Immunolocalization of the PmSUC1 Sucrose Transporter in Plantago major Flowers and Reporter-Gene Analyses of the PmSUC1 Promoter Suggest a Role in Sucrose Release from the Inner Integument

Abstract

This paper presents a detailed analysis of the PmSUC1 gene from Plantago major, of its promoter activity in Arabidopsis, and of the tissue specific localization of the encoded protein in Plantago. PmSUC1 promoter activity was detected in the innermost layer of the inner integument (the endothel) of Arabidopsis plants expressing the gene of the green fluorescent protein (GFP) under the control of the PmSUC1 promoter. This promoter activity was confirmed with a PmSUC1-specific antiserum that identified the PmSUC1 protein in the endothel of Plantago and of Arabidopsis plants expressing the PmSUC1 gene under the control of its own promoter. PmSUC1 promoter activity and PmSUC1 protein were also detected in pollen grains during maturation inside the anthers and in pollen tubes during and after germination. These results demonstrate that PmSUC1 is involved in sucrose partitioning to the young embryo and to the developing pollen and growing pollen tube. In the innermost cell layer of the inner integument, a tissue that delivers nutrients to the endosperm and the embryo, PmSUC1 may catalyze the release of sucrose into the apoplast.

Key words

Inner integument - Plantago major - PmSUC1 - pollen - sink tissue.

References

• 1 Aoki N., Hirose T., Scofield G. N., Whitfeld P. R., Furbank R. T.. The sucrose transporter gene family in rice.  Plant and Cell Physiology. (2003);  44 223-232
• 2 Barker L., Kühn C., Weise A., Schulz A., Gebhardt C., Hirner B., Hellmann H., Schulze W., Ward J. M., Frommer W. B.. SUT2, a putative sucrose sensor in sieve elements.  Plant Cell. (2000);  12 1153-1164
• 3 Barth I., Meyer S., Sauer N.. PmSUC3: Characterization of a SUT2/SUC3-type sucrose transporter from Plantago major.  Plant Cell. (2003);  15 1375-1385
• 4 Becker D., Kemper E., Schell J., Masterson R.. New plant binary vectors with selectable markers located proximal to the left T‐DNA border.  Plant Molecular Biology. (1992);  20 1195-1197
• 5 Carpaneto A., Geiger D., Bamberg E., Sauer N., Fromm J., Hedrich R.. Phloem-localized, proton-coupled sucrose carrier ZmSUT1 mediates sucrose efflux under control of sucrose gradient and pmf.  Journal of Biological Chemistry. (2005);  280 21437-21443
• 6 Davies C., Wolf T., Robinson S. P.. Three putative sucrose transporters are differentially expressed in grapevine tissues.  Plant Science. (1999);  147 93-100
• 7 Endler A., Meyer S., Schelbert S., Schneider T., Weschke W., Peters S. W., Keller F., Baginsky S., Martinoia E., Schmidt U. G.. Identification of a vacuolar sucrose transporter in barley and Arabidopsis mesophyll cells by a tonoplast proteomic approach.  Plant Physiology. (2006);  141 196-207
• 8 Gahrtz M., Schmelzer E., Stolz J., Sauer N.. Expression of the PmSUC1 sucrose carrier gene from Plantago major L. is induced during seed development.  The Plant Journal. (1996);  9 93-100
• 9 Gahrtz M., Stolz J., Sauer N.. A phloem-specific sucrose-H⁺ symporter from Plantago major L. supports the model of apoplastic phloem loading.  The Plant Journal. (1994);  6 697-706
• 10 Garcia M. L., Viitanen P., Foster D. L., Kaback H. R.. Mechanism of lactose translocation in proteoliposomes reconstituted with lac carrier protein purified from Escherichia coli. 1. Effect of pH and imposed membrane potential on efflux, exchange, and counterflow.  Biochemistry. (1983);  22 2524-2531
• 11 Gottwald J. R., Krysan P. J., Young J. C., Evert R. F., Sussman M. R.. Genetic evidence for the in planta role of phloem-specific plasma membrane sucrose transporters.  Proceedings of the National Academy of Sciences of the USA. (2000);  97 13979-13984
• 39 Hanahan D.. Studies on transformation of E. coli with plasmids.  Journal of Molecular Biology. (1983);  166 557-580
• 12 Heinemeyer W., Kleinschmidt J. A., Saidowsky J., Escher C., Wolf D. H.. Proteinase yscE, the yeast proteasome/multicatalytic-multifunctional proteinase: mutants unravel its function in stress induced proteolysis and uncover its necessity for cell survival.  The EMBO Journal. (1991);  10 555-562
• 40 Holsters M., Silva B., Van Vliet F., Genetello C., De Block M., Dhaese P., Depicker A., Inze D., Engler G., Villarroel R., Van Montagu M., Schell J.. The functional organization of the nopaline Agrobacterium tumefaciens plasmid pTiC58.  Plasmid. (1980);  3 212-230
• 13 Komor E., Haass D., Tanner W.. Unusual features of the active hexose uptake system of Chlorella vulgaris.  Biochimica et Biophysica Acta. (1972);  266 649-660
• 14 Komor E., Haass D., Komor B., Tanner W.. The active hexose-uptake system of Chlorella vulgaris.  European Journal of Biochemistry. (1973);  39 193-200
• 15 Kühn C., Franceschi V. R., Schulz A., Lemoine R., Frommer W. B.. Macromolecular trafficking indicated by localization and turnover of sucrose transporters in enucleate sieve elements.  Science. (1997);  275 1298-1300
• 16 Lalanne E., Mathieu C., Roche O., Vedel F., De Pape R.. Structure and specific expression of a Nicotiana sylvestris putative amino-acid transporter gene in mature and in vitro germinating pollen.  Plant Molecular Biology. (1997);  35 855-864
• 17 Lemoine R., Bürkle L., Barker L., Sakr S., Kühn C., Regnacq M., Gaillard C., Delrot S., Frommer W. B.. Identification of a pollen-specific sucrose transporter-like protein NtSUT3 from tobacco.  FEBS Letters. (1999);  454 325-330
• 19 Liu Y. G., Whittier R. F.. Thermal asymmetric interlaced PCR: automatable amplification and sequencing of insert end fragments from P1 and YAC clones for chromosome walking.  Genomics. (1995);  25 674-681
• 20 Meyer S., Lauterbach C., Niedermeier M., Barth I., Sjolund R. D., Sauer N.. Wounding enhances expression of AtSUC3, a sucrose transporter from Arabidopsis sieve elements and sink tissues.  Plant Physiology. (2004);  134 684-693
• 21 Meyer S., Truernit E., Hümmer C., Besenbeck R., Stadler R., Sauer N.. AtSUC3, a gene encoding a new Arabidopsis sucrose transporter, is expressed in cells adjacent to the vascular tissue and in a carpel cell layer.  The Plant Journal. (2000);  24 869-882
• 42 Riesmeier J. W., Willmitzer L., Frommer W. B.. Isolation and characterization of a sucrose carrier cDNA from spinach by functional expression in yeast.  The EMBO Journal. (1992);  11 4705-4713
• 41 Riesmeier J. W., Hirner B., Frommer W. B.. Potato sucrose transporter expression in minor veins indicates a role in phloem loading.  Plant Cell. (1993);  5 1591-1598
• 22 Ruan Y.-L., Llewellyn D. J., Furbank R. T.. The control of single-celled cotton fiber elongation by developmentally reversible gating of plasmodesmata an coordinated expression of sucrose and K⁺ transporters and expansin.  Plant Cell. (2001);  13 47-60
• 43 Sauer N., Ludwig A., Knoblauch A., Rothe P., Gahrtz M., Klebl F.. AtSUC8 and AtSUC9 encode functional sucrose transporters, but the closely related AtSUC6 and AtSUC7 genes encode aberrant proteins in different Arabidopsis ecotypes.  The Plant Journal. (2004);  40 120-130
• 23 Sauer N., Stadler R.. A sink-specific H⁺/monosaccharide co-transporter from Nicotiana tabacum: cloning and heterologous expression in baker's yeast.  The Plant Journal. (1993);  4 601-610
• 44 Sauer N., Stolz J.. SUC1 and SUC2: two sucrose transporters from Arabidopsis thaliana; expression and characterization in baker's yeast and identification of the histidine tagged protein.  The Plant Journal. (1994);  6 67-77
• 24 Schneidereit A., Scholz-Starke J., Büttner M.. Functional characterization and expression analyses of the glucose-specific AtSTP9 monosaccharide transporter in pollen of Arabidopsis.  Plant Physiology. (2003);  133 182-190
• 25 Schneidereit A., Scholz-Starke J., Sauer N., Büttner M.. AtSTP11, a pollen tube-specific monosaccharide transporter in Arabidopsis.  Planta. (2005);  221 48-55
• 26 Scholz-Starke J., Büttner M., Sauer N.. AtSTP6, a new pollen-specific H⁺-monosaccharide symporter from Arabidopsis.  Plant Physiology. (2003);  131 70-77
• 27 Schwacke R., Grallath S., Breitkreuz K. E., Stransky E., Stransky H., Frommer W. B., Rentsch D.. LeProT1, a transporter for proline, glycine betaine, and gamma-amino butyric acid in tomato pollen.  Plant Cell. (1999);  11 377-392
• 28 Stadler R., Brandner J., Schulz A., Gahrtz M., Sauer N.. Phloem loading by the PmSUC2 sucrose carrier from Plantago major occurs into companion cells.  Plant Cell. (1995);  7 1545-1554
• 45 Stadler R., Sauer N.. The Arabidopsis thaliana AtSUC2 gene is specifically expressed in companion cells.  Botanica Acta. (1996);  109 299-306
• 29 Stadler R., Truernit E., Gahrtz M., Sauer N.. The AtSUC1 sucrose carrier may represent the osmotic driving force for anther dehiscence and pollen tube growth in Arabidopsis.  The Plant Journal. (1999);  19 269-278
• 30 Stadler R., Wright K. M., Lauterbach C., Amon G., Gahrtz M., Feuerstein A., Oparka K. J., Sauer N.. Expression of GFP-fusions in Arabidopsis companion cells reveals non-specific protein trafficking into sieve elements and identifies a novel post-phloem domain in roots.  The Plant Journal. (2005 a);  41 319-331
• 31 Stadler R., Lauterbach C., Sauer N.. Cell-to-cell movement of GFP reveals post-phloem transport in the outer integument and identifies symplastic domains in Arabidopsis seeds and embryos.  Plant Physiology. (2005 b);  41 319-331
• 32 Therisod H., Ghazi A., Houssin C., Shechterk E. I.. Lactose transport in Escherichia coli cells. Evidence in favor of a permease-catalyzed efflux of lactose without protons.  FEBS Letters. (1982);  140 181-184
• 33 Truernit E., Sauer N.. The promoter of the Arabidopsis thaliana SUC2 sucrose-H⁺ symporter gene directs expression of β-glucuronidase to the phloem: evidence for phloem loading and unloading by SUC2.  Planta. (1995);  196 564-570
• 34 Truernit E., Stadler R., Baier K., Sauer N.. A male gametophyte-specific monosaccharide transporter in Arabidopsis.  The Plant Journal. (1999);  17 191-201
• 35 Weber H., Borisjuk L., Heim U., Sauer N., Wobus U.. A role for sugar transporters during seed development: molecular characterization of a hexose and a sucrose carrier in Fava bean seeds.  Plant Cell. (1997);  9 895-908
• 36 Weise A., Barker L., Kühn C., Lalonde S., Buschmann H., Frommer W. B., Ward J. M.. A new subfamily of sucrose transporters, SUT4, with low affinity/high capacity is localized in enucleate sieve elements of plants.  Plant Cell. (2000);  12 1345-1356
• 37 Ylstra B., Garrido D., Busscher J., van Tunen A. J.. Hexose transport in growing petunia pollen tubes and characterization of a pollen-specific, putative monosaccharide transporter.  Plant Physiology. (1998);  118 297-304
• 38 Yu J., Hu S., Wang J., Wong G. K., Li S., Liu B., Deng Y., Dai L., Zhou Y., Zhang X., Cao M., Liu J., Sun J., Tang J., Chen Y., Huang X., Lin W., Ye C., Tong W., Cong L., Geng J., Han Y., Li L., Li W., Hu G., Huang X., Li W., Li J., Liu Z., Li L., Liu J., Qi Q., Liu J., Li L., Li T., Wang X., Lu H., Wu T., Zhu M., Ni P., Han H., Dong W., Ren X., Feng X., Cui P., Li X., Wang H., Xu X., Zhai W., Xu Z., Zhang J., He S., Zhang J., Xu J., Zhang K., Zheng X., Dong J., Zeng W., Tao L., Ye J., Tan J., Ren X., Chen X., He J., Liu D., Tian W., Tian C., Xia H., Bao Q., Li G., Gao H., Cao T., Wang J., Zhao W., Li P., Chen W., Wang X., Zhang Y., Hu J., Wang J., Liu S., Yang J., Zhang G., Xiong Y., Li Z., Mao L., Zhou C., Zhu Z., Chen R., Hao B., Zheng W., Chen S., Guo W., Li G., Liu S., Tao M., Wang J., Zhu L., Yuan L., Yang H.. A draft sequence of the rice genome (Oryza sativa L. ssp. indica).  Science. (2002);  296 79-92

Editor: A. Weber