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The CBF1-dependent low temperature signalling pathway, regulon and increase in freeze tolerance are conserved in Populus spp
Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
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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. Vol. 29, no 7, 1259-1272 p.
Keyword [en]
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
URN: urn:nbn:se:umu:diva-15841DOI: 10.1111/j.1365-3040.2006.01505.xPubMedID: 17080948OAI: diva2:155513
Available from: 2007-08-10 Created: 2007-08-10 Last updated: 2015-04-29Bibliographically approved
In thesis
1. Cold Acclimation: Dissecting the plant low temperature signaling pathway using functional genomics
Open this publication in new window or tab >>Cold Acclimation: Dissecting the plant low temperature signaling pathway using functional genomics
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.
cold acclimation, functional genomics, microarray, Populus tremula, Arabidopsis thaliana, gene voting, regulon, enhancer-blocking
National Category
urn:nbn:se:umu:diva-885 (URN)91-7264-188-6 (ISBN)
Public defence
2006-10-27, KB3B1, KBC, KBC, Umeå, 10:00 (English)
Available from: 2006-10-05 Created: 2006-10-05 Last updated: 2011-03-30Bibliographically approved

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Benedict, CatherineBhalerao, RishikeshHurry, Vaughan
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