Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

Genotype-dependent contribution of CBF transcription factors to long-term acclimation to high light and cool temperature

Journal Article · · Plant, Cell and Environment
DOI:https://doi.org/10.1111/pce.14231· OSTI ID:2470672
 [1];  [2];  [1];  [1];  [1];  [3];  [2];  [2]
  1. Univ. of California, Berkeley, CA (United States). Howard Hughes Medical Institute
  2. Univ. of Colorado, Boulder, CO (United States)
  3. Univ. of California, Berkeley, CA (United States). Howard Hughes Medical Institute; Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
When grown under cool temperature, winter annuals upregulate photosynthetic capacity as well as freezing tolerance. Here, the role of three cold-induced C-repeat-binding factor (CBF1–3) transcription factors in photosynthetic upregulation and freezing tolerance was examined in two Arabidopsis thaliana ecotypes originating from Italy (IT) or Sweden (SW), and their corresponding CBF1–3-deficient mutant lines it:cbf123 and sw:cbf123. Photosynthetic, morphological and freezing-tolerance phenotypes, as well as gene expression profiles, were characterized in plants grown from the seedling stage under different combinations of light level and temperature. Under high light and cool (HLC) growth temperature, a greater role of CBF1–3 in IT versus SW was evident from both phenotypic and transcriptomic data, especially with respect to photosynthetic upregulation and freezing tolerance of whole plants. Overall, features of SW were consistent with a different approach to HLC acclimation than seen in IT, and an ability of SW to reach the new homeostasis through the involvement of transcriptional controls other than CBF1–3. These results provide tools and direction for further mechanistic analysis of the transcriptional control of approaches to cold acclimation suitable for either persistence through brief cold spells or for maximisation of productivity in environments with continuous low temperatures.
Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
Gordon and Betty Moore Foundation; National Science Foundation (NSF); USDOE
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
2470672
Journal Information:
Plant, Cell and Environment, Journal Name: Plant, Cell and Environment Journal Issue: 2 Vol. 45; ISSN 0140-7791
Publisher:
WileyCopyright Statement
Country of Publication:
United States
Language:
English

References (84)

Genetic and physiological mechanisms of freezing tolerance in locally adapted populations of a winter annual journal November 2019
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method journal December 2001
The grand design of photosynthesis: Acclimation of the photosynthetic apparatus to environmental cues journal November 1995
Photosynthetic response to varying light intensity in ecotypes of Solanum dulcamara L. from shaded and exposed habitats journal January 1976
Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants journal July 1993
Hormonal control of cold stress responses in plants journal November 2015
Distinct leaf developmental and gene expression responses to light quantity depend on blue-photoreceptor or plastid-derived signals, and can occur in the absence of phototropins journal August 2007
Differences in light-harvesting, acclimation to growth-light environment, and leaf structural development between Swedish and Italian ecotypes of Arabidopsis thaliana journal July 2015
Freezing sensitivity in the gigantea mutant of Arabidopsis is associated with sugar deficiency journal June 2007
Low temperature acclimation of photosynthetic capacity and leaf morphology in the context of phloem loading type journal July 2012
Acclimation of Swedish and Italian ecotypes of Arabidopsis thaliana to light intensity journal August 2017
Energy balance and acclimation to light and cold journal June 1998
A plant for all seasons: alterations in photosynthetic carbon metabolism during cold acclimation in Arabidopsis journal June 2002
AP2/ERF family transcription factors in plant abiotic stress responses journal February 2012
Interaction of two intrinsically disordered plant stress proteins (COR15A and COR15B) with lipid membranes in the dry state journal September 2010
Photosynthetic acclimation, vernalization, crop productivity and ‘the grand design of photosynthesis’ journal September 2016
Environmental regulation of intrinsic photosynthetic capacity: an integrated view journal June 2017
Regulation of the Arabidopsis thaliana vitamin B6 biosynthesis genes by abiotic stress journal February 2007
Molecular Regulation of CBF Signaling in Cold Acclimation journal July 2018
Arabidopsis Transcriptional Activators CBF1, CBF2, and CBF3 have Matching Functional Activities journal March 2004
Overexpression of Multiple Dehydrin Genes Enhances Tolerance to Freezing Stress in Arabidopsis journal March 2004
Daily photosynthetic and C‐export patterns in winter wheat leaves during cold stress and acclimation journal April 2003
StringTie enables improved reconstruction of a transcriptome from RNA-seq reads journal February 2015
Fiji: an open-source platform for biological-image analysis journal June 2012
NIH Image to ImageJ: 25 years of image analysis journal June 2012
Structure and differential expression of the four members of the Arabidopsis thaliana ferritin gene family journal October 2001
Two different strategies for light utilization in photosynthesis in relation to growth and cold acclimation journal June 2002
Normal growth of Arabidopsis requires cytosolic invertase but not sucrose synthase journal May 2009
Photoperiodic regulation of the C-repeat binding factor (CBF) cold acclimation pathway and freezing tolerance in Arabidopsis thaliana journal August 2012
Genetic mapping of adaptation reveals fitness tradeoffs in Arabidopsis thaliana journal December 2013
Plastidial transporters KEA1, -2, and -3 are essential for chloroplast osmoregulation, integrity, and pH regulation in Arabidopsis journal May 2014
eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant journal June 1998
Arabidopsis thaliana avoids freezing by supercooling journal September 2006
Realizing pipe dreams – a detailed picture of vascular development journal December 2016
Genetic basis of photosynthetic responses to cold in two locally adapted populations of Arabidopsis thaliana journal December 2017
Primer3—new capabilities and interfaces journal June 2012
The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update journal May 2018
The Effect of Overexpression of Two Brassica CBF/DREB1-like Transcription Factors on Photosynthetic Capacity and Freezing Tolerance in Brassica napus journal September 2005
Identification of Reference Genes for RT–qPCR Expression Analysis in Arabidopsis and Tomato Seeds journal August 2011
Abundantly and Rarely Expressed Lhc Protein Genes Exhibit Distinct Regulation Patterns in Plants journal March 2006
Metabolic Pathways Involved in Cold Acclimation Identified by Integrated Analysis of Metabolites and Transcripts Regulated by DREB1A and DREB2A     journal June 2009
Acclimation of Arabidopsis Leaves Developing at Low Temperatures. Increasing Cytoplasmic Volume Accompanies Increased Activities of Enzymes in the Calvin Cycle and in the Sucrose-Biosynthesis Pathway journal April 1999
Cold-Induced Freezing Tolerance in Arabidopsis1 journal June 1999
Mutational Evidence for the Critical Role of CBF Transcription Factors in Cold Acclimation in Arabidopsis journal June 2016
COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS journal January 1949
Arabidopsis Transcriptome Profiling Indicates That Multiple Regulatory Pathways Are Activated during Cold Acclimation in Addition to the CBF Cold Response Pathway journal July 2002
Tissue-Autonomous Promotion of Palisade Cell Development by Phototropin 2 in Arabidopsis journal October 2011
Protein Phosphatase 2Cs and Microtubule-Associated Stress Protein 1 Control Microtubule Stability, Plant Growth, and Drought Response journal December 2016
Developmental process of sun and shade leaves in Chenopodium album L. journal June 2004
Functional‐genomics‐based identification of genes that regulate Arabidopsis responses to multiple abiotic stresses journal March 2008
Temporal heterogeneity of cold acclimation phenotypes in Arabidopsis leaves journal February 2010
The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses: AtGenExpress global abiotic stress data set journal March 2007
Arabidopsis has a cytosolic fumarase required for the massive allocation of photosynthate into fumaric acid and for rapid plant growth on high nitrogen: Cytosolic fumarase and growth on nitrogen journal February 2010
Polarographic Measurement of Photosynthetic Oxygen Evolution by leaf Discs journal October 1981
Seduced by the dark side: integrating molecular and ecological perspectives on the influence of light on plant defence against pests and pathogens journal May 2006
Clinal variation in freezing tolerance among natural accessions of Arabidopsis thaliana journal November 2007
Reciprocal transplants demonstrate strong adaptive differentiation of the model organism Arabidopsis thaliana in its native range journal March 2012
Low-temperature perception leading to gene expression and cold tolerance in higher plants journal July 2012
QTL mapping of freezing tolerance: links to fitness and adaptive trade-offs journal August 2014
Adaptation to warmer climates by parallel functional evolution of CBF genes in Arabidopsis thaliana journal July 2016
Natural variation of C-repeat-binding factor ( CBF s) genes is a major cause of divergence in freezing tolerance among a group of Arabidopsis thaliana populations along the Yangtze River in China journal May 2013
The cbfs triple mutants reveal the essential functions of CBFs in cold acclimation and allow the definition of CBF regulons in Arabidopsis journal June 2016
Distinct palisade tissue development processes promoted by leaf autonomous signalling and long‐distance signalling in Arabidopsis thaliana journal November 2014
Acclimation of metabolism to light in A rabidopsis thaliana : the glucose 6-phosphate/phosphate translocator GPT2 directs metabolic acclimation: Metabolic acclimation to light: the role of GPT2 journal January 2015
Growth temperature impact on leaf form and function in Arabidopsis thaliana ecotypes from northern and southern Europe: Impact of temperature on A. thaliana ecotypes journal April 2016
Leaf anatomical and photosynthetic acclimation to cool temperature and high light in two winter versus two summer annuals journal February 2014
Leaf architectural, vascular and photosynthetic acclimation to temperature in two biennials journal June 2014
Light, temperature and tocopherol status influence foliar vascular anatomy and leaf function in Arabidopsis thaliana journal March 2017
Natural variation in the C-repeat binding factor cold response pathway correlates with local adaptation of Arabidopsis ecotypes journal October 2015
Multiple steps of leaf thickening during sun‐leaf formation in Arabidopsis journal September 2019
PLANT COLD ACCLIMATION: Freezing Tolerance Genes and Regulatory Mechanisms journal June 1999
Comparative Photosynthesis of Sun and Shade Plants journal June 1977
Photosynthetic Response and Adaptation to Temperature in Higher Plants journal June 1980
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 journal December 2014
The coordination of ploidy and cell size differs between cell layers in leaves journal January 2016
Auxin Influx Carriers Control Vascular Patterning and Xylem Differentiation in Arabidopsis thaliana journal April 2015
CBF-dependent and CBF-independent regulatory pathways contribute to the differences in freezing tolerance and cold-regulated gene expression of two Arabidopsis ecotypes locally adapted to sites in Sweden and Italy journal December 2018
EGR2 phosphatase regulatesOST1 kinase activity and freezing tolerance inArabidopsis journal November 2018
Chloroplast redox imbalance governs phenotypic plasticity: the “grand design of photosynthesis” revisited journal January 2012
Foliar phloem infrastructure in support of photosynthesis journal January 2013
Minor loading vein acclimation for three Arabidopsis thaliana ecotypes in response to growth under different temperature and light regimes journal January 2013
Association between minor loading vein architecture and light- and CO2-saturated rates of photosynthetic oxygen evolution among Arabidopsis thaliana ecotypes from different latitudes journal January 2013
Habitat Temperature and Precipitation of Arabidopsis thaliana Ecotypes Determine the Response of Foliar Vasculature, Photosynthesis, and Transpiration to Growth Temperature journal July 2016
Phosphoprotein SAK1 is a regulator of acclimation to singlet oxygen in Chlamydomonas reinhardtii journal May 2014