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A clonally reproducing generalist aphid pest colonises diverse host plants by rapid transcriptional plasticity of duplicated gene clusters

View ORCID ProfileThomas C Mathers, Yazhou Chen, Gemy Kaithakottil, Fabrice Legeai, Sam T Mugford, Patrice Baa-Puyoulet, Anthony Bretaudeau, Bernardo Clavijo, Stefano Colella, Olivier Collin, Tamas Dalmay, Thomas Derrien, Honglin Feng, Toni Gabaldón, Anna Jordan, Irene Julca, Graeme J Kettles, Krissana Kowitwanich, Dominique Lavenier, Paolo Lenzi, Sara Lopez-Gomollon, Damian Loska, Daniel Mapleson, Florian Maumus, Simon Moxon, Daniel R G Price, Akiko Sugio, Manuella van Munster, Marilyne Uzest, Darren Waite, Georg Jander, Denis Tagu, Alex C C Wilson, Cock van Oosterhout, David Swarbreck, Saskia A Hogenhout
doi: https://doi.org/10.1101/063610
Thomas C Mathers
Earlham Institute;
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Yazhou Chen
John Innes Centre;
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Gemy Kaithakottil
Earlham Institute;
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Fabrice Legeai
Institute of Genetics Environment and Plant Protection;
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Sam T Mugford
John Innes Centre;
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Patrice Baa-Puyoulet
INSA-Lyon;
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Anthony Bretaudeau
Institute of Genetics Environment and Plant Protection;
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Bernardo Clavijo
Earlham Institute;
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Stefano Colella
INSA-Lyon;
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Olivier Collin
IRISA/INRIA;
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Tamas Dalmay
University of East Anglia;
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Thomas Derrien
Institut de Génétique et Developpement de Rennes;
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Honglin Feng
University of Miami;
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Toni Gabaldón
Centre for Genomic Regulation;
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Anna Jordan
John Innes Centre;
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Irene Julca
Centre for Genomic Regulation;
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Graeme J Kettles
John Innes Centre;
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Krissana Kowitwanich
John Innes Centre;
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Dominique Lavenier
IRISA/INRIA;
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Paolo Lenzi
John Innes Centre;
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Sara Lopez-Gomollon
University of East Anglia;
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Damian Loska
Centre for Genomic Regulation;
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Daniel Mapleson
Earlham Institute;
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Florian Maumus
Unité de Recherche Génomique-Info;
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Simon Moxon
Earlham Institute;
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Daniel R G Price
University of Miami;
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Akiko Sugio
John Innes Centre;
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Manuella van Munster
UMR BGPI;
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Marilyne Uzest
UMR BGPI;
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Darren Waite
Earlham Institute;
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Georg Jander
Boyce Thompson Institute for Plant Research;
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Denis Tagu
Institute of Genetics Environment and Plant Protection;
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Alex C C Wilson
University of Miami;
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Cock van Oosterhout
University of East Anglia;
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David Swarbreck
Earlham Institute;
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Saskia A Hogenhout
Jaohn Innes Centre
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  • For correspondence: saskia.hogenhout@jic.ac.uk
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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 up-regulate 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 up-regulation 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.

Copyright 
The copyright holder for this preprint is the author/funder. It is made available under a CC-BY-NC-ND 4.0 International license.
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  • Posted July 19, 2016.

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A clonally reproducing generalist aphid pest colonises diverse host plants by rapid transcriptional plasticity of duplicated gene clusters
Thomas C Mathers, Yazhou Chen, Gemy Kaithakottil, Fabrice Legeai, Sam T Mugford, Patrice Baa-Puyoulet, Anthony Bretaudeau, Bernardo Clavijo, Stefano Colella, Olivier Collin, Tamas Dalmay, Thomas Derrien, Honglin Feng, Toni Gabaldón, Anna Jordan, Irene Julca, Graeme J Kettles, Krissana Kowitwanich, Dominique Lavenier, Paolo Lenzi, Sara Lopez-Gomollon, Damian Loska, Daniel Mapleson, Florian Maumus, Simon Moxon, Daniel R G Price, Akiko Sugio, Manuella van Munster, Marilyne Uzest, Darren Waite, Georg Jander, Denis Tagu, Alex C C Wilson, Cock van Oosterhout, David Swarbreck, Saskia A Hogenhout
bioRxiv 063610; doi: https://doi.org/10.1101/063610
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A clonally reproducing generalist aphid pest colonises diverse host plants by rapid transcriptional plasticity of duplicated gene clusters
Thomas C Mathers, Yazhou Chen, Gemy Kaithakottil, Fabrice Legeai, Sam T Mugford, Patrice Baa-Puyoulet, Anthony Bretaudeau, Bernardo Clavijo, Stefano Colella, Olivier Collin, Tamas Dalmay, Thomas Derrien, Honglin Feng, Toni Gabaldón, Anna Jordan, Irene Julca, Graeme J Kettles, Krissana Kowitwanich, Dominique Lavenier, Paolo Lenzi, Sara Lopez-Gomollon, Damian Loska, Daniel Mapleson, Florian Maumus, Simon Moxon, Daniel R G Price, Akiko Sugio, Manuella van Munster, Marilyne Uzest, Darren Waite, Georg Jander, Denis Tagu, Alex C C Wilson, Cock van Oosterhout, David Swarbreck, Saskia A Hogenhout
bioRxiv 063610; doi: https://doi.org/10.1101/063610

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