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Plant Priming of Anti-Herbivore Defence by Insect Oviposition: Dynamics and fitness Consequences

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Plant Priming of Anti-Herbivore Defence by Insect Oviposition: Dynamics and fitness Consequences Plant priming of anti-herbivore defence by insect oviposition: Dynamics and fitness consequences Inaugural-Dissertation to obtain the academic degree Doctor rerum naturalium (Dr. rer. nat.) submitted to the Department of Biology, Chemistry, Pharmacy of Freie Universität Berlin by Rainer Ernst Hermann Cramer 2021 The work presented in this thesis was edited from October 2016 until March 2021 at the Molecular Ecology group led by Prof. Dr. Anke Steppuhn, Institute of Biology at Freie Universität Berlin. First reviewer Prof. Dr. Anke Steppuhn Second reviewer Prof. Dr. Britta Tietjen Date of Disputation: 04.06.2021 Affidavit I hereby declare that my thesis, entitled Plant priming of anti-herbivore defence by insect oviposition: Dynamics and fitness consequences, is the result of my own work. I did not receive any help or support from commercial consultants. All sources and/or materials applied in this thesis are listed and specified. Further- more, I confirm that this thesis has not yet been submitted as part of another examination process neither in identical nor in similar form. Berlin, 01. March 2021 Rainer E.H. Cramer Contents I Main Part 1 Abstract .......................................................................................... 1 1.1 Summary ........................................................................................... 1 1.2 Zusammenfassung ............................................................................... 4 2 Introduction .................................................................................... 8 2.1 Insect herbivory.................................................................................. 8 2.2 Plant responses to insect herbivory....................................................... 9 2.2.1 Plant tolerance to herbivory....................................................... 10 2.2.2 Plant defence strategies ............................................................. 11 2.2.3 Fitness consequences of herbivory............................................... 12 2.2.4 Priming of plant defence ............................................................ 13 2.3 Physiological plant responses to herbivory............................................. 16 2.3.1 Perception of herbivory.............................................................. 16 2.3.2 Processing of the herbivory signal............................................... 18 2.3.3 Phytohormonal signalling in response to herbivory ....................... 20 2.3.3.1 Jasmonate signalling ......................................................... 21 2.3.3.2 Abscisic acid..................................................................... 26 2.3.3.3 Salicylic acid..................................................................... 27 2.3.3.4 Other defence related phytohormones ................................. 31 2.3.4 Induced anti-herbivore defences .................................................. 32 2.4 Plant responses to insect oviposition..................................................... 36 2.4.1 Perception of insect eggs and subsequent signalling ...................... 36 2.4.2 Plant defence against insect eggs ................................................ 38 2.4.3 Priming of anti-herbivore defence by oviposition .......................... 40 2.5 Study system...................................................................................... 47 2.5.1 The bittersweet nightshade and its interaction with herbivores...... 47 2.5.2 The wild tobacco and its interaction with herbivores .................... 50 2.6 Main research questions and thesis outline ............................................ 53 2.6.1 Dynamics of the primed state in S. dulcamara ............................. 53 2.6.2 Fitness consequences of oviposition priming for N. attenuata......... 55 3 Material and methods .................................................................... 59 3.1 Plant culture ...................................................................................... 59 3.1.1 Solanum dulcamara ................................................................... 59 3.1.2 Nicotiana attenuata................................................................... 59 3.2 Insect rearing ..................................................................................... 60 3.2.1 Acrolepia autumnitella............................................................... 60 3.2.2 Spodoptera exigua...................................................................... 60 3.2.3 Manduca sexta .......................................................................... 61 3.3 Experimental setup ............................................................................. 61 3.3.1 Experiments examining the dynamics of the primed state in S. dulcamara ........................................................................... 61 3.3.2 Experiments examining the fitness consequences of oviposition priming for N. attenuata ........................................................... 66 3.4 Experimental procedures ..................................................................... 70 3.4.1 Plant exposure to oviposition ..................................................... 70 3.4.2 Plant exposure to natural and simulated herbivory....................... 71 3.5 Phytohormone quantification ............................................................... 72 3.6 Quantification of gene expression.......................................................... 74 3.6.1 RNA isolation, quality check and quantification ........................... 74 3.6.2 Reverse transcription................................................................. 76 3.6.3 Quantitative real time polymerase chain reaction ......................... 77 3.7 Measurement of plant growth and fitness .............................................. 78 3.8 Statistical analysis .............................................................................. 79 4 Results............................................................................................. 82 4.1 Dynamics of the primed state in S. dulcamara ....................................... 82 4.1.1 Temporal pattern of phytohormonal responses to S. exigua oviposition................................................................................ 82 4.1.2 Temporal pattern of transcriptional responses to S. exigua oviposition................................................................................ 84 4.1.3 Temporal pattern of phytohormonal and transcriptional responses to A. autumnitella oviposition ..................................... 87 4.1.4 Phytohormonal and transcriptional responses to oviposition and natural herbivory in the beginning of the attack .......................... 88 4.1.5 Phytohormonal and transcriptional accumulation after oviposition and simulated herbivory during the onset of the response ................................................................................... 92 4.2 Fitness consequences of oviposition priming for N. attenuata .................. 94 4.2.1 Growth and fitness consequences of oviposition and larval feeding by S. exigua ............................................................................ 94 4.2.2 Growth and fitness consequences of oviposition and larval feeding by M. sexta ............................................................................. 98 4.2.3 Growth and fitness consequences of oviposition and simulated herbivory...................................................................100 4.2.4 Effect of oviposition and larval feeding before defoliation on fitness of regrown plants ......................................................................101 4.2.5 Fitness consequences of prior oviposition and larval feeding when defoliation occurs in young rosette or flowering stage....................103 5 Discussion........................................................................................106 5.1 Dynamics of the primed state in S. dulcamara .......................................106 5.1.1 Temporal dynamics of phytohormonal and transcriptional responses to oviposition............................................................................106 5.1.1.1 Oviposition-induced salicylic acid signalling is limited to the period of egg exposure.......................................................106 5.1.1.2 Low-level jasmonate induction in response to oviposition ......108 5.1.1.3 Transcriptional response to S. exigua oviposition .................110 5.1.1.4 Persistent transcriptional induction of phenylpropanoid metabolism in response to oviposition .................................112 5.1.1.5 Temporal expression patterns of responses to oviposition ......113 5.1.1.6 Response of S. dulcamara to A. autumnitella oviposition ......115 5.1.2 Phytohormonal and transcriptional induction during onset of oviposition primed response to herbivory.....................................117 5.1.2.1 Salicylic acid induction during onset of oviposition-primed response to herbivory ........................................................118 5.1.2.2 Additive effect of oviposition and larval feeding on abscisic acid during the onset of oviposition primed response to herbivory......................................................................120 5.1.2.3 Primed jasmonate induction during onset of herbivory .........122 5.1.2.4 Primed induction of marker genes for phytohormonal and phenylpropanoid pathways during the onset of herbivory ......124 5.1.2.5 Earlier or faster feeding-induced defence..............................125
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