The map-1 Gene Family in Root-Knot Nematodes, Meloidogyne spp.: A Set of Taxonomically Restricted Genes Specific to Clonal Species

Taxonomically restricted genes (TRGs), i.e., genes that are restricted to a limited subset of phylogenetically related organisms, may be important in adaptation. In parasitic organisms, TRG-encoded proteins are possible determinants of the specificity of host-parasite interactions. In the root-knot nematode (RKN) Meloidogyne incognita, the map-1 gene family encodes expansin-like proteins that are secreted into plant tissues during parasitism, thought to act as effectors to promote successful root infection. MAP-1 proteins exhibit a modular architecture, with variable number and arrangement of 58 and 13-aa domains in their central part. Here, we address the evolutionary origins of this gene family using a combination of bioinformatics and molecular biology approaches. Map-1 genes were solely identified in one single member of the phylum Nematoda, i.e., the genus Meloidogyne, and not detected in any other nematode, thus indicating that the map-1 gene family is indeed a TRG family. A phylogenetic analysis of the distribution of map-1 genes in RKNs further showed that these genes are specifically present in species that reproduce by mitotic parthenogenesis, with the exception of M. floridensis, and could not be detected in RKNs reproducing by either meiotic parthenogenesis or amphimixis. These results highlight the divergence between mitotic and meiotic RKN species as a critical transition in the evolutionary history of these parasites. Analysis of the sequence conservation and organization of repeated domains in map-1 genes suggests that gene duplication(s) together with domain loss/duplication have contributed to the evolution of the map-1 family, and that some strong selection mechanism may be acting upon these genes to maintain their functional role(s) in the specificity of the plant-RKN interactions

Data from: Tracking changes in life-history traits related to unnecessary virulence in a plant-parasitic nematode

Evaluating trade-offs in life-history traits of plant pathogens is essential to understand the evolution and epidemiology of diseases. In particular, virulence costs when the corresponding host resistance gene is lacking play a major role in the adaptive biology of pathogens and contribute to the maintenance of their genetic diversity. Here, we investigated whether life-history traits directly linked to the establishment of plant–nematode interactions, that is, ability to locate and move toward the roots of the host plant, and to invade roots and develop into mature females, are affected in Meloidogyne incognita lines virulent against the tomato Mi-1.2 resistance gene. Virulent and avirulent near-isogenic lines only differing in their capacity to reproduce or not on resistant tomatoes were compared in single inoculation or pairwise competition experiments. Data highlighted (1) a global lack of trade-off in traits associated with unnecessary virulence with respect to the nematode ability to successfully infest plant roots and (2) variability in these traits when the genetic background of the nematode is considered irrespective of its (a)virulence status. These data suggest that the variation detected here is independent from the adaptation of M. incognita to host resistance, but rather reflects some genetic polymorphism in this asexual organism

Isolation of microsatellites from an enriched genomic library of the plant-parasitic nematode Meloidogyne incognita and their detection in other root-knot nematode species

International audienceThe root-knot nematode Meloidogyne incognita is a polyphagous pest distributed from temperate to tropical regions. However, the lack of suitable markers leads to a poor knowledge of its population genetic structure and colonization process. Here we describe the first characterization of 15 microsatellite loci from this nematode, that were developed from an enriched genomic library. Although the variability of these microsatellites was generally low, three of them exhibited a significant level of intrapopulation polymorphism, with three to seven alleles detected. The observed and expected heterozygosities ranged from 0.025 to 0.385 and from 0.024 to 0.779, respectively. Thus, these new microsatellite markers have potential value for the implementation of genotyping experiments in this nematode. Furthermore, successful cross-amplification of the variable microsatellite loci in seven other Meloidogyne species provides the opportunity of using these markers for population genetic studies in these damaging plant-parasitic nematodes

DataSet for ECE-2015-06-00341.R1

- Distribution of Meloidogyne incognita juveniles around tomato root tips at 90, 180, 270 and 360 min post-inoculation. Ka, Kv, Ma, Mv = Kursk, Morelos avirulent and virulent, respectively. - Distribution of Meloidogyne incognita females in tomato roots in competition experiments. Ka, Kv, Ma, Mv = Kursk, Morelos avirulent and virulent, respectively

Multiple alignment of the repetitive domains of the MAP-1.1 deduced protein sequences from <i>Meloidogyne</i> spp.

<p>Dashes indicate deletions. Yellow boxes indicate mutated positions compared to the MAP-1.1 sequence from <i>M. incognita.</i></p

Hypothetical model for the evolution of <i>map-1</i> genes in root-knot nematodes.

<p>The actual distribution of <i>map-1</i> genes in <i>Meloidogyne</i> species is indicated at the bottom of the figure. Putative individual evolutionary events leading to such a distibution are indicated in circles according to the following code: D, L  =  gene duplication or loss, respectively; d, l, t  =  domain duplication, loss or truncation, respectively. Orange and blue boxes represent the 58-aa and 13-aa domains in MAP-1 encoded proteins, respectively.</p

Distribution of <i>map-1</i> genes in root-knot nematodes.

<p>A neighbor-joining phylogenetic tree of the species used in this study was built using SSU rDNA sequences shown in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0038656#pone.0038656.s004" target="_blank">Table S2</a>. Bootstrap support was calculated from 1,000 replicates and values >50% are indicated at the corresponding nodes. The red dot shows the clade clustering species that reproduce by mitotic parthenogenesis, except for <i>M. floridensis.</i> Red and green lines show the species that reproduce by mitotic parthenogenesis or meiotic parthenogenesis/amphimixis, respectively. Orange and blue boxes represent the 58-aa and 13-aa domains in MAP-1 encoded proteins, respectively.</p

The Meloidogyne incognita Nuclear Effector MiEFF1 Interacts With Arabidopsis Cytosolic Glyceraldehyde-3-Phosphate Dehydrogenases to Promote Parasitism

International audienceRoot-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 Meloidogyne incognita MiEFF1 is one of the rare effectors of phytopathogenic nematodes to have been located in vivo in feeding cells. This effector specifically targets the giant cell nuclei. We investigated the Arabidopsis 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 Arabidopsis 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

aCGH_Raw_Data

aCGH_Raw_Dat

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

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, e.g., resistant hosts. Here we used a genome-wide 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