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Development- and organ-specific expression of the genes for sucrose synthase and three isoenzymes of acid β-fructofuranosidase in carrot

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Abstract

The steady-state levels of transcripts for cellwall β-fructofuranosidase (cwβF), for isoenzymes I and II of soluble acid β-fructofuranosidase (sI, sII), and for sucrose synthase (ss) were determined in the sink and source organs of developing carrot (Daucus carota L.) plants. The expression patterns of the four genes clearly differed. The expression of the gene for cwβF was development-specific but not organ-specific; high transcript levels were only found in plants with primary roots, with about equal amounts in leaf lamina, petioles and roots. The genes for sI and sII were mainly expressed in roots, sI predominating in primary roots and sII in developing tap roots. Transcripts for ss were found at a low level in all developing plant organs and were markedly up-regulated during the development of young leaves and during the transition of primary roots to tap roots. Developing tap roots contained only transcripts for sII and for ss. Marked alterations in the expression of these two genes after manipulation of the source/sink balance of these plants indicates their importance in sucrose partitioning. We suggest that ss regulates sucrose utilization in developing tap roots, whereas sII located in the vacuole controls sucrose storage and sugar composition.

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Abbreviations

cw:

cell wall

βF:

β-fructofuranosidase

sI, sII:

isoenzymes I and II of carrot soluble acid β-fructofuranosidase

ss:

sucrose synthase

References

  • Alabran, D.M., Mabrouk, A.F. (1973) Carrot flavor. Sugars and free nitrogenous compounds in fresh carrots. J. Agric. Food Chem. 21, 205–208

    Google Scholar 

  • Amthor, J.S., McCree, K.J. (1990) Carbon balance of stressed plants: A conceptual model for integrating research results. In: Adaptation and acclimation mechanisms, pp. 1–15, Alscher, R.G., Cumming, J.R., eds. Wiley-Liss, New York

    Google Scholar 

  • Ap Rees, T. (1984) Sucrose metabolism. In: Storage carbohydrates in vascular plants, pp. 53–73, Lewis, D.H., ed. Cambridge University Press, Cambridge

    Google Scholar 

  • Arai, M., Mori, H., Imaseki, H. (1991) Roles of sucrose-metabolizing enzymes in growth of seedlings. Purification of acid invertase from growing hypocotyls of mung bean seedlings. Plant Cell Physiol. 32, 1291–1298

    Google Scholar 

  • Benhamou, N., Grenier, J., Chrispeels, M.J. (1991) Accumulation of β-fructosidase in the cell walls of tomato roots following infection by a fungal wilt pathogen. Plant Physiol. 97, 739–750

    Google Scholar 

  • Bradford, K.J., Hsiao, T.C. (1982) Physiological responses to moderate water stress. In: Encyclopedia of plant physiology, N.S., vol. 12B, pp. 264–323, Lange, O.L., Nobel, P.S., Osmond, C.B., Ziegler, H., eds. Springer Verlag, Berlin

    Google Scholar 

  • Chapleo, S., Hall, J.L. (1989) Sugar unloading in roots of Ricinus communis L. New Phytol. 111, 391–396

    Google Scholar 

  • Copeland, L. (1990) Enzymes of sucrose metabolism. Methods Plant Biochem. 3, 73–85

    Google Scholar 

  • Copping, L.G., Street, H.E. (1972) Properties of the invertases of cultured sycamore cells and changes in their activity during culture growth. Physiol. Plant. 25, 346–354

    Google Scholar 

  • Daie, J. (1984) Characterization of sugar transport in storage tissue of carrot. J. Am. Soc. Hort. Sci. 109, 718–722

    Google Scholar 

  • Daie, J. (1989) Phloem loading of sucrose: update and opportunities in molecular biology. Plant Mol. Biol. Rep. 7, 106–115

    Google Scholar 

  • Esau, K. (1940) Developmental anatomy of the fleshy storage organ of Daucus carota. Hilgardia 13, 175–209

    Google Scholar 

  • Eschrich, W. (1980) Free space invertase, its possible role in phloem unloading. Ber. Dtsch. Bot. Ges. 93, 363–378

    Google Scholar 

  • Eschrich, W. (1989) Phloem unloading of photoassimilates. In: Transport of photoassimilates, pp. 206–263, Baker, D.A., Mil burn, J.A., eds. John Wiley & Sons, New York

    Google Scholar 

  • Freeman, R.E., Simon, P.W. (1983) Evidence for simple genetic control of sugar type in carrot (Daucus carota L.). J. Am. Soc. Hort. Sci. 108, 50–54

    Google Scholar 

  • Getz, H.P. (1991) Sucrose transport in tonoplast vesicles of red beet roots is linked to ATP hydrolysis. Planta 185, 261–268

    Google Scholar 

  • Getz, H.P., Grosclaude, J., Kurkdjian, A., Lelièvre, F., Maretzki, A., Guern, J. (1993) Immunological evidence for the existence of a carrier protein for sucrose transport in tonoplast vesicles from red beet (Beta vulgaris L.) root storage tissue. Plant Physiol. 102, 751–760

    Google Scholar 

  • Giaquinta, R.T. (1980) Translocation of sucrose and oligosaccharides. Biochem Plants 3, 271–320

    Google Scholar 

  • Giaquinta, R.T., Lin, W, Sadler, N.L., Franceschi, V.R. (1983) Pathway of phloem unloading of sucrose in corn roots. Plant Physiol. 72, 362–367

    Google Scholar 

  • Gifford, R.M., Thorne, J.H., Hitz, W.D., Giaquinta, R.T. (1984) Crop productivity and photoassimilate partitioning. Science 225, 801–808

    Google Scholar 

  • Ho, L.C. (1988) Metabolism and compartmentation of imported sugars in sink organs in relation to sink strength. Annu. Rev. Plant Physiol. Plant Mol. Biol. 39, 355–378

    Google Scholar 

  • Ho. L.C., Baker, D.A. (1982) Regulation of loading and unloading in long distance transport systems. Physiol. Plant. 56, 225–230

    Google Scholar 

  • Hole, C.C., Dearman, J. (1994) Sucrose uptake by the phloem parenchyma of carrot storage root. J. Exp. Bot. 45, 7–15

    Google Scholar 

  • Isla, M.I., Vattuone, M.A., Sampietro, A.R. (1991) Modulation of potato invertase activity by fructose. Phytochemistry 30, 423–426

    Google Scholar 

  • Kempers, R., Prior, D.A.M., Van Bel, A.J.E., Oparka, K.J. (1993) Plasmodesmata between sieve element and companion cell of extrafascicular stem phloem of Curcubita maxima permit passage of 3 kDa fluorescent probes. Plant J. 4, 567–575

    Google Scholar 

  • Klann, E.M., Chetelat, R.T, Bennett, A.B. (1993) Expression of acid invertase gene controls sugar composition in tomato (Lycopersicon) fruit. Plant Physiol. 103, 863–870

    Google Scholar 

  • Kruger, N.J. (1990) Carbohydrate synthesis and degradation. In: Plant physiology, biochemistry and molecular biology, pp. 59–79, Dennis, D.T. Turpin, D.H., eds. Longman Scientific & Technical, Essex, UK

    Google Scholar 

  • Laurière, M., Laurière, C., Sturm, A., Faye, L., Chrispeels, M.J. (1988) Characterization of β-fructosidase, an extracellular glycoprotein of carrot cells. Biochimie 70, 1483–1491

    Google Scholar 

  • Leigh, R.A., ap Rees, T., Fuller, W.A., Banfield, J. (1979) The location of acid invertase activity and sucrose in the vacuoles of storage roots of beetroots (Beta vulgaris). Biochem. J. 178, 539–547

    Google Scholar 

  • Lester, G.E., Baker, L.R., Kelly, J.F. (1982) Physiology of sugar accumulation in carrot breeding lines and cultivars. J. Am. Soc. Hort. Sci. 107, 381–387

    Google Scholar 

  • Linge, S.E. (1989) Evidence for the uptake of sucrose intact into sugar cane internodes. Plant Physiol. 90, 6–8

    Google Scholar 

  • Lopez, M.E., Vattuone, M.A., Sampietro, A.R. (1988) Partial purification and properties of invertase from Carica papaya fruits. Phytochemistry 27, 3077–3081

    Google Scholar 

  • Maniatis T., Frisch, E., Sambrook J. (1989) Molecular cloning. A laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.

    Google Scholar 

  • Merlo, L., Geigenberger, P., Hajirezaei, M., Stitt, M. (1993) Changes of carbohydrates, metabolites and enzyme activities in potato tubers during development, and within a single tuber along a stolon-apex gradient. J. Plant Physiol. 142, 392–402

    Google Scholar 

  • Morell, M., Copeland, L. (1985) Sucrose synthase of soybean nodules. Plant Physiol. 78, 149–154

    Google Scholar 

  • Morris, D.A., Arthur, E.D. (1985) Effect of gibberellic acid on patterns of carbohydrate distribution and acid invertase activity in Phaseolus vulgaris. Physiol. Plant. 65, 257–262

    Google Scholar 

  • Nolte, K.D., Koch, K.E. (1993) Companion-cell specific localization of sucrose synthase in zones of phloem loading and unloading. Plant Physiol. 101, 899–905

    Google Scholar 

  • Oparka, K.J. (1990) What is phloem unloading? Plant Physiol. 94, 393–396

    Google Scholar 

  • Parr, D.R., Edelman, J., Hawker, J.S. (1976) Growth and sucrose metabolism of carrot callus strains with normal and low acid invertase activity. Physiol. Plant. 37, 223–228

    Google Scholar 

  • Patrick, J.W. (1990) Sieve element unloading: cellular pathway, mechanism and control. Physiol. Plant. 78, 298–308

    Google Scholar 

  • Phan, C.T., Hsu, H. (1973) Physical and chemical changes occurring in the carrot root during growth. Can. J. Plant Sci. 53, 629–634

    Google Scholar 

  • Pollock, C.J., Lloyd, E.J. (1977) The distribution of acid invertase in developing leaves of Lolium tetnulentum L. Planta 133, 197–200

    Google Scholar 

  • Prescott, A., Martin, C. (1987) A rapid method for the quantitative assessment of levels of specific mRNAs in plants. Plant Mol. Biol. Rep. 4, 219–224

    Google Scholar 

  • Ricardo, C.P.P. (1974) Alkaline β-fructosidase of tuberous roots: Possible physiological function. Planta 118, 333–343

    Google Scholar 

  • Ricardo, C.P.P., Ap Rees, T. (1970) Invertase activity during the development of carrot roots. Phytochemistry 9, 239–247

    Google Scholar 

  • Ricardo, C.P.P., Sovia, D. (1974) Development of tuberous roots and sugar accumulation as related to invertase activity and mineral nutrition. Planta 114, 43–55

    Google Scholar 

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

    Google Scholar 

  • Sampietro, A.R., Vattuone, M.A., Prado, F.E. (1980) A regulatory invertase from sugar can leaf-sheaths. Phytochemistry 19, 1637–1642

    Google Scholar 

  • Schmalstig, J.G., Hitz, W.D. (1987) Contribution of sucrose synthase and invertase to the metabolism of sucrose in developing leaves. Plant Physiol. 85, 407–412

    Google Scholar 

  • Sharpe, R.E., Davies, W.J. (1979) Solute regulation and growth by roots and shoots of water-stressed maize plants. Planta 147, 43–49

    Google Scholar 

  • Silva, M.P., Ricardo, C.P.P. (1992) β-Fructosidases and in vitro dedifferentiation-redifferentiation of carrot cells. Phytochemistry 31, 1507–1511

    Google Scholar 

  • Silvus, J.E., Snyder, F.W. (1979) Photosynthate partitioning and enzymes of sucrose metabolism in sugar beet roots. Physiol. Plant. 46, 169–173

    Google Scholar 

  • Sowokinos, J.R., Varns, J.L. (1992) Induction of sucrose synthase in potato tissue culture: effect of carbon source and metabolic regulators on sink strength. J. Plant Physiol. 139, 672–679

    Google Scholar 

  • Stommel, J.R., Simon, P.W. (1990) Multiple forms of invertase from Daucus carota cell cultures. Phytochemistry 7, 2087–2089

    Google Scholar 

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

    Google Scholar 

  • Sun, J., Loboda, T., Sung, S.S., Black, C.C. Jr (1992) Sucrose synthase in wild tomato, Lycopersicon chmielewskii, and tomato fruit sink strength. Plant Physiol. 98, 1163–1169

    Google Scholar 

  • Sung, S.-J.S., Xu, D.-P., Black, C.C. (1989) Identification of actively filling sucrose sinks. Plant Physiol. 89, 1117–1121

    Google Scholar 

  • Thorn, M., Maretzki, A. (1992) Evidence of direct uptake of sucrose by sugercane stalk tissue. J. Plant Physiol. 139, 555–559

    Google Scholar 

  • Turgeon, R. (1989) The sink-source transition in leaves. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 119–138

    Google Scholar 

  • Unger, C., Hofsteenge, J., Sturm, A. (1992) Purification and characterization of a soluble β-fructofuranosidase from Daucus carota. Eur. J. Biochem. 204, 915–921

    Google Scholar 

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

    Google Scholar 

  • Van Bel, A.J.E. (1993) Strategies of phloem loading. Annu. Rev. Plant. Physiol. Plant Mol. Biol. 44, 253–281

    Google Scholar 

  • Vattuone, M.A., Fleischmacher, O.L., Prado, F.E., Vinals, A.L., Sampietro, A.R. (1983) Localization of invertase activities in Ricinus communis leaves. Phytochemistry 22, 1361–1365

    Google Scholar 

  • Walker, A.J., Ho, L.C., Baker, D.A. (1978) Carbon translocation in the tomato: pathways of carbon metabolism in fruit. Ann. Bot. 42, 901–909

    Google Scholar 

  • Wang, A.-Y., Yu, W.-P., Juang, R.-H., Huang. J.-W, Sung, H.-Y, 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

    Google Scholar 

  • Wang, F., Sanz, A., Brenner, M.L., Smith, A. (1993a). Sucrose synthase, starch accumulation, and tomato fruit sink strength. Plant Physiol. 101, 321–327

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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Author notes

  1. Veronika Šebková

    Present address: Department of Biochemistry and Microbiology, Institute of Chemical Technology, Technicka 5, 6, Prague, Czech Republic

Authors and Affiliations

  1. Friedrich-Miescher-Institut, Postfach 2543, CH-4002, Basel, Switzerland

    Arnd Sturm, Veronika Šebková, Kathrin Lorenz, Markus Hardegger & Susanne Lienhard

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  1. Arnd Sturm
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  2. Veronika Šebková
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  3. Kathrin Lorenz
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  4. Markus Hardegger
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  5. Susanne Lienhard
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  6. Christoph Unger
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We thank our colleagues Jürg Bilang, Thomas Boller, Pat King and Fred Meins (Friedrich-Miescher-Institut), Prem Chourey (University of Florida, Gainesville, Fla. USA) and Walter Eschrich (University of Göttingen, Germany) for critical reading of the manuscript and for constructive criticism.

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Sturm, A., Šebková, V., Lorenz, K. et al. Development- and organ-specific expression of the genes for sucrose synthase and three isoenzymes of acid β-fructofuranosidase in carrot. Planta 195, 601–610 (1995). https://doi.org/10.1007/BF00195721

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