Movements of transposable elements contribute to the genomic plasticity and species diversification in an asexually reproducing nematode pest

  1. Djampa K. L. Kozlowski
  2. Rahim Hassanaly‐Goulamhoussen
  3. Martine Da Rocha
  4. Georgios D. Koutsovoulos
  5. Marc Bailly‐Bechet
  6. Etienne G. J. Danchin

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Abstract

Despite reproducing without sexual recombination, Meloidogyne incognita is an adaptive and versatile phytoparasitic nematode. This species displays a global distribution, can parasitize a large range of plants, and can overcome plant resistance in a few generations. The mechanisms underlying this adaptability remain poorly known. At the whole‐genome level, only a few single nucleotide variations have been observed across different geographical isolates with distinct ranges of compatible hosts. Exploring other factors possibly involved in genomic plasticity is thus important. Transposable elements (TEs), by their repetitive nature and mobility, can passively and actively impact the genome dynamics. This is particularly expected in polyploid hybrid genomes such as the one of M .  incognita . Here, we have annotated the TE content of M .  incognita , analyzed the statistical properties of this TE landscape, and used whole‐genome pool‐seq data to estimate the mobility of these TEs across twelve geographical isolates, presenting variations in ranges of compatible host plants. DNA transposons are more abundant than retrotransposons, and the high similarity of TE copies to their consensus sequences suggests they have been at least recently active. We have identified loci in the genome where the frequencies of presence of a TE showed substantial variations across the different isolates. Overall, variations in TE frequencies across isolates followed their phylogenetic divergence, suggesting TEs participate in the species diversification. Compared with the M .  incognita reference genome, we detected isolate and lineage‐specific de novo insertion of some TEs, including within genic regions or in the upstream regulatory regions. We validated by PCR the insertion of some of these TEs inside genic regions, confirming TE movements have possible functional impacts. Overall, we show DNA transposons can drive genomic plasticity in M .  incognita and their role in genome evolution of other parthenogenetic animal deserves further investigation.

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  1. Version published to 10.1111/eva.13246
  2. Peer Community in Evolutionary Biology

    Duplications, mutations and recombination may be considered the main sources of genomic variation and evolution. In addition, sexual recombination is essential in purging deleterious mutations and allowing advantageous allelic combinations to occur (Glémin et al. 2019). However, in parthenogenetic asexual organisms, variation cannot be explained by sexual recombination, and other mechanisms must account for it. Although it is known that transposable elements (TE) may influence on genome structure and gene expression patterns, their role as a primary source of genomic variation and rapid adaptability has received less attention. An important role of TE on adaptive genome evolution has been documented for fungal phytopathogens (Faino et al. 2016), suggesting that TE activity might explain the evolutionary dynamics of this type of organisms.
    The phytopathogen nematode Meloidogyne incognita is one of the worst agricultural pests in warm climates (Savary et al. 2019). This species, as well as other root-knot nematodes (RKN), shows a wide geographical distribution range infecting diverse groups of plants. Although allopolyploidy may have played an important role on the wide adaptation of this phytopathogen, it may not explain by itself the rapid changes required to overcome plant resistance in a few generations. Paradoxically, M. incognita reproduces asexually via mitotic parthenogenesis (Trudgill and Blok 2001; Castagnone-Sereno and Danchin 2014) and only few single nucleotide variations were identified between different host races isolates (Koutsovoulos et al. 2020). Therefore, this is an interesting model to explore other sources of genomic variation such the TE activity and its role on the success and adaptability of this phytopathogen.
    To address these questions, Kozlowski et al. (2020) estimated the TE mobility across 12 geographical isolates that presented phenotypic variations in Meloidogyne incognita, concluding that recent activity of TE in both genic and regulatory regions might have given rise to relevant functional differences between genomes. This was the first estimation of TE activity as a mechanism probably involved in genome plasticity of this root-knot nematode. This study also shed light on evolutionary mechanisms of asexual organisms with an allopolyploid origin. These authors re-annotated the 185 Mb triploid genome of M. incognita for TE content analysis using stringent filters (Kozlowski 2020a), and estimated activity by their distribution using a population genomics approach including isolates from different crops and locations. Canonical TE represented around 4.7% of the M. incognita genome of which mostly correspond to TIR (Terminal Inverted Repeats) and MITEs (Miniature Inverted repeat Transposable Elements) followed by Maverick DNA transposons and LTR (Long Terminal Repeats) retrotransposons. The result that most TE found were represented by DNA transposons is similar to the previous studies with the nematode species model Caenorhabditis elegans (Bessereau 2006; Kozlowski 2020b) and other nematodes as well. Canonical TE annotations were highly similar to their consensus sequences containing transposition machinery when TE are autonomous, whereas no genes involved in transposition were found in non-autonomous ones. These findings suggest recent activity of TE in the M. incognita genome. Other relevant result was the significant variation in TE presence frequencies found in more than 3,500 loci across isolates, following a bimodal distribution within isolates. However, variation in TE frequencies was low to moderate between isolates recapitulating the phylogenetic signal of isolates DNA sequences polymorphisms. A detailed analysis of TE frequencies across isolates allowed identifying polymorphic TE loci, some of which might be neo-insertions mostly of TIRs and MITEs (Kozlowski 2020c). Interestingly, the two thirds of the fixed neo-insertions were located in coding regions or in regulatory regions impacting expression of specific genes in M. incognita. Future research on proteomics is needed to evaluate the functional impact that these insertions have on adaptive evolution in M. incognita. In this line, this pioneer research of Kozlowski et al. (2020) is a first step that is also relevant to remark the role that allopolyploidy and reproduction have had on shaping nematode genomes.

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  3. Version published to 10.1101/2020.04.30.069948 on bioRxiv