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Survey of gene expression in winter rye during changes in growth temperature, irradiance or excitation pressure

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Abstract

Previous comparisons of winter rye plants (Secale cereale L. cv. Musketeer) grown in a combination of specific temperature (°C)/irradiance (μmol m−2 s−1) regimes (20/50; 20/250; 20/800; 5/50; 5/250) revealed (1) that photosynthetic acclimation to low temperature mimics photosynthetic acclimation to high light because both conditions result in comparable reduction states of photosystem II (PSII), that is, comparable PSII excitation pressure; (2) that the relative redox state of PSII also appears to regulate a specific cold acclimation gene, Wcs19. In order to identify additional genes regulated differentially by either low temperature, irradiance or excitation pressure, we initiated a detailed analysis of gene expression. We identified and characterized 42 differentially expressed genes from wheat and rye. Based on their patterns of regulation under the five growth conditions employed, 37 of the cDNAs could be classified into four groups: genes regulated by PSII excitation pressure, low temperature, growth irradiance and interaction between growth temperature and irradiance. Partial sequence analyses revealed that several of these genes encode known chloroplastic proteins such as ELIPs, transketolase, carbonic anhydrase and Mg-chelatase. However, five of the genes could not be classified unambiguously into any one of these four categories. The implications of these results and the limitations of the experimental design are discussed in terms of larger-scale genomic studies designed to understand the interactions of multiple abiotic stresses to which a plant may be exposed when examining regulation of gene expression.

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References

  • Adams, W.W. III, Hoehn, A. and Demmig-Adams, B. 1995. Chilling temperatures and the xanthophyll cycle. A comparison of warmgrown and overwintering spinach. Aust. J. Plant Physiol. 22: 75–85.

    Google Scholar 

  • Adamska, I. 1997. ELIPs: light induced stress proteins. Plant Physiol. 100: 794–805.

    Google Scholar 

  • Anderson, M.B., Folta, K., Warpeha, K.M., Gibbons, J., Gao, J. and Kaufman, L.S. 1999. Blue light-directed destabilization of the pea Lhcb1* 4 transcript depends on sequences within the 5′ untranslated region. Plant Cell 11: 1579–1590.

    Google Scholar 

  • Chauvin, L.-P., Houde, M. and Sarhan, F. 1993. A leaf specific gene stimulated by light during wheat acclimation to low temperature. Plant Mol. Biol. 23: 255–265.

    Google Scholar 

  • Churin, Y., Hess, W.R. and Borner, T. 1999. Cloning and characterization of three cDNAs encoding chloroplast RNA-binding proteins from barley (Hordeum vulgare L.): differential regulation of expression by light and plastid development. Curr. Genet. 36: 173–181.

    Google Scholar 

  • Danyluk, J. and Sarhan, F. 1990. Differential mRNA expression during the induction of freezing tolerance in spring and winter wheat. Plant Cell Physiol. 31: 609–619.

    Google Scholar 

  • Danyluk, J., Perron, A., Houde, M., Limin, A., Fowler, B., Ben-hamou, N. and Sarhan, F. 1998. Accumulation of an acidic dehydrin in the vicinity of the plasma membrane during cold acclimation of wheat. Plant Cell 10: 623–638

    Google Scholar 

  • Dexter, S.T. 1933. Effects of several environmental factors on the hardening of plants. Plant Physiol. 8: 123–139.

    Google Scholar 

  • Dickey, L.F., Gallo-Meagher, M. and Thompson, W.F. 1992. Light regulatory sequences are located within the 5′ portion of the Fed-1 message sequence. EMBO J. 11: 2311–2317.

    Google Scholar 

  • Dickey, L.F., Nguyen, T.T., Allen, G.C. and Thompson, W.F. 1994. Light modulation of ferredoxin mRNA abundance requires an open reading frame. Plant Cell 6: 1171–1176.

    Google Scholar 

  • Dykema, P.E., Sipes, P.R., Marie, A., Biermann, B.J., Crowell, D.N. and Randall, S.K. 1999. A new class of proteins capable of binding transition metals. Plant Mol. Biol. 41: 139–150.

    Google Scholar 

  • Elliott, R.C., Pedersen, T.J., Fristensky, B., White, M.J., Dickey, L.F. and Thompson, W.F. 1989. Characterization of a single copy gene encoding ferredoxin I from pea. Plant Cell 1: 681–690.

    Google Scholar 

  • Esaki, B., Gardner, R.C., Esaki, Y. and Matsumoto, H. 2000. Ex-pression of aluminum-induced genes in transgenic Arabidopsis plants can ameliorate aluminum stress and/or oxidative stress. Plant Physiol. 122: 657–665.

    Google Scholar 

  • Fowler, D.B. and Carles, R.J. 1979. Growth, development and cold tolerance of fall acclimated cereal grains. Crop Sci. 19: 915–922.

    Google Scholar 

  • Fridlyand, L.E., Backhausen, J.E. and Scheibe, R. 1999. Homeostatic regulation upon changes of enzyme activities in the Calvin cycle as an example for general mechanisms of flux control. What can we expect from transgenic plants? Photosynth. Res. 61: 227–239.

    Google Scholar 

  • Gray, G.R., Savitch, L.V., Ivanov, A.G. and Huner, N.P.A. 1996. Photosystem II excitation pressure and development of resistance to photoinhibition. II. Adjustment of photosynthetic capacity in winter wheat and winter rye. Plant Physiol. 110: 61–71.

    Google Scholar 

  • Gray, G.R., Chauvin, L.-P., Sarhan, F. and Huner, N.P.A. 1997. Cold acclimation and freezing tolerance. A complex interaction of light and temperature. Plant Physiol. 114: 467–474.

    Google Scholar 

  • Gray, G.R., Ivanov, A.G., Krol, M. and Huner, N.P.A. 1998. Adjustment of thylakoid plastoquinone content and electron donor pool size in response to growth temperature and growth irradiance in winter rye (Secale cereale L.). Photosynth. Res 56: 209–221.

    Google Scholar 

  • Guy, C.L. 1990. Cold acclimation and freezing tolerance: role of protein metabolism. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41: 187–223.

    Google Scholar 

  • Heldt, H.W. 1997. Plant Biochemistry and Molecular Biology. Oxford University Press, New York.

    Google Scholar 

  • Houde, M., Danyluk, J., Laliberté, J.-F., Rassart, E., Dhindsa, R.S. and Sarhan, F. 1992. Cloning, characterization, and expression of a cDNA encoding a 50–kilodalton protein specifically induced by cold acclimation in wheat. Plant Physiol. 99: 1381–1387.

    Google Scholar 

  • Huner, N.P.A., Elfman, B., Krol, M. and MacIntosh, A. 1984. Growth and development at cold hardening temperatures. Chloroplast ultrastructure, pigment content and composition. Can. J. Bot. 62: 53–60.

    Google Scholar 

  • Huner, N.P.A., Öquist, G. and Sarhan, F. 1998. Energy balance and acclimation to light and cold. Trends Plant Sci. 3: 224–230.

    Google Scholar 

  • Hurkman, W.J. and Tanaka, C.J. 1986. Solubilization of plant membrane proteins for analysis by two-dimensional gel elec-trophoresis. Plant Physiol. 81: 802–806.

    Google Scholar 

  • Hurry, V., Huner, N.P.A., Selstam, E., Gardestrom, P. and Öquist, G. 1998. Photosynthesis at low growth temperatures. In: A.S. Raqhavendra (Ed.) Photosynthesis: A Comprehensive Treatise, Cambridge University Press, Cambridge, UK, pp. 238–249.

    Google Scholar 

  • Karpinski, S., Reynolds, H., Karpinska, B., Wingsle, G., Creissen, G. and Mullineaux, P. 1999. Systemic signalling and acclimation in response to excess excitation energy in Arabidopsis. Science 284: 654–657.

    Google Scholar 

  • Kaufman, L.S. 1993. Transduction of blue light signals. Plant Physiol. 102: 333–337.

    Google Scholar 

  • Krol, M., Ivanov, A.G., Jansson, S., Kloppstech, K. and Huner, N.P.A. 1999. Greening under high light or cold temperature affects the level of xanthophyll-cycle pigments, early light-inducible proteins, and light-harvesting polypeptides in wild-type barley and the chlorina f2 mutant. Plant Physiol. 120: 193–203.

    Google Scholar 

  • Levitt, J. 1980. Responses of Plants to Environmental Stresses, vol. 1. Chilling, Freezing, and High Temperature Stresses. Academic Press, New York.

    Google Scholar 

  • Limin, A.E., Houde, M., Chauvin, L.-P., Fowler, D.B. and Sarhan, F. 1995. Expression of the cold-induced wheat gene Wcs120 and its homologs in related species and interspecific combinations. Genome 38: 1023–1031.

    Google Scholar 

  • Markgraf, T. and Berry, J. 1990. Measurement of photochemical and non-photochemical quenching: correction of turnover of PSII during steady-state photosynthesis. In: M. Baltscheffsky (Ed.) Current Research in Photosynthesis IV, Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 279–282.

    Google Scholar 

  • Marrs, K.A. and Kaufman, L.S. 1991. Rapid transcriptional regulation of the Cab and pEA207 gene families by blue light in the absence of cytoplasmic protein synthesis. Planta 183: 327–333.

    Google Scholar 

  • Maxwell, D.P., Falk, S., Trick, C.G. and Huner, N.P.A. 1994. Growth at low temperature mimics high-light acclimation in Chlorella vulgaris. Plant Physiol. 105: 535–543.

    Google Scholar 

  • Maxwell, D.P., Falk, S. and Huner, N.P.A. 1995a. Photosystem II excitation pressure and development of resistance to photoinhibition I. LHCII abundance and zeaxanthin content in Chlorella vulgaris. Plant Physiol. 107: 687–694.

    Google Scholar 

  • Maxwell, D.P., Laudenbach, D.E. and Huner, N.P.A. 1995b. Redox regulation of light-harvesting complex II and cab mRNA abundance in Dunaliella salina. Plant Physiol. 109: 787–795.

    Google Scholar 

  • Miskiewicz, E., Ivanov, A.G., Williams, J.P., Khan, M.U., Falk, S. and Huner, N.P.A. 2000. Photosynthetic acclimation of the filamentous cyanobacterium, Plectonema boryanum UTEX 485, to temperature and light. Plant Cell Physiol. 41, in press.

  • Montane, M.H., Petzold, B. and Kloppstech, K. 1999. Formation of early-light-inducible protein complexes and status of xanthophyll levels under high light and cold stress in barley (Hordeum vulgare L.). Planta 208: 519–527.

    Google Scholar 

  • Ouellet, F., Houde, M. and Sarhan, F. 1993. Purification, characterization and cDNA cloning of the 200 kDa protein induced by cold acclimation in wheat. Plant Cell Physiol. 34: 59–65.

    Google Scholar 

  • Richards, K.D., Schott, E.J., Sharma, Y.K., Davis, K.R. and Gardner, R.C. 1998. Aluminum induced oxidative stress genes in Arabidopsis thaliana. Plant Physiol. 116: 409–418.

    Google Scholar 

  • Rosen, K. M. and Villa-Komaroff, L. 1990. An alternative method for the visualization of RNA in formaldehyde agarose gel. Focus 12: 23–24.

    Google Scholar 

  • Sambrook, J., Fritsch, E.F. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Plainview, NY.

    Google Scholar 

  • Schreiber, U., Schliwa, U. and Bilger, W. 1986. Continuous recording of photochemical and non-photochemical chlorophyll fluo-rescence quenching with a new type of modulation fluorometer. Photosynth. Res. 10: 51–62.

    Google Scholar 

  • Steponkus, P.L. 1984. Role of the plasma membrane in freezing injury and cold acclimation. Annu. Rev. Plant Physiol. 35: 543–584.

    Google Scholar 

  • Strand, A., Hurry, V., Henkes, S., Huner, N., Gustafsson, P., Gardeström, P. and Stitt, M. 1999. 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. Plant Physiol. 119: 1387–1397

    Google Scholar 

  • Thomashow, M.F. 1998. Role of cold-responsive genes in plant freezing tolerance. Plant Physiol. 118: 1–7.

    Google Scholar 

  • Thompson, D.M. and Meagher, R.B. 1990. Transcriptional and post-transcriptional processes regulate expression of RNA encoding the small subunit of ribulose-1,5–biphosphate carboxylase differently in petunia and in soybean. Nucl. Acids Res. 18: 3621–3629.

    Google Scholar 

  • Walker, C.J. and Weinstein, J.D. 1994. The magnesium-insertion step of chlorophyll biosynthesis is a two-stage reaction. Biochem. J. 299: 277–284.

    Google Scholar 

  • Warpeha, K.M.F. and Kaufman, L.S. 1990. Two distinct blue-light systems regulate specific nuclear-coded transcripts in pea. Planta 182: 553–558.

    Google Scholar 

  • Wedel, N. Soll, J. and Paap, B.K. 1997. CP12 provides a new mode of light regulation of Calvin cycle activity in higher plants. Proc. Natl. Acad. Sci. USA 94: 10479–10484.

    Google Scholar 

  • Wolpert, T.J., Navarre, D.A., Moore, D.L. and Macko, V. 1995. Inhibition of the glycine decarboxylase multienzyme complex by the host-selective toxin victorin. Plant Cell 7: 463–471.

    Google Scholar 

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Ndong, C., Danyluk, J., Huner, N.P. et al. Survey of gene expression in winter rye during changes in growth temperature, irradiance or excitation pressure. Plant Mol Biol 45, 691–703 (2001). https://doi.org/10.1023/A:1010684719225

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