What happens in the pith stays in the pith: tissue‐localized defense responses facilitate chemical niche differentiation between two spatially separated herbivores

Abstract

Herbivore attack is known to elicit systemic defense responses that spread throughout the host plant and influence the performance of other herbivores. While these plant-mediated indirect competitive interactions are well described, and the co-existence of herbivores from different feeding guilds is common, the mechanisms of co-existence are poorly understood. In both field and glasshouse experiments with a native tobacco, Nicotiana attenuata, we found no evidence of negative interactions when plants were simultaneously attacked by two spatially separated herbivores: a leaf chewer Manduca sexta and a stem borer Trichobaris mucorea. T. mucorea attack elicited jasmonic acid (JA) and jasmonoyl-l-isoleucine bursts in the pith of attacked stems similar to those that occur in leaves when M. sexta attacks N. attenuata leaves. Pith chlorogenic acid (CGA) levels increased 1000-fold to levels 6-fold higher than leaf levels after T. mucorea attack; these increases in pith CGA levels, which did not occur in M. sexta-attacked leaves, required JA signaling. With plants silenced in CGA biosynthesis (irHQT plants), CGA, as well as other caffeic acid conjugates, was demonstrated in both glasshouse and field experiments to function as a direct defense protecting piths against T. mucorea attack, but not against leaf chewers or sucking insects. T. mucorea attack does not systemically activate JA signaling in leaves, while M. sexta leaf-attack transiently induces detectable but minor pith JA levels that are dwarfed by local responses. We conclude that tissue-localized defense responses allow tissue-specialized herbivores to share the same host and occupy different chemical defense niches in the same hostplant.

Elicitor and Receptor Molecules: Orchestrators of Plant Defense and Immunity

“…Unlike prosystemin, Pep epitopes are in the C-terminus of PROPEP, and these epitopes recognize class XI LRR-RLKs PEPR1/PEPR2 in A. thaliana. The Pep-PERR complex activates broad-spectrum resistance against pathogens, nematodes, and insects [22,[315][316][317][318]. In addition, the lack of an N-terminal on PROPEP implies that this protein is released through membrane damage [319].…”

“…To date, more plasma membrane receptor molecules have been identified for PAMPs, while MAMP-related receptors have not been reported. In theory, MAMPs would also require some form of binding site for the activation of the defense response [34,145,318,[344][345][346]. The same is true of DAMPs and HAMPs, where little is known on receptors and the receptor-elicitor interactions.…”

Priming and filtering of antiherbivore defences among Nicotiana attenuata plants connected by mycorrhizal networks

“…Verified defensive metabolites in N. attenuata were analysed to evaluate if the priming of the W + OS-elicited JA burst was translated into amplified defence responses. Rutin, nicotine, and chlorogenic acid (CGA) were selected as noninducible compounds (Lee, Joo, Kim, & Baldwin, 2017;Li et al, 2017), and as expected, they were nearly at the same levels after OS treatment within the four groups ( Figure 6).…”

“…Verified defensive metabolites in N. attenuata were analysed to evaluate if the priming of the W + OS‐elicited JA burst was translated into amplified defence responses. Rutin, nicotine, and chlorogenic acid (CGA) were selected as noninducible compounds (Lee, Joo, Kim, & Baldwin, ; Li et al, ), and as expected, they were nearly at the same levels after OS treatment within the four groups (Figure ). Although W + OS‐elicited larger Arg levels in the “receiver 2” plants of the group T mesocosm plants (Figure ), one of its down‐stream products, CGA did not differ significantly among the elicited plants of the four mesocosms (Figure ).…”

Using natural variation to achieve a whole‐plant functional understanding of the responses mediated by jasmonate signaling

“…Different variants of the canonical JA signaling cascade will activate different metabolites in a tissue-specific manner. For example, chlorogenic acid is specifically upregulated in the pith of stems when larvae of the pith-feeding weevil Trichobaris mucorea attack stems of N. attenuata, the regulation of which is locally mediated by JA (Lee et al, 2017). Interestingly, this phenolic is neither regulated by JA nor elicited by herbivory in tissues other than the pith, such as leaves, where it functions as a 'sun screen' that accumulates in response to UVB exposure (Ballar e et al, 1996;Ðinh et al, 2013).…”