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.

Highlights

  • Because they are both sessile organisms and at the base of most food chains, plants are under strong pressure to produce effective defenses in the face of mobile herbivores

  • 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

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Summary

Introduction

Because they are both sessile organisms and at the base of most food chains, plants are under strong pressure to produce effective defenses in the face of mobile herbivores. Several theories have been developed in an attempt to quantify plant defense responses as a function of different factors, in order to explain and predict patterns observed under natural conditions, with varying degrees of success (see Schuman & Baldwin, 2016). Many of these theories attempt to determine trade-offs between growth and defense (Herms & Mattson, 1992), both of which depend on the same limited resources (Bryant et al, 1983; Chapin et al, 1990) and can be alternatively prioritized among plant tissues with different fitness values (McKey, 1974, 1979; Rhoades, 1979). Individual components of the clock have been shown to modulate responses to a variety of external stimuli and stresses, including herbivory (Takase et al, 2013; Seo & Mas, 2015; Sharma & Bhatt, 2015; Joo et al, 2018; Zhang et al, 2019)

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