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Evolutionary history predicts plant defense against an invasive pest.

ABSTRACT: It has long been hypothesized that invasive pests may be facilitated by the evolutionary naïveté of their new hosts, but this prediction has never been examined in a phylogenetic framework. To address the hypothesis, we have been studying the invasive viburnum leaf beetle (Pyrrhalta viburni), which is decimating North American native species of Viburnum, a clade of worldwide importance as understory shrubs and ornamentals. In a phylogenetic field experiment using 16 species of Viburnum, we show that old-world Viburnum species that evolved in the presence of Pyrrhalta beetles mount a massive defensive wound response that crushes eggs of the pest insect; in contrast, naïve North American species that share no evolutionary history with Pyrrhalta beetles show a markedly lower response. This convergent continental difference in the defensive response of Viburnum spp. against insect oviposition contrasts with little difference in the quality of leaves for beetle larvae. Females show strong oviposition preferences that correspond with larval performance regardless of continental origin, which has facilitated colonization of susceptible North American species. Thus, although much attention has been paid to escape from enemies as a factor in the establishment and spread of nonnative organisms, the colonization of undefended resources seems to play a major role in the success of invasive species such as the viburnum leaf beetle.

SUBMITTER: Desurmont GA

PROVIDER: S-EPMC3084082 | biostudies-other | 2011 Apr

REPOSITORIES: biostudies-other

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Evolutionary history predicts plant defense against an invasive pest.

Desurmont Gaylord A GA Donoghue Michael J MJ Clement Wendy L WL Agrawal Anurag A AA

Proceedings of the National Academy of Sciences of the United States of America 20110411 17

It has long been hypothesized that invasive pests may be facilitated by the evolutionary naïveté of their new hosts, but this prediction has never been examined in a phylogenetic framework. To address the hypothesis, we have been studying the invasive viburnum leaf beetle (Pyrrhalta viburni), which is decimating North American native species of Viburnum, a clade of worldwide importance as understory shrubs and ornamentals. In a phylogenetic field experiment using 16 species of Viburnum, we show ...[more]

PMID: 21482779

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Project description:BackgroundSorbitol dehydrogenase (SDH, EC 1.1.1.14) is the key enzyme involved in sorbitol metabolism in higher plants. SDH genes in some Rosaceae species could be divided into two groups. L-idonate-5-dehydrogenase (LIDH, EC 1.1.1.264) is involved in tartaric acid (TA) synthesis in Vitis vinifera and is highly homologous to plant SDHs. Despite efforts to understand the biological functions of plant SDH, the evolutionary history of plant SDH genes and their phylogenetic relationship with the V. vinifera LIDH gene have not been characterized.ResultsA total of 92 SDH genes were identified from 42 angiosperm species. SDH genes have been highly duplicated within the Rosaceae family while monocot, Brassicaceae and most Asterid species exhibit singleton SDH genes. Core Eudicot SDHs have diverged into two phylogenetic lineages, now classified as SDH Class I and SDH Class II. V. vinifera LIDH was identified as a Class II SDH. Tandem duplication played a dominant role in the expansion of plant SDH family and Class II SDH genes were positioned in tandem with Class I SDH genes in several plant genomes. Protein modelling analyses of V. vinifera SDHs revealed 19 putative active site residues, three of which exhibited amino acid substitutions between Class I and Class II SDHs and were influenced by positive natural selection in the SDH Class II lineage. Gene expression analyses also demonstrated a clear transcriptional divergence between Class I and Class II SDH genes in V. vinifera and Citrus sinensis (orange).ConclusionsPhylogenetic, natural selection and synteny analyses provided strong support for the emergence of SDH Class II by positive natural selection after tandem duplication in the common ancestor of core Eudicot plants. The substitutions of three putative active site residues might be responsible for the unique enzyme activity of V. vinifera LIDH, which belongs to SDH Class II and represents a novel function of SDH in V. vinifera that may be true also of other Class II SDHs. Gene expression analyses also supported the divergence of SDH Class II at the expression level. This study will facilitate future research into understanding the biological functions of plant SDHs.

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Evolutionary history predicts plant defense against an invasive pest.

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Evolutionary history predicts plant defense against an invasive pest.

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