Divergence of defensive cucurbitacins in independent Cucurbita pepo domestication events leads to differences in specialist herbivore preference

Lauren J. Brzozowski, Michael A. Gore, Anurag A. Agrawal, Michael Mazourek

Research output: Contribution to journalArticlepeer-review

15 Scopus citations

Abstract

Crop domestication and improvement often concurrently affect plant resistance to pests and production of secondary metabolites, creating challenges for isolating the ecological implications of selection for specific metabolites. Cucurbitacins are bitter triterpenoids with extreme phenotypic differences between Cucurbitaceae lineages, yet we lack integrated models of herbivore preference, cucurbitacin accumulation, and underlying genetic mechanisms. In Cucurbita pepo, we dissected the effect of cotyledon cucurbitacins on preference of a specialist insect pest (Acalymma vittatum) for multiple tissues, assessed genetic loci underlying cucurbitacin accumulation in diverse germplasm and a biparental F2 population (from a cross between two independent domesticates), and characterized quantitative associations between gene expression and metabolites during seedling development. Acalymma vittatum affinity for cotyledons is mediated by cucurbitacins, but other traits contribute to whole-plant resistance. Cotyledon cucurbitacin accumulation was associated with population structure, and our genetic mapping identified a single locus, Bi-4, containing genes relevant to transport and regulation – not biosynthesis – that diverged between lineages. These candidate genes were expressed during seedling development, most prominently a putative secondary metabolite transporter. Taken together, these findings support the testable hypothesis that breeding for plant resistance to insects involves targeting genes for regulation and transport of defensive metabolites, in addition to core biosynthesis genes.

Original languageEnglish
Pages (from-to)2812-2825
Number of pages14
JournalPlant Cell and Environment
Volume43
Issue number11
DOIs
StatePublished - Nov 1 2020

Bibliographical note

Publisher Copyright:
© 2020 John Wiley & Sons Ltd

Keywords

  • Acalymma vittatum
  • plant-herbivore interactions
  • secondary metabolite
  • squash
  • terpenoid

ASJC Scopus subject areas

  • Physiology
  • Plant Science

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