Mechanisms of Resistance to Insect Herbivores in Isolated Breeding Lineages of Cucurbita pepo
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Although crop wild ancestors are often reservoirs of resistance traits lost during domestication, examining diverse cultivated germplasm may also reveal novel resistance traits due to distinct breeding histories. Using ten cultivars from two independent domestication events of Cucurbita pepo (ssp. pepo and texana), we identified divergences in constitutive and induced resistance measured by growth of generalist caterpillars and leaf traits. C. p. texana cultivars were consistently more resistant to Trichoplusia ni and Spodoptera exigua, and this was not due to expected mechanisms including cucurbitacins, nitrogen, sticky phloem sap, or toxicity. Although more susceptible on average, C. p. pepo cultivars showed stronger induced resistance, suggesting a trade-off between constitutive and induced resistance. To test the hypothesis that leaf volatiles accounted for differences in resistance to caterpillars, we devised a novel method to evaluate resistance on artificial diet while larvae are exposed to leaf volatiles. In both subspecies, cultivar-specific induced volatiles that reduced T. ni growth were present in highly inducible cultivars, but absent in those that showed no induction. These results have important agricultural implications as cultivar-specific resistance to caterpillars mirrored that of specialist beetles from field trials. Overall, the eponymous cucurbitacin defenses of the Cucurbitaceae are not the mechanistic basis of differences in constitutive or induced resistance between C. pepo subspecies or cultivars. Instead, deterrent cultivar-specific volatiles appear to provide general resistance to insect herbivores. Divergence during breeding history within and between subspecies revealed this pattern and novel resistance mechanism, defining new targets for plant breeding.
KeywordsCucurbita pepo Cucurbitacins Herbivore induced plant volatiles Plant-herbivore interactions Trichoplusia ni
We thank Wendy Kain and Ping Wang for providing T. ni, Georg Jander for providing S. exigua, William Holdsworth for assistance with cultivar selection, Amy Hastings for supporting laboratory and greenhouse work, Katalin Boroczky for development of HPLC-MS methods for cucurbitacin detection, Taylor Anderson for development of cucurbitacin solid phase extraction protocol, and the Cornell University Agricultural Experiment Station greenhouse staff for providing excellent care of plant material. The manuscript was improved by thoughtful comments from Katja Poveda and two anonymous reviewers. LB was supported by a Cornell University Presidential Life Science Fellowship (2014-2015) and a Seed Matters Graduate Student Fellowship (2015-2019). This work was supported by the United States Department of Agriculture National Institute of Food and Agriculture Multi-State Hatch Project 1008470, Harnessing Chemical Ecology to Address Agricultural Pest and Pollinator Priorities.
LB was supported by a Cornell University Presidential Life Science Fellowship (2014–2015), and a Seed Matters Graduate Student Fellowship (2015–2019). This work was supported by the USDA National Institute of Food and Agriculture, Multi-State Hatch Project 1008470, Harnessing Chemical Ecology to Address Agricultural Pest and Pollinator Priorities.
Compliance with Ethical Standards
Conflict of Interest
LB and AA declare that they have no conflict of interest. MM is the co-founder of, but has no financial stake in, Row 7, a company that sells organic seed.
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