Key pathogenicity determinants of the adaptation of a nematode pest to a resistant host plant – ADMIRE

Plant-parasitic nematodes cause several hundred billion € loss to agricultural production annually. To meet projected global food requirements in 2050, the Food and Agriculture Organization estimates that food production will need to increase by 70%. A major constraint to achieve these targets is crop loss due to pests and diseases, which account for up to 70% of crop losses in developing countries.
Root-knot nematodes (RKNs), Meloidogyne spp., have collectively been ranked #1 in the list raised with respect to their economic importance. These biotrophic parasites have a worldwide distribution and can infect almost all cultivated plants.
Until recently, control of RKNs was performed mainly using chemical nematicides. However, because of their toxic side effects and the stringency of conditions for approval of chemicals for agriculture, the future use of effective nematicides is largely prohibited. In many cases, no effective replacement solution is available.
Plant resistance is currently the most efficient control strategy, although resistance genes may be overcome by virulent populations in many commercially viable cultivar, which raises concern about the durability of resistance.
The most devastating RKN species reproduce exclusively by parthenogenesis, which involves mitotic division with no reduction in the chromosome number. Asexual reproduction is usually considered as an evolutionary dead-end, and difficulties for asexual lineages to adapt to a fluctuating environment are anticipated due to the lack of sufficient genetic plasticity. However, asexual RKN species exhibit remarkable capacities of adaptation, among which their ability to overcome plant resistance genes, although the mechanisms behind the generation of heritable phenotypic variants in the progeny of these clonal species remains enigmatic. Thus, these clonal organisms appear as an outstanding evolutionary paradox regarding current theories on the benefits of sex, and raise questions about the molecular mechanisms that allow adaptation of an asexual animal to a biotic stress (i.e., host resistance). Previous analyses have shown that genomic polymorphism could not be directly correlated to observed avirulence/virulence patterns in RKNs. Although accumulation of point mutations and/or structural rearrangements might be involved, this could result in genome decay in an asexually-reproducing organism. Furthermore, our previous experiments have shown that the ability to overcome resistance is not inherited as a Mendelian character.
Recently, we have made a series of breakthroughs in the understanding of the genome structure and epigenome of the RKN species M. incognita, which indicate that now is the right time to explore how parthenogenetic RKNs overcome plant resistance and how this knowledge could help to control them.
In this context, we propose to (1) identify the mechanisms (at the genome, epigenome and transcriptome levels) by which these asexual pests can adapt to plant resistance and (2) validate (some of) these mechanisms at the functional level. The model chosen for this study is the interaction between the parthenogenetic species M. incognita and tomatoes carrying the Mi-1.2 resistance gene. This biological system has been routinely manipulated in the laboratory for many years, genomic/transcriptomic resources are fully available, and epigenetic signatures were identified in the nematode.
Thus, deciphering the mechanisms and rate of variability in parthenogenetic nematodes in relation to their adaptation to host resistance is very challenging but undoubtedly of general interest, identifying the relative contributions of genetics and epigenetics to micro-evolution, and strategies for sustainable management of resources. In the short term, our findings could lead to the development of diagnostic molecular markers of RKN virulence and guidance of efficient agricultural countermeasures in the field, i.e. optimal deployment of the resistance.