Diane Jofuku Okamuro
IOS Division of Integrative Organismal Systems
BIO Directorate for Biological Sciences
Start Date:
September 1, 2001
Expires:
August 31, 2008 (Estimated)
Awarded Amount to Date:
$5591234
Investigator(s):
Michael Thomashow thomash6@msu.edu (Principal Investigator)
Tony Chen (Co-Principal Investigator) Patrick Hayes (Co-Principal Investigator) Eric Stockinger (Co-Principal Investigator)
Sponsor:
Michigan State University
CONTRACT AND GRANT ADMINISTRATIO
EAST LANSING, MI 48824 517/355-5040
NSF Program(s):
PLANT GENOME RESEARCH PROJECT
Field Application(s):
Program Reference Code(s):
BIOT, 9109
Program Element Code(s):
1329
ABSTRACT
Plants vary greatly in their responses to cold temperatures. At one extreme are plants from tropical and subtropical regions such as soybean and rice, which suffer injury when exposed to chilling temperatures between 0 and 12 degrees Celcius. In sharp contrast, plants from temperate regions are not only chilling tolerant, but many, such as Arabidopsis and wheat, can survive freezing after exposure to low nonfreezing temperatures, a phenomenon known as "cold acclimation."
The overall goal of this project is to understand the "genomic" basis of cold tolerance. The specific focus will be to develop a more detailed understanding of how plants respond to low temperature in terms of altering gene expression. This emphasis is motivated by the recent demonstration in Arabidopsis that cold acclimation involves the action of cold-regulated genes including the CBF regulon, a group of genes that imparts freezing tolerance and is coordinately regulated by the CBF transcriptional activators.
This project will comprise three related lines of investigation. In the first, a low temperature "wiring diagram" will be constructed that includes a definition of low temperature regulatory circuits and the gene regulons that they control. The second line of investigation will be to determine the similarities and differences of low temperature-regulated genes in plants that differ in freezing tolerance. The third line of investigation will be to determine whether the Arabidopsis CBF cold-response pathway is highly conserved in other plants and whether differences in plant cold tolerance can be traced to differences in CBF cold-response pathways. Comparative and functional genomics approaches will be used to address these issues including gene expression profiling using DNA microarrays.
In sum, these lines of investigation will provide a deeper understanding of the "genomic mechanisms" that plants have evolved to cope with low temperature and have the potential to provide "genetic tools" to improve the cold tolerance of plants, traits of considerable agronomic and economic importance. In as much as the CBF regulon not only imparts freezing tolerance, but dehydration tolerance as well, the results of this project also have the potential to provide genetic tools to improve the drought and salinity tolerance of agriculturally important plants.
Deliverables:
Microarray data and other information about the project can be found at:
http://aztec.stanford.edu/cold.
PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH
Benedict, C, JS Skinner, R Meng, Y Chang, R Bhalerao, NPA Huner, CE Finn, THH Chen, and V Hurry. 2006.. "The CBF1-dependent low temperature signalling pathway, regulon and increase in freeze tolerance are conserved in Populus spp.," Plant, Cell and Environment, v.29, 2006, p. 1259.
Cook D., S. Fowler, O. Fiehn and M.F. Thomashow.. "A prominent role of the CBF cold response pathway in configuring the low temperature metabolome of Arabidopsis. (article is subject of associated commentary).," Proc Natl Acad Sci USA, v.101, 2004, p. 15243.
Fowler S and MF Thomashow. "Arabidopsis transcriptome profiling indicates multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold-response pathway," The Plant Cell, v.14, 2002, p. 1675.
Fowler, S.G., D. Cook, and M.F. Thomashow.. "Low temperature induction of Arabidopsis CBF1-3 is gated by the circadian clock.," Plant Physiol, v.137, 2005, p. 961.
Francia, E., F. Rizza, L. Cattivelli, A.M. Stanca, G. Galiba, B. Toth, P.M. Hayes, J.S. Skinner, and N. Pecchioni.. "Two loci on chromosome 5H determine low-temperature tolerance in a 'Nure' (winter) x 'Tremois' (spring) barley map.," Theor Appl Genet, v.108, 2004, p. 670.
Francia, E; Barabaschi, D; Tondelli, A; Laido, G; Rizza, F; Stanca, AM; Busconi, M; Fogher, C; Stockinger, EJ; Pecchioni, N. "Fine mapping of a HvCBF gene cluster at the frost resistance locus Fr-H2 in barley," THEORETICAL AND APPLIED GENETICS, v.115, 2007, p. 1083-1091.
Fu, D., P. Szű cs, L. Yan, M. Helguera, J.S. Skinner, J. von Zitzewitz, P.M. Hayes and J. Dubcovsky.. "Large deletions within the first intron in VRN-1 are associated with spring growth habit in barley and wheat.," Mol Genet Genom., v.273, 2005, p. 54.
Gilmour S.J., S.G. Fowler and M.F. Thomashow.. "Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities.," Plant Mol Biol, v.54, 2004, p. 767.
Karsai, I; Szucs, P; Koszegi, B; Hayes, PM; Casas, A; Bedo, Z; Veisz, O. "Effects of photo and thermo cycles on flowering time in barley: a genetical phenomics approach," JOURNAL OF EXPERIMENTAL BOTANY, v.59, 2008, p. 2707-2715.
Karsai, I; Szucs, P; Meszaros, K; Filichkina, T; Hayes, PM; Skinner, JS; Lang, L; Bedo, Z. "The Vrn-H2 locus is a major determinant of flowering time in a facultative x winter growth habit barley (Hordeum vulgare L.) mapping population," THEORETICAL AND APPLIED GENETICS, v.110, 2005, p. 1458-1466.
Knox, AK; Li, CX; Vagujfalvi, A; Galilba, G; Stockinger, EJ; Dubcovsky, J. "Identification of candidate CBF genes for the frost tolerance locus Fr-A(m)2 in Triticum monococcum," PLANT MOLECULAR BIOLOGY, v.67, 2008, p. 257-270.
Koti, K; Karsai, I; Szucs, P; Horvath, C; Meszaros, K; Kiss, GB; Bedo, Z; Hayes, PM. "Validation of the two-gene epistatic model for vernalization response in a winter x spring barley cross," EUPHYTICA, v.152, 2006, p. 17-24.
Limin, A; Corey, A; Hayes, P; Fowler, DB. "Low-temperature acclimation of barley cultivars used as parents in mapping populations: response to photoperiod, vernalization and phenological development," PLANTA, v.226, 2007, p. 139-146.
Pennycooke, JC; Cheng, H; Stockinger, EJ. "Comparative genomic sequence and expression analyses of Medicago truncatula and alfalfa subspecies falcata COLD-ACCLIMATION-SPECIFIC genes," PLANT PHYSIOLOGY, v.146, 2008, p. 1242-1254.
Pennycooke, JC; Cheng, HM; Roberts, SM; Yang, QF; Rhee, SY; Stockinger, EJ. "The low temperature-responsive, Solanum CBF1 genes maintain high identity in their upstream regions in a genomic environment undergoing gene duplications, deletions, and rearrangements," PLANT MOLECULAR BIOLOGY, v.67, 2008, p. 483-497.
Pino, MT; Skinner, JS; Jeknic, Z; Hayes, PM; Soeldner, AH; Thomashow, MF; Chen, THH. "Ectopic AtCBF1 over-expression enhances freezing tolerance and induces cold acclimation-associated physiological modifications in potato," PLANT CELL AND ENVIRONMENT, v.31, 2008, p. 393-406.
Pino, MT; Skinner, JS; Jeknic, Z; Park, EJ; Hayes, PM; Chen, THH. "Ectopic overexpression of AtCBF1 in potato enhances freezing tolerance in: Cold hardiness in plants: molecular genetics," PLANT BIOTECHNOLOGY JOURNAL, v.5, 2007, p. 676-676.
Pino, MT; Skinner, JS; Park, EJ; Jeknic, Z; Hayes, PM; Thornashow, MF; Chen, THH. "Use of a stress inducible promoter to drive ectopic AtCBF expression improves potato freezing tolerance while minimizing negative effects on tuber yield," PLANT BIOTECHNOLOGY JOURNAL, v.5, 2007, p. 591-604.
Skinner, J.S., P. Szûcs, J. von Zitzewitz, L. Marquez-Cedillo, T. Filichkin, M.F. Thomashow, E.J. Stockinger, TH.H. Chen, and P.M. Hayes.. "Mapping of barley homologs to genes that regulate low temperature tolerance in Arabidopsis.," Theor. Appl. Genet., v.112, 2006, p. 832.
Skinner, J.S., Szucs, P., von Zitzewitz, J., Marquez-Cedillo, L., Filichkin, T., Stockinger, E.J., Thomashow, M.F., Chen, T.H. and Hayes, P.M. "Mapping of barley homologs to genes that regulate low temperature tolerance in Arabidopsis.," Theor. Appl. Genet, v.112, 2006, p. 832.
Skinner, J.S., von Zitzewitz, J., Szucs, P., Marquez-Cedillo, L., Filichkin, T., Amundsen, K., Stockinger, E.J., Thomashow, M.F., Chen, T.H. and Hayes, P.M.. "Structural, Functional, and Phylogenetic Characterization of a Large CBF Gene Family in Barley.," Plant Mol. Biol., v.59, 2005, p. 533.
Stockinger, EJ; Skinner, JS; Gardner, KG; Francia, E; Pecchioni, N. "Expression levels of barley Cbf genes at the Frost resistance-H2 locus are dependent upon alleles at Fr-H1 and Fr-H2," PLANT JOURNAL, v.51, 2007, p. 308-321.
Szûcs, P., I. Karsai, J. von Zitzewitz, K. Mészáros, L.L.D. Cooper, Y.Q. Gu, T.H.H. Chen, P.M. Hayes, and J.S. Skinner.. "Positional relationships between photoperiod response QTL and photoreceptor and vernalization genes in barley.," Theor. Appl. Genet, v.112, 2006, p. 1277.
Szûcs, P., J. Skinner, I. Karsai, A. Cuesta-Marcos, K.G. Haggard, A.E. Corey, T.H.H. Chen, and P.M. Hayes. "Validation of the VRN-H2/VRN-H1 epistatic model in barley reveals that intron length variation in VRN-H1 may account for a continuum of vernalization sensitivity.," Mol. Genet. Genomics, v.277, 2007, p. 249.
Szucs, P; Skinner, JS; Karsai, I; Cuesta-Marcos, A; Haggard, KG; Corey, AE; Chen, THH; Hayes, PM. "Validation of the VRN-H2/VRN-H1 epistatic model in barley reveals that intron length variation in VRN-H1 may account for a continuum of vernalization sensitivity," MOLECULAR GENETICS AND GENOMICS, v.277, 2007, p. 249-261.
Tondelli, A; Francia, E; Barabaschi, D; Aprile, A; Skinner, JS; Stockinger, EJ; Stanca, AM; Pecchioni, N. "Mapping regulatory genes as candidates for cold and drought stress tolerance in barley," THEORETICAL AND APPLIED GENETICS, v.112, 2006, p. 445-454.
Van Buskirk, HA; Thomashow, MF. "Arabidopsis transcription factors regulating cold acclimation," PHYSIOLOGIA PLANTARUM, v.126, 2006, p. 72-80.
Vogel, J.T., D.G. Zarka, H.A. Van Buskirk, S.G. Fowler, and M.F. Thomashow.. "Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis.," Plant J, v.41, 2005, p. 195.
von Zitzewitz, J., P. Szű cs, J. Dubcovsky, L. Yan, E. Francia, N. Pecchioni, A. Casas, T.H.H. Chen, P.M. Hayes and J.S. Skinner.. "Structural and functional characterization of barley vernalization genes.," Plant Mol Biol, v.59, 2005, p. 449.
von Zitzewitz, J; Szucs, P; Dubcovsky, J; Yan, LL; Francia, E; Pecchioni, N; Casas, A; Chen, THH; Hayes, PM; Skinner, JS. "Molecular and structural characterization of barley vernalization genes," PLANT MOLECULAR BIOLOGY, v.59, 2005, p. 449-467.
Yan, LL; von Zitzewitz, J; Skinner, JS; Hayes, PM; Dubcovsky, J. "Molecular characterization of the duplicated meristem identity genes HvAP1a and HvAP1b in barley," GENOME, v.48, 2005, p. 905-912.
Zhang, X., S. Fowler, H. Cheng, Y. Lou, S.Y. Rhee, E.J. Stockinger and M.F. Thomashow.. "Freezing sensitive tomato has a functional CBF cold response pathway, but a CBF regulon that differs from that of freezing tolerant Arabidopsis.
," Plant J, v.39, 2004, p. 905.