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Light, Stress and Herbivory from Photoprotection to Trophic Interactions Using Arabidopsis Thaliana As a Model Organism

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Light, Stress and Herbivory from Photoprotection to Trophic Interactions Using Arabidopsis Thaliana As a Model Organism Light, stress and herbivory from photoprotection to trophic interactions using Arabidopsis thaliana as a model organism Av Martin Frenkel Akademisk avhandling som med vederbörligt tillstånd av Rektorsämbetet vid Umeå universitet för avläggande av doktorsexamen i filosofi doktorsexamen i ekologi kommer att offentligen försvaras i lilla hörsalen, KBC-huset, Umeå universitet. Onsdagen den 4 juni 2008, kl. 10.00. Avhandlingen kommer att försvaras på engelska. Examinator: Prof. Lars Ericson, Umeå universitet. Fakultetsopponent: Dr. Don Cipollini, Wright State University, USA Department of Ecology and Environmental Science Umeå University 901 87 Umeå Sweden Organisation Document name Umeå University Doctoral Dissertation Department of Ecology and Date of issue Environmental Science 2008-05-14 SE-901 87 Umeå, Sweden Author Martin Frenkel Title Light, stress and herbivory – from photoprotection to trophic interactions using Arabidopsis thaliana as a model organism Abstract Photosynthesis is the most important process for nearly all life on earth. Photosynthetic organisms capture and transfer light energy from the sun into chemical energy which in turn provides a resource base for heterotrophic organisms. Natural light regimes are irregular and vary over magnitudes. At a certain light intensity, metabolic processes cannot keep up with the electron flow produced by the primary photoreactions, and thus reactive oxygen species (ROS) are produced. ROS are highly reactive and can damage the photosynthesis apparatus and hence plants have evolved several photoprotection mechanisms to avoid the formation of ROS. The aim of this thesis was to examine the ecological effects of variations in photoprotection in plants. In particular I wanted to study the effect on fitness and the interaction with herbivorous insects of plants with different ability in photoprotection. To study this I used wild-type and transgenic Arabidopsis thaliana plants and grew them under natural conditions in field experiments in our botanical garden in Umeå, northern Sweden. For the investigation of the plant-insect interaction, a specialist on Brassicaceae (Plutella xylostella – diamondback moth) and a generalist herbivore (Spodoptera littoralis - Egyptian cotton worm) were used. Plants that are genetically deficient in one of the photoprotection mechanisms showed reduced fitness under natural conditions. I could thus show that feedback de-excitation (FDE) is the most important photoprotection mechanism, because a lack of FDE showed the highest reduction in fitness. The comparison of field grown wild-type with FDE mutant plants, using molecular biology methods, revealed large changes in gene transcription and metabolic composition. In particular, the jasmonate pathway was upregulated in light stressed plants, especially in plants lacking FDE. Jasmonate in turn is known to be a chemical compound which induces herbivore resistance genes and other stress responses. Specialist and generalist insect herbivores responded differently in feeding (dual-choice and no-choice) and oviposition experiments with field grown plants that differed in FDE. Female diamondback moths were attracted by induced defense compounds whereas the larvae avoided these plants in feeding experiments. Generalist larvae preferred, and showed a higher survival rate, on less light-stressed plants compared to more light- stressed plants. Combining molecular biology with ecological experiments is a challenging task. To summarize my experiences, I have produced a guide for experiments on transgenic plants in common gardens. In future investigations it is important to examine natural variations in photoprotection to elucidate selection pressures on specific genes. Key words: Arabidopsis thaliana, photoprotection, herbivory, light-stress, jasmonate, fitness, FDE, dual- choice Language: Englisch ISBN: 978-91-7264-543-1 Number of pages: Signature: Date: May 2008 Light, stress and herbivory from photoprotection to trophic interactions using Arabidopsis thaliana as a model organism Av Martin Frenkel Department of Ecology and Environmental Science Umeå University 901 87 Umeå Sweden Copyright © 2008 by Martin Frenkel ISBN 978‐91‐7264‐543‐1 Printed by VMC, KBC huset, Umeå University, Umeå, 2008 TABLE OF CONTENTS LIST OF PAPERS ............................................................................................................... i ABBREVIATIONS ............................................................................................................ ii INTRODUCTION .............................................................................................................. 1 Light................................................................................................................................ 1 Photosynthesis of higher plants .................................................................................. 1 Noncyclic and cyclic electron transport...................................................................... 2 Reactive oxygen species ............................................................................................. 3 Photoprotection........................................................................................................... 4 Stress............................................................................................................................... 5 Stress responses, and stress signal pathways .............................................................. 5 Herbivory ........................................................................................................................ 7 Plant defense ............................................................................................................... 7 Plant defense is costly................................................................................................. 8 EXPERIMENTAL ORGANISMS AND SETUPS ............................................................ 9 Arabidopsis thaliana (as a model plant) ......................................................................... 9 Insect herbivores ............................................................................................................. 9 Plutella xylostella – Diamondback moth.................................................................. 10 Spodoptera littoralis – Egyptian Cotton Worm........................................................ 10 Field site........................................................................................................................ 10 Methods......................................................................................................................... 10 Fitness ....................................................................................................................... 10 Molecular biology analyses ...................................................................................... 11 Feeding experiments ................................................................................................. 12 Oviposition experiments ........................................................................................... 12 Simulation of fluctuating light.................................................................................. 13 RESULTS ......................................................................................................................... 13 Objectives ..................................................................................................................... 14 Summary of Papers....................................................................................................... 14 MAJOR RESULTS AND DISCUSSION ........................................................................ 16 FUTURE OUTLOOKS .................................................................................................... 18 ACKNOWLEGDMENT................................................................................................... 19 REFERENCES ................................................................................................................. 19 APPENDIX....................................................................................................................... 22 LIST OF PAPERS This thesis is based on the following papers, which will be referred to in the text by corresponding Roman numerals: I Frenkel M, Bellafiore S, Rochaix J-D and Jansson S (2007). Hierarchy amongst photosynthetic acclimation responses for plant fitness. Physiologia Plantarum 129: 455-459 II Frenkel M, Külheim C, Johansson Jänkänpää H, Skogström O, Frigerio S, Ågren J, Bassi R, Moritz T, Moen J and Jansson S. Improper regulation of light harvesting in Arabidopsis results in a metabolic reprogramming. (submitted manuscript) III Frenkel M, Johansson Jänkänpää H, Jansson S and Moen J. Plant photoprotection influence herbivore preferences. (submitted manuscript) IV Frenkel M, Johansson Jänkänpää H, Moen J and Jansson S. An illustrated gardener’s guide to transgenic Arabidopsis field experiments. (submitted manuscript) Paper I is reproduced with kind permission of the publisher. i ABBREVIATIONS ABA abscisic acid ATP; ADP adenosine triphospate; adenosine diphosphat CO2 carbon dioxide DNA deoxyribonucleic acid FDE feedback de-excitation; qE-type of NPQ H2O water H2O2 hydrogen peroxide JA jasmonic acid LHC light harvesting complex NADP+ nicotine adenine dinucleotide phosphate (oxidized form) NADPH+H+ nicotine adenine dinucleotide phosphate (reduzed
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