PMC
March 2013

Contribution of lateral gene transfers to the genome composition and parasitic ability of root-knot nematodes.

PLoS One 2012 30;7(11):e50875. Epub 2012 Nov 30.

Aix-Marseille Université, Centre National de la Recherche Scientifique, LATP, UMR 7353, Evolution Biologique et Modélisation, Marseille, France.

Lateral gene transfers (LGT), species to species transmission of genes by means other than direct inheritance from a common ancestor, have played significant role in shaping prokaryotic genomes and are involved in gain or transfer of important biological processes. Whether LGT significantly contributed to the composition of an animal genome is currently unclear. In nematodes, multiple LGT are suspected to have favored emergence of plant-parasitism. With the availability of whole genome sequences it is now possible to assess whether LGT have significantly contributed to the composition of an animal genome and to establish a comprehensive list of these events. We generated clusters of homologous genes and automated phylogenetic inference, to detect LGT in the genomes of root-knot nematodes and found that up to 3.34% of the genes originate from LGT of non-metazoan origin. After their acquisition, the majority of genes underwent series of duplications. Compared to the rest of the genes in these species, several predicted functional categories showed a skewed distribution in the set of genes acquired via LGT. Interestingly, functions related to metabolism, degradation or modification of carbohydrates or proteins were substantially more frequent. This suggests that genes involved in these processes, related to a parasitic lifestyle, have been more frequently fixed in these parasites after their acquisition. Genes from soil bacteria, including plant-pathogens were the most frequent closest relatives, suggesting donors were preferentially bacteria from the rhizosphere. Several of these bacterial genes are plasmid-borne, pointing to a possible role of these mobile genetic elements in the transfer mechanism. Our analysis provides the first comprehensive description of the ensemble of genes of non-metazoan origin in an animal genome. Besides being involved in important processes regarding plant-parasitism, genes acquired via LGT now constitute a substantial proportion of protein-coding genes in these nematode genomes.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0050875PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3511272PMC
May 2013

CCS52 and DEL1 genes are key components of the endocycle in nematode-induced feeding sites.

Plant J 2012 Oct 23;72(2):185-98. Epub 2012 Aug 23.

Institut National de la Recherche Agronomique, UMR 1355 ISA/Centre National de la Recherche Scientifique, UMR 7254 ISA/Université de Nice-Sophia Antipolis, UMR ISA, 400 Route des Chappes, Sophia-Antipolis, France.

The establishment of galls and syncytia as feeding sites induced by root-knot and cyst nematodes, respectively, involves a progressive increase in nuclear and cellular size. Here we describe the functional characterization of endocycle activators CCS52A, CCS52B and a repressor of the endocycle, DEL1, during two types of nematode feeding site development in Arabidopsis thaliana. In situ hybridization analysis showed that expression of CCS52A1 and CCS52B was strongly induced in galls and syncytia and DEL1 was stably but weakly expressed throughout feeding site development. Down-regulation and over-expression of CCS52 and DEL1 in Arabidopsis drastically affected giant cell and syncytium growth, resulting in restrained nematode development, illustrating the need for mitotic activity and endo-reduplication for feeding site maturation. Exploiting the mechanism of endo-reduplication may be envisaged as a strategy to control plant-parasitic nematodes.
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http://dx.doi.org/10.1111/j.1365-313X.2012.05054.xDOI Listing
October 2012
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