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Effects of Chronic Cold Treatment on Root Elongation and Gene Expression in Arabidopsis Thaliana

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Effects of Chronic Cold Treatment on Root Elongation and Gene Expression in Arabidopsis Thaliana Effects of Chronic Cold Treatment on Root Elongation and Gene Expression in Arabidopsis thaliana Inauguraldissertation zur Erlangung der Würde eines Doktors der Philosophie vorgelegt der Philosophisch-Naturwissenschaftlichen Fakultät der Universität Basel von Yang Ping Lee aus Malaysia 2008 Friedrich Miescher Institut Basel Genehmigt von der Philosophisch-Naturwissenschaftlichen Fakultät auf Auftrag von Prof. Dr. Frederick Meins Jr., Prof. Dr. Christian Körner und Prof. Dr. Thomas Boller Basel, den 19. Februar 2008 Prof. Dr. Hans-Peter Hauri (Dekan) Summary Low temperature is a major limitation of plant growth. Cold adaptation is important for the survival and distribution of plant species at high elevations and high latitudes. Much is known about the molecular basis for cold acclimation and freezing tolerance, which are triggered by acute cold treatment. The causes of growth limitation at low, non-freezing temperatures are largely unexplored. To better understand the mechanisms limiting plant growth in cold environments, I studied the elongation-growth of roots and patterns of gene expression in Arabidopsis accessions from diverse habitats. Arabidopsis thaliana (L.) Heyhn is a small, annual weed that is widely distributed in different growth environments and is well-suited for molecular genetic studies. My initial study of 23 accessions failed to detect ecotypic differentiation for root elongation rates at low, non- freezing temperatures (10 °C); however, evidence was obtained implicating the cell-cycle gene CYCB1;1 as part of a compensatory mechanism for maintaining proliferation under these conditions. I used microarray technology to obtain a global picture of cold-responsive gene expression in the temperate Col-0 accession and the high-altitude (3400 m) Sha accession, which is expected to be adapted for a cold environment. I compared the effects of acute-cold treatment (4 h at 10 °C) and chronic-cold treatment (6 weeks at 10 °C) using plants grown at 21 °C as a control. Cold-treatment had major effects on gene expression at the mRNA level: 11% of the 24,000 genes represented on the Affymetrix ATH1 GeneChip responded by at least 2-fold to either or both cold treatments. A substantial fraction of cold-responsive genes, 35%, responded specifically to chronic cold treatment. This suggests there are fundamental differences in the response of plants to acute-cold treatment and growth at low, nonfreezing temperatures. Datasets of annotated genes were screened for significant, non-redundant enrichment for Gene Ontology (GO) terms to identify functional groups and processes. GO-term enrichment provided a rough picture of major trends in gene expression associated with cold- responses, which were then verified by examining the expression patterns of individual genes. Flavonoid biosynthesis, particularly the activation of anthocyanin biosynthesis, was the only major function induced by both acute- and chronic-cold treatment. In contrast, genes concerned with electron transport and light-reactions in photosynthesis were repressed by both cold treatments. This is consistent with the well-documented, general reduction of these functions associated with growth at low temperatures. Thus, regulation at the mRNA level appears to be an important mechanism for down-regulating energy metabolism in cold environments. Acute-cold treatment induced numerous genes concerned with responses to pathogen infection, cold, drought, salt stress, and UV damage. The breadth of these stress responses emphasizes that brief exposure to cold, even at temperatures as high as 10 °C, is perceived by plants as a form of stress. Unexpectedly, global induction of stress-related genes was restricted primarily to the acute-cold response. This strongly suggests that in contrast to “cold shock,” growth at low, non-freezing temperatures is not recognized by Arabidopsis plants as a stress per se. Therefore, mechanisms exist for suppressing prolonged stress responses in the cold. This implies that general stress responses are not essential for growth of Arabidopsis at low temperatures. Several other processes and pathways responded primarily to chronic- cold treatment and are likely to be relevant to growth at low temperatures. Sha-specific, chronic-cold induction of genes encoding ion transporters; genes concerned with compensation for Pi deprivation; and, genes required for formation of root hairs, comprised the only major functional group showing ecotypic differentiation. Induction of genes encoding primary wall constituents and enzymes concerned with cell enlargement and pectin metabolism were induced specifically by chronic-cold treatment, while those genes important for secondary wall formation such as those encoding cellulose synthase and laccase required for lignification were repressed. These findings and the cold- repression of genes concerned with fiber and vascular tissue formation suggest as a working hypothesis that chronic cold treatment increases the flexibility of roots and cell wall extensibility as a compensatory response to the reduced root growth in the cold. In summary, the present study identified several functional groups of genes showing novel regulation by chronic cold treatment. These findings provide the starting point for future studies using informative mutants and biochemical profiling to establish causal relationships between gene expression and adaptations for growth in cold environments. Acknowledgements My work and my thesis have been designed and developed with the aid of many people. First of all, I would like to thank Prof. Dr. Frederick Meins Jr. and Prof. Dr. Christian Körner, my supervisors for their help and intellectual contribution to the work described in this thesis. Both of them inspired me to work on the project and guided me to become an independent researcher. Also to express my appreciation to my committee, Prof. Dr. Thomas Boller, and Dr. Yoshikuni Nagamine for their guidance and advise during the course of this project. My appreciation is also extended to Estelle Arn and Jerome Ailhas for helping me to process my purchase and ordering chemicals. Many thanks to Dr. Franck Vazquez, Dr. Azeddine Si-Ammour, Dr. Konstantina Boutsika, Dr. Quanan Hu, Dr.Todd Blevins, and Dr. Claudia Kutter of my lab members, for their willingness in sharing experimental protocols, guidance, and discussion during my work. I am thankful to Dr. Jens Paulsen and Dr. Günter Hoch at the Botanical Institute of the University of Basel for advice on ecophysiological aspects. Thanks to Dr. Edward Oakeley and Dr. Herbert Angliker from Functional genomics, and Dr. Michael Stadler from Bioinformatics groups for their fruitful discussion on transcript profiling and statistical aspects. A special thanks to my funding agency. My project would not be started without a 'Zürich-Basel Plant Science Center' doctoral Studentship funded by Syngenta, AG, and by the Novartis Research Foundation (FMI) which awarded to me. Last but not least, warmest thanks to my wife, Ley Poh and family for their love, encouragement and understanding throughout my study at FMI. Table of Contents 1.0 Introduction .................................................................................1 1.1 Plants and cold environments........................................................ 1 1.2 Cold sensing and the molecular basis of cold acclimation ............ 3 1.2.1 Cold signaling pathways.................................................................. 4 1.2.2 CBF-dependent pathway................................................................. 6 1.2.3 CBF-independent pathway .............................................................. 9 1.2.4 Role of cold-responsive genes in freezing tolerance ..................... 11 1.3 Biochemical and physiological changes in response to cold ....... 12 1.4 Natural variation of Arabidopsis thaliana ..................................... 16 1.5 Aim of the dissertation ................................................................. 17 2.0 Materials and methods..............................................................18 2.1 Plant materials ............................................................................. 18 2.2 Growth conditions and low temperature treatments .................... 18 2.2.1 Measurement of root elongation rate............................................. 18 2.2.2 Acute and chronic low temperature treatments ............................. 19 2.2.3 Low temperature treatments for RNA profiling experiment............ 19 2.3 Molecular biology techniques....................................................... 22 2.3.1 Isolation of high molecular weight of RNA ..................................... 22 2.3.2 Primer design and preparation of double-stranded DNA probes ... 22 2.3.3 RNA blot hybridization................................................................... 23 2.3.4 Quantitative real-time PCR............................................................ 24 2.4 RNA profiling................................................................................ 26 2.4.1 GeneChip hybridization and raw data collection............................ 26 2.4.2 Data processing and analyses ...................................................... 26 2.5 Statistical analysis........................................................................ 26 2.5.1 General.......................................................................................... 26 2.5.2 RNA expression data....................................................................
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