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

Abstract

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.

Keywords: ecology; epigenetics; evolution; herbivory.

Fig. 1.

Depiction of the full factorial experimental design of herbivore induction across two generations to study current and transgenerational effects of herbivory on plant defenses during ontogeny. First, an F1 generation of half-sib plants from a noninduced grandmaternal family (P) was produced. Mother plants (F1) were then either subjected to herbivory by P. rapae (H and caterpillar icon) or never exposed to herbivory (N, and icon crossed out). We then grew their progenies (F2), which were also subjected to herbivory or kept naïve to study plant responses to herbivory (inducibility, transgenerational induction, and transgenerational priming) at seedling (gray plant icons) and reproductive (black plant icons) stages.

Fig. 2.

Effect of herbivory experienced by mother plants and their offspring on the methylation probability per locus in 402 genome makers of 94 wild radishes after the occurrence of a 2 wk herbivory event. The first letter refers to the maternal treatment and the second letter the current or progeny treatment. For example, HN refers to a naïve offspring from a mother that was attacked by herbivory (“H,” caterpillar icon). Asterisks indicate statistically significant results of pairwise contrasts (with P < 0.05). Bars indicate SE.

Fig. 3.

Plant defense plasticity across life stages. Intra- and intergenerational defense of plants experiencing herbivory (H) or no herbivory (N). Ontogenetic changes in constitutive defenses are shown through differences between naïve seedlings and adults (A). Inducibility is shown by exposing the progeny of naïve mothers to herbivory and examining changes between seedlings and adults in induced physical and chemical antiherbivore defenses (A). Transgenerational induction is shown by comparing the progeny of both attacked and naïve mother plants (B). Transgenerational priming is examined by comparing attacked and nonattacked progeny of both attacked and naïve mother plants (C). Asterisks indicate statistically significant results of pairwise contrasts (with P < 0.05) within each model. Bars indicate means ± SE. Statistical significance of the main effects and interactions is indicated in Table 2.