Flowers prepare thyselves: leaf and root herbivores induce specific changes in floral phytochemistry with consequences for plant interactions with florivores

Abstract

Summary The phenotypic plasticity of flowering plants in response to herbivore damage to vegetative tissues can affect plant interactions with flower‐feeding organisms. Such induced systemic responses are probably regulated by defence‐related phytohormones that signal flowers to alter secondary chemistry that affects resistance to florivores. Current knowledge on the effects of damage to vegetative tissues on plant interactions with florivores and the underlying mechanisms is limited. We compared the preference and performance of two florivores on flowering Brassica nigra plants damaged by one of three herbivores feeding from roots or leaves. To investigate the underlying mechanisms, we quantified expression patterns of marker genes for defence‐related phytohormonal pathways, and concentrations of phytohormones and glucosinolates in buds and flowers. Florivores displayed contrasting preferences for plants damaged by herbivores feeding on roots and leaves. Chewing florivores performed better on plants damaged by folivores, but worse on plants damaged by the root herbivore. Chewing root and foliar herbivory led to specific induced changes in the phytohormone profile of buds and flowers. This resulted in increased glucosinolate concentrations for leaf‐damaged plants, and decreased glucosinolate concentrations for root‐damaged plants. The outcome of herbivore–herbivore interactions spanning from vegetative tissues to floral tissues is unique for the inducing root/leaf herbivore and receiving florivore combination.

Chemodiversity in flowers of Tanacetum vulgare has consequences on a florivorous beetle

“…Previous research has mainly focused on investigating differences in chemical profiles of these chemotypes in relation to leaves, studying their consequences on herbivorous invertebrates and pathogens (Whitehead & Bowers 2013;Salazar et al 2016;Tewes & M€ uller 2020;. In contrast, there is limited knowledge regarding chemotypic variation in flowers and its consequences for mutualistic or antagonistic flower-visiting insects (Egan et al 2018;Eilers et al 2021;Kessler et al 2013;Rusman et al 2022).…”

Density-Dependent Effects of Simultaneous Root and Floral Herbivory on Plant Fitness and Defense

“…From the caterpillar perspective, it seems logical that flower number and GLS concentrations to some extent determine their development. Other pierid species such as Pieris brassicae preferably feed on GLS-rich reproductive tissues, in which they sustain higher growth rates [ 78 ], gain more weight [ 49 ], and probably increase their survival and fitness [ 85 ]. Indeed, faster development correlates with higher pupal mass in this species [ 64 ].…”

“…Through systemic induction of chemical defenses aboveground [ 29 , 46 ], and nutrient allocation to reproductive tissues [ 30 ], root herbivores can affect aboveground herbivore performance and damage on plants [ 47 , 48 , 49 , 50 ]. Less known are the effects of floral herbivores on herbivores belowground and their joint effects on plants.…”

“…Less known are the effects of floral herbivores on herbivores belowground and their joint effects on plants. Although probably very common in nature, few studies have investigated the effects of simultaneous root and floral herbivory [ 49 , 51 ], and even fewer have quantified their transgenerational effects in plants [ 52 ]. Herbivore-induced transgenerational effects such as changes in seedling emergence on offspring occur through alterations in maternal seed provisioning and/or modifications in inherited gene expression regulation between other mechanisms [ 53 , 54 , 55 , 56 , 57 , 58 ].…”

Insect trash is a plant’s treasure: effects of insect exuviae as soil amendment on pollinator performance and plant reproduction

“…It is known that the same phytohormones that mediate resistance to antagonists also influence plant reproduction (Chrétien et al, 2018). The induction of phytohormones by attackers can thus interfere with the regulation of plant reproduction (Chrétien et al, 2018;Rusman et al, 2021). Previous studies have demonstrated that upon herbivore attack flowering plants undergo primary and secondary metabolic changes in flowers, rather than in leaves (Lucas-Barbosa, 2016).…”