Arabidopsis Transcriptome Profiling Indicates That Multiple Regulatory Pathways Are Activated during Cold Acclimation in Addition to the CBF Cold Response Pathway[W]
Tóm tắt
Many plants, including Arabidopsis, increase in freezing tolerance in response to low, nonfreezing temperatures, a phenomenon known as cold acclimation. Previous studies established that cold acclimation involves rapid expression of the CBF transcriptional activators (also known as DREB1 proteins) in response to low temperature followed by induction of the CBF regulon (CBF-targeted genes), which contributes to an increase in freezing tolerance. Here, we present the results of transcriptome-profiling experiments indicating the existence of multiple low-temperature regulatory pathways in addition to the CBF cold response pathway. The transcript levels of ∼8000 genes were determined at multiple times after plants were transferred from warm to cold temperature and in warm-grown plants that constitutively expressed CBF1, CBF2, or CBF3. A total of 306 genes were identified as being cold responsive, with transcripts for 218 genes increasing and those for 88 genes decreasing threefold or more at one or more time points during the 7-day experiment. These results indicate that extensive downregulation of gene expression occurs during cold acclimation. Of the cold-responsive genes, 48 encode known or putative transcription factors. Two of these, RAP2.1 and RAP2.6, were activated by CBF expression and thus presumably control subregulons of the CBF regulon. Transcriptome comparisons indicated that only 12% of the cold-responsive genes are certain members of the CBF regulon. Moreover, at least 28% of the cold-responsive genes were not regulated by the CBF transcription factors, including 15 encoding known or putative transcription factors, indicating that these cold-responsive genes are members of different low-temperature regulons. Significantly, CBF expression at warm temperatures repressed the expression of eight genes that also were downregulated by low temperature, indicating that in addition to gene induction, gene repression is likely to play an integral role in cold acclimation.
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Abler, M.L., and Green, P.L. (1996). Control of mRNA stability in higher plants. Plant Mol. Biol. 32 , 63–78.
Adamska, I. (1997). ELIPs: Light induced stress proteins. Physiol. Plant. 100 , 794–805.
Baker, S.S., Wilhelm, K.S., and Thomashow, M.F. (1994). The 5′-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant Mol. Biol. 24 , 701–713.
Beator, J., Pötter, E., and Kloppstech, K. (1992). Coordinated circadian regulation of mRNA levels for light-regulated genes and of the capacity for accumulation of chlorophyll protein complexes. Plant Physiol. 100 , 1780–1786.
Ciardi, J.A., Deikman, J., and Orzolek, M.D. (1997). Increased ethylene synthesis enhances chilling tolerance in tomato. Physiol. Plant. 101 , 333–340.
Desikan, R., A.-H.-Mackerness, S., Hancock, J.T., and Neill, S.J. (2001). Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol. 127 , 159–172.
Eimert, K., Wang, S.-M., Lue, W.-L., and Chen, J. (1995). Monogenic recessive mutations causing both late floral initiation and excess starch accumulation in Arabidopsis. Plant Cell 7 , 1703–1712.
Fowler, S., Lee, K., Onouchi, H., Samach, A., Richardson, K., Morris, B., Coupland, G., and Putterill, J. (1999). GIGANTEA: A circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. EMBO J. 18 , 4679–4688.
Fujimoto, S.Y., Ohta, M., Usui, A., Shinshi, H., and Ohme-Takagi, M. (2000). Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box–mediated gene expression. Plant Cell 12 , 393–404.
Gilmour, S.J., Sebolt, A.M., Salazar, M.P., Everard, J.D., and Thomashow, M.F. (2000). Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol. 124 , 1854–1865.
Gilmour, S.J., Zarka, D.G., Stockinger, E.J., Salazar, M.P., Houghton, J.M., and Thomashow, M.F. (1998). Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J. 16 , 433–442.
Hajela, R.K., Horvath, D.P., Gilmour, S.J., and Thomashow, M.F. (1990). Molecular cloning and expression of cor (cold-regulated) genes in Arabidopsis thaliana. Plant Physiol. 93 , 1246–1252.
Heddad, M., and Adamska, I. (2000). Light stress-regulated two-helix proteins in Arabidopsis thaliana related to the chlorophyll a/b-binding gene family. Proc. Natl. Acad. Sci. USA 97 , 3741–3746.
Heintzen, C., Melzer, S., Fischer, R., Kappeler, S., Apel, K., and Staiger, D. (1994). A light- and temperature-entrained circadian clock controls expression of transcripts encoding nuclear proteins with homology to RNA-binding proteins in meristematic tissue. Plant J. 5 , 799–813.
Huner, P.A., Öquist, G., and Sarhan, F. (1998). Energy balance and acclimation to light and cold. Trends Plant Sci. 3 , 224–230.
Huq, E., Tepperman, J.M., and Quail, P.H. (2000). GIGANTEA is a nuclear protein involved in phytochrome signaling in Arabidopsis. Proc. Natl. Acad. Sci. USA 97 , 9789–9794.
Jaglo, K.R., Kleff, S., Amundsen, K.L., Zhang, X., Haake, V., Zhang, J.Z., Deits, T., and Thomashow, M.F. (2001). Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. Plant Physiol. 127 , 910–917.
Jaglo-Ottosen, K.R., Gilmour, S.J., Zarka, D.G., Schabenberger, O., and Thomashow, M.F. (1998). Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280 , 104–106.
Kagaya, Y., Ohmiya, K., and Hattori, T. (1999). RAV1, a novel DNA-binding protein, binds to bipartite recognition sequence through two distinct DNA-binding domains uniquely found in higher plants. Nucleic Acids Res. 27 , 470–478.
Kasuga, M., Liu, Q., Miura, S., Yamaguchi-Shinozaki, K., and Shinozaki, K. (1999). Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat. Biotechnol. 17 , 287–291.
Kloppstech, K., Otto, B., and Sierralta, W. (1991). Cyclic temperature treatments of dark-grown pea seedlings induce a rise in specific transcript levels of light-regulated genes related to photomorphogenesis. Mol. Gen. Genet. 225 , 468–473.
Koornneef, M., Hanhart, C.J., and van der Veen, J.H. (1991). A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol. Gen. Genet. 229 , 57–66.
Kranz, H.D., et al. (1998). Towards functional characterization of the members of the R2R3-MYB gene family from Arabidopsis thaliana. Plant J. 16 , 263–276.
Krapp, A., and Stitt, M. (1995). An evaluation of direct and indirect mechanisms for the “sink-regulation” of photosynthesis in spinach: Changes in gas exchange, carbohydrates, metabolites, enzyme activities and steady-state transcript levels after cold-girdling source leaves. Planta 195 , 313–323.
Kyte, J., and Doolittle, R.F. (1982). A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157 , 105–132.
Lee, Y.H., and Chun, J.Y. (1998). A new homeodomain-leucine zipper gene from Arabidopsis thaliana induced by water stress and abscisic acid treatment. Plant Mol. Biol. 37 , 377–384.
Levitt, J. (1980). Responses of Plants to Environmental Stresses, 2nd ed. (New York: Academic Press).
Lipshutz, R.J., Fodor, S.P., Gingeras, T.R., and Lockhart, D.J. (1999). High density synthetic oligonucleotide arrays. Nat. Genet. 21 , 20–24.
Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K., and Shinozaki, K. (1998). 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. Plant Cell 10 , 1391–1406.
Marrs, K.A. (1996). The functions and regulation of glutathione S-transferases in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47 , 127–158.
Mayer, K., et al. (1999). Sequence and analysis of chromosome 4 of the plant Arabidopsis thaliana. Nature 402 , 769–777.
McWatters, H.G., Bastow, R.M., Hall, A., and Millar, A.J. (2000). The ELF3 zeitnehmer regulates light signalling to the circadian clock. Nature 408 , 716–720.
Meissner, R., and Michael, A.J. (1997). Isolation and characterization of a diverse family of Arabidopsis two and three-fingered C2H2 zinc finger protein genes and cDNAs. Plant Mol. Biol. 33 , 615–624.
Morgan, P.W., and Drew, M.C. (1997). Ethylene and plant responses to stress. Physiol. Plant. 100 , 620–630.
Moscovici-Kadouri, S., and Chamovitz, D.A. (1997). Characterization of a cDNA encoding the early light-inducible protein (ELIP) (accession no. U89014) from Arabidopsis (PGR 97-155). Plant Physiol. 115 , 1287.
Okamuro, J.K., Caster, B., Villarroel, R., Van Montagu, M., and Jofuku, K.D. (1997). The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. Proc. Natl. Acad. Sci. USA 94 , 7076–7081.
Østergaard, L., Pedersen, A.G., Jespersen, H.M., Brunak, S., and Welinder, K.G. (1998). Computational analyses and annotations of the Arabidopsis peroxidase gene family. FEBS Lett. 433 , 98–102.
Park, D.H., Somers, D.E., Kim, Y.S., Choy, Y.H., Lim, H.K., Soh, M.S., Kim, H.J., Kay, S.A., and Nam, H.G. (1999). Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. Science 285 , 1579–1582.
Seki, M., Narusaka, M., Abe, H., Kasuga, M., Yamaguchi-Shinozaki, K., Carninci, P., Hayashizaki, Y., and Shinozaki, K. (2001). Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 13 , 61–72.
Shinozaki, K., and Yamaguchi-Shinozaki, K. (2000). Molecular responses to dehydration and low temperature: Differences and cross-talk between two stress signaling pathways. Curr. Opin. Plant Biol. 3 , 217–223.
Shinwari, Z.K., Nakashima, K., Miura, S., Kasuga, M., Seki, M., Yamaguchi-Shinozaki, K., and Shinozaki, K. (1998). An Arabidopsis gene family encoding DRE/CRT binding proteins involved in low-temperature-responsive gene expression. Biochem. Biophys. Res. Commun. 250 , 161–170.
Steponkus, P.L. (1984). Role of the plasma membrane in freezing injury and cold acclimation. Annu. Rev. Plant Physiol. 35 , 543–584.
Steponkus, P.L., Uemura, M., Joseph, R.A., Gilmour, S.J., and Thomashow, M.F. (1998). Mode of action of the COR15a gene on the freezing tolerance of Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 95 , 14570–14575.
Stockinger, E.J., Gilmour, S.J., and Thomashow, M.F. (1997). 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. Proc. Natl. Acad. Sci. USA 94 , 1035–1040.
Strand, Å., Hurry, V., Gustafsson, P., and Gardeström, P. (1997). Development of Arabidopsis thaliana leaves at low temperatures releases the suppression of photosynthesis and photosynthetic gene expression despite the accumulation of soluble carbohydrates. Plant J. 12 , 605–614.
Taji, T., Ohsumi, C., Iuchi, S., Seki, M., Kasuga, M., Kobayashi, M., Yamaguchi-Shinozaki, K., and Shinozaki, K. (2002). Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J. 29 , 417–426.
Terryn, N., Gielen, J., De Keyser, A., Van Den Daele, H., Ardiles, W., Neyt, P., De Clercq, R., Coppieters, J., Dehais, P., Villarroel, R., Rouze, P., and Van Montagu, M. (1998). Sequence analysis of a 40-kb Arabidopsis thaliana genomic region located at the top of chromosome 1. Gene 215 , 11–17.
Thomashow, M.F. (1999). Plant cold acclimation, freezing tolerance genes and regulatory mechanisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50 , 571–599.
Thomashow, M.F. (2001). So what's new in the field of plant cold acclimation? Lots! Plant Physiol. 125 , 89–93.
Wanner, L.A., and Junttila, O. (1999). Cold-induced freezing tolerance in Arabidopsis. Plant Physiol. 120 , 391–400.
Xia, B., Ke, H., and Inouye, M. (2001). Acquirement of cold sensitivity by quadruple deletion of the cspA family and its suppression by PNPase S1 domain in Escherichia coli. Mol. Microbiol. 40 , 179–188.
Xin, Z., and Browse, J. (1998). eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant. Proc. Natl. Acad. Sci. USA 95 , 7799–7804.
Yamaguchi-Shinozaki, K., and Shinozaki, K. (1994). A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6 , 251–264.
Yamanaka, K. (1999). Cold shock response in Escherichia coli. J. Mol. Microbiol. Biotechnol. 1 , 193–202.