Phenotypic plasticity in plant defense across life stages: Inducibility, transgenerational induction, and transgenerational priming in wild radish

Abstract

Significance Herbivore attack on plants is known to elicit defensive responses. Such environmentally induced responses can also be expressed by the offspring of attacked plants via DNA methylation—an epigenetic response—but little is known about if and how epigenetic induction varies with plant ontogeny (e.g., seedlings, reproductive plants). Here, we report that herbivory by caterpillars induced changes in the plant epigenome and chemical and physical defenses within and across generations in wild radish. We show that herbivore offense in a plant’s generation affects its progeny’s deployment of defenses throughout its life cycle and that herbivory operates as an important and nuanced driver of phenotypic diversity in plant populations. As they develop, many plants deploy shifts in antiherbivore defense allocation due to changing costs and benefits of their defensive traits. Plant defenses are known to be primed or directly induced by herbivore damage within generations and across generations by long-lasting epigenetic mechanisms. However, little is known about the differences between life stages of epigenetically inducible defensive traits across generations. To help fill this knowledge gap, we conducted a multigenerational experiment to determine whether defense induction in wild radish plants was reflected in chromatin modifications (DNA methylation); we then examined differences between seedlings and reproductive plants in current and transgenerational plasticity in chemical (glucosinolates) and physical (trichomes) defenses in this species. Herbivory triggered genome methylation both in targeted plants and their offspring. Within one generation, both defenses were highly inducible at the seedling stage, but only chemical defenses were inducible in reproductive plants. Across generations, herbivory experienced by mother plants caused strong direct induction of physical defenses in their progeny, with effects lasting from seedling to reproductive stages. For chemical defenses, however, this transgenerational induction was evident only in adults. Transgenerational priming was observed in physical and chemical defenses, particularly in adult plants. Our results show that transgenerational plasticity in plant defenses in response to herbivore offense differs for physical and chemical defense and changes across plant life stages.