A comparison of the low temperature transcriptomes and CBF regulons of three plant species that differ in freezing tolerance: Solanum commersonii, Solanum tuberosum, and Arabidopsis thaliana

Carvallo, Marcela A.; Pino, María-Teresa; Jeknić, Zoran; Zou, Cheng; Doherty, Colleen J.; Shiu, Shin-Han; Chen, Tony H.  H.; Thomashow, Michael F.

doi:10.1093/jxb/err066

A comparison of the low temperature transcriptomes and CBF regulons of three plant species that differ in freezing tolerance: Solanum commersonii, Solanum tuberosum, and Arabidopsis thaliana

Journal Article · Thu Apr 21 00:00:00 EDT 2011 · Journal of Experimental Botany

DOI:https://doi.org/10.1093/jxb/err066· OSTI ID:1625370

Carvallo, Marcela A. ^[1]; Pino, María-Teresa ^[2]; Jeknić, Zoran ^[2]; Zou, Cheng ^[3]; Doherty, Colleen J. ^[4]; Shiu, Shin-Han ^[3]; Chen, Tony H. H. ^[2]; Thomashow, Michael F. ^[5]

Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory; DOE/OSTI
Oregon State Univ., Corvallis, OR (United States). Dept. of Horticulture
Michigan State Univ., East Lansing, MI (United States). Dept. of Plant Biology
Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory; Michigan State Univ., East Lansing, MI (United States). Dept. of Crop and Soil Sciences

Solanum commersonii and Solanum tuberosum are closely related plant species that differ in their abilities to cold acclimate; whereas S. commersonii increases in freezing tolerance in response to low temperature, S. tuberosum does not. In Arabidopsis thaliana, cold-regulated genes have been shown to contribute to freezing tolerance, including those that comprise the CBF regulon, genes that are controlled by the CBF transcription factors. The low temperature transcriptomes and CBF regulons of S. commersonii and S. tuberosum were therefore compared to determine whether there might be differences that contribute to their differences in ability to cold acclimate. The results indicated that both plants alter gene expression in response to low temperature to similar degrees with similar kinetics and that both plants have CBF regulons composed of hundreds of genes. However, there were considerable differences in the sets of genes that comprised the low temperature transcriptomes and CBF regulons of the two species. Thus differences in cold regulatory programmes may contribute to the differences in freezing tolerance of these two species. However, 53 groups of putative orthologous genes that are cold-regulated in S. commersonii, S. tuberosum, and A. thaliana were identified. Given that the evolutionary distance between the two Solanum species and A. thaliana is 112–156 million years, it seems likely that these conserved coldregulated genes—many of which encode transcription factors and proteins of unknown function—have fundamental roles in plant growth and development at low temperature.

View Accepted Manuscript (DOE)

Research Organization:: Michigan State Univ., East Lansing, MI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: FG02-91ER20021

OSTI ID:: 1625370

Journal Information:: Journal of Experimental Botany, Journal Name: Journal of Experimental Botany Journal Issue: 11 Vol. 62; ISSN 0022-0957

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (61)

AnArabidopsisGene Family Encoding DRE/CRT Binding Proteins Involved in Low-Temperature-Responsive Gene Expression Shinwari, Zabta K.; Nakashima, Kazuo; Miura, Setsuko Biochemical and Biophysical Research Communications, Vol. 250, Issue 1 https://doi.org/10.1006/bbrc.1998.9267	journal	September 1998
Rates of Nucleotide Substitution in Angiosperm Mitochondrial DNA Sequences and Dates of Divergence Between Brassica and Other Angiosperm Lineages Yang, Yau-Wen; Lai, Kun-Nan; Tai, Pon-Yean Journal of Molecular Evolution, Vol. 48, Issue 5 https://doi.org/10.1007/pl00006502	journal	May 1999
The low temperature-responsive, Solanum CBF1 genes maintain high identity in their upstream regions in a genomic environment undergoing gene duplications, deletions, and rearrangements Pennycooke, Joyce C.; Cheng, Hongmei; Roberts, Stephanie M. Plant Molecular Biology, Vol. 67, Issue 5 https://doi.org/10.1007/s11103-008-9333-5	journal	April 2008
Identification of genes associated with cold acclimation in perennial ryegrass Zhang, Chunzhen; Fei, Shui-zhang; Warnke, Scott Journal of Plant Physiology, Vol. 166, Issue 13 https://doi.org/10.1016/j.jplph.2009.03.001	journal	September 2009
Cold stress regulation of gene expression in plants Chinnusamy, Viswanathan; Zhu, Jianhua; Zhu, Jian-Kang Trends in Plant Science, Vol. 12, Issue 10 https://doi.org/10.1016/j.tplants.2007.07.002	journal	October 2007
An AP2 domain transcription factor HvCBF1 activates expression of cold-responsive genes in barley through interaction with a (G/a)(C/t)CGAC motif Xue, Gang-Ping Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression, Vol. 1577, Issue 1 https://doi.org/10.1016/s0167-4781(02)00410-4	journal	August 2002
Arabidopsis Transcriptional Activators CBF1, CBF2, and CBF3 have Matching Functional Activities Gilmour, Sarah J.; Fowler, Sarah G.; Thomashow, Michael F. Plant Molecular Biology, Vol. 54, Issue 5 https://doi.org/10.1023/b:plan.0000040902.06881.d4	journal	March 2004
Evolution of gene expression in the Drosophila melanogaster subgroup Rifkin, Scott A.; Kim, Junhyong; White, Kevin P. Nature Genetics, Vol. 33, Issue 2 https://doi.org/10.1038/ng1086	journal	January 2003
Comparing genomic expression patterns across species identifies shared transcriptional profile in aging McCarroll, Steven A.; Murphy, Coleen T.; Zou, Sige Nature Genetics, Vol. 36, Issue 2 https://doi.org/10.1038/ng1291	journal	January 2004
Early light-induced proteins protect Arabidopsis from photooxidative stress Hutin, C.; Nussaume, L.; Moise, N. Proceedings of the National Academy of Sciences, Vol. 100, Issue 8 https://doi.org/10.1073/pnas.0736939100	journal	April 2003
Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit Stockinger, E. J.; Gilmour, S. J.; Thomashow, M. F. Proceedings of the National Academy of Sciences, Vol. 94, Issue 3 https://doi.org/10.1073/pnas.94.3.1035	journal	February 1997
affy--analysis of Affymetrix GeneChip data at the probe level Gautier, L.; Cope, L.; Bolstad, B. M. Bioinformatics, Vol. 20, Issue 3 https://doi.org/10.1093/bioinformatics/btg405	journal	February 2004
Simpleaffy: a BioConductor package for Affymetrix Quality Control and data analysis Wilson, C. L.; Miller, C. J. Bioinformatics, Vol. 21, Issue 18 https://doi.org/10.1093/bioinformatics/bti605	journal	August 2005
Exploration, normalization, and summaries of high density oligonucleotide array probe level data Irizarry, Rafael A.; Hobbs, Bridget; Collin, Francois Biostatistics, Vol. 4, Issue 2, p. 249-264 https://doi.org/10.1093/biostatistics/4.2.249	journal	April 2003
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A. Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402 https://doi.org/10.1093/nar/25.17.3389	journal	September 1997
The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis Lee, H. Genes & Development, Vol. 14, Issue 18 https://doi.org/10.1101/gad.813600	journal	September 2000
Barley Cbf3 Gene Identification, Expression Pattern, and Map Location Choi, Dong-Woog; Rodriguez, Edmundo M.; Close, Timothy J. Plant Physiology, Vol. 129, Issue 4 https://doi.org/10.1104/pp.003046	journal	June 2002
Heterology Expression of the Arabidopsis C-Repeat/Dehydration Response Element Binding Factor 1 Gene Confers Elevated Tolerance to Chilling and Oxidative Stresses in Transgenic Tomato Hsieh, Tsai-Hung; Lee, Jent-Turn; Yang, Pei-Tzu Plant Physiology, Vol. 129, Issue 3 https://doi.org/10.1104/pp.003442	journal	June 2002
Importance of Lineage-Specific Expansion of Plant Tandem Duplicates in the Adaptive Response to Environmental Stimuli Hanada, Kousuke; Zou, Cheng; Lehti-Shiu, Melissa D. Plant Physiology, Vol. 148, Issue 2 https://doi.org/10.1104/pp.108.122457	journal	August 2008
Overexpression of the Arabidopsis CBF3 Transcriptional Activator Mimics Multiple Biochemical Changes Associated with Cold Acclimation Gilmour, Sarah J.; Sebolt, Audrey M.; Salazar, Maite P. Plant Physiology, Vol. 124, Issue 4 https://doi.org/10.1104/pp.124.4.1854	journal	December 2000
Arabidopsis Transcriptome Profiling Indicates That Multiple Regulatory Pathways Are Activated during Cold Acclimation in Addition to the CBF Cold Response Pathway Fowler, Sarah; Thomashow, Michael F. The Plant Cell, Vol. 14, Issue 8 https://doi.org/10.1105/tpc.003483	journal	July 2002
Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems Maruyama, Kyonoshin; Sakuma, Yoh; Kasuga, Mie The Plant Journal, Vol. 38, Issue 6 https://doi.org/10.1111/j.1365-313x.2004.02100.x	journal	June 2004
Expressed sequence tag analysis of the response of apple (Malus x domestica ‘Royal Gala’) to low temperature and water deficit Wisniewski, Michael; Bassett, Carole; Norelli, John Physiologia Plantarum, Vol. 133, Issue 2 https://doi.org/10.1111/j.1399-3054.2008.01063.x	journal	June 2008
Use of a stress inducible promoter to drive ectopic AtCBF expression improves potato freezing tolerance while minimizing negative effects on tuber yield Pino, María-Teresa; Skinner, Jeffrey S.; Park, Eung-Jun Plant Biotechnology Journal, Vol. 5, Issue 5 https://doi.org/10.1111/j.1467-7652.2007.00269.x	journal	September 2007
Sex-Dependent Gene Expression and Evolution of the Drosophila Transcriptome Ranz, J. M. Science, Vol. 300, Issue 5626 https://doi.org/10.1126/science.1085881	journal	June 2003
Arabidopsis CBF1 Overexpression Induces COR Genes and Enhances Freezing Tolerance Jaglo-Ottosen, K. R. Science, Vol. 280, Issue 5360 https://doi.org/10.1126/science.280.5360.104	journal	April 1998
Comparative analyses reveal distinct sets of lineage-specific genes within Arabidopsis thaliana Lin, Haining; Moghe, Gaurav; Ouyang, Shu BMC Evolutionary Biology, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2148-10-41	journal	January 2010
Evolution of Stress-Regulated Gene Expression in Duplicate Genes of Arabidopsis thaliana Zou, Cheng; Lehti-Shiu, Melissa D.; Thomashow, Michael PLoS Genetics, Vol. 5, Issue 7 https://doi.org/10.1371/journal.pgen.1000581	journal	July 2009
Two Transcription Factors, DREB1 and DREB2, with an EREBP/AP2 DNA Binding Domain Separate Two Cellular Signal Transduction Pathways in Drought- and Low-Temperature-Responsive Gene Expression, Respectively, in Arabidopsis Liu, Qiang; Kasuga, Mie; Sakuma, Yoh The Plant Cell, Vol. 10, Issue 8 https://doi.org/10.2307/3870648	journal	August 1998
NAC genes Jensen, Michael Krogh; Kjaersgaard, Trine; Petersen, Klaus Plant Signaling & Behavior, Vol. 5, Issue 7 https://doi.org/10.4161/psb.5.7.12099	journal	July 2010
Bioinformatics and Computational Biology Solutions Using R and Bioconductor Gentleman, Robert; Carey, Vincent J.; Huber, Wolfgang Statistics for Biology and Health https://doi.org/10.1007/0-387-29362-0	book	January 2005
Rates of Nucleotide Substitution in Angiosperm Mitochondrial DNA Sequences and Dates of Divergence Between Brassica and Other Angiosperm Lineages Yang, Yau-Wen; Lai, Kun-Nan; Tai, Pon-Yean Journal of Molecular Evolution, Vol. 48, Issue 5 https://doi.org/10.1007/PL00006502	journal	May 1999
An AP2 domain transcription factor HvCBF1 activates expression of cold-responsive genes in barley through interaction with a (G/a)(C/t)CGAC motif Xue, Gang-Ping Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression, Vol. 1577, Issue 1 https://doi.org/10.1016/S0167-4781(02)00410-4	journal	August 2002
Gene expression in potato during cold exposure: Changes in carbohydrate and polyamine metabolisms Oufir, Mouhssin; Legay, Sylvain; Nicot, Nathalie Plant Science, Vol. 175, Issue 6 https://doi.org/10.1016/j.plantsci.2008.08.010	journal	December 2008
Genome-wide identification of lineage-specific genes in Arabidopsis, Oryza and Populus Yang, Xiaohan; Jawdy, Sara; Tschaplinski, Timothy J. Genomics, Vol. 93, Issue 5 https://doi.org/10.1016/j.ygeno.2009.01.002	journal	May 2009
Arabidopsis Transcriptional Activators CBF1, CBF2, and CBF3 have Matching Functional Activities Gilmour, Sarah J.; Fowler, Sarah G.; Thomashow, Michael F. Plant Molecular Biology, Vol. 54, Issue 5 https://doi.org/10.1023/B:PLAN.0000040902.06881.d4	journal	March 2004
A genetic signature of interspecies variations in gene expression Tirosh, Itay; Weinberger, Adina; Carmi, Miri Nature Genetics, Vol. 38, Issue 7 https://doi.org/10.1038/ng1819	journal	June 2006
The Arabidopsis thaliana NAC transcription factor family: structure–function relationships and determinants of ANAC019 stress signalling Jensen, Michael K.; Kjaersgaard, Trine; Nielsen, Michael M. Biochemical Journal, Vol. 426, Issue 2 https://doi.org/10.1042/BJ20091234	journal	February 2010
Sugar/osmoticum levels modulate differential abscisic acid-independent expression of two stress-responsive sucrose synthase genes in Arabidopsis DÉJardin, Annabelle; Sokolov, Lubomir N.; Kleczkowski, Leszek A. Biochemical Journal, Vol. 344, Issue 2 https://doi.org/10.1042/bj3440503	journal	November 1999
OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression Dubouzet, Joseph G.; Sakuma, Yoh; Ito, Yusuke The Plant Journal, Vol. 33, Issue 4 https://doi.org/10.1046/j.1365-313X.2003.01661.x	journal	February 2003
Low temperature regulation of theArabidopsisCBF family of AP2 transcriptional activators as an early step in cold-inducedCORgene expression Gilmour, Sarah J.; Zarka, Daniel G.; Stockinger, Eric J. The Plant Journal, Vol. 16, Issue 4 https://doi.org/10.1046/j.1365-313x.1998.00310.x	journal	November 1998
Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis Umezawa, T.; Sugiyama, N.; Mizoguchi, M. Proceedings of the National Academy of Sciences, Vol. 106, Issue 41 https://doi.org/10.1073/pnas.0907095106	journal	September 2009
Statistical significance for genomewide studies Storey, J. D.; Tibshirani, R. Proceedings of the National Academy of Sciences, Vol. 100, Issue 16, p. 9440-9445 https://doi.org/10.1073/pnas.1530509100	journal	July 2003
Cluster analysis and display of genome-wide expression patterns Eisen, M. B.; Spellman, P. T.; Brown, P. O. Proceedings of the National Academy of Sciences, Vol. 95, Issue 25 https://doi.org/10.1073/pnas.95.25.14863	journal	December 1998
Phylogeny and substitution rates of angiosperm actin genes Moniz de Sa, M.; Drouin, G. Molecular Biology and Evolution, Vol. 13, Issue 9 https://doi.org/10.1093/oxfordjournals.molbev.a025685	journal	November 1996
A Combination of the Arabidopsis DREB1A Gene and Stress-Inducible rd29A Promoter Improved Drought- and Low-Temperature Stress Tolerance in Tobacco by Gene Transfer Kasuga, Mie; Miura, Setsuko; Shinozaki, Kazuo Plant and Cell Physiology, Vol. 45, Issue 3 https://doi.org/10.1093/pcp/pch037	journal	March 2004
Using the quantitative genetic threshold model for inferences between and within species Felsenstein, Joseph Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 360, Issue 1459 https://doi.org/10.1098/rstb.2005.1669	journal	July 2005
Components of the Arabidopsis C-Repeat/Dehydration-Responsive Element Binding Factor Cold-Response Pathway Are Conserved in Brassica napus and Other Plant Species Jaglo, Kirsten R.; Kleff, Susanne; Amundsen, Keenan L. Plant Physiology, Vol. 127, Issue 3 https://doi.org/10.1104/pp.010548	journal	November 2001
The Arabidopsis CBF Gene Family Is Composed of Three Genes Encoding AP2 Domain-Containing Proteins Whose Expression Is Regulated by Low Temperature but Not by Abscisic Acid or Dehydration Medina, Joaquı́n; Bargues, Mónica; Terol, Javier Plant Physiology, Vol. 119, Issue 2 https://doi.org/10.1104/pp.119.2.463	journal	February 1999
Characteristics of Cold Acclimation and Deacclimation in Tuber-bearing Solanum Species Chen, Hwei-Hwang; Li, Paul H. Plant Physiology, Vol. 65, Issue 6 https://doi.org/10.1104/pp.65.6.1146	journal	June 1980
Two Transcription Factors, DREB1 and DREB2, with an EREBP/AP2 DNA Binding Domain Separate Two Cellular Signal Transduction Pathways in Drought- and Low-Temperature-Responsive Gene Expression, Respectively, in Arabidopsis Liu, Qiang; Kasuga, Mie; Sakuma, Yoh The Plant Cell, Vol. 10, Issue 8 https://doi.org/10.1105/tpc.10.8.1391	journal	August 1998
The age of the Angiosperms: a Molecular Timescale Without a Clock Bell, Charles D.; Soltis, Douglas E.; Soltis, Pamela S. Evolution, Vol. 59, Issue 6 https://doi.org/10.1111/j.0014-3820.2005.tb01775.x	journal	June 2005
The CBF1-dependent low temperature signalling pathway, regulon and increase in freeze tolerance are conserved in Populus spp. Benedict, Catherine; Skinner, Jeffrey S.; Meng, Rengong Plant, Cell and Environment, Vol. 29, Issue 7 https://doi.org/10.1111/j.1365-3040.2006.01505.x	journal	July 2006
Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems Maruyama, Kyonoshin; Sakuma, Yoh; Kasuga, Mie The Plant Journal, Vol. 38, Issue 6 https://doi.org/10.1111/j.1365-313X.2004.02100.x	journal	June 2004
Freezing-sensitive tomato has a functional CBF cold response pathway, but a CBF regulon that differs from that of freezing-tolerant Arabidopsis Zhang, Xin; Fowler, Sarah G.; Cheng, Hongmei The Plant Journal, Vol. 39, Issue 6 https://doi.org/10.1111/j.1365-313X.2004.02176.x	journal	September 2004
Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis: Arabidopsis low temperature transcriptome Vogel, Jonathan T.; Zarka, Daniel G.; Van Buskirk, Heather A. The Plant Journal, Vol. 41, Issue 2 https://doi.org/10.1111/j.1365-313X.2004.02288.x	journal	November 2004
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 Kilian, Joachim; Whitehead, Dion; Horak, Jakub The Plant Journal, Vol. 50, Issue 2 https://doi.org/10.1111/j.1365-313X.2007.03052.x	journal	March 2007
Nuclear-mitochondrial cross-talk during heat shock in Arabidopsis cell culture: Nuclear-mitochondrial cross-talk Rikhvanov, Eugene G.; Gamburg, Kim Z.; Varakina, Nina N. The Plant Journal, Vol. 52, Issue 4 https://doi.org/10.1111/j.1365-313X.2007.03275.x	journal	September 2007
Arabidopsis transcription factors regulating cold acclimation Van Buskirk, Heather A.; Thomashow, Michael F. Physiologia Plantarum, Vol. 126, Issue 1 https://doi.org/10.1111/j.1399-3054.2006.00625.x	journal	January 2006
Putative cold acclimation pathways in Arabidopsis thaliana identified by a combined analysis of mRNA co-expression patterns, promoter motifs and transcription factors Chawade, Aakash; Bräutigam, Marcus; Lindlöf, Angelica BMC Genomics, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2164-8-304	journal	January 2007
Linear Models and Empirical Bayes Methods for Assessing Differential Expression in Microarray Experiments Smyth, Gordon K. Statistical Applications in Genetics and Molecular Biology, Vol. 3, Issue 1 https://doi.org/10.2202/1544-6115.1027	journal	January 2004

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Effects of low temperature and low irradiance on the physiological characteristics and related gene expression of different pepper species Ou, L. J.; Wei, G.; Zhang, Z. Q. Photosynthetica, Vol. 53, Issue 1 https://doi.org/10.1007/s11099-015-0084-7	journal	March 2015
Tomato expressing Arabidopsis glutaredoxin gene AtGRXS17 confers tolerance to chilling stress via modulating cold responsive components Hu, Ying; Wu, Qingyu; Sprague, Stuart A. Horticulture Research, Vol. 2, Issue 1 https://doi.org/10.1038/hortres.2015.51	journal	November 2015
DNA binding by the plant-specific NAC transcription factors in crystal and solution: a firm link to WRKY and GCM transcription factors Welner, Ditte H.; Lindemose, Søren; Grossmann, J. Günter Biochemical Journal, Vol. 444, Issue 3 https://doi.org/10.1042/bj20111742	journal	May 2012
Low-Temperature Triggered Varied Antioxidant Responses in Tomato Khan, Tanveer A.; Fariduddin, Qazi; Yusuf, Mohammad International Journal of Vegetable Science, Vol. 21, Issue 4 https://doi.org/10.1080/19315260.2014.881453	journal	August 2014
RhERF113 Functions in Ethylene-Induced Petal Senescence by Modulating Cytokinin Content in Rose Khaskheli, Allah Jurio; Ahmed, Waqas; Ma, Chao Plant and Cell Physiology https://doi.org/10.1093/pcp/pcy162	journal	August 2018
Functional characterization of two almond C-repeat-binding factors involved in cold response Barros, P. M.; Goncalves, N.; Saibo, N. J. M. Tree Physiology, Vol. 32, Issue 9 https://doi.org/10.1093/treephys/tps067	journal	July 2012
Topological features of a gene co-expression network predict patterns of natural diversity in environmental response Des Marais, David L.; Guerrero, Rafael F.; Lasky, Jesse R. Proceedings of the Royal Society B: Biological Sciences, Vol. 284, Issue 1856 https://doi.org/10.1098/rspb.2017.0914	journal	June 2017
Rapid and dynamic alternative splicing impacts the Arabidopsis cold response transcriptome Calixto, Cristiane P. G.; Guo, Wenbin; James, Allan B. The Plant Cell https://doi.org/10.1101/251876	posted_content	January 2018
Rapid and Dynamic Alternative Splicing Impacts the Arabidopsis Cold Response Transcriptome Calixto, Cristiane P. G.; Guo, Wenbin; James, Allan B. The Plant Cell, Vol. 30, Issue 7 https://doi.org/10.1105/tpc.18.00177	journal	May 2018
Low-temperature perception leading to gene expression and cold tolerance in higher plants Knight, Marc R.; Knight, Heather New Phytologist, Vol. 195, Issue 4 https://doi.org/10.1111/j.1469-8137.2012.04239.x	journal	July 2012
Growth temperature impact on leaf form and function in Arabidopsis thaliana ecotypes from northern and southern Europe: Impact of temperature on A. thaliana ecotypes Stewart, Jared J.; Demmig-Adams, Barbara; Cohu, Christopher M. Plant, Cell & Environment, Vol. 39, Issue 7 https://doi.org/10.1111/pce.12720	journal	April 2016
Low temperature sensors in plants: Hypotheses and assumptions Markovskaya, E. F.; Shibaeva, T. G. Biology Bulletin, Vol. 44, Issue 2 https://doi.org/10.1134/s1062359017020145	journal	March 2017
Identification of Genes Differentially Expressed in Response to Cold in Pisum sativum Using RNA Sequencing Analyses Bahrman, Nasser; Hascoët, Emilie; Jaminon, Odile Plants, Vol. 8, Issue 8 https://doi.org/10.3390/plants8080288	journal	August 2019

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