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Title:Hydrogen peroxide from photosynthesis: Theory and experiments linking elevated atmospheric CO2 with C3 plant chemical defense
Author(s):Gog, Linus
Director of Research:DeLucia, Evan H.
Doctoral Committee Chair(s):Ainsworth, Elizabeth A.
Doctoral Committee Member(s):Berenbaum, May R.; Ort, Don R.; Clough, Steven
Department / Program:Plant Biology
Discipline:Plant Biology
Degree Granting Institution:University of Illinois at Urbana-Champaign
Chemical Defense
Abstract:Elevated atmospheric CO2 alters C3 plant chemical defense for reasons that remain unclear. To explain the influence of elevated CO2 on plant chemical defense, this dissertation proposes, then tests, the hypotheses that: 1. C3 plant chloroplasts exert control over chemical defense against biotic agents, and 2. the mechanism of this control is sensitive to atmospheric concentrations of CO2. Chapter 1 reviews available research concerning the influence of elevated CO2 on C3 plant chemical defense against biotic agents, herbivorous insects in particular. The argument that emerges from this review is that photosynthesis is the most likely operating cause behind the observed alteration of defense in C3 plants growing under elevated CO2. The proposed mechanism holds that elevated CO2 relaxes the induction of non-photochemical quenching during exposure to excess light, causing more excess excitation energy to enter the photosynthetic electron transport chain than under ambient CO2. In principle, this excess of energy would have nowhere to go except directly to the reduction of oxygen, to form oxygen radicals. The innate immune system of plants in response to both pathogens and herbivorous insects responds to changes in internal redox environment. Thus, if photosynthesis generates increased amounts of reactive oxygen with rising CO2, one might expect the downstream expression of chemical defense to differ as well. Chapter 2 tests the proximate mechanism of chloroplast retrograde signaling proposed in the previous chapter. The hypothesis -that elevated CO2 influences plant chemical defense by altering retrograde signals emerging from C3 plant chloroplasts- necessarily depends on some measurable change in the output of reactive oxygen under variable CO2. To model this effect, the metabolic pathway responsible for generating hydrogen peroxide in plant chloroplasts was incorporated into the e-Photosynthesis in silico model of photosynthesis. At the same time, soybean grown at the soyFACE (Free Air CO2 Enrichment) field site were tested for their response to sudden transitions from dark-to-bright light under ambient and elevated CO2. Both in-silico modeling and field experiments are consistent with the initial hypothesis. Elevated CO2 relaxes induction of non-photochemical quenching in response to bright light, thus increasing the amount of excess excitation energy entering the photosynthetic electron transport chain. Chapter 3 tests the ultimate effects of variable CO2 and light environment on C3 plant chemical defense against herbivorous insects. According to the photosynthetic mechanism described in the preceding two chapters, the combination of elevated CO2 and fluctuating conditions of light should increase output of reactive oxygen from photosynthesis. What follows is that plants grown under combination of elevated CO2 and fluctuating light should be vulnerable to herbivory from insects relative to the combination of ambient CO2 and steady light environment. To test this hypothesis, Arabidopsis thaliana was cultivated in controlled environment growth chambers in 2x2 factorial experiments, varying between ambient and elevated CO2 levels, continuous and dynamic light. Following a period of growth, individual plants were paired with larval cabbage looper, Trichoplusia ni. The pattern of induction of defense hormones salicylic and jasmonic acid was consistent with experimental predictions, in that growth under variable CO2 and variable light yielded patterns unique to each environment. In particular, herbivory under elevated CO2 induced biosynthesis of salicylic acid except under dynamic light. At the same time, dynamic light significantly suppressed foliar content of total glucosinolates, the major chemical defense of A. thaliana against insect herbivores. Ultimately, consistent with experimental predictions, caterpillars removed more leaf tissue from A. thaliana grown under elevated CO2 and dynamic light. Although the pattern of results suggest that chloroplast retrograde signaling is not the only factor influencing insect herbivory in variable environments, the broad outcome of the experiment provides empirical support for a controlling role of photosynthesis in C3 plant chemical defense. Chapter 4 considers the influence of starch metabolism on insect herbivory and how it might be untangled from the effects of secondary metabolism. If starch content, or the ratio of carbon to nitrogen present in foliar tissue, were the only nutritional factor governing insect herbivory on plants, then the effects of elevated CO2 could be simulated through genetic manipulation of plant starch metabolism. In previous work by Tang (2007), consumption of A. thaliana foliar tissue by Trichoplusia ni corresponded to foliar starch content. However, it was apparent that A. thaliana chemical defense, in terms of glucosinolate profiles, confounded the effectiveness of the system as a physiological model for the effects of elevated CO2 on insect herbivory. To control for the confounding influence of secondary metabolism on efforts to predict insect herbivory from starch content, portions of Tang’s research were repeated with a specialist herbivore, the imported European cabbageworm Pieris rapae. When P. rapae fed on mutants of A. thaliana with altered starch metabolism, P. rapae caterpillars differentiated between genotypes that accumulate starch versus genotypes that under-accumulate starch. Together with the work of Tang (2007), the results suggest that manipulation of starch content can effectively mimic the influence of elevated CO2 on insect herbivory, provided the simultaneous influence of plant chemical defense is controlled. In conclusion, the development of a hypothesis for photosynthetic control over chemical defense, together with tests of proximate mechanism and ultimate effects, amounts to a theory of chloroplast retrograde signaling to C3 plant chemical defense under elevated CO2. The signal transduction pathways connecting photosynthesis with defense are best understood as a complex network; untangling this network will require more sophisticated experimental approaches and computational techniques than this dissertation research could provide. Instead, this dissertation offers a practical blueprint for future research on chloroplast retrograde signaling.
Issue Date:2018-03-08
Rights Information:Copyright 2018 Linus Gog
Date Available in IDEALS:2018-09-04
Date Deposited:2018-05

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