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Identification and characterization of the duplicate rice sucrose synthase genes OsSUS5 and OsSUS7 which are associated with the plasma membrane

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Molecules and Cells

Abstract

Systematic searches using the complete genome sequence of rice (Oryza sativa) identified OsSUS7, a new member of the rice sucrose synthase (OsSUS) gene family, which shows only nine single nucleotide substitutions in the OsSUS5 coding sequence. Comparative genomic analysis revealed that the synteny between OsSUS5 and OsSUS7 is conserved, and that significant numbers of transposable elements are scattered at both loci. In particular, a 17.6-kb genomic region containing transposable elements was identified in the 5′ upstream sequence of the OsSUS7 gene. GFP fusion experiments indicated that OsSUS5 and OsSUS7 are largely associated with the plasma membrane and partly with the cytosol in maize mesophyll protoplasts. RT-PCR analysis and transient expression assays revealed that OsSUS5 and OsSUS7 exhibit similar expression patterns in rice tissues, with the highest expression evident in roots. These results suggest that two redundant genes, OsSUS5 and OsSUS7, evolved via duplication of a chromosome region and through the transposition of transposable elements.

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References

  • Anguenot, R., Nguyen-Quoc, B., Yelle, S., and Michaud, D. (2006). Protein phosphorylation and membrane association of sucrose synthase in developing tomato fruit. Plant Physiol. Biochem. 44, 294–300.

    Article  PubMed  CAS  Google Scholar 

  • Arai, M., Mori, H., and Imaseki, H. (1992). Expression of the gene for sucrose synthase during growth of mung bean seedlings. Plant Cell Physiol. 33, 503–506.

    CAS  Google Scholar 

  • Balk, P.A., and de Boer, A.D. (1999). Rapid stalk elongation in tulip (Tulipa gesneriana L. cv. Apeldoorn) and the combined action of cold-induced invertase and the water-channel protein gammaTIP. Planta 209, 346–354.

    Article  PubMed  CAS  Google Scholar 

  • Barratt, D.H., Barber, L., Kruger, N.J., Smith, A.M., Wang, T.L., and Martin, C. (2001). Multiple, distinct isoforms of sucrose synthase in pea. Plant Physiol. 127, 655–664.

    Article  PubMed  CAS  Google Scholar 

  • Barratt, D.H., Derbyshire, P., Findlay, K., Pike, M., Wellner, N., Lunn, J., Feil, R., Simpson, C., Maule, A.J., and Smith, A.M. (2009). Normal growth of Arabidopsis requires cytosolic invertase but not sucrose synthase. Proc. Natl. Acad. Sci. USA 106, 13124–13129.

    Article  PubMed  CAS  Google Scholar 

  • Baud, S., Vaultier, M.N., and Rochat, C. (2004). Structure and expression profile of the sucrose synthase multigene family in Arabidopsis. J. Exp. Bot. 55, 397–409.

    Article  PubMed  CAS  Google Scholar 

  • Bieniawska, Z., Paul Barratt, D.H., Garlick, A.P., Thole, V., Kruger, N.J., Martin, C., Zrenner, R., and Smith, A.M. (2007). Analysis of the sucrose synthase gene family in Arabidopsis. Plant J. 49, 810–828.

    Article  PubMed  CAS  Google Scholar 

  • Carlson, S.J., Chourey, P.S., Helentjaris, T., and Datta, R. (2002). Gene expression studies on developing kernels of maize sucrose synthase (SuSy) mutants show evidence for a third SuSy gene. Plant Mol. Biol. 49, 15–29.

    Article  PubMed  CAS  Google Scholar 

  • Chengappa, S., Guilleroux, M., Phillips, W., and Shields, R. (1999). Transgenic tomato plants with decreased sucrose synthase are unaltered in starch and sugar accumulation in the fruit. Plant Mol. Biol. 40, 213–221.

    Article  PubMed  CAS  Google Scholar 

  • Cho, J.I., Lee, S.K., Ko, S., Kim, H.K., Jun, S.H., Lee, Y.H., Bhoo, S.H., Lee, K.W., An, G., Hahn, T.R., et al. (2005). Molecular cloning and expression analysis of the cell-wall invertase gene family in rice (Oryza sativa L.). Plant Cell Rep. 24, 225–236.

    Article  PubMed  CAS  Google Scholar 

  • Cho, J.I., Ryoo, N., Ko, S., Lee, S.K., Lee, J., Jung, K.H., Lee, Y.H., Bhoo, S.H., Winderickx, J., An, G., et al. (2006). Structure, expression, and functional analysis of the hexokinase gene family in rice (Oryza sativa L.). Planta 224, 598–611.

    Article  PubMed  CAS  Google Scholar 

  • Cho, J.I., Ryoo, N., Eom, J.S., Lee, D.W., Kim, H.B., Jeong, S.W., Lee, Y.H., Kwon, Y.K., Cho, M.H., Bhoo, S.H., et al. (2009). Role of the rice hexokinases OsHXK5 and OsHXK6 as glucose sensors. Plant Physiol. 149, 745–759.

    Article  PubMed  CAS  Google Scholar 

  • Cho, J.I., Burla, B., Lee, D.W., Ryoo, N., Hong, S.K., Kim, H.B., Eom, J.S., Choi, S.B., Cho, M.H., Bhoo, S.H., et al. (2010). Expression analysis and functional characterization of the monosaccharide transporters, OsTMTs, involving vacuolar sugar transport in rice (Oryza sativa). New Phytol. 186, 657–668.

    Article  PubMed  CAS  Google Scholar 

  • Chourey, P.S., Taliercio, E.W., Carlson, S.J., and Ruan, Y.L. (1998). Genetic evidence that the two isozymes of sucrose synthase present in developing maize endosperm are critical, one for cell wall integrity and the other for starch biosynthesis. Mol. Gen. Genet. 259, 88–96.

    Article  PubMed  CAS  Google Scholar 

  • Craig, J., Barratt, P., Tatge, H., Dejardin, A., Handley, L., Gardner, C.D., Barber, L., Wang, T., Hedley, C., Martin, C., et al. (1999). Mutations at the rug4 locus alter the carbon and nitrogen metabolism of pea plants through an effect on sucrose synthase. Plant J. 17, 353–362.

    Article  CAS  Google Scholar 

  • D’Aoust, M.A., Yelle, S., and Nguyen-Quoc, B. (1999). Antisense inhibition of tomato fruit sucrose synthase decreases fruit setting and the sucrose unloading capacity of young fruit. Plant Cell 11, 2407–2418.

    Article  PubMed  Google Scholar 

  • Duncan, K.A., and Huber, S.C. (2007). Sucrose synthase oligomerization and F-actin association are regulated by sucrose concentration and phosphorylation. Plant Cell Physiol. 48, 1612–1623.

    Article  PubMed  CAS  Google Scholar 

  • Etxeberria, E., and Gonzalez, P. (2003). Evidence for a tonoplast-associated form of sucrose synthase and its potential involvement in sucrose mobilization from the vacuole. J. Exp. Bot. 54, 1407–1414.

    Article  PubMed  CAS  Google Scholar 

  • Fallahi, H., Scofield, G.N., Badger, M.R., Chow, W.S., Furbank, R.T., and Ruan, Y.L. (2008). Localization of sucrose synthase in developing seed and siliques of Arabidopsis thaliana reveals diverse roles for SUS during development. J. Exp. Bot. 59, 3283–3295.

    Article  PubMed  CAS  Google Scholar 

  • Feng, Q., Zhang, Y., Hao, P., Wang, S., Fu, G., Huang, Y., Li, Y., Zhu, J., Liu, Y., Hu, X., et al. (2002). Sequence and analysis of rice chromosome 4. Nature 420, 316–320.

    Article  PubMed  CAS  Google Scholar 

  • Fu, H., and Park, W.D. (1995). Sink- and vascular-associated sucrose synthase functions are encoded by different gene classes in potato. Plant Cell 7, 1369–1385.

    Article  PubMed  CAS  Google Scholar 

  • Godt, D.E., Riegel, A., and Roitsch, T. (1995). Regulation of sucrose synthase expression in Chenopodium rubrum: characterization of sugar induced expression in photoautotrophic suspension cultures and sink tissue specific expression in plants. J. Plant Physiol. 146, 231–238.

    CAS  Google Scholar 

  • Goff, S.A., Ricke, D., Lan, T.H., Presting, G., Wang, R., Dunn, M., Glazebrook, J., Sessions, A., Oeller, P., Varma, H., et al. (2002). A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296, 92–100.

    Article  PubMed  CAS  Google Scholar 

  • Harada, T., Satoh, S., Yoshioka, T., and Ishizawa, K. (2005). Expression of sucrose synthase genes involved in enhanced elongation of pondweed (Potamogeton distinctus) turions under anoxia. Ann. Bot. (Lond) 96, 683–692.

    Article  CAS  Google Scholar 

  • Hesse, H., and Willmitzer, L. (1996). Expression analysis of a sucrose synthase gene from sugar beet (Beta vulgaris L.). Plant Mol. Biol. 30, 863–872.

    Article  PubMed  CAS  Google Scholar 

  • Hirochika, H., Sugimoto, K., Otsuki, Y., Tsugawa, H., and Kanda, M. (1996). Retrotransposons of rice involved in mutations induced by tissue culture. Proc. Natl. Acad. Sci. USA 93, 7783–7788.

    Article  PubMed  CAS  Google Scholar 

  • Hirose, T., Scofield, G.N., and Terao, T. (2008). An expression analysis profile for the entire sucrose synthase gene family in rice. Plant Sci. 174, 534–543.

    CAS  Google Scholar 

  • Hohnjec, N., Becker, J.D., Puhler, A., Perlick, A.M., and Kuster, H. (1999). Genomic organization and expression properties of the MtSucS1 gene, which encodes a nodule-enhanced sucrose synthase in the model legume Medicago truncatula. Mol. Gen. Genet. 261, 514–522.

    Article  PubMed  CAS  Google Scholar 

  • Horst, I., Welham, T., Kelly, S., Kaneko, T., Sato, S., Tabata, S., Parniske, M., and Wang, T.L. (2007). TILLING mutants of Lotus japonicus reveal that nitrogen assimilation and fixation can occur in the absence of nodule-enhanced sucrose synthase. Plant Physiol. 144, 806–820.

    Article  PubMed  CAS  Google Scholar 

  • Huang, J.W., Chen, J.T., Yu, W.P., Shyur, L.F., Wang, A.Y., Sung, H.Y., Lee, P.D., and Su, J.C. (1996). Complete structures of three rice sucrose synthase isogenes and differential regulation of their expressions. Biosci. Biotechnol. Biochem. 60, 233–239.

    Article  PubMed  CAS  Google Scholar 

  • Hwang, I., and Sheen, J. (2001). Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413, 383–389.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Jiang, N., Feschotte, C., Zhang, X., and Wessler, S.R. (2004). Using rice to understand the origin and amplification of miniature inverted repeat transposable elements (MITEs). Curr. Opin. Plant Biol. 7, 115–119.

    Article  PubMed  CAS  Google Scholar 

  • Jun, S.H., Han, M.J., Lee, S., Seo, Y.S., Kim, W.T., and An, G. (2004). OsEIN2 is a positive component in ethylene signaling in rice. Plant Cell. Physiol. 45, 281–289.

    Article  PubMed  CAS  Google Scholar 

  • Karimi, M., Inze, D., and Depicker, A. (2002). Gateway vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193–195.

    Article  PubMed  CAS  Google Scholar 

  • Karimi, M., Bleys, A., Vanderhaeghen, R., and Hilson, P. (2007). Building blocks for plant gene assembly. Plant Physiol. 145, 1183–1191.

    Article  PubMed  CAS  Google Scholar 

  • Kim, J., Jun, S.H., Kang, H.G., Lee, J., and An, G. (2002). Molecular characterization of a GA-inducible gene, Cvsus1, in developing watermelon seeds. Mol. Cells 14, 255–260.

    PubMed  CAS  Google Scholar 

  • Kleines, M., Elster, R.C., Rodrigo, M.J., Blervacq, A.S., Salamini, F., and Bartels, D. (1999). Isolation and expression analysis of two stress-responsive sucrose-synthase genes from the resurrection plant Craterostigma plantagineum (Hochst.). Planta 209, 13–24.

    Article  PubMed  CAS  Google Scholar 

  • Klotz, K.L., and Haagenson, D.M. (2008). Wounding, anoxia and cold induce sugarbeet sucrose synthase transcriptional changes that are unrelated to protein expression and activity. J. Plant Physiol. 165, 423–434.

    Article  PubMed  CAS  Google Scholar 

  • Komatsu, A., Moriguchi, T., Koyama, K., Omura, M., and Akihama, T. (2002). Analysis of sucrose synthase genes in citrus suggests different roles and phylogenetic relationships. J. Exp. Bot. 53, 61–71.

    Article  PubMed  CAS  Google Scholar 

  • Komatsu, M., Shimamoto, K., and Kyozuka, J. (2003). Two-step regulation and continuous retrotransposition of the rice LINE-type retrotransposon Karma. Plant Cell 15, 1934–1944.

    Article  PubMed  CAS  Google Scholar 

  • Kwon, S.J., Park, K.C., Son, J.H., Bureau, T., Park, C.H., and Kim, N.S. (2009). Sequence diversity of a domesticated transposase gene, MUG1, in Oryza species. Mol. Cells 30, 459–465.

    Article  Google Scholar 

  • Li, C.R., Zhang, X.B., Huang, C.H., and Hew, C.S. (2004). Cloning, characterization and tissue specific expression of a sucrose synthase gene from tropical epiphytic CAM orchid Mokara Yellow. J. Plant Physiol. 161, 87–94.

    Article  PubMed  CAS  Google Scholar 

  • Ronald, P.C. (1998). Resistance gene evolution. Curr. Opin. Plant Biol. 1, 294–298.

    Article  PubMed  CAS  Google Scholar 

  • Ruan, Y.L., Llewellyn, D.J., and Furbank, R.T. (2003). Suppression of sucrose synthase gene expression represses cotton fiber cell initiation, elongation, and seed development. Plant Cell 15, 952–964.

    Article  PubMed  CAS  Google Scholar 

  • Salanoubat, M., and Belliard, G. (1987). Molecular cloning and sequencing of sucrose synthase cDNA from potato (Solanum tuberosum L.): preliminary characterization of sucrose synthase mRNA distribution. Gene 60, 47–56.

    Article  PubMed  CAS  Google Scholar 

  • Sánchez de la Hoz, P., Vicente-Carbajosa, J., Mena, M., and Carbonero, P. (1992). Homologous sucrose synthase genes in barley (Hordeum vulgare) are located in chromosomes 7H (syn. 1) and 2H. Evidence for a gene translocation? FEBS Lett. 310, 46–50.

    Article  PubMed  Google Scholar 

  • Sasaki, T., Matsumoto, T., Yamamoto, K., Sakata, K., Baba, T., Katayose, Y., Wu, J., Niimura, Y., Cheng, Z., Nagamura, Y., et al. (2002). The genome sequence and structure of rice chromosome 1. Nature 420, 312–316.

    Article  PubMed  CAS  Google Scholar 

  • Sebkova, V., Unger, C., Hardegger, M., and Sturm, A. (1995). Biochemical, physiological, and molecular characterization of sucrose synthase from Daucus carota. Plant Physiol. 108, 75–83.

    Article  PubMed  CAS  Google Scholar 

  • Silvente, S., Camas, A., and Lara, M. (2003). Heterogeneity of sucrose synthase genes in bean (Phaseolus vulgaris L.): evidence for a nodule-enhanced sucrose synthase gene. J. Exp. Bot. 54, 749–755.

    Article  PubMed  CAS  Google Scholar 

  • Sturm, A. (1999). Invertase. Primary structures, functions, and roles in plant development and sucrose partitioning. Plant Physiol. 121, 1–7.

    Article  PubMed  CAS  Google Scholar 

  • Sturm, A., and Tang, G.Q. (1999). The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends Plant Sci. 4, 401–407.

    Article  PubMed  Google Scholar 

  • Sturm, A., Lienhard, S., Schatt, S., and Hardegger, M. (1999). Tissue-specific expression of two genes for sucrose synthase in carrot (Daucus carota L.). Plant Mol. Biol. 39, 349–360.

    Article  PubMed  CAS  Google Scholar 

  • Subbaiah, C.C., Palaniappan, A., Duncan, K., Rhoads, D.M., Huber, S.C., and Sachs, M.M. (2006) Mitochondrial localization and putative signaling function of sucrose synthase in maize. J. Biol. Chem. 281, 15625–15635.

    Article  PubMed  CAS  Google Scholar 

  • Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007). MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596–1599.

    Article  PubMed  CAS  Google Scholar 

  • Thompson, J.D., Higgins, D.G., and Gibson, T.J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680.

    Article  PubMed  CAS  Google Scholar 

  • Ueda, T., Yamaguchi, M., Uchimiya, H., and Nakano, A. (2001). Ara6, a plantunique novel type Rab GTPase, functions in the endocytic pathway of Arabidopsis thaliana. EMBO J. 20, 4730–4741.

    Article  PubMed  CAS  Google Scholar 

  • Uemura, T., Ueda, T., Ohniwa, R.L., Nakano, A., Takeyasu, K., and Sato, M.H. (2004). Systematic analysis of SNARE molecules in Arabidopsis: dissection of the post-Golgi network in plant cells. Cell Struct. Funct. 29, 49–65.

    Article  PubMed  CAS  Google Scholar 

  • van Ghelue, M., Ribeiro, A., Solheim, B., Akkermans, A.D., Bisseling, T., and Pawlowski, K. (1996). Sucrose synthase and enolase expression in actinorhizal nodules of Alnus glutinosa: comparison with legume nodules. Mol. Gen. Genet. 250, 437–446.

    Article  PubMed  Google Scholar 

  • Wang, A.Y., Yu, W.P., Juang, R.H., Huang, J.W., Sung, H.Y., and Su, J.C. (1992). Presence of three rice sucrose synthase genes as revealed by cloning and sequencing of cDNA. Plant Mol. Biol. 18, 1191–1194.

    Article  PubMed  CAS  Google Scholar 

  • Wang, F., Smith, A.G., and Brenner, M.L. (1993). Isolation and sequencing of tomato fruit sucrose synthase cDNA. Plant Physiol. 103, 1463–1464.

    Article  PubMed  CAS  Google Scholar 

  • Werr, W., Frommer, W.B., Maas, C., and Starlinger, P. (1985). Structure of the sucrose synthase gene on chromosome 9 of Zea mays L. EMBO J. 4, 1373–1380.

    PubMed  CAS  Google Scholar 

  • Winter, H., Huber, J.L., and Huber, S.C. (1997). Membrane association of sucrose synthase: changes during the graviresponse and possible control by protein phosphorylation. FEBS Lett. 420, 151–155.

    Article  PubMed  CAS  Google Scholar 

  • Winter, H., Huber, J.L., and Huber, S.C. (1998). Identification of sucrose synthase as an actin-binding protein. FEBS Lett. 430, 205–208.

    Article  PubMed  CAS  Google Scholar 

  • Yu, J., Hu, S., Wang, J., Wong, GK., Li, S., Liu, B., Deng, Y., Dai, L., Zhou, Y., Zhang, X., et al. (2002). A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296, 79–92.

    Article  PubMed  CAS  Google Scholar 

  • Zrenner, R., Salanoubat, M., Willmitzer, L., and Sonnewald, U. (1995). Evidence of the crucial role of sucrose synthase for sink strength using transgenic potato plants (Solanum tuberosum L.). Plant J. 7, 97–107.

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Jong-Seong Jeon.

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Cho, JI., Kim, HB., Kim, CY. et al. Identification and characterization of the duplicate rice sucrose synthase genes OsSUS5 and OsSUS7 which are associated with the plasma membrane. Mol Cells 31, 553–561 (2011). https://doi.org/10.1007/s10059-011-1038-y

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