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Cold Acclimation: Dissecting the plant low temperature signaling pathway using functional genomics
Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
2006 (Swedish)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The physiological process of cold acclimation protects plants native to the temperate regions of the world from the deleterious effects of low and freezing temperatures. This is achieved by a series of transcriptional, regulatory, and metabolic changes that enable continued growth and survival. Within minutes of exposure to temperatures below ca. 10°C, a complex cascade of transcriptional events is initiated to accomplish these changes. The initial alarm phase favors the rapid induction of a library of stress proteins with protective functions (e.g. COR proteins). This is followed by a cold hardened phase, characterized by maximal freezing tolerance, which continues until either the stress is removed, or the plant's metabolic and/or developmental state can no longer support maximal resistance.

We have studied some of the important transcription factors and transcriptional changes associated with the initial alarm and later hardened phases of cold acclimation in the herbaceous annual Arabidopsis thaliana and the woody perennial Populus spp. We confirmed the functionality of the CBF-mediated signaling cascade in Poplar overexpressing AtCBF1, but noted that regulon composition and endogenous poplar CBF ortholog induction appeared to be tissue-specific. The lack of statistically significant DRE enrichment in the Poplar AtCBF1 regulons led us to investige cis-element abundance in the cold-associated transcription factor regulons of publicly available microarray data from Arabidopsis, leading to the development of a gene voting method of microarray analysis that we used to test for regulatory associations between transcription factors and their downstream cis-elements and gene targets. This analysis resulted in a new transcriptional model of the ICE1-mediated signaling cascade and implicated a role for phytochrome A. Application of this same method to microarray data from arabidopsis leaves developed at low temperature allowed us to identify a new cis-element, called DDT, which possessed enhancer-blocking function during the alarm stage of cold stress, but was enriched in the promoters of genes upregulated during the later cold hardened stages. As leaf growth and development at low temperature correlated with the enhancement freeze tolerance in Arabidopsis, we compared the transcriptomes of rapidly growing and fully grown poplar leaves at night (when both low temperatures and PhyA status might play important roles in nature), in the hopes of comparing this data with that of cold-treated leaves in the future. We identified the nocturnal mode of leaf growth in Populus deltoides as predominantly proliferative as opposed to expansive, and potentially linked to cellular carbohydrate status.

Place, publisher, year, edition, pages
Umeå: Fysiologisk botanik , 2006. , 51 p.
Keyword [en]
cold acclimation, functional genomics, microarray, Populus tremula, Arabidopsis thaliana, gene voting, regulon, enhancer-blocking
National Category
Botany
Identifiers
URN: urn:nbn:se:umu:diva-885ISBN: 91-7264-188-6 (print)OAI: oai:DiVA.org:umu-885DiVA: diva2:144883
Public defence
2006-10-27, KB3B1, KBC, KBC, Umeå, 10:00 (English)
Opponent
Supervisors
Available from: 2006-10-05 Created: 2006-10-05 Last updated: 2011-03-30Bibliographically approved
List of papers
1. The CBF1-dependent low temperature signalling pathway, regulon and increase in freeze tolerance are conserved in Populus spp
Open this publication in new window or tab >>The CBF1-dependent low temperature signalling pathway, regulon and increase in freeze tolerance are conserved in Populus spp
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2006 (English)In: Plant, Cell and Environment, ISSN 0140-7791, E-ISSN 1365-3040, Vol. 29, no 7, 1259-1272 p.Article in journal (Refereed) Published
Abstract [en]

The meristematic tissues of temperate woody perennials must acclimate to freezing temperatures to survive the winter and resume growth the following year. To determine whether the C-repeat binding factor (CBF) family of transcription factors contributing to this process in annual herbaceous species also functions in woody perennials, we investigated the changes in phenotype and transcript profile of transgenic Populus constitutively expressing CBF1 from Arabidopsis (AtCBF1). Ectopic expression of AtCBF1 was sufficient to significantly increase the freezing tolerance of non-acclimated leaves and stems relative to wild-type plants. cDNA microarray experiments identified genes up-regulated by ectopic AtCBF1 expression in Populus, demonstrated a strong conservation of the CBF regulon between Populus and Arabidopsis and identified differences between leaf and stem regulons. We studied the induction kinetics and tissue specificity of four CBF paralogues identified from the Populus balsamifera subsp. trichocarpa genome sequence (PtCBFs). All four PtCBFs are cold-inducible in leaves, but only PtCBF1 and PtCBF3 show significant induction in stems. Our results suggest that the central role played by the CBF family of transcriptional activators in cold acclimation of Arabidopsis has been maintained in Populus. However, the differential expression of the PtCBFs and differing clusters of CBF-responsive genes in annual (leaf) and perennial (stem) tissues suggest that the perennial-driven evolution of winter dormancy may have given rise to specific roles for these 'master-switches' in the different annual and perennial tissues of woody species.

Place, publisher, year, edition, pages
Oxford: Blackwell Scientific Publications Ltd, 2006
Keyword
abscisic acid/metabolism, adaptation; physiological, amino acid sequence, arabidopsis/metabolism, arabidopsis proteins/chemistry/genetics/*metabolism, cluster analysis, dna-binding proteins/chemistry/genetics/*metabolism, freezing, gene expression regulation; plant, genes; plant/genetics, genome; plant/genetics, microarray analysis, molecular sequence data, natural disasters, plant leaves/physiology, plant stems/physiology, plants; genetically modified, populus/genetics/*metabolism/physiology, regulon/*genetics, response elements/genetics, signal transduction, trans-activators/chemistry/genetics/*metabolism, transcription factors/metabolism, up-regulation/genetics
Identifiers
urn:nbn:se:umu:diva-15841 (URN)10.1111/j.1365-3040.2006.01505.x (DOI)17080948 (PubMedID)
Available from: 2007-08-10 Created: 2007-08-10 Last updated: 2015-04-29Bibliographically approved
2. Consensus by democracy. Using meta-analyses of microarray and genomic data to model the cold acclimation signaling pathway in Arabidopsis.
Open this publication in new window or tab >>Consensus by democracy. Using meta-analyses of microarray and genomic data to model the cold acclimation signaling pathway in Arabidopsis.
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2006 (English)In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 141, no 4, 1219-1232 p.Article in journal (Refereed) Published
Abstract [en]

The whole-genome response of Arabidopsis (Arabidopsis thaliana) exposed to different types and durations of abiotic stress has now been described by a wealth of publicly available microarray data. When combined with studies of how gene expression is affected in mutant and transgenic Arabidopsis with altered ability to transduce the low temperature signal, these data can be used to test the interactions between various low temperature-associated transcription factors and their regulons. We quantized a collection of Affymetrix microarray data so that each gene in a particular regulon could vote on whether a cis-element found in its promoter conferred induction (+1), repression (–1), or no transcriptional change (0) during cold stress. By statistically comparing these election results with the voting behavior of all genes on the same gene chip, we verified the bioactivity of novel cis-elements and defined whether they were inductive or repressive. Using in silico mutagenesis we identified functional binding consensus variants for the transcription factors studied. Our results suggest that the previously identified ICEr1 (induction of CBF expression region 1) consensus does not correlate with cold gene induction, while the ICEr3/ICEr4 consensuses identified using our algorithms are present in regulons of genes that were induced coordinate with observed ICE1 transcript accumulation and temporally preceding genes containing the dehydration response element. Statistical analysis of overlap and cis-element enrichment in the ICE1, CBF2, ZAT12, HOS9, and PHYA regulons enabled us to construct a regulatory network supported by multiple lines of evidence that can be used for future hypothesis testing.

Keyword
Acclimatization/*physiology, Arabidopsis/genetics/*metabolism, Arabidopsis Proteins/genetics/*metabolism/physiology, Cold, Computational Biology/methods, Gene Expression Profiling, Gene Expression Regulation; Plant, Genomics/*methods, Models; Biological, Mutagenesis, Mutation, Oligonucleotide Array Sequence Analysis, Plants; Genetically Modified/metabolism, Promoter Regions (Genetics), Regulon, Signal Transduction/*physiology, Transcription Factors/genetics/metabolism/physiology
National Category
Biological Sciences
Identifiers
urn:nbn:se:umu:diva-15834 (URN)doi:10.1104/pp.106.083527 (DOI)16896234 (PubMedID)
Available from: 2007-08-02 Created: 2007-08-02 Last updated: 2015-04-29
3. The novel enhancer-blocking cis-element DDT is enriched in genes associated with long-term acclimation in Arabidopsis thaliana
Open this publication in new window or tab >>The novel enhancer-blocking cis-element DDT is enriched in genes associated with long-term acclimation in Arabidopsis thaliana
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Manuscript (Other academic)
Identifiers
urn:nbn:se:umu:diva-5382 (URN)
Available from: 2006-10-05 Created: 2006-10-05 Last updated: 2010-01-13Bibliographically approved
4. Nocturnal changes in leaf growth of Populus deltoides are controlled by cytoplasmic growth
Open this publication in new window or tab >>Nocturnal changes in leaf growth of Populus deltoides are controlled by cytoplasmic growth
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2006 (English)In: Planta, ISSN 0032-0935, E-ISSN 1432-2048, Vol. 223, no 6, 1315-1328 p.Article in journal (Refereed) Published
Abstract [en]

Growing leaves do not expand at a constantrate but exhibit pronounced diel growth rhythms.However, the mechanisms giving rise to distinct dielgrowth dynamics in different species are still largelyunknown. As a first step towards identifying genescontrolling rate and timing of leaf growth, we analysedthe transcriptomes of rapidly expanding and fully expandedleaves of Populus deltoides Bartr. ex. Marsh atpoints of high and low expansion at night. Tissues withwell defined temporal growth rates were harvested usingan online growth-monitoring system based on a digitalimage sequence processing method developed forquantitative mapping of dicot leaf growth. Unlike plantsstudied previously, leaf growth in P. deltoides wascharacterised by lack of a base-tip gradient across thelamina, and by maximal and minimal growth at duskand dawn, respectively. Microarray analysis revealedthat the nocturnal decline in growth coincided with aconcerted down-regulation of ribosomal protein genes,indicating deceleration of cytoplasmic growth. In asubsequent time-course experiment, Northern blottingand real-time RT-PCR confirmed that the ribosomalprotein gene RPL12 and a cell-cycle gene H2B weredown-regulated after midnight following a decrease incellular carbohydrate concentrations. Thus, we proposethat the spatio-temporal growth pattern in leaves ofP. deltoides primarily arises from cytoplasmic growthwhose activity increases from afternoon to midnight andthereafter decreases in this species.

Place, publisher, year, edition, pages
Berlin: Springer-Verlag, 2006
Keyword
Cell cycle, cytoplasmic growth, leaf growth, microarray, populus, ribosomal protein
Identifiers
urn:nbn:se:umu:diva-5383 (URN)10.1007/s00425-005-0181-0 (DOI)
Available from: 2006-10-05 Created: 2006-10-05 Last updated: 2015-03-18Bibliographically approved

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