Cultivar-Specific Defense Responses in Wild and Cultivated Squash Induced by Belowground and Aboveground Herbivory

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Plant domestication often alters plant traits, including chemical and physical defenses against herbivores. In squash, domestication leads to reduced levels of cucurbitacins and leaf trichomes, influencing interactions with insects. However, the impact of domestication on inducible defenses in squash remains poorly understood. Here, we investigated the chemical and physical defensive traits of wild and domesticated squash (Cucurbita argyrosperma), and compared their responses to belowground and aboveground infestation by the root-feeding larvae and the leaf-chewing adults of the banded cucumber beetle Diabrotica balteata (Coleoptera: Chrysomelidae). Wild populations contained cucurbitacins in roots and cotyledons but not in leaves, whereas domesticated varieties lacked cucurbitacins in all tissues. Belowground infestation by D. balteata larvae did not increase cucurbitacin levels in the roots but triggered the expression of cucurbitacin biosynthetic genes, irrespective of domestication status, although the response varied among different varieties. Conversely, whereas wild squash had more leaf trichomes than domesticated varieties, the induction of leaf trichomes in response to herbivory was greater in domesticated plants. Leaf herbivory varied among varieties but there was a trend of higher leaf damage on wild squash than domesticated varieties. Overall, squash plants responded to both belowground and aboveground herbivory by activating chemical defense-associated gene expression in roots and upregulating their physical defense in leaves, respectively. While domestication suppressed both chemical and physical defenses, our findings suggest that it may enhance inducible defense mechanisms by increasing trichome induction in response to herbivory.