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Molecular cloning and expression analysis of a monosaccharide transporter gene OsMST4 from rice (Oryza sativa L.)

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Abstract

Monosaccharide transporters mediate the membrane transport of a variable range of monosaccharides, which plays a crucial role in sugar distribution throughout the plant. To investigate the significance of monosaccharide transporters for rice (Oryza sativa L.) seed development, cDNA of a new putative monosaccharide transporter gene OsMST4 was isolated. The deduced OsMST4 protein shows typical features of monosaccharide transporters, and shares high homology with other plant homologues. Heterologous expression in yeast (Saccharomyces cerevisiae) showed that OsMST4 is a functional monosaccharide transporter capable of transporting glucose, fructose, mannose and galactose. Transcriptional analysis revealed that OsMST4 is expressed in all tested organs/tissues. In developing caryopses, its expression is high at the early and middle grain filling stages, and declines gradually to low levels after that. Further analysis revealed that it is expressed in both the maternal tissue and the filial tissue, with its highest expression in embryo. Cellular location in young caryopses through RNA in situ hybridization showed that OsMST4 mRNA mainly accumulates in the vascular parenchyma of the chalazal vein, cross-cells, nucellar tissue and endosperm. The expression pattern of OsMST4 was further confirmed by histochemical analysis of the OsMST4-promoter-β-glucuronidase (GUS) transgenic rice plants. These data indicate that OsMST4 is actively involved in monosaccharides supply for seed development during the course of grain filling. In addition, the cell type-specific expression patterns of OsMST4 in other sink and source tissues were also investigated, and its corresponding physiological roles were discussed.

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Abbreviations

DAF:

day(s) after flowering

DIG:

digoxigenin

EST:

expressed sequence tag

References

  • Aoki N, Hirose T, Scofield GN, Whitfeld PR, Furbank RT (2003) The sucrose transporter gene family in rice. Plant Cell Physiol 44:223–232

    Article  PubMed  CAS  Google Scholar 

  • Butowt R, Granot D, Rodriguez-Garcia MI (2003) A putative plastidic glucose translocator is expressed in heterotrophic tissues that do not contain starch, during olive (Olea europea L.) fruit ripening. Plant Cell Physiol 44:1152–1161

    Article  PubMed  CAS  Google Scholar 

  • Büttner M, Sauer N (2000) Monosaccharide transporters in plants: structure, function and physiology. Biochim Biophys Acta 1465:263–274

    Article  PubMed  Google Scholar 

  • Büttner M, Truernit E, Baier K, Scholz-Starke J, Sontheim M, Lauterbach C, Huss V, Sauer N (2000) AtSTP3, a green leaf-specific, low affinity monosaccharide-H+ symporter of Arabidopsis thaliana. Plant Cell Environ 23:175–184

    Article  Google Scholar 

  • Cheng WH, Taliercio EW, Chourey PS (1996) The miniature1 seed locus of maize encodes a cell wall invertase required for normal development of endosperm and maternal cells in the pedicel. Plant Cell 8:971–983

    Article  PubMed  CAS  Google Scholar 

  • Chiou TJ, Bush DR (1996) Molecular cloning, immunochemical localization to the vacuole, and expression in transgenic yeast and tobacco of a putative sugar transporter from sugar beet. Plant Physiol 110:511–520

    Article  PubMed  CAS  Google Scholar 

  • Cho JI, Lee SK, Ko S, Kim HK, Jun SH, Lee YH, Bhoo SH, Lee KW, An G, Hahn TR, Jeon JS (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 

  • Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159

    Article  PubMed  CAS  Google Scholar 

  • Ebenezer GAI, Amirthalingam M, Ponsamuel J, Dayanandan P (1990) Role of palea and lemma in the development of rice caryopsis. J Indian Bot Soc 69:245–250

    Google Scholar 

  • Ehness R, Roitsch T (1997) Co-ordinated induction of mRNAs for extracellular invertase and a glucose transporter in Chenopodium rubrum by cytokinins. Plant J 11:539–548

    Article  PubMed  CAS  Google Scholar 

  • Fotopoulos V, Gilbert MJ, Pittman JK, Marvier AC, Buchanan AJ, Sauer N, Hall JL, Williams LE (2003) The monosaccharide transporter gene, AtSTP4, and the cell-wall invertase, Atbetafruct1, are induced in Arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum. Plant Physiol 132:821–829

    Article  PubMed  CAS  Google Scholar 

  • Gear ML, McPhillips ML, Patrick JW, McCurdy DW (2000) Hexose transporters of tomato: molecular cloning, expression analysis and functional characterization. Plant Mol Biol 44:687–697

    Article  PubMed  CAS  Google Scholar 

  • Harrison MJ (1996) A sugar transporter from Medicago truncatula: altered expression pattern in roots during vesicular-arbuscular (VA) mycorrhizal associations. Plant J 9:491–503

    Article  PubMed  CAS  Google Scholar 

  • Hausler RE, Baur B, Scharte J, Teichmann T, Eicks M, Fischer KL, Flugge UI, Schubert S, Weber A, Fischer K (2000) Plastidic metabolite transporters and their physiological functions in the inducible crassulacean acid metabolism plant Mesembryanthemum crystallinum. Plant J 24:285–296

    Article  PubMed  CAS  Google Scholar 

  • Henderson PJ, Baldwin SA, Cairns MT, Charalambous BM, Dent HC, Gunn F, Liang WJ, Lucas VA, Martin GE, McDonald TP (1992) Sugar-cation symport systems in bacteria. Int Rev Cytol 137:149–208

    Article  PubMed  CAS  Google Scholar 

  • Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6:271–282

    Article  PubMed  CAS  Google Scholar 

  • Hirose T, Imaizumi N, Scofield GN, Furbank RT, Ohsugi R (1997) cDNA cloning and tissue specific expression of a gene for sucrose transporter from rice (Oryza sativa L.). Plant Cell Physiol 38:1389–1396

    PubMed  CAS  Google Scholar 

  • Hirose T, Takano M, Terao T (2002) Cell wall invertase in developing rice caryopsis: molecular cloning of OsCIN1 and analysis of its expression in relation to its role in grain filling. Plant Cell Physiol 43:452–459

    Article  PubMed  CAS  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusion: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    PubMed  CAS  Google Scholar 

  • Johnson DA, Hill JP, Thomas MA (2006) The monosaccharide transporter gene family in land plants is ancient and shows differential subfamily expression and expansion across lineages. BMC Evol Biol 6:64

    Article  PubMed  Google Scholar 

  • Krishnan S, Dayanandan P (2003) Structural and histochemical studies on grain-filling in the caryopsis of rice (Oryza sativa L.). J Biosci 28:455–469

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Lemoine R (2000) Sucrose transporters in plants: update on function and structure. Biochim Biophys Acta 1465:246–262

    Article  PubMed  CAS  Google Scholar 

  • Leterrier M, Atanassova R, Laquitaine L, Gaillard C, Coutos-Thevenot P, Delrot S (2003) Expression of a putative grapevine hexose transporter in tobacco alters morphogenesis and assimilate partitioning. J Exp Bot 54:1193–1204

    Article  PubMed  CAS  Google Scholar 

  • Mamun EA, Alfred S, Cantrill LC, Overall RL, Sutton BG (2006) Effects of chilling on male gametophyte development in rice. Cell Biol Int 30:583–591

    Article  PubMed  CAS  Google Scholar 

  • Marger MD, Saier MHJ (1993) A major superfamily of transmembrane facilitators that catalyse uniport, symport and antiport. Trends Biochem Sci 18:13–20

    Article  PubMed  CAS  Google Scholar 

  • Meyer S, Melzer M, Truernit E, Hümmer C, Besenbeck R, Stadler R, Sauer N (2000) AtSUC3, a gene encoding a new Arabidopsis sucrose transporter, is expressed in cells adjacent to the vascular tissue and in a carpel cell layer. Plant J 24:869–882

    Article  PubMed  CAS  Google Scholar 

  • Miller ME, Chourey PS (1992) The maize invertase-deficient miniature-1 seed mutation is associated with aberrant pedicel and endosperm development. Plant Cell 4:297–305

    Article  PubMed  CAS  Google Scholar 

  • Ngampanya B, Sobolewska A, Takeda T, Toyofuku K, Narangajavana J, Ikeda A, Yamaguchi J (2003) Characterization of rice functional monosaccharide transporter, OsMST5. Biosci Biotechnol Biochem 67:556–562

    Article  PubMed  CAS  Google Scholar 

  • Pao SS, Paulsen IT, Saier MH Jr (1998) Major facilitator superfamily. Microbiol Mol Biol Rev 62:1–34

    PubMed  CAS  Google Scholar 

  • Sauer N, Tanner W (1989) The hexose carrier from Chlorella. cDNA cloning of a eucaryotic H+-cotransporter. FEBS Lett 259:43–46

    Article  PubMed  CAS  Google Scholar 

  • Schneidereit A, Scholz-Starke J, Sauer N, Büttner M (2005) AtSTP11, a pollen tube-specific monosaccharide transporter in Arabidopsis. Planta 221:48–55

    Article  PubMed  CAS  Google Scholar 

  • Szarka A, Horemans N, Banhegyi G, Asard H (2004) Facilitated glucose and dehydroascorbate transport in plant mitochondria. Arch Biochem Biophys 428:73–80

    Article  PubMed  CAS  Google Scholar 

  • Takeda T, Toyofuku K, Matsukura C, Yamaguchi J (2001) Sugar transporters involved in flowering and grain development of rice. J Plant Physiol 158:465–470

    Article  CAS  Google Scholar 

  • Toyofuku K, Kasahara M, Yamaguchi J (2000) Characterization and expression of monosaccharide transporters (OsMSTs) in rice. Plant Cell Physiol 41:940–947

    Article  PubMed  CAS  Google Scholar 

  • Wang HX, Weerasinghe RR, Perdue TD, Cakmakci NG, Taylor JP, Marzluff WF, Jones AM (2006) A Golgi-localized hexose transporter is involved in heterotrimeric G protein-mediated early development in Arabidopsis. Mol Biol Cell 17:4257–4269

    Article  PubMed  CAS  Google Scholar 

  • Weber H, Borisjuk L, Heim U, Sauer N, Wobus U (1997) A role for sugar transporters during seed development: molecular characterization of a hexose and a sucrose carrier in fava bean seeds. Plant Cell 9:895–908

    Article  PubMed  CAS  Google Scholar 

  • Weber A, Servaites JC, Geiger DR, Kofler H, Hille D, Groner F, Hebbeker U, Flugge UI (2000) Identification, purification, and molecular cloning of a putative plastidic glucose translocator. Plant Cell 12:787–802

    Article  PubMed  CAS  Google Scholar 

  • Weschke W, Panitz R, Gubatz S, Wang Q, Radchuk R, Weber H, Wobus U (2003) The role of invertases and hexose transporters in controlling sugar ratios in maternal and filial tissues of barley caryopses during early development. Plant J 33:395–411

    Article  PubMed  CAS  Google Scholar 

  • Wieczorke R, Krampe S, Weierstall T, Freidel K, Hollenberg CP, Boles E (1999) Concurrent knock-out of at least 20 transporter genes is required to block uptake of hexoses in Saccharomyces cerevisiae. FEBS Lett 464:123–128

    Article  PubMed  CAS  Google Scholar 

  • Weschke W, Panitz R, Sauer N, Wang Q, Neubohn B, Weber H, Wobus U (2000) Sucrose transport into barley seeds: molecular characterization of two transporters and implications for seed development and starch accumulation. Plant J 21:455–467

    Article  PubMed  CAS  Google Scholar 

  • Williams LE, Lemoine R, Sauer N (2000) Sugar transporters in higher plants – a diversity of roles and complex regulation. Trends Plant Sci 5:283–290

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Dr. Eckhard Boles (Heinrich-Heine-Universität, Düsseldorf, Germany) for providing the S. cerevisiae strain EBY.VW4000 and Dr. Michael Büttner (Universität Erlangen-Nürnberg, Erlangen, Germany) for providing the S. cerevisiae/E. coli shuttle vector pEX-Tag. We are grateful to Dr. Yule Liu of the Tsinghua University for valuable advice on revision of the manuscript. This work is supported by grants from National Program on Key Basic Research Projects (2004CB720406), Innovation Foundation of Chinese Academy of Science (KSCX2-SW-306 and KSCX1-SW-03), the Programme for Strategic Scientific Alliances (04-PSA-BD-04) between China and the Netherlands of the Royal Netherlands Academy of Arts and Sciences (KNAW) for P.B.F.O. and the KNAW China Exchange Programme (04CDP022) for Y.X.

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Authors and Affiliations

  1. State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Datun Road, Beijing, 100101, China

    Yongqin Wang, Honglin Xu, Xiaoli Wei, Chenglin Chai, Yuguo Xiao, Yu Zhang, Bin Chen, Guifang Xiao & Zhen Zhu

  2. Graduate School of the Chinese Academy of Sciences, Beijing, 100049, China

    Yongqin Wang, Chenglin Chai, Yuguo Xiao, Yu Zhang & Bin Chen

  3. Department of Molecular and Developmental Genetics, Institute of Biology (IBL), Leiden University, P.O. Box 9505, 2300 RA, Leiden, The Netherlands

    Yuguo Xiao, Yu Zhang, Pieter B. F. Ouwerkerk & Mei Wang

  4. TNO Quality of Life, Zernikedreef 9, 2333 CK, Leiden, The Netherlands

    Mei Wang

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  1. Yongqin Wang
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Correspondence to Zhen Zhu.

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Wang, Y., Xu, H., Wei, X. et al. Molecular cloning and expression analysis of a monosaccharide transporter gene OsMST4 from rice (Oryza sativa L.). Plant Mol Biol 65, 439–451 (2007). https://doi.org/10.1007/s11103-007-9228-x

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  • DOI: https://doi.org/10.1007/s11103-007-9228-x

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