TOC1 in Nicotiana attenuata regulates efficient allocation of nitrogen to defense metabolites under herbivory stress

Abstract

The circadian clock contextualizes plant responses to environmental signals. Plants use temporal information to respond to herbivory, but many of the functional roles of circadian clock components in these responses, and their contribution to fitness, remain unknown. We investigate the role of the central clock regulator TIMING OF CAB EXPRESSION 1 (TOC1) in Nicotiana attenuata's defense responses to the specialist herbivore Manduca sexta under both field and glasshouse conditions. We utilize 15 N pulse-labeling to quantify nitrogen incorporation into pools of three defense compounds: caffeoylputrescine (CP), dicaffeoyl spermidine (DCS) and nicotine. Nitrogen incorporation was decreased in CP and DCS and increased in nicotine pools in irTOC1 plants compared to empty vector (EV) under control conditions, but these differences were abolished after simulated herbivory. Differences between EV and irTOC1 plants in nicotine, but not phenolamide production, were abolished by treatment with the ethylene agonist 1-methylcyclopropene. Using micrografting, TOC1's effect on nicotine was isolated to the root and did not affect the fitness of heterografts under field conditions. These results suggest that the circadian clock contributes to plant fitness by balancing production of metabolically expensive nitrogen-rich defense compounds and mediating the allocation of resources between vegetative biomass and reproduction.

Ethylene is a local modulator of jasmonate‐dependent phenolamide accumulation during Manduca sexta herbivory in Nicotiana attenuata

“…In conclusion, this study sheds light on the local interplay of JA‐ET signalling sectors for defensive phenolamide production. Interestingly, a recent genetic repression of the circadian clock evening loop component TOC1 in N. attenuata led to increase herbivory‐induced levels of nicotine concomitant with lower ET signalling and strong decreases in phenolamide investments (Valim et al, 2020). Future integrative studies combining metabolome and transcriptome analyses during different types of herbivory could hence provide a clearer picture on the role of ET as one of the key orchestrators of nitrogen allocation to defence metabolite production.…”

Spatially specific mechanisms and functions of the plant circadian clock

“…Furthermore, the clock has roles in balancing resource allocation to defense metabolites. TOC1 silenced plants show decreased accumulation of the defense metabolite dicaffeoylspermidine and increased nicotine accumulation ( Valim et al, 2020 ). The increase in nicotine accumulation depends on functional ethylene signaling.…”

“…Ethylene is induced during herbivore feeding and modulates defense responses in conjunction with jasmonate signaling. Blocking ethylene signaling reverses differences in nicotine accumulation between wild-type and TOC1 silenced N. attenuata plants ( Valim et al, 2020 ). In Arabidopsis, loss of function mutants in another clock gene XAP5 CIRCADIAN TIMEKEEPER show specific defects in response to ethylene in aerial tissues, but not in roots ( Ellison et al, 2011 ).…”

Coordinated resource allocation to plant growth–defense tradeoffs

“…Growth-defense tradeoffs are influenced by genetic and environmental factors, as well as inherent physiological constraints such as internal resource recycling. Consequently, the causes of negatively associated allocational patterns and their impacts on fitness have been challenging to resolve (Reznick, 1985;Bergelson & Purrington, 1996;Koricheva, 2002a;Hahn & Maron, 2016;Ullmann-Zeunert et al, 2016;Valim et al, 2020). The pursuit of studies at the cellular scale improves our understanding of the controls over resource allocation patterns and clarifies the modes by which selection favors tradeoffs (Futuyma & Moreno, 1988;Schuman & Baldwin, 2016;Züst & Agrawal, 2017).…”