Genome Evolution and Adaptations to Plant Parasitism in Nematodes Etienne Danchin

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Genome Evolution and Adaptations to Plant Parasitism in Nematodes Etienne Danchin Genome evolution and adaptations to plant parasitism in nematodes Etienne Danchin To cite this version: Etienne Danchin. Genome evolution and adaptations to plant parasitism in nematodes. Life Sciences [q-bio]. Université Nice Sophia Antipolis, 2014. tel-02801776 HAL Id: tel-02801776 https://hal.inrae.fr/tel-02801776 Submitted on 5 Jun 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Genome evolution and adaptations to plant parasitism in nematodes Etienne G.J. Danchin Habilitation à Diriger des Recherches Ecole Doctorale des Sciences de la Vie et de la Santé (ED85) Université de Nice - Sophia Antipolis Soutenue le 11 Mars 2014, devant le jury constitué de: Institut de Génétique, Environnement et Protection des Dr. Jean-Christophe Simon Plantes, UMR INRA, Agrocampus Ouest, Université de Rapporteur Rennes I, Rennes, France Royal Belgian Institute of Natural Science, Freshwater Prof. Isa Schön Rapporteur Biology, Bruxelles, Belgique Ecologie et Biologie des Interactions, UMR: CNRS, Dr. Richard Cordaux Rapporteur Université de Poitiers, Poitiers, France Institut de Pharmacologie Moléculaire et Cellulaire, UMR: Dr. Pascal Barbry CNRS, Université de Nice - Sophia Antipolis, Sophia Examinateur Antipolis, France Institut Sophia Agrobiotech, UMR: INRA, Université de Prof. Marylène Poirié Examinateur Nice - Sophia Antipolis, CNRS, Sophia Antipolis, France Institut Sophia Agrobiotech, UMR: INRA, Université de Dr. Pierre Abad Examinateur Nice - Sophia Antipolis, CNRS, Sophia Antipolis, France Table of Contents 1 Scientific and agronomic context .................................................................................................... 1 1.1 Nematodes .............................................................................................................................. 1 1.2 Evolution of plant parasitism in nematodes ........................................................................... 4 1.3 Economic impact of plant-parasitic nematodes ...................................................................... 5 1.4 Root-knot nematodes.............................................................................................................. 7 1.5 Genomes and transcriptomes of plant-parasitic nematodes.................................................. 9 2 Research Topics ............................................................................................................................. 11 2.1 Genomic signatures of adaptation to plant parasitism in nematodes .................................. 12 2.1.1 Lateral gene transfers .................................................................................................... 15 2.1.2 Parasitism genes specific to nematodes ....................................................................... 25 2.2 Genome evolution in an asexually-reproducing animal ....................................................... 32 2.2.1 A genome mainly composed of pairs of regions re-arranged along scaffolds. ............. 32 2.2.2 A high proportion of mobile elements and repeats. ..................................................... 37 3 Perspectives, projects and future directions ................................................................................. 39 3.1 New target genes for the development of specific control methods against root-knot nematodes ......................................................................................................................................... 39 3.2 Origin of the genome structure observed in M. incognita .................................................... 40 3.3 Biological consequences of a genome structure in copies .................................................... 43 3.4 Genome evolution and adaptation in asexually-reproducing animal lineages ..................... 45 3.5 Upcoming plant-parasitic nematode genomes and transcriptomes .................................... 48 4 Concluding remarks ....................................................................................................................... 51 5 Curriculum Vitae ............................................................................................................................ 52 6 Bibliography ................................................................................................................................... 59 7 Selected Publications..................................................................................................................... 68 Index of illustrations Figure 1 Schematic phylogeny of Nematoda .......................................................................................... 3 Figure 2 Life cycle of parthenogenetic root-knot nematodes ................................................................. 8 Figure 3 Plant-parasitic nematodes viewed as gene-stealers ............................................................... 19 Figure 4 Roles and origin of genes acquired via LGT in plant-parasitic nematodes .............................. 21 Figure 5 Topology searched to identify LGT in root-knot nematode genomes .................................... 23 Figure 6 Species included in the NEMATARGETS OrthoMCL filtering step ........................................... 28 Figure 7 M. incognita developmental life stages used for illumina sequencing. .................................. 30 Figure 8. M. incognita peculiar genome structure ................................................................................ 34 Figure 9. Re-arranged genome of Adineta vaga showing absence of chromosome-scale synteny ..... 36 Figure 10 Proportion of repetitive elements in nematode genomes ................................................... 37 Figure 11. Relative phylogenetic position of the six animal lineages containing asexual species ........ 47 Index of tables Table 1 Damages caused by plant-parasitic nematodes to crops annually in billion € ........................... 6 Table 2 Putative plant cell wall-degrading enzymes in nematode genomes ........................................ 13 Table 3 Putative detoxification genes in M. incognita and C. elegans .................................................. 14 Table 4 Putative chitinases and chitin-binding proteins in nematode genomes .................................. 14 Table 5 Highest similarities to M. incognita proteins active on plant sugars. ...................................... 16 Table 6 "Orphan" genes in M. incognita potentially contain novel parasitism genes .......................... 26 Résumé : évolution génomique et adaptations au parasitisme des plantes chez les nématodes Les nématodes sont des vers ronds non segmentés pour la plupart translucides et mesurant moins d'un mm. Bien que peu visibles, ils constituent l'un des groupes d'animaux les plus riches en espèces et en individus. La majorité des nématodes sont des espèces libres se nourrissant de bactéries ou de champignons mais les espèces les plus connues de l'homme sont les parasites d'animaux et de plantes. Les nématodes parasites de plantes causent des dégâts considérables à l'agriculture mondiale. Ils sont responsables de pertes économiques avoisinant une centaine de milliards d'euros par an. Le parasitisme des plantes est apparu au moins quatre fois indépendamment au cours de l'histoire évolutive des nématodes. Des similitudes morphologiques ont émergé de manière convergente chez ces parasites et il est possible que des singularités caractéristiques se retrouvent également dans leurs génomes. Le premier génome d'un nématode parasite de plantes, celui du nématode à galles Meloidogyne incognita a été séquencé et annoté en 2008 dans le cadre d'un consortium international coordonné par notre équipe. Dès lors, la comparaison avec les génomes d'autres nématodes a permis de révéler des singularités pouvant êtres liées à une adaptation au parasitisme des plantes. Une partie importante de ma recherche est consacrée à l'identification de singularités dans les génomes de nématodes, en lien avec le parasitisme des plantes. J'ai pu montrer que les nématodes avaient acquis, par transferts horizontaux, des gènes d'origines bactérienne et fongique impliqués dans le succès parasitaire (effecteurs). Ces événements évolutifs, considérés comme très rares chez les animaux, auraient joué un rôle important dans l'adaptation au parasitisme des plantes. La comparaison des génomes de parasites de plantes à ceux d'autres eukaryotes nous a également permis de mettre en évidence un jeu de gènes absents de toutes les autres espèces. Cette spécificité aux phyto-parasites, suggère que ces gènes seraient impliqués dans le parasitisme des plantes. Nos travaux ont montré que l'inactivation de ces gènes atténuait considérablement le succès parasitaire des nématodes. Etant absents des génomes d'autres espèces, ces gènes constituent des cibles particulièrement intéressants pour le développement de nouvelles méthode de luttes plus spécifiques. Une autre singularité du génome de Meloidogyne incognita, concerne sa structure. En effet, le génome
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