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Genome Biol. 2017 Feb 13;18(1):27. doi: 10.1186/s13059-016-1145-3.

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

Author information

1
Earlham Institute, Norwich Research Park, Norwich, NR4 7UZ, UK.
2
The International Aphid Genomics Consortium, Miami, USA.
3
John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK.
4
INRA, UMR 1349 IGEPP (Institute of Genetics Environment and Plant Protection), Domaine de la Motte, 35653, Le Rheu Cedex, France.
5
IRISA/INRIA, GenOuest Core Facility, Campus de Beaulieu, Rennes, 35042, France.
6
Univ Lyon, INSA-Lyon, INRA, BF2I, UMR0203, F-69621, Villeurbanne, France.
7
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.
8
School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, NR4 7TJ, UK.
9
CNRS, UMR 6290, Institut de Génétique et Developpement de Rennes, Université de Rennes 1, 2 Avenue du Pr. Léon Bernard, 35000, Rennes, France.
10
Department of Biology, University of Miami, Coral Gables, FL, 33146, USA.
11
Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Dr. Aiguader 88, Barcelona, 08003, Spain.
12
Universitat Pompeu Fabra (UPF), 08003, Barcelona, Spain.
13
Institució Catalana de Recerca i Estudis Avançats (ICREA), Pg. Lluís Companys 23, 08010, Barcelona, Spain.
14
Present address: Rothamsted Research, Harpenden, Hertforshire, ALF5 2JQ, UK.
15
Present address: J. R. Simplot Company, Boise, ID, USA.
16
Present address: Alson H. Smith Jr. Agriculture and Extension Center, Virginia Tech, Winchester, 22602, VA, USA.
17
Present address: Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge, CB2 3EA, UK.
18
Unité de Recherche Génomique-Info (URGI), INRA, Université Paris-Saclay, 78026, Versailles, France.
19
Present address: Moredun Research Institute, Pentlands Science Park, Bush Loan, Penicuik, Midlothian, EH26 0PZ, UK.
20
INRA, UMR BGPI, CIRAD TA-A54K, Campus International de Baillarguet, 34398, Montpellier Cedex 5, France.
21
Boyce Thompson Institute for Plant Research, Ithaca, NY, 14853, USA.
22
School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich, NR4 7TJ, UK.
23
Earlham Institute, Norwich Research Park, Norwich, NR4 7UZ, UK. david.swarbreck@earlham.ac.uk.
24
The International Aphid Genomics Consortium, Miami, USA. david.swarbreck@earlham.ac.uk.
25
School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich, NR4 7TJ, UK. david.swarbreck@earlham.ac.uk.
26
John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK. saskia.hogenhout@jic.ac.uk.
27
The International Aphid Genomics Consortium, Miami, USA. saskia.hogenhout@jic.ac.uk.
28
School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich, NR4 7TJ, UK. saskia.hogenhout@jic.ac.uk.

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.

KEYWORDS:

Gene duplication; Genome sequence; Hemiptera; Myzus persicae; Parasite; Plasticity; RNA interference (RNAi); Sap-feeding insects; Transcriptome

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