Abstract
We dissected the regulatory region of the AVP1 gene encoding the vacuolar H+-pyrophosphatase (V-PPase) of Arabidopsis thaliana by using a GUS-reporter assay system. The cloned 1.4 kb 5′-regulatory region in the GUS-reporter transgenic plants was sufficient for the light-induced repression. Furthermore, the 1.4 kb regulatory region was active in all tissues examined and its activity was especially enhanced in pollen, whereas the shorter 0.4 kb regulatory region was active only in pollen. Further detailed analyses revealed that the GUS activity in pollen was regulated by at least three cis-acting regions in an additive or synergetic manner. These findings establish a distinct mechanism of the tissue-specific regulation of V-PPase expression in developing pollen, and imply the biological significance of the V-PPase in pollen maturation.
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REFERENCES
Bate, N. and Twell, D. 1998. Functional architecture of a late pollen promoter: pollen-specific transcription is developmentally regulated by multiple stage-specific and co-dependent activator elements. Plant Mol. Biol. 37: 859–869.
Bechtold, N., Ellis, J. and Pelletier, G. 1993. In planta Agrobac-terium-mediated gene transfer by infiltration of adult Arabidop-sis thaliana plants. C.R. Acad. Sci. Paris, Sci. Vie/Life Sci. 316: 1194–1199.
Boller, T. and Wiemken, A. 1986. Dynamics of vacuolar compart-mentalization. Annu. Rev. Plant Physiol. 37: 137–164.
Bowman, J.L. 1993. Flowers. In: J.L. Bowman (Ed.) Arabidop-sis: An Atlas of Morphology and Development, Springer-Verlag, New York, pp. 133–145.
Bowman, J.L., Dawson, J., Wilson, Z.A., Briarty, L.G. and Mulli-gan, B.J. 1993. Pollen. In: J.L. Bowman (Ed.) Arabidopsis: An Atlas of Morphology and Development, Springer-Verlag, NewYork, pp. 275–279.
Bradford, M.M. 1976. A rapid and sensitive method for the quanti-tation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248–254.
Carystinos, G.D., MacDonald, H.R., Monroy, A.F., Dhindsa, R.S. and Poole, R.J. 1995. Vacuolar H+-translocating pyrophos-phatase is induced by anoxia or chilling in seedlings of rice. Plant Physiol. 108: 641–649.
Darley, C.P., Davies, J.M. and Sanders, D. 1995. Chill-induced changes in the activity and abundance of the vacuolar proton-pumping pyrophosphatase from mung bean hypocotyls. Plant Physiol. 109: 659–665.
Eyal, Y., Curie, C. and McCormick, S. 1995. Pollen specificity elements reside in 30 bp of the proximal promoters of two pollen-expressed genes. Plant Cell 7: 373–384.
Forgac, M. 1999. Structure and properties of the vacuolar H+ ¶ATPases. J. Biol. Chem. 274: 12951–12954.
Gubler, F., Kalla, R., Roberts, J.K. and Jacobsen, J.V. 1995. Gibberellin-regulated expression of a myb gene in barley aleurone cells: evidence for Myb transactivation of a high-pI α-amylase gene promoter. Plant Cell 7: 1879–1891.
Hamilton, D.A., Schwarz, Y.H. and Mascarenhas, J.P. 1998. A monocot pollen-specific promoter contains separable pollen-specific and quantitative elements. Plant Mol. Biol. 38: 663–669.
Hedrich, R. and Schroeder, J.I. 1989. The physiology of ion channels and electrogenic pumps in higher plants. Annu. Rev. Plant Physiol. 40: 539–569.
Higo, K., Ugawa, Y., Iwamoto, M. and Korenaga, T. 1999. Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucl. Acids Res. 27: 297–300.
Houlne, G. and Boutry, M. 1994. Identification of an Arabidopsis thaliana gene encoding a plasma membrane H+-ATPase whose expression is restricted to anther tissue. Plant J. 5: 311–317.
Huang, N., Sutliff, T.D., Litts, J.C. and Rodriguez, R.L. 1990. Classification and characterization of the rice α-amylase multigene family. Plant Mol. Biol. 14: 655–668
Hwang, Y.S., Karrer, E.E., Thomas, B.R., Chen, L. and Rodriguez, R.L. 1998. Three cis-elements required for rice α-amylase Amy3D expression during sugar starvation. Plant Mol. Biol. 36: 331–341.
Jefferson, R.A., Kavanagh, T.A. and Bevan, M.W. 1987. GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6: 3901–3907.
Koch, K.E. 1996. Carbohydrate-modulated gene expression in plants. Annu. Rev. Plant Mol. Biol. 47: 509–540.
Krapp, A. and Stitt, M. 1994. Influence of high-carbohydrate content on the activity of plastidic and cytosolic isoenzyme pairs in photosynthetic tissues. Plant Cell Environ. 17: 861–866.
Lerchl, J., Konig, S., Zrenner, R. and Sonnewald, U. 1995. Molecular cloning, characterization and expression analysis of iso-forms encoding tonoplast-bound proton-translocating inorganic pyrophosphatase in tobacco. Plant Mol. Biol. 29: 833–840.
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.
Lu, C.A., Lim, E.K. and Yu, S.M. 1998. Sugar response sequence in the promoter of a rice alpha-amylase gene serves as a transcriptional enhancer. J. Biol. Chem. 273: 10120–10131.
Martile, P. 1978. Biochemistry and function of vacuoles. Annu. Rev. Plant Physiol. 29: 193–213.
Martinoia, E. 1992. Transport processes in vacuoles of higher plants. Bot. Acta. 105: 232–245.
Marty, F. 1999. Plant vacuole. Plant Cell 11: 587–599.
Murray, M.G. and Thompson, W.F. 1980. Rapid isolation of high-molecular-weight plant DNA. Nucl. Acids Res. 8: 4321–4325.
Nakanishi, Y. and Maeshima, M. 1998. Molecular cloning of vacuolar H+-pyrophosphatase and its developmental expression in growing hypocotyl of mung bean. Plant Physiol. 116: 589–597.
Rea, P.A. and Poole, R.J. 1993. Vacuolar H+-translocating pyrophosphatase. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44: 157–180.
Regan, S.M. and Moffatt, B.A. 1990. Cytochemical analysis of pollen-development in wild-type Arabidopsis and male-sterile mutant. Plant Cell 2: 877–889.
Sambrook, J., Fritsch, E.F. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manial, 2nd ed. Cold Spring Harbor Laboratory Press, Plainview, NY.
Sarafian, V., Kim, Y., Poole, R.J. and Rea, P.A. 1992. Molecular cloning and sequence of cDNA encoding the pyrophosphate-energized vacuolar membrane proton pump of Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 89: 1775–1779.
Shiina, T., Nishii, A., Toyoshima, Y. and Bogorad, L. 1997. Identification of promoter elements involved in the cytosolic Ca2+-mediated photoregulation of maize cab-m1 expression. Plant Physiol. 115: 477–483.
Sze, H., Li, X. and Palmgren, M.G. 1999. Energization of plant cell membranes by H+-pumping ATPases: regulation and biosynthesis. Plant Cell 11: 677–689.
Taiz, L. 1992. The plant vacuole. J. Exp. Biol. 172: 113–122.
Truernit, E., Schmid, J., Epple, P., Illig, J. and Sauer, N. 1996. The sink-specific and stress-regulated Arabidopsis STP4 gene: enhanced expression of a gene encoding a monosaccharide transporter by wounding, elicitors, and pathogen challenge. Plant Cell 8: 2169–2182.
Truernit, E., Stadler, R., Baier, K. and Sauer, N. 1999. A male gametophyte-specific monosaccharide transporter in Arabidop-sis. Plant J. 17: 191–201.
Twell, D., Wing, R.A., Ushiba, J. and McCormick, S. 1991. Promote analysis of genes that are coordinately expressed during pollen development reveals pollen-specific enhancer sequences and shared regulatory elements. Genes Dev. 5: 496–507.
Twell, D., Yamaguchi, J. and McCormick, S. 1990. Pollen-specific gene expression in transgenic plants: coordinate regulation of two different tomato gene promoters during microsporogenesis. Development 109: 705–713.
Weterings, K., Schrauwen, J., Wullems, G. and Twell, D. 1995. Functional dissection of the promoter of the pollen-specific gene NPT303 reveals a novel pollen-specific, and conserved cis-regulatory element. Plant J. 8: 55–63.
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.
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Mitsuda, N., Takeyasu, K. & Sato, M.H. Pollen-specific regulation of vacuolar H+-PPase expression by multiple cis-acting elements. Plant Mol Biol 46, 185–192 (2001). https://doi.org/10.1023/A:1010681129557
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DOI: https://doi.org/10.1023/A:1010681129557