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

Mathers, Thomas C., Chen, Yazhou, Kaithakottil, Gemy, Legeai, Fabrice, Mugford, Sam T., Baa-Puyoulet, Patrice, Bretaudeau, Anthony, Clavijo, Bernardo, Colella, Stefano, Collin, Olivier, Dalmay, Tamas ORCID: https://orcid.org/0000-0003-1492-5429, Derrien, Thomas, Feng, Honglin, Gabaldón, Toni, Jordan, Anna, Julca, Irene, Kettles, Graeme J., Kowitwanich, Krissana, Lavenier, Dominique, Lenzi, Paolo, Lopez-Gomollon, Sara, Loska, Damian, Mapleson, Daniel, Maumus, Florian, Moxon, Simon ORCID: https://orcid.org/0000-0003-4644-1816, Price, Daniel R. G., Sugio, Akiko, van Munster, Manuella, Uzest, Marilyne, Waite, Darren, Jander, Georg, Tagu, Denis, Wilson, Alex C. C., van Oosterhout, Cock ORCID: https://orcid.org/0000-0002-5653-738X, Swarbreck, David and Hogenhout, Saskia A. (2017) Rapid transcriptional plasticity of duplicated gene clusters enables a clonally reproducing aphid to colonise diverse plant species. Genome Biology, 18. ISSN 1474-760X

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Abstract

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.

Item Type:	Article
Additional Information:	Erratum available at dx.doi.org/10.1186/s13059-017-1202-6
Uncontrolled Keywords:	plasticity,genome sequence,myzus persicae,transcriptome,gene duplication,rna interference (rnai),hemiptera,parasite,sap-feeding insects
Faculty \ School:	Faculty of Science > School of Biological Sciences Faculty of Science > School of Environmental Sciences
UEA Research Groups:	Faculty of Science > Research Groups > Plant Sciences Faculty of Science > Research Centres > Centre for Ecology, Evolution and Conservation
Depositing User:	Pure Connector
Date Deposited:	15 Feb 2017 02:22
Last Modified:	09 May 2024 10:30
URI:	https://ueaeprints.uea.ac.uk/id/eprint/62608
DOI:	10.1186/s13059-016-1145-3

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