title: Rapid transcriptional plasticity of duplicated gene clusters enables a clonally reproducing aphid to colonise diverse plant species.
abstract: 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.
  
  
  
  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.
  
  
  
  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.
authors.affiliation: Earlham Institute, Norwich Research Park, Norwich, NR4 7UZ, UK.|The International Aphid Genomics Consortium, Miami, USA.
authors.forename: Thomas C
authors.initials: TC
authors.lastname: Mathers
authors.affiliation: John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK.|The International Aphid Genomics Consortium, Miami, USA.
authors.forename: Yazhou
authors.initials: Y
authors.lastname: Chen
authors.affiliation: Earlham Institute, Norwich Research Park, Norwich, NR4 7UZ, UK.
authors.forename: Gemy
authors.initials: G
authors.lastname: Kaithakottil
authors.affiliation: The International Aphid Genomics Consortium, Miami, USA.|INRA, UMR 1349 IGEPP (Institute of Genetics Environment and Plant Protection), Domaine de la Motte, 35653, Le Rheu Cedex, France.|IRISA/INRIA, GenOuest Core Facility, Campus de Beaulieu, Rennes, 35042, France.
authors.forename: Fabrice
authors.initials: F
authors.lastname: Legeai
authors.affiliation: John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK.|The International Aphid Genomics Consortium, Miami, USA.
authors.forename: Sam T
authors.initials: ST
authors.lastname: Mugford
authors.affiliation: The International Aphid Genomics Consortium, Miami, USA.|Univ Lyon, INSA-Lyon, INRA, BF2I, UMR0203, F-69621, Villeurbanne, France.
authors.forename: Patrice
authors.initials: P
authors.lastname: Baa-Puyoulet
authors.affiliation: The International Aphid Genomics Consortium, Miami, USA.|INRA, UMR 1349 IGEPP (Institute of Genetics Environment and Plant Protection), Domaine de la Motte, 35653, Le Rheu Cedex, France.|IRISA/INRIA, GenOuest Core Facility, Campus de Beaulieu, Rennes, 35042, France.
authors.forename: Anthony
authors.initials: A
authors.lastname: Bretaudeau
authors.affiliation: Earlham Institute, Norwich Research Park, Norwich, NR4 7UZ, UK.
authors.forename: Bernardo
authors.initials: B
authors.lastname: Clavijo
authors.affiliation: The International Aphid Genomics Consortium, Miami, USA.|Univ Lyon, INSA-Lyon, INRA, BF2I, UMR0203, F-69621, Villeurbanne, France.|Present Address: INRA, UMR1342 IRD-CIRAD-INRA-SupAgro-Université de Montpellier, Laboratoire des Symbioses Tropicales et Méditéranéennes, Campus International de Baillarguet, TA-A82/J, F-34398, Montpellier cedex 5, France.
authors.forename: Stefano
authors.initials: S
authors.lastname: Colella
authors.affiliation: IRISA/INRIA, GenOuest Core Facility, Campus de Beaulieu, Rennes, 35042, France.
authors.forename: Olivier
authors.initials: O
authors.lastname: Collin
authors.affiliation: School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, NR4 7TJ, UK.
authors.forename: Tamas
authors.initials: T
authors.lastname: Dalmay
authors.affiliation: CNRS, UMR 6290, Institut de Génétique et Developpement de Rennes, Université de Rennes 1, 2 Avenue du Pr. Léon Bernard, 35000, Rennes, France.
authors.forename: Thomas
authors.initials: T
authors.lastname: Derrien
authors.affiliation: The International Aphid Genomics Consortium, Miami, USA.|Department of Biology, University of Miami, Coral Gables, FL, 33146, USA.
authors.forename: Honglin
authors.initials: H
authors.lastname: Feng
authors.affiliation: The International Aphid Genomics Consortium, Miami, USA.|Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Dr. Aiguader 88, Barcelona, 08003, Spain.|Universitat Pompeu Fabra (UPF), 08003, Barcelona, Spain.|Institució Catalana de Recerca i Estudis Avançats (ICREA), Pg. Lluís Companys 23, 08010, Barcelona, Spain.
authors.forename: Toni
authors.initials: T
authors.lastname: Gabaldón
authors.affiliation: John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK.
authors.forename: Anna
authors.initials: A
authors.lastname: Jordan
authors.affiliation: The International Aphid Genomics Consortium, Miami, USA.|Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Dr. Aiguader 88, Barcelona, 08003, Spain.|Universitat Pompeu Fabra (UPF), 08003, Barcelona, Spain.
authors.forename: Irene
authors.initials: I
authors.lastname: Julca
authors.affiliation: John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK.|Present address: Rothamsted Research, Harpenden, Hertforshire, ALF5 2JQ, UK.
authors.forename: Graeme J
authors.initials: GJ
authors.lastname: Kettles
authors.affiliation: John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK.|Present address: J. R. Simplot Company, Boise, ID, USA.
authors.forename: Krissana
authors.initials: K
authors.lastname: Kowitwanich
authors.affiliation: IRISA/INRIA, GenOuest Core Facility, Campus de Beaulieu, Rennes, 35042, France.
authors.forename: Dominique
authors.initials: D
authors.lastname: Lavenier
authors.affiliation: John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK.|Present address: Alson H. Smith Jr. Agriculture and Extension Center, Virginia Tech, Winchester, 22602, VA, USA.
authors.forename: Paolo
authors.initials: P
authors.lastname: Lenzi
authors.affiliation: School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, NR4 7TJ, UK.|Present address: Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge, CB2 3EA, UK.
authors.forename: Sara
authors.initials: S
authors.lastname: Lopez-Gomollon
authors.affiliation: The International Aphid Genomics Consortium, Miami, USA.|Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Dr. Aiguader 88, Barcelona, 08003, Spain.|Universitat Pompeu Fabra (UPF), 08003, Barcelona, Spain.
authors.forename: Damian
authors.initials: D
authors.lastname: Loska
authors.affiliation: Earlham Institute, Norwich Research Park, Norwich, NR4 7UZ, UK.
authors.forename: Daniel
authors.initials: D
authors.lastname: Mapleson
authors.affiliation: The International Aphid Genomics Consortium, Miami, USA.|Unité de Recherche Génomique-Info (URGI), INRA, Université Paris-Saclay, 78026, Versailles, France.
authors.forename: Florian
authors.initials: F
authors.lastname: Maumus
authors.affiliation: Earlham Institute, Norwich Research Park, Norwich, NR4 7UZ, UK.
authors.forename: Simon
authors.initials: S
authors.lastname: Moxon
authors.affiliation: The International Aphid Genomics Consortium, Miami, USA.|Department of Biology, University of Miami, Coral Gables, FL, 33146, USA.|Present address: Moredun Research Institute, Pentlands Science Park, Bush Loan, Penicuik, Midlothian, EH26 0PZ, UK.
authors.forename: Daniel R G
authors.initials: DR
authors.lastname: Price
authors.affiliation: John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK.|INRA, UMR 1349 IGEPP (Institute of Genetics Environment and Plant Protection), Domaine de la Motte, 35653, Le Rheu Cedex, France.
authors.forename: Akiko
authors.initials: A
authors.lastname: Sugio
authors.affiliation: The International Aphid Genomics Consortium, Miami, USA.|INRA, UMR BGPI, CIRAD TA-A54K, Campus International de Baillarguet, 34398, Montpellier Cedex 5, France.
authors.forename: Manuella
authors.initials: M
authors.lastname: van Munster
authors.affiliation: The International Aphid Genomics Consortium, Miami, USA.|INRA, UMR BGPI, CIRAD TA-A54K, Campus International de Baillarguet, 34398, Montpellier Cedex 5, France.
authors.forename: Marilyne
authors.initials: M
authors.lastname: Uzest
authors.affiliation: Earlham Institute, Norwich Research Park, Norwich, NR4 7UZ, UK.
authors.forename: Darren
authors.initials: D
authors.lastname: Waite
authors.affiliation: The International Aphid Genomics Consortium, Miami, USA.|Boyce Thompson Institute for Plant Research, Ithaca, NY, 14853, USA.
authors.forename: Georg
authors.initials: G
authors.lastname: Jander
authors.affiliation: The International Aphid Genomics Consortium, Miami, USA.|INRA, UMR 1349 IGEPP (Institute of Genetics Environment and Plant Protection), Domaine de la Motte, 35653, Le Rheu Cedex, France.
authors.forename: Denis
authors.initials: D
authors.lastname: Tagu
authors.affiliation: The International Aphid Genomics Consortium, Miami, USA.|Department of Biology, University of Miami, Coral Gables, FL, 33146, USA.
authors.forename: Alex C C
authors.initials: AC
authors.lastname: Wilson
authors.affiliation: The International Aphid Genomics Consortium, Miami, USA.|School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich, NR4 7TJ, UK.
authors.forename: Cock
authors.initials: C
authors.lastname: van Oosterhout
authors.affiliation: Earlham Institute, Norwich Research Park, Norwich, NR4 7UZ, UK. david.swarbreck@earlham.ac.uk.|The International Aphid Genomics Consortium, Miami, USA. david.swarbreck@earlham.ac.uk.|School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich, NR4 7TJ, UK. david.swarbreck@earlham.ac.uk.
authors.forename: David
authors.initials: D
authors.lastname: Swarbreck
authors.affiliation: John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK. saskia.hogenhout@jic.ac.uk.|The International Aphid Genomics Consortium, Miami, USA. saskia.hogenhout@jic.ac.uk.|School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich, NR4 7TJ, UK. saskia.hogenhout@jic.ac.uk.
authors.forename: Saskia A
authors.initials: SA
authors.lastname: Hogenhout
keywords: Gene duplication; Genome sequence; Hemiptera; Myzus persicae; Parasite; Plasticity; RNA interference (RNAi); Sap-feeding insects; Transcriptome