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Expression of tandem invertase genes associated with sexual and vegetative growth cycles in potato

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Abstract

The organisation of two invertase genes (invGE and invGF) linked in direct tandem repeat within the potato genome is detailed. The genes exhibit a similar intron/exon structure which differs from previously described plant invertase genes; while intron locations are conserved between the genes, minor differences in exon length are seen. Both genes encode enzymes with putative extracellular location. Biochemical analysis of gene expression showed expression in floral tissues for both genes, with expression of the upstream gene (invGE) also detected in leaf tissue. Promoter sequences from both genes have been fused to the β-glucuronidase (GUS) reporter gene (uidA) and transformed into potato. One promoter-GUS reporter construct was also transformed into tobacco. Histochemical analysis of transgenic lines defined specific expression from the downstream (invGF) promoter in potato and tobacco pollen, with expression first detected in the late uninucleate stage of tobacco microspore development. The invGE promoter determined expression in pollen and other floral tissues, but also at lateral nodes in stem, root and tuber. An association of invertase expression with generative tissue, both in vegetative and sexual modes of growth, is indicated.

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References

  • Albani, D., Sardana, R., Robert, L.S., Altosaar, I., Arnison, P.G. and Fabijanski, S.F. 1992. A Brassica napus gene family which shows sequence similarity to ascorbate oxidase is expressed in developing pollen: molecular characterisation and analysis of promoter activity in transgenic tobacco plants. Plant J. 2: 331–342.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Bate, N., Spurr, C., Foster, G.D. and Twell, D. 1996. Maturation-specific translational enhancement mediated by the 5 0-UTR of a late pollen transcript. Plant J. 10: 613–623.

    PubMed  Google Scholar 

  • Bournay, A-S., Hedley, P.E., Maddison, A., Waugh, R. and Machray, G.C. 1996. Exon skipping induced by cold stress in a potato invertase gene transcript. Nucl. Acid Res. 24: 2347–2351.

    Google Scholar 

  • Chan, M-T. and Yu, S-M. 1998. 3 0 untranslated region of a rice _-amylase gene mediates sugar-dependent abundance of mRNA. Plant J. 15: 685–695.

    PubMed  Google Scholar 

  • Davies, C. and Robinson, S.P. 1996. Sugar accumulation in grape berries. Cloning of two putative vacuolar invertase cDNAs and their expression in grapevine tissues. Plant Physiol. 111: 275–283.

    PubMed  Google Scholar 

  • Dellaporta, S.J., Wood, J. and Hicks, J.B. 1983. A plant DNA minipreparation: version II. Plant Mol. Biol. Rep. 1: 19–21.

    Google Scholar 

  • Elliott, K.J., Butler, W.O., Dickinson, C.D., Konno, Y., Vedvick, L.F. and Mirkow, E. 1993. Isolation and characterization of fruit vacuolar invertase genes from two tomato species and tempo-ral differences in mRNA levels during fruit ripening. Plant Mol. Biol. 21: 515–524.

    PubMed  Google Scholar 

  • Fu, H., Kim, S.Y. and Park, W.D. 1995. High-level tuber expression and sucrose inducibility of a potato Sus4 sucrose synthase gene require 5 0 and 3 0 flanking sequences and the leader intron. Plant Cell 7: 1387–1394.

    PubMed  Google Scholar 

  • Godt, D.E. and Roitsch, T. 1997. Regulation and tissue-specific dis-tribution of mRNAs for three extracellular invertase isoenzymes of tomato suggests an important function in establishing and maintaining sink metabolism. Plant Physiol 115: 273–282.

    PubMed  Google Scholar 

  • Greiner, S., Weil, M., Krausgrill, S. and Rausch, T. 1995. A tobacco cDNA coding for cell-wall invertase. Plant Physiol. 108: 825–826.

    PubMed  Google Scholar 

  • Grotewold, E., Drummond, B., Bowen, B. and Peterson, T. 1994. The myb-homologous P gene controls phlobaphene pigmenta-tion in maize floral organs by directly activating a flavonoid biosynthetic gene subset. Cell 76: 543–553.

    Article  PubMed  Google Scholar 

  • Guerineau, F. and Waugh, R. 1993. The U6 small nuclear RNA gene family of potato. Plant Mol. Biol. 22: 807–818.

    PubMed  Google Scholar 

  • Haouazine-Takvorian, N., Tymowska-Lalanne, Z., Takvorian, A., Tregear, J., Lejeune, B., Lecharny, A. and Kreis, M. 1997. Characterisation of two members of the Arabidopsis gene family, At_fruct3 and At_fruct4, coding for vacuolar invertases. Gene 197: 239–251.

    PubMed  Google Scholar 

  • Hedley, P.E., Machray, G.C., Davies, H.V., Burch, L. and Waugh, R. 1993. cDNA cloning and expression of a potato (Solanum tuberosum) invertase. Plant Mol. Biol. 22: 917–922.

    PubMed  Google Scholar 

  • Hedley, P.E., Machray, G.C., Davies, H.V., Burch, L. and Waugh, R. 1994. Potato (Solanum tuberosum) invertase-encoding cDNAs and their differential expression. Gene 145: 211–214.

    PubMed  Google Scholar 

  • Heinemeyer, T., Wingender, E., Reuter, I., Hermjakob, H., Kel, A.E., Kel, O.V., Ignatieva, E.V., Ananko, E.A., Podkolodnaya, O.A., Kolpakov, F.A., Podkolodny, N.L. and Kolchanov, N.A. 1998. Databases on transcriptional regulation: TRANSFAC, TRRD, and COMPEL. Nucl. Acids Res. 26: 364–370.

    Google Scholar 

  • Horsch, R.B., Fry, J.E., Hoffman, N.L., Eichholtz, D., Rogers, S.G. and Fraley, R.T. 1985. A simple and general method for transferring genes into plants. Science 227: 1229–1231.

    Google Scholar 

  • Huang, H., Mizukami, Y., Yu, Y. and Ma, H. 1993. Isolation and characterization of the binding sequences for the product of the Arabidopsis floral homeotic gene AGAMOUS. Nucl. Acids Res. 21: 4769–4776.

    PubMed  Google Scholar 

  • Hulme, J.S., Higgins, E.S. and Shields, R. 1992. An efficient genotype-independent method for regeneration of potato plants from leaf tissue. Plant Cell Tiss Org Cult 31: 161–167.

    Google Scholar 

  • Jefferson, R.A., Kavanagh, T.A. and Bevan, M.W. 1987. GUS fu-sions: _-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6: 3901–3907.

    PubMed  Google Scholar 

  • Lorenz, K., Lienhard, S. and Sturm, A. 1995. Structural organisation and differential expression of carrot _-fructofuranosidase genes: identification of a gene coding for a flower bud-specific isozyme. Plant Mol. Biol. 28: 189–194.

    PubMed  Google Scholar 

  • Maddison, A.L. 1997. Studies of invertase gene organisation and expression in potato. Ph.D. thesis, University of Dundee, UK.

  • Mercier, R.W. and Gogarten, J.P. 1995. A second cell wall acid invertase gene in Arabidopsis thaliana. Plant Physiol. 107: 659–660.

    PubMed  Google Scholar 

  • Miller, W.B. and Ranwala, A.P. 1994. Characterization and local-ization of three soluble invertase forms from Lilium longiflorum flower buds. Physiol. Plant. 92: 247–253.

    Google Scholar 

  • Ramloch-Lorenz, K., Knudsen, S. and Sturm, A. 1993. Molecular characterisation of the gene for carrot cell wall _-fructosidase. Plant J. 4: 545–554.

    PubMed  Google Scholar 

  • Rothnie, H.M. 1996. Plant mRNA 3 0 end information. Plant Mol. Biol. 32: 43–61.

    PubMed  Google Scholar 

  • Saiki, R.K., Gelfand, D.H., Stoffel, S., Scharf, S.J., Higuchi, R., Horn, G.T., Mullis, K.B. and Erlich, H.A. 1988. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239: 487–491.

    PubMed  Google Scholar 

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

    Google Scholar 

  • Sato, T., Iwatsubo, T., Takanashi, M., Nakagawa, H., Ogura, N. and Mori, H. 1993. Intercellular localization of acid invertase in tomato fruit and molecular cloning of a cDNA for the enzyme. Plant Cell Physiol. 34: 263–269.

    PubMed  Google Scholar 

  • Schroder, G., Brown, J.W.S. and Sinibaldi, R. 1988. Molecular analysis of resveratrol synthase. Eur. J. Biochem. 172: 161–169.

    PubMed  Google Scholar 

  • Sessa, G., Morelli, G. and Ruberti, I. 1993. The Athb-1 and Athb-2 HD-Zip domains homodimerize forming complexes of different DNA-binding specificities. EMBO J. 12: 3507–3517.

    PubMed  Google Scholar 

  • Solano, R., Nieto, C., Avila, J., Canas, L., Diaz, I. and Pazares, J. 1995. Dual DNA-binding specificity of a petal epidermis-specific MYB transcription factor (MYB.Ph3) from Petunia hybrida. EMBO J. 14: 1773–1784.

    PubMed  Google Scholar 

  • Sonnewald, U., Brauer, M., von Schaewen, A., Stitt, M. and Willmitzer, L. 1991. Transgenic tobacco plants expressing yeast-derived invertase in either the cytosol, vacuole or apoplast: a powerful tool for studying sucrose metabolism and sink/source interactions. Plant J. 1: 95–106.

    PubMed  Google Scholar 

  • Sturm, A. and Chrispeels, M.J. 1990. cDNA cloning of carrot extracellular _-fructosidase and its expression in response to wounding and bacterial infection. Plant Cell 2: 1107–1119.

    Article  PubMed  Google Scholar 

  • Sunderland, N. and Roberts, M. 1977. New approach to pollen culture. Nature 270: 236–238.

    Google Scholar 

  • Tang, G-Q., Luscher, M. and Sturm, A. 1999. Antisense repression of vacuolar and cell wall invertase in transgenic carrot alters early plant development and sucrose partitioning. Plant Cell 11: 177–189.

    Article  PubMed  Google Scholar 

  • Truernit, E., Stadler, R., Baier, K. and Sauer, N. 1999. A male gametophyte-specific monosaccharide transporter in Arabidop-sis. Plant J. 17: 191–201.

    PubMed  Google Scholar 

  • Twell, D., Yamaguchi, J., Wing, R.A., Ushiba, J. and McCormick, S. 1991. Promoter analysis of genes that are coordinately ex-pressed during pollen development reveals pollen-specific en-hancer sequences and shared regulatory elements. Genes Dev. 5: 496–507.

    PubMed  Google Scholar 

  • Tymowska-Lalanne, Z. and Kreis, M. 1998a. The plant invertases: physiology, biochemistry and molecular biology. Adv. Bot. Res. 28: 70–117.

    Google Scholar 

  • Tymowska-Lalanne, Z. and Kreis, M. 1998b. Expression of the Ara-bidopsis thaliana invertase gene family. Planta 207: 259–265.

    PubMed  Google Scholar 

  • Tymowska-Lalanne, Z., Schwebel-Dugue, N., Lecharny, A. and Kreis, M. 1996. Expression and cis-acting elements of the At_fruct1 gene from Arabidopsis thaliana encoding a cell wall invertase. Plant Physiol. Biochem. 34: 431–442.

    Google Scholar 

  • Unger, C., Hardegger, M., Lienhard, S. and Sturm, A. 1994. cDNA cloning of carrot (Daucus carota) soluble acid _-fructosidases and comparison with the cell wall isoenzyme. Plant Physiol. 104: 1351–1357.

    PubMed  Google Scholar 

  • Weber, H., Borisjuk, L. and Wobus, U. 1996. Controlling seed development and seed size in Vicia faba: a role for seed coat-associated invertases and carbohydrate state. Plant J. 10: 823–834.

    Google Scholar 

  • Weterings, K., Schrauwen, J., Willems, G. and Twell, D. 1995. Functional dissection of the promoter of the pollen-specific gene Ntp303 reveals a novel pollen-specific and conserved cis-regulatory element. Plant J. 8: 55–63.

    PubMed  Google Scholar 

  • Xu, J., Avigne, W.T., McCarty, D.R. and Koch, K.E. 1996. A similar dichotomy of sugar modulation and developmental expression affects both paths of sucrose metabolism: evidence from a maize invertase gene family. Plant Cell 8: 1209–1220.

    PubMed  Google Scholar 

  • Zhou, D., Mattoo, A., Li, N., Imaseki, H. and Solomos, T. 1994. Complete nucleotide sequence of potato acid invertase cDNA. Plant Physiol. 106: 397–398.

    PubMed  Google Scholar 

  • Zou, J.T., Zhan, X.Y., Wu, H.M., Wang, H. and Cheung, A.Y. 1994. Characterization of a rice pollen-specific gene and its expression. Am. J. Bot. 81: 552–561.

    Google Scholar 

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Maddison, A.L., Hedley, P.E., Meyer, R.C. et al. Expression of tandem invertase genes associated with sexual and vegetative growth cycles in potato. Plant Mol Biol 41, 741–752 (1999). https://doi.org/10.1023/A:1006389013179

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