Population genomics supports clonal reproduction and multiple independent gains and losses of parasitic abilities in the most devastating nematode pest

Abstract

The root-knot nematodes are the most devastating worms to worldwide agriculture with Meloidogyne incognita being the most widely distributed and damaging species. This parasitic and ecological success seems surprising given its supposed obligatory clonal reproduction. Clonal reproduction has been suspected based on cytological observations but, so far, never confirmed by population genomics data. As a species, M. incognita is highly polyphagous with thousands of host plants. However, different M. incognita isolates present distinct and overlapping patterns of host compatibilities.Historically, four "host races" had been defined as a function of ranges of compatible and incompatible plants. In this study, we used population genomics to assess whether (a) reproduction is actually clonal in this species, (b) the host races follow an underlying phylogenetic signal or, rather represent multiple independent transitions, and (c) how genome variations associate with other important biological traits such as the affected crops and geographical distribution. We sequenced the genomes of 11 M. incognita isolates across Brazil that covered the four host races in replicates.By aligning the genomic reads of these isolates to the M. incognita reference genome assembly, we identified point variations. Analysis of linkage disequilibrium and 4gametes test showed no evidence for recombination, corroborating the clonal reproduction of M. incognita. The few point variations between the isolates showed no significant association with the host races, the geographical origin of the samples, or the crop on which they have been collected. Addition of isolates from other locations around the world confirmed this lack of underlying phylogenetic signal. This suggests multiple gains and losses of parasitic abilities and adaptations to different environments account for the broad host spectrum and wide geographical distribution of | 443 KOUTSOVOULOS eT aL.

Transposable Elements are an evolutionary force shaping genomic plasticity in the parthenogenetic root-knot nematode Meloidogyne incognita

“…The 11 other isolates come from different locations across Brazil, and present four different ranges of compatible hosts (referred to as R1, R2, R3, R4, see sup. Fig S4) and currently infected crop species (Koutsovoulos et al 2020). Pool-seq paired-end Illumina data has been generated for all these isolates.…”

“…The mechanisms underlying the adaptability of parthenogenetic RKN without sex remain elusive. Recent population genomics analyses showed that only a few single nucleotide variations (SNV) could be identified by comparing different Brazilian M. incognita isolates showing distinct ranges of host compatibility (Koutsovoulos et al 2020). Addition of further isolates from different geographical locations across the world did not substantially expand the number of variable positions in the genome.…”

“…From an evolutionary point of view, the parthenogenetic root-knot nematode M. incognita represents an interesting model to study the activity of TEs and their impact on the genome, including in coding or regulatory regions. Indeed, being a plant parasite, M. incognita is engaged in an arms race with the plant defence systems and point mutations alone are not expected to be a major mechanism supporting adaptation in this species (Koutsovoulos et al 2020). In a broader perspective, little is known yet about the TE dynamics in nematode genomes and their possible impact on adaptive evolution, including in the model C. elegans, despite being the first sequenced animal genome since 1998 (The C. elegans Genome Sequencing Consortium 1998).…”

“…We have then tested whether the frequencies of presence/absence of these TEs across the genome varied between different isolates. To test for variations in frequencies, we have used population genomics data from eleven M. incognita isolates collected on different crops and locations and differing in their ranges of compatible hosts (Koutsovoulos et al 2020). From the set of TE loci that presented the most contrasted patterns of presence/absence across the isolates, we investigated whether some could represent neo-insertions.…”

MiDaf16-like and MiSkn1-like gene families are reliable targets to develop biotechnological tools for the control and management of Meloidogyne incognita

“…Recently, Koutsovoulos et al 65 sequenced the genomes of 11M. incognita isolates race 1 to 4 infecting different host plant across Brazil (including the race 3, used in this study) and showed that cumulative fixed divergence across these Brazilian isolates and the reference genome (M. incognita strain Morelos) reached approximately 0.02% of the nucleotides.…”