Abstract
Tomato (Solanum lycopersicum) plants have four fructokinase genes, SlFRK1-4. The SlFRK4 is expressed only in pollen whereas the other three are expressed in all plant parts. While SlFRK2 and SlFRK3 are involved in vascular tissue development and affects the shape, size, and cell-wall width of xylem vessels and xylem fibers, the role of SlFRK1 has not been studied previously. The current work investigates the expression of SlFRK1 using transgenic tomato plants expressing the β-glucuronidase reporter gene under the SlFRK1 promoter, as well as the role of SlFRK1 using transgenic plants with antisense suppression of SlFRK1. The SlFRK1 promoter is expressed primarily in vascular tissues and specific suppression of SlFRK1 reduces water transport in stems, but has no other anatomical or phenotypic effects. Combined suppression of SlFRK1 and SlFRK2 severely inhibited plant growth and an anatomical analysis revealed a reduction in secondary xylem area and distorted phloem fibers characterized by thin cell walls and reduced lignification. The results suggest that SlFRK1 is involved in vascular tissue development and hydraulic conductivity in tomato plants and that SlFRK1 is important for normal phloem fiber development, together with SlFRK2.
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Abbreviations
- FRK:
-
fruktokinase
- GUS:
-
β-glucuronidase
- HXK:
-
hexokinase
- Kh:
-
hydraulic conductivity
- SUS:
-
sucrose synthase
References
Aloni, R.: Role of auxin and sucrose in the differentiation of sieve and tracheary elements in plant tissue cultures. - Planta 150: 255–263, 1980.
Dai, N., Kandel, M., Petreikov, M., Levine, I., Ricard, B., Rothan, C., Schaffer, A.A., Granot, D.: The tomato hexokinase LeHXK1: cloning, mapping, expression pattern and phylogenetic relationships. - Plant Sci. 163: 581–590, 2002.
Dai, N., Schaffer, A., Petreikov, M., Granot, D.: Potato (Solanum tuberosum L.) fructokinase expressed in yeast exhibits inhibition by fructose of both in vitro enzyme activity and rate of cell proliferation. - Plant Sci. 128: 191–197, 1997.
Damari-Weissler, H., Kandel-Kfir, M., Gidoni, D., Mett, A., Belausov, E., Granot, D.: Evidence for intracellular spatial separation of hexokinases and fructokinases in tomato plants. - Planta 224: 1495–1502, 2006.
Damari-Weissler, H., Rachamilevitch, S., Aloni, R., German, M.A., Cohen, S., Zwieniecki, M.A., Holbrook, N.M., Granot, D.: LeFRK2 is required for phloem and xylem differentiation and the transport of both sugar and water. - Planta. 230: 795–805, 2009.
David-Schwartz, R., Weintraub, L., Vidavski, R., Zemach, H., Murakhovsky, L., Swartzberg, D., Granot, D.: The SlFRK4 promoter is active only during late stages of pollen and anther development. - Plant Sci. 199-200: 61–70, 2013.
Dennis, D.T., Blakeley, S.D.: Carbohydrate Metabolism. - American Society of Plant Physiologists, Rockville 2000.
Gardner, A., Davies, H.V., Burch, L.R.: Purification and properties of fructokinase from developing tubers of potato (Solanum tuberosum L.). - Plant Physiol. 100: 178–183, 1992.
German, M.A., Asher, I., Petreikov, M., Dai, N., Schaffer, A.A., Granot, D.: Cloning, expression and characterization of LeFRK3, the fourth tomato (Lycopersicon esculentum Mill.) gene encoding fructokinase. - Plant Sci. 166: 285–291, 2004.
German, M.A., Dai, N., Chmelnitsky, I., Sobolev, I., Salts, Y., Barg, R., Schaffer, A.A., Granot, D.: LeFRK4, a novel tomato (Lycopersicon esculentum Mill.) fructokinase specifically expressed in stamens. - Plant Sci. 163: 607–613, 2002.
German, M.A., Dai, N., Matsevitz, T., Hanael, R., Petreikov, M., Bernstein, N., Ioffe, M., Shahak, Y., Schaffer, A.A., Granot, D.: Suppression of fructokinase encoded by LeFRK2 in tomato stem inhibits growth and causes wilting of young leaves. - Plant J. 34: 837–846, 2003.
Gorska, A., Ye, Q., Holbrook, N.M., Zwieniecki, M.A.: Nitrate control of root hydraulic properties in plants: translating local information to whole plant response. - Plant Physiol. 148: 1159–1167, 2008.
Granot, D.: Role of tomato hexose kinases. - Funct. Plant Biol. 34: 564–570, 2007.
Granot, D., David-Schwartz, R., Kelly, G.: Hexose kinases and their role in sugar-sensing and plant development. - Front. Plant Sci. 4: 44, 2013.
Hoagland, D.R., Arnon, D.I.: The water culture method for growing plants without soil. - Calif. Agr. Exp. Sta. Circular 347: 1–39, 1950.
Kanayama, Y., Dai, N., Granot, D., Petreikov, M., Schaffer, A., Bennett, A.B.: Divergent fructokinase genes are differentially expressed in tomato. - Plant Physiol. 113: 1379–1384, 1997.
Odanaka, S., Bennett, A.B., Kanayama, Y.: Distinct physiological roles of fructokinase isozymes revealed by genespecific suppression of frk1 and frk2 expression in tomato. - Plant Physiol. 129: 1119–1126, 2002.
Petreikov, M., Dai, N., Granot, D., Schaffer, A.A.: Characterization of native and yeast-expressed tomato fruit fructokinase enzymes. - Phytochemistry 58: 841–847, 2001.
Renz, A., Stitt, M.: Substrate-specificity and product inhibition of different forms of fructokinases and hexokinases in developing potato tubers. - Planta 190: 166–175, 1993.
Roach, M., Gerber, L., Sandquist, D., Gorzsas, A., Hedenstrom, M., Kumar, M., Steinhauser, M.C., Feil, R., Daniel, G., Stitt, M., Sundberg, B., Niittyla, T.: Fructokinase is required for carbon partitioning to cellulose in aspen wood. - Plant J. cell. mol. Biol. 70: 967–977, 2012.
Ruzin, S.E.: Plant Microtechnique and Microscopy. - Oxford University Press, Oxford - New York, 1999.
Stein, O., Avin-Wittenberg, T., Krahnert, I., Zemach, H., Bogol, V., Daron, O., Aloni, R., Fernie, A.R., Granot, D.: Arabidopsis fructokinases are important for seed oil accumulation and vascular development. - Front. Plant Sci. 7: 2047. doi: 10.3389/fpls.2016.02047, 2017.
Stein, O., Damari-Weissler, H., Secchi, F., Rachamilevitch, S., German, M.A., Yeselson, Y., Amir, R., Schaffer, A., Holbrook, N.M., Aloni, R., Zwieniecki, M.A., Granot, D.: The tomato plastidic fructokinase SlFRK3 plays a role in xylem development. - New Phytol. 209: 1484–1495, 2016.
Townsley, B.T., Sinha, N.R., Kang, J.: KNOX1 genes regulate lignin deposition and composition in monocots and dicots. - Front. Plant Sci. 4: 121, 2013.
Weise, A., Lalonde, S., Kuhn, C., Frommer, W.B., Ward, J.M.: Introns control expression of sucrose transporter LeSUT1 in trichomes, companion cells and in guard cells. - Plant mol. Biol. 68: 251–262, 2008.
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Stein, O., Secchi, F., German, M.A. et al. The tomato cytosolic fructokinase FRK1 is important for phloem fiber development. Biol Plant 62, 353–361 (2018). https://doi.org/10.1007/s10535-017-0762-3
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DOI: https://doi.org/10.1007/s10535-017-0762-3