Mechanisms of Resistance to Insect Herbivores in Isolated Breeding Lineages of Cucurbita pepo

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

doi:10.1007/s10886-019-01046-8

Cited by 17 publications

(17 citation statements)

References 63 publications

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“…pepo (CPP) over C. pepo ssp. ovifera (CPO) (Brzozowski et al, 2016; Ferguson et al, 1983; Hoffmann et al, 1996), despite neither domesticate having cucurbitacins in leaf tissue (Brzozowski et al, 2019; Metcalf et al, 1980, 1982). We sought to isolate the effect of cotyledon cucurbitacins on herbivore preference from other factors associated with subspecies, like defence inducibility (Brzozowski et al, 2019) and morphological traits (Paris, Lebeda, Křistkova, Andres, & Nee, 2012).…”

Section: Discussionmentioning

confidence: 99%

“…Cucurbitacins were extracted from root, cotyledon, and leaf tissue at different developmental stages using protocols similar to (Brzozowski, Mazourek, & Agrawal, 2019), and detailed in Method S1. Briefly, fresh tissue was homogenized in methanol and purified by solid phase extraction.…”

Section: Cucurbitacin Extractionsmentioning

confidence: 99%

“…A positive Log2FoldChange value indicates greater expression in CPP, and negative corresponds to greater expression in CPO. The hypothesized role of genes in regulation ("R") or transport ("T") is given in the column "Role" having cucurbitacins in leaf tissue (Brzozowski et al, 2019;Metcalf et al, 1980Metcalf et al, , 1982. We sought to isolate the effect of cotyledon cucurbitacins on herbivore preference from other factors associated with subspecies, like defence inducibility (Brzozowski et al, 2019) and morphological traits (Paris, Lebeda, Křistkova, Andres, & Nee, 2012).…”

Section: Isolating Effects Of Cotyledon Cucurbitacins On Herbivore mentioning

confidence: 99%

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

Brzozowski

Gore

Agrawal

et al. 2020

Plant Cell & Environment

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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 F 2 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 wholeplant 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 regulationnot biosynthesisthat 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.

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Section: Discussionmentioning

confidence: 99%

Section: Cucurbitacin Extractionsmentioning

confidence: 99%

Section: Isolating Effects Of Cotyledon Cucurbitacins On Herbivore mentioning

confidence: 99%

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

Brzozowski

Gore

Agrawal

et al. 2020

Plant Cell & Environment

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“…These induced VOC blends convey additional information to herbivores about changes in environmental conditions. Plant VOCs also play important roles in direct defense against herbivores and pathogens, as some volatile compounds have toxic or anti-microbial properties [140] or deter foraging or oviposition by herbivores [141]. Plant volatiles induced by herbivore or pathogen attack also provide indirect protection for plants by recruiting herbivore natural enemies [142] or beneficial microbes [143].…”

Section: Olfactory Cuesmentioning

confidence: 99%

The Role of Plant-Associated Microbes in Mediating Host-Plant Selection by Insect Herbivores

Grunseich

Thompson

Aguirre

et al. 2019

Plants

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There is increasing evidence that plant-associated microorganisms play important roles in shaping interactions between plants and insect herbivores. Studies of both pathogenic and beneficial plant microbes have documented wide-ranging effects on herbivore behavior and performance. Some studies, for example, have reported enhanced insect-repellent traits or reduced performance of herbivores on microbe-associated plants, while others have documented increased herbivore attraction or performance. Insect herbivores frequently rely on plant cues during foraging and oviposition, suggesting that plant-associated microbes affecting these cues can indirectly influence herbivore preference. We review and synthesize recent literature to provide new insights into the ways pathogenic and beneficial plant-associated microbes alter visual, olfactory, and gustatory cues of plants that affect host-plant selection by insect herbivores. We discuss the underlying mechanisms, ecological implications, and future directions for studies of plant-microbial symbionts that indirectly influence herbivore behavior by altering plant traits.

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“…Herbivore-induced plant volatiles also directly defend plants against herbivores, reducing herbivore performance through toxic or deterrent properties (Brzozowski, Mazourek, & Agrawal, 2019;Veyrat, Robert, Turlings, & Erb, 2016). Furthermore, volatile production is often correlated or metabolically linked to other defences (Christensen et al, 2013).…”

Section: Hipvs As Honest Signals Of Reward and Riskmentioning

confidence: 99%

Risky roots and careful herbivores: Sustained herbivory by a root‐feeding herbivore attenuates indirect plant defences

et al. 2020

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Above‐ground plant tissues produce characteristic blends of volatile compounds in response to insect herbivory. These herbivore‐induced plant volatiles (HIPVs) function in plant defence and mediate foraging decisions by herbivores and their natural enemies. The ecological roles of HIPVs as foraging cues for different trophic levels highlight an important conflict for herbivores that need to locate suitable host plants while avoiding competition and predation. Plant roots also emit HIPVs following herbivory, but our understanding of root‐produced volatiles and their ecological functions in soil environments remains limited. Moreover, recent studies have documented the effects of temporal dynamics of plant volatile production on ecological interactions, but little is known about how root HIPVs change throughout herbivory or the resulting ecological implications from such changes. In this study, we examined the roles of HIPVs from roots of cucumber plants Cucumis sativus as foraging cues for a specialist herbivore, striped cucumber beetle Acalymma vittatum and its natural enemies, entomopathogenic nematodes (EPNs). We predicted HIPVs from A. vittatum‐damaged roots would attract EPNs, while repelling conspecific larvae that avoid competition, induced plant defences and increased risk of predation by EPNs. To capture the temporal dynamics of root HIPVs, we determined how HIPV‐mediated interactions change over time with sustained herbivory. Initially (after 24 hr), A. vittatum herbivory on C. sativus, or mechanical wounding, induced greater production of root volatiles. These root HIPVs recruited EPNs and repelled foraging A. vittatum larvae, although larval performance was not affected by prior damage. Sustained (7 days) herbivory by larvae reduced HIPVs to levels indistinguishable from undamaged control roots while mechanically damaged roots continued to produce higher levels of volatiles. Attenuation of HIPVs impaired indirect defence responses of C. sativus by reducing recruitment of EPNs and deterrence of A. vittatum larvae. These results suggest that root HIPVs function as honest signals that indicate the presence of herbivores, induction of indirect plant defences and increased risk of predation by natural enemies. However, some herbivores may overcome this line of plant defence by attenuating production of HIPVs and thus altering the outcomes of subsequent interactions among plants, herbivores and natural enemies. A free Plain Language Summary can be found within the Supporting Information of this article.

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Mechanisms of Resistance to Insect Herbivores in Isolated Breeding Lineages of Cucurbita pepo

Cited by 17 publications

References 63 publications

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

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

The Role of Plant-Associated Microbes in Mediating Host-Plant Selection by Insect Herbivores

Risky roots and careful herbivores: Sustained herbivory by a root‐feeding herbivore attenuates indirect plant defences

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