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

Abstract

BackgroundThe 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.ResultsTo 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.ConclusionsPrevious 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-016-1145-3) contains supplementary material, which is available to authorized users.

Identification of the prothoracicotropic hormone (Ptth) coding gene and localization of its site of expression in the pea aphid Acyrthosiphon pisum

“…Aiming at identifying the gene encoding the neurohormone PTTH in aphids, amino acid sequences NP_001285550.1 and NP_001037349.1, described as D. melanogaster and B. mori PTTH, respectively, were used in BlastP searches against the A. pisum RefSeq peptides available from NCBI (https://www.ncbi.nlm.nih.gov/) and A. pisum predictions available in the Aphidbase database (http://bipaa.genouest.org/is/aphidbase/acyrthosiphon_pisum/). The identified A. pisum sequence was used to search for similar sequences in the genome of the aphid M. persicae (http://bipaa.genouest.org/is/aphidbase/myzus_persicae/; Mathers et al ., ). The identified aphid sequences were aligned with a set of PTTH protein sequences including representatives of several insect orders.…”

Integrative transcriptomic and genomic analysis of odorant binding proteins and chemosensory proteins in aphids

“…Insect CSPs, on other hand, have four conserved cysteines that are linked to form disulphide bridges (Angeli et al ., ). So far, the genomic sequences of four aphid species have been published: the pea aphid Acyrthosiphon pisum (The International Aphid Genomics Consortium, ), the Russian wheat aphid Diuraphis noxia (Nicholson et al ., ), the green peach aphid M. persicae (Mathers et al ., ) and the soybean aphid Aphis glycines (Wenger et al ., ). Meanwhile, the transcriptomic data of several aphid species are also available (Gu et al ., ; Xue et al ., ).…”

Interplay of Plasma Membrane and Vacuolar Ion Channels, Together with BAK1, Elicits Rapid Cytosolic Calcium Elevations in Arabidopsis during Aphid Feeding

“…persicae is a significant agricultural pest due to its highly polyphagous nature (Blackman and Eastop, 2000;Schoonhoven et al, 2005;Blackman and Eastop, 2007;Mathers et al, 2017). Aphids pierce plant tissue using specialized mouthparts, called stylets, to establish long-term feeding from the phloem (Dixon, 1998).…”