Rapid transcriptional plasticity of duplicated gene clusters enables a clonally reproducing aphid to colonise diverse plant species

Thomas C. Mathers (1, 2) , Yazhou Chen (1, 2) , Gemy Kaithakottil (1) , Fabrice Legeai (3, 2, 4) , Sam T. Mugford (1, 2) , Patrice Baa-Puyoulet (2, 5) , Anthony Bretaudeau (2, 4, 3) , Bernardo Clavijo (1) , Stefano Colella (2, 5) , Olivier Collin (3) , Tamas Dalmay (1) , Thomas Derrien (6) , Honglin Feng (2, 7) , Toni Gabaldon (2, 8, 9, 10) , Anna Jordan (1) , Irene Julca (2, 8, 10) , Graeme J. Kettles (1) , Krissana Kowitwanich (1) , Dominique Lavenier (11) , Paolo Lenzi (1) , Sara Lopez-Gomollon (1) , Damian Loska (10, 2, 8) , Daniel Mapleson (1) , Florian Maumus (2, 12) , Simon Moxon (1) , Daniel R. G. Price (2, 7) , Akiko Sugio (1, 4) , Manuella van Munster (2, 13) , Marilyne Uzest (2, 13) , Darren Waite (1) , Georg Jander (2, 14) , Denis Tagu (2, 4) , Alex C. C. Wilson (2, 7) , Cock van Oosterhout (15) , David Swarbreck (1, 2, 15) , Saskia A. Hogenhout (1, 2, 15)

1 Norwich Research Park
2 IAGC - International Aphid Genomics Consortium
3 Plateforme bioinformatique GenOuest [Rennes]
4 IGEPP - Institut de Génétique, Environnement et Protection des Plantes
5 BF2I - Biologie Fonctionnelle, Insectes et Interactions
6 IGDR - Institut de Génétique et Développement de Rennes
7 University of Miami [Coral Gables]
8 UPF - Universitat Pompeu Fabra [Barcelona]
9 ICREA - Institució Catalana de Recerca i Estudis Avançats
10 CRG - Centre for Genomic Regulation
11 GenScale - Scalable, Optimized and Parallel Algorithms for Genomics
12 URGI - Unité de Recherche Génomique Info
13 UMR BGPI - Biologie et Génétique des Interactions Plante-Parasite
14 Boyce Thompson Institute [Ithaca]
15 UEA - University of East Anglia [Norwich]

BACKGROUND: The prevailing paradigm of host-parasite evolution is that arms races lead to increasing specialisation via genetic adaptation. Insect herbivores are no exception and the majority have evolved to colonise a small number of closely related host species. Remarkably, the green peach aphid, Myzus persicae, colonises plant species across 40 families and single M. persicae clonal lineages can colonise distantly related plants. This remarkable ability makes M. persicae a highly destructive pest of many important crop species. RESULTS: To investigate the exceptional phenotypic plasticity of M. persicae, we sequenced the M. persicae genome and assessed how one clonal lineage responds to host plant species of different families. We show that genetically identical individuals are able to colonise distantly related host species through the differential regulation of genes belonging to aphid-expanded gene families. Multigene clusters collectively upregulate in single aphids within two days upon host switch. Furthermore, we demonstrate the functional significance of this rapid transcriptional change using RNA interference (RNAi)-mediated knock-down of genes belonging to the cathepsin B gene family. Knock-down of cathepsin B genes reduced aphid fitness, but only on the host that induced upregulation of these genes. CONCLUSIONS: Previous research has focused on the role of genetic adaptation of parasites to their hosts. Here we show that the generalist aphid pest M. persicae is able to colonise diverse host plant species in the absence of genetic specialisation. This is achieved through rapid transcriptional plasticity of genes that have duplicated during aphid evolution.

Keywords: genome sequence; plasticity; hemiptera; gene duplication; parasite; rna interference (rnai); sap-feeding insects; transcriptome; myzus persicae

Domains: Life Sciences [q-bio]; Genetics

Thomas C. Mathers, Yazhou Chen, Gemy Kaithakottil, Fabrice Legeai, Sam T. Mugford, et al.. Rapid transcriptional plasticity of duplicated gene clusters enables a clonally reproducing aphid to colonise diverse plant species. Genome Biology, 2017, 18 (1), pp.27. ⟨10.1186/s13059-016-1145-3⟩. ⟨hal-01500475⟩