Caterpillars induce jasmonates in flowers and alter plant responses to a second attacker

Abstract

Summary In nature, herbivorous insects and plant pathogens are generally abundant when plants are flowering. Thus, plants face a diversity of attackers during their reproductive phase. Plant responses to one attacker can interfere with responses to a second attacker, and phytohormones that orchestrate plant reproduction are also involved in resistance to insect and pathogen attack. We quantified phytohormonal responses of flowering plants exposed to single or dual attack and studied resistance mechanisms of plants in the flowering stage.Flowering Brassica nigra were exposed to either a chewing caterpillar, a phloem‐feeding aphid or a bacterial pathogen, and plant hormonal responses were compared with dual attack situations. We quantified phytohormones in inflorescences and leaves, and determined the consequences of hormonal changes for components of direct and indirect plant resistance.Caterpillars were the main inducers of jasmonates in inflorescences, and the phytohormonal profile of leaves was not affected by either insect or pathogen attack. Dual attack increased plant resistance to caterpillars, but compromised resistance to aphids. Parasitoid performance was negatively correlated with the performance of their hosts.We conclude that plants prioritize resistance of reproductive tissues over vegetative tissues, and that a chewing herbivore species is the main driver of responses in flowering B. nigra.

Dual‐guild herbivory disrupts predator‐prey interactions in the field

“…Because defense induction varies considerably through time and across larval instars, (Clavijo McCormick et al 2014, Chr etien et al 2017, the limited exposure to caterpillars in the field experiment likely underestimates both the direct effects of induced secondary metabolites on aphids in the field and the indirect effects mediated by volatile induction. In the absence of natural enemies in the greenhouse, caterpillar feeding reduced aphid densities, consistent with asymmetrical competition arising from induced defenses in response to chewing injury (reviewed in Z€ ust and Agrawal 2017).…”

“…Importantly, the duration of chewing herbivory treatments was much shorter in the field experiment (72 h) compared with the greenhouse experiment (larvae fed until pupation). Because defense induction varies considerably through time and across larval instars, (Clavijo McCormick et al 2014, Chr etien et al 2017, the limited exposure to caterpillars in the field experiment likely underestimates both the direct effects of induced secondary metabolites on aphids in the field and the indirect effects mediated by volatile induction.…”

Quint Rusman

“…This approach is both invigorating and rewarding, which is apparent in both his experimental (Schiestl et al ., ) and theoretical work (Schiestl, ). Some more recent papers I wish to highlight are the works by Øystein H. Opedal on the evolutionary potential of plant traits (Opedal, ), and by Lucille Chretién and colleagues on plant‐mediated interactions with flowering plants (Chrétien et al ., ). Both papers highlight the fact that flowers are unique plant organs, and although plants function as one integrated unit, plant responses to herbivory are different in flowers compared to leaves (Chrétien et al ., ), and flowers have different evolutionary potential compared to vegetative tissues (Opedal, ).…”

Promises and challenges in insect–plant interactions

“…Future challenges include the following: 1 To integrate species interactions and related traits in multitrophic-multitrait systems at the scale of the entire community. Integrating studies of plant defence and plant reproduction will help to understand the factors that influence interactions of plants with various interactants (Lucas- Barbosa et al, 2016;Chr etien et al, 2018). Ideally, such approach should map the various effectors and elicitors from each partner acting across the networks.…”

“…3 To connect plant defence and reproduction. Integrating studies of plant defence and plant reproduction will help to understand the factors that influence interactions of plants with various interactants (Lucas- Barbosa et al, 2016;Chr etien et al, 2018). One important challenge nowadays is to understand pollinator decline (Biesmeijer et al, 2006), or even insect declines in general (Hallmann et al, 2017;Vogel, 2017) and the decline of ecosystem services such as pollination.…”