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Long-Term Effects of the Circadian Clock on Plant Fitness in the Face of Abiotic and Biotic Stress

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Long-Term Effects of the Circadian Clock on Plant Fitness in the Face of Abiotic and Biotic Stress Long-term effects of the circadian clock on plant fitness in the face of abiotic and biotic stress DISSERTATION zur Erlangung des akademischen Grades Doctor rerum naturalium (Dr.rer.nat.) vorgelegt dem Rat der Biologisch-Pharmazeutischen Fakultät der Friedrich-Schiller-Universität Jena von Henrique Fernandes de Aguiar Valim, B.A. geboren am 16. Oktober 1991 in Araras Max-Planck-Institut für chemische Ökologie Gutachter: Beginn der Promotion: Eingereicht am: Tag der Verteidigung: Contents Contents Introduction ..................................................................................................................................... 1 The importance of timing for plant responses to stress ............................................................... 1 Abiotic and biotic challenges faced by Nicotiana attenuata....................................................... 2 The circadian clock machinery and its outputs: dealing with external cues and stresses ........... 3 Overview of the dissertation ....................................................................................................... 5 References ................................................................................................................................... 6 Overview of Manuscripts .......................................................................................................... 12 1. Temporal dynamics of plant volatiles: mechanistic bases and functional consequences ...... 16 Abstract ..................................................................................................................................... 16 1.1 Introduction ......................................................................................................................... 16 1.1.1 A Brief Introduction to Plant Volatiles ......................................................................... 17 1.1.2 Why Are Plant Volatiles Synthesized and Emitted in Certain Tissues at Certain Times? ............................................................................................................................................... 24 1.1.3 How Is the Induced, Diurnal and Ontogenetic Timing of Volatile Biosynthesis and Emission Regulated? ............................................................................................................. 27 1.2 The Importance of Timing in Plant Volatile Emission ....................................................... 27 ............................................................................................................................................... 28 1.2.1 Plant Volatiles as Induced Defences and Defence Signals ........................................... 29 1.2.2 Diurnal and Circadian Rhythms of Stress-Induced Volatiles ....................................... 30 1.2.3 Circadian Timing of Floral Volatile Emission ............................................................. 33 1.2.4 Ontogenetic Changes in Plant Volatiles: Theory and Observation .............................. 34 1.3 Conclusion ........................................................................................................................... 36 References ................................................................................................................................. 37 2. Early developmental transitions influence drought resistance strategies and confound the quantification of genotypic diversity in drought responses .......................................................... 52 Abstract ..................................................................................................................................... 52 2.1. Introduction .................................................................................................................... 52 2.2. Materials and Methods ................................................................................................... 55 2.3. Results ............................................................................................................................ 57 i Contents 2.3.1. A synchronized drought treatment is required to compare drought responses among genotypes planted individually in a glasshouse ..................................................................... 57 2.3.2. Un-synchronized drought treatments confound the observation of physiological and ontogenetic drought responses, even within one genotype ................................................... 58 2.3.3. Developmental control ensures simultaneous drought onsets in a synchronized drought treatment for genotypes with high developmental variance .................................... 60 2.3.4. Developmental stage significantly explains variance in plant physiological responses to a drought treatment ........................................................................................... 62 Table 1. Variance decomposition analysis of Figure 3B ....................................................... 63 2.3.5. ABA levels best explain variance in RIL drought responses in both onset of drought and prolonged drought treatments ............................................................................ 64 2.4. Discussion ...................................................................................................................... 64 References ................................................................................................................................. 67 Supplemental files ..................................................................................................................... 73 3. The clock gene TOC1 in shoots, not roots, determines fitness of Nicotiana attenuata under drought .......................................................................................................................................... 74 Abstract ..................................................................................................................................... 74 3.1. Introduction .................................................................................................................... 75 3.2. Results ............................................................................................................................ 77 3.2.1. N. attenuata TOC1 is required to maintain fitness under controlled drought conditions............................................................................................................................... 77 3.2.2. Plants silenced in TOC1 in both shoots and roots show different responses in co- expression modules under drought conditions ...................................................................... 82 3.2.3. TOC1-silenced drought responses are not explained by impaired red/far-red light perception .............................................................................................................................. 84 3.2.4. Impaired photoperiodic flowering control is not sufficient to explain drought responses and developmental phenotypes in TOC1-silenced plants ..................................... 86 3.3. Discussion ...................................................................................................................... 86 3.4. Conclusion ...................................................................................................................... 90 3.5. Methods .......................................................................................................................... 91 Literature cited ....................................................................................................................... 95 Supplemental files ............................................................................................................... 101 ii Contents 4. TOC1 in Nicotiana attenuata regulates efficient production of nitrogen-rich defense metabolites under herbivory stress.............................................................................................. 118 Summary ................................................................................................................................. 118 4.1. Introduction .................................................................................................................. 119 4.2. Materials and Methods ................................................................................................. 122 4.3. Results .......................................................................................................................... 124 4.3.1. TOC1 silencing in Nicotiana attenuata leads to a shift in JA signaling, and defense- related transcripts after simulated herbivory ....................................................................... 124 4.3.2. Silencing TOC1 leads to increases in nicotine accumulation and decreases in accumulation of both inducible and constitutive phenolamides after simulated herbivory 126 4.3.3. Allocation of nitrogen is shifted towards nicotine in TOC1-silenced plants ........ 126 4.3.4. Blocking ethylene signaling by 1-methylcyclopropene treatment abolishes differences between EV and TOC1-silenced nicotine accumulation .................................. 129 4.3.5. TOC1 in roots limits nicotine accumulation, but changes to reproductive allocation depend on TOC1 in shoots................................................................................................... 129 4.4. Discussion ...................................................................................................................
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