DNA transposons drive genome evolution of the root-knot nematode Meloidogyne incognita
Transposable Elements are an evolutionary force shaping genomic plasticity in the parthenogenetic root-knot nematode Meloidogyne incognita
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.
 Bessereau J-L. 2006. Transposons in C. elegans. WormBook. 10.1895/wormbook.1.70.1
 Castagnone-Sereno P, Danchin EGJ. 2014. Parasitic success without sex - the nematode experience. J. Evol. Biol. 27:1323-1333. 10.1111/jeb.12337
 Faino L, Seidl MF, Shi-Kunne X, Pauper M, Berg GCM van den, Wittenberg AHJ, Thomma BPHJ. 2016. Transposons passively and actively contribute to evolution of the two-speed genome of a fungal pathogen. Genome Res. 26:1091-1100. 10.1101/gr.204974.116
 Glémin S, François CM, Galtier N. 2019. Genome Evolution in Outcrossing vs. Selfing vs. Asexual Species. In: Anisimova M, editor. Evolutionary Genomics: Statistical and Computational Methods. Methods in Molecular Biology. New York, NY: Springer. p. 331-369. 10.1007/978-1-4939-9074-0_11
 Koutsovoulos GD, Marques E, Arguel M-J, Duret L, Machado ACZ, Carneiro RMDG, Kozlowski DK, Bailly-Bechet M, Castagnone-Sereno P, Albuquerque EVS, et al. 2020. Population genomics supports clonal reproduction and multiple independent gains and losses of parasitic abilities in the most devastating nematode pest. Evol. Appl. 13:442-457. 10.1111/eva.12881
 Kozlowski D. 2020a. Transposable Elements prediction and annotation in the M. incognita genome. Portail Data INRAE. 10.15454/EPTDOS
 Kozlowski D. 2020b. Transposable Elements prediction and annotation in the C. elegans genome. Portail Data INRAE. 10.15454/LQCIW0
 Kozlowski D. 2020c. TE polymorphisms detection and analysis with PopoolationTE2. Portail Data INRAE. 10.15454/EWJCT8
 Kozlowski DK, Hassanaly-Goulamhoussen R, Da Rocha M, Koutsovoulos GD, Bailly-Bechet M, Danchin EG (2020) Transposable Elements are an evolutionary force shaping genomic plasticity in the parthenogenetic root-knot nematode Meloidogyne incognita. bioRxiv, 2020.04.30.069948, ver. 4 peer-reviewed and recommended by PCI Evolutionary Biology. 10.1101/2020.04.30.069948
 Savary S, Willocquet L, Pethybridge SJ, Esker P, McRoberts N, Nelson A. 2019. The global burden of pathogens and pests on major food crops. Nat. Ecol. Evol. 3:430-439. 10.1038/s41559-018-0793-y
 Trudgill DL, Blok VC. 2001. Apomictic, polyphagous root-knot nematodes: exceptionally successful and damaging biotrophic root pathogens. Annu Rev Phytopathol 39:53-77. 10.1146/annurev.phyto.39.1.53
Ines Alvarez (2020) DNA transposons drive genome evolution of the root-knot nematode Meloidogyne incognita. Peer Community in Evolutionary Biology, 100106. 10.24072/pci.evolbiol.100106
Evaluation round #203 Aug 2020
DOI or URL of the preprint: 10.1101/2020.04.30.069948
Version of the preprint: 3
Decision by Ines Alvarez
Thanks to the authors.
I'm satisfied with their modifications and just ask them to make the minor modifications of reviewer 3 and to include the link to their dataverse website (https://data.inrae.fr/dataverse/TE-mobility-in-MiV3) in the main manuscript.
A message will be sent to the authors with the formatting instructions.
Reviewed by anonymous reviewer, 13 Jul 2020
Reviewed by anonymous reviewer, 02 Aug 2020
Reviewed by Daniel Vitales, 17 Jul 2020
Evaluation round #102 Jun 2020
DOI or URL of the preprint: 10.1101/2020.04.30.069948
Version of the preprint: 2
Decision by Ines Alvarez
This is a valuable piece of work, very relevant in knot-root nematode M. incognita genome evolution. It is interesting for the community and I think it could be recommendable after addressing reviewers main concerns, other minor questions, and incorporating their suggestions. Three reviewers coincided in the good quality and relevance of the study and therefore, it has a positive feedback, but I also agree that there are several points that should be clarified before its recommendation.
Major concerns are related with the recapitulation of the actual knowledge on TEs in nematodes in order to highlight the relevance of the present study, as well as other study cases in which TEs activity directly affect regulatory and coding regions. Other major concern is that TEs activity drives adaptive evolution seems not conclusive here. This is not demonstrated with the data presented here and it should be noticed. There are several paragraphs dificult to follow and understand (see reviewers anotations). Please, respond to each question of all reviewers and make changes in the text accordingly in order to produce a recomendable new version of your manuscript.
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