Variations in Carbohydrate Content and Sucrose-Metabolizing Enzymes in Tomato (Solanum lycopersicum L.) Stamen Parts during Pollen Maturation


The formation of mature and fertile pollen grains, taking place inside the anther, depends on supply of assimilates, in the form of sucrose, provided mainly by the leaves. Data is limited, however, with respect to the understanding of sucrose metabolism in microspores and the supporting tissues. The aims of the present work were to 1) follow the changes in total and relative concentrations of sucrose, glucose, fructose and starch in the stamen parts and microspores up until anthesis, 2) follow the activities of sucrose-metabolism-related enzymes, in the anther walls fraction and microspores of the crop plant tomato. Sucrose was found to be partially cleaved in the filament, decreasing by more than twofold in the anther wall layers and the locular fluid, and to accumulate in the mature pollen grains, constituting 80% of total soluble sugars. Thus, sucrose was both the starting sugar, supporting microspore development, and the main carbohydrate accumulated at the end of the pollen-development program. The major invertase found to be active in both the anther wall layers and in maturing microspores was cell-wall-bound invertase. High fructokinase 2 and sucrose phosphate synthase activities during pollen maturation coincided with sucrose accumulation. The potential importance of sucrose accumulation during pollen dehydration phase and germination is discussed.

Share and Cite:

E. Pressman, R. Shaked, S. Shen, L. Altahan and N. Firon, "Variations in Carbohydrate Content and Sucrose-Metabolizing Enzymes in Tomato (Solanum lycopersicum L.) Stamen Parts during Pollen Maturation," American Journal of Plant Sciences, Vol. 3 No. 2, 2012, pp. 252-260. doi: 10.4236/ajps.2012.32030.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] W. Eschrich, “Phloem Unloading Following Reactivation in Predarkened Mature Maize Leaves,” Planta, Vol. 161, No. 2, 1984, pp. 113-119. doi:10.1007/BF00395470
[2] C. Clement and J. C. Audran, “Anther Wall Layers Control Pollen Sugar Nutrition in Lilum,” Protoplasma, Vol. 187, No. 1-4, 1995, pp. 172-181. doi:10.1007/BF01280246
[3] C. Clement, P. Mischler, M. Burrus and J. C. Audran, “Characteristics of the Photosynthetic Apparatus and CO2 Fixation in the Flower Bud of Lilium. I. Corolla,” International Journal of Plant Sciences, Vol. 158, No. 6, 1997, pp. 794-800. doi:10.1086/297492
[4] R. B. Goldberg, T. P. Beals and P. M. Sanders, “Anther Development: Basic Principles and Practical Applications,” The Plant Cell, Vol. 5, No. 10, 1993, pp. 1217-1229.
[5] P. L. Polowick and V. K. Sawhney, “Defferentiation of the Ttapetum during Microsporogenesis in Tomato (Lycopersicon esculentum Mill.), with Special Reference to the Tapetal Cell Wall,” Annals of Botany, Vol. 72, No. 6, 1993, pp. 595 -605. doi:10.1006/anbo.1993.1150
[6] G. Suzuki, “Recent Progress in Plant Reproduction Research: The Story of the Male Gametophyte Through to Successful Fertilization,” Plant and Cell Physiology, Vol. 50, No. 11, 2009, pp. 1857-1864. doi:10.1093/pcp/pcp142
[7] C. Clement, P. Laporte and J. C. Audran, “The Loculus Content and Tapetum during Pollen Development in Lilium,” Sexual Plant Reproduction, Vol. 11, No. 1, 1998, pp. 94-106.
[8] A. J. Castro and C. Clement, “Sucrose and Starch Catabolism in the Anther of Lilium during Its Development: A Comparative Study among the Anther Wall, Locular Fluid and Microspore/Pollen Fractions,” Planta, Vol. 225, No. 6, 2007, pp. 1573-1582. doi:10.1007/s00425-006-0443-5
[9] N. J. Kruger, “Carbohydrate Synthesis and Degradation,” In: D. T. Dennis and D. H. Turpin, Eds., Plant Physiology, Biochemistry and Molecular Biology, Longman Scientific and Technical, Harlow, 1990, pp. 59-79.
[10] Z. Tymowska-Lalanne and M. Kreis, “The Plant Invertases: Physiology, Biochemistry and Molecular Biology,” Advances in Botanical Research, Vol. 28, No. 1, 1998, pp. 71-117. doi:10.1016/S0065-2296(08)60294-3
[11] A. Strum, D. Hess, H. S. Lee and S. Lienhard, “Neutral Invertase is a Novel Type of Sucrose-Cleaving Enzyme,” Physiologia Plantarum, Vol. 107, No. 2, 1999, pp. 159-165. doi:10.1034/j.1399-3054.1999.100202.x
[12] J. Q. Chen and C. C. Black, “Biochemical and Immunological Properties of Alkaline Invertase Isolated from Sprouting Soybean Hypocotyls,” Archives of Biochemistry and Biophysics, Vol. 295, No. 1, 1992, pp. 61-69. doi:10.1016/0003-9861(92)90488-I
[13] J. Y. Park, T. Canam, K. Y. Kang , D. D. Ellis and S. D. Mansfield, “Over-Expression of an Arabidopsis Family a Sucrose Phosphate Synthase (SPS) Gene Alters Plant Growth and Fibre Development,” Transgenic Research, Vol. 17, No. 2, 2008, pp. 181-192. doi:10.1007/s11248-007-9090-2
[14] P. Geigenberger, R. Reimholz, M. Geiger, L. Merlo, V. Canale and M. Stitt, “Regulation of Sucrose and Starch Metabolism in Potato Tubers in Response to Short-term Water Deficit,” Planta, Vol. 201, No. 4, 1997, pp. 502-518. doi:10.1007/s004250050095
[15] S. C. Huber and J. L. Huber, “Role and Regulation of Sucrose Phosphate Synthase in Higher Plants,” Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 47, No. 1, 1996, pp. 431-444. doi:10.1146/annurev.arplant.47.1.431
[16] S. Chen, M. Hajirezaei and F. Bornke, “Differential Expression of Sucrose-Phosphate Synthase Isoenzymes in Tobacco Reflects their Functional Specialization during Dark-Governed Starch Mobilization in Source Leaves,” Plant Physiology, Vol. 139, No. 3, 2005, pp. 1163-1174. doi:10.1104/pp.105.069468
[17] C. J. Baxter, C. H. Foyer, J. Turner, S. A. Rolfe and W. P. Quick, “Elevated Sucrose-Phosphate Synthase Activity in Transgenic Tobacco Sustains Photosynthesis in Older Leaves and Alters Development,” Journal of Experimental Botany, Vol. 54, No. 389, 2003, pp. 1813-1820. doi:10.1093/jxb/erg196
[18] M. M. Laporte, J. A. Galagan, A. L. Prasch, P. J. Vanderveer, D. T. Hanson, C. K. Shewmaker and T. D. Sharkey, “Promoter Strength and Tissue Specificity Effects on Growth of Tomato Plants Transformed with Maize Sucrose-Phosphate Synthase,” Planta, Vol. 212, No. 5-6, 2001, pp. 817-822. doi:10.1007/s004250000433
[19] C. H. Haigler, M. Ivanova-Datcheva, P. S. Hogan, V. V. Salnikov, S. Hwang, K. Martin and D. P. Delmer, “Carbon Partitioning to Cellulose Synthesis,” Plant Molecular Biology, Vol. 47, No. 1-2, 2001, pp. 29-51. doi:10.1023/A:1010615027986
[20] M. A. German, N. Dai, I. Chmelnitsky, I. Sobolev, Y. Salts, R. Barg, A. A. Schaffer and D. Granot, “LeFRK4, a Novel Tomato (Lycopersicon esculentum Mill.) Fructokinase Specifically Expressed in Stamens,” Plant Science, Vol. 163, No. 3, 2002, pp. 607-613. doi:10.1016/S0168-9452(02)00170-X
[21] E. Pressman, M. M. Peet and D. M. Pharr, “The Effect of Heat Stress on Tomato Pollen Characteristics Is Associated with Changes in Carbohydrate Concentration in the Developing Anthers,” Annals of Botany, Vol. 90, No. 5, 2002, pp. 631-636. doi:10.1093/aob/mcf240
[22] V. K. Sawhney and S. K. Bhadula, “Microsporogenesis in the Normal and Male-Sterile Stamenless-2 Mutant of Tomato (Lycopersicon esculentum),” Canadian Journal of Botany, Vol. 866, No. 10, 1988, pp. 2013-2021.
[23] N. Aouali, P. Laporte and C. Clement, “Pectin Secretion and Distribution in the Anther during Pollen Development in Lilium,” Planta, Vol. 213, No. 1, 2001, pp. 71-79. doi:10.1007/s004250000469
[24] N. L. Hubbard, D. M. Pharr and S. C. Huber, “Role of Sucrose Phosphate Syntase in Sucrose Biosynthesis in Ripening Bananas and its Relationship to the Respiratory Climacteric,” Plant Physiology, Vol. 94, No. 1, 1990, pp. 201-208. doi:10.1104/pp.94.1.201
[25] J. M. H. Stoop and D. M. Pharr, “Mannitol Metabolism in Celery Stressed by Excess Macronutrients,” Plant Physiology, Vol. 106, No. 2, 1994, pp. 503-511.
[26] D. Miron, M. Petreikov, N. Carmi, S. Shen, I. Levin, D. Granot, E. Zamski and A. A. Schaffer, “Sucrose Uptake, Invertase Localization and Gene Expression in Developing Fruit of Lycopersicon esculentum and the Sucrose-Accumulating Lycopersicon hirsutum,” Physiologia Plantarum, Vol. 115, No. 1, 2002, pp. 35-47. doi:10.1034/j.1399-3054.2002.1150104.x
[27] A. A. Schaffer, B. Aloni and E. Fogelman, “Sucrose Metabolism in Developing Fruit of Cucumis,” Phytochemistry, Vol. 26, No. 7, 1987, pp. 1883-1887. doi:10.1016/S0031-9422(00)81721-5
[28] G. L. Miller, “Use of Dinitrosalicylic Acid Reagent for Determination of Reducing Sugars,” Analytical Chemistry, Vol. 31, No. 3, 1959, pp. 426-428. doi:10.1021/ac60147a030
[29] M. M. Bradford, “A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Using the Principle of Dye Binding,” Analytical Biochemistry, Vol. 72, No. 1-2, 1976, pp. 143-147. doi:10.1016/0003-2697(76)90527-3
[30] A. A. Schaffer and M. Petreikov, “Sucrose to Starch Metabolism in Tomato Fruit Undergoing Transient Starch Accumulation,” Plant Physiology, Vol. 113, No. 3, 1997, pp. 739-746.
[31] N. L. Hubbard, S. C. Huber and D. M. Phar, “Sucrose Phosphate Synthase and Acid Invertase as Determinants of Sucrose Concentration in Developing Muskmelon (Cucumis melo L.) Fruits,” Plant Physiology, Vol. 91, No. 4, 1989, pp. 1527-1534. doi:10.1104/pp.91.4.1527
[32] R. Shaked, K. Rosenfeld and E. Pressman, “The Effect of Low Night Temperatures on Carbohydrate Metabolism in Developing Pollen Grains of Pepper in Relation to their Number and Functioning,” Scientia Horticulturae, Vol. 102, No. 1, 2004, pp. 29-36. doi:10.1016/j.scienta.2003.12.007
[33] N. Firon, R. Shaked, M. M. Peet, D. M. Pharr, E. Zamski, K. Rosenfeld, L. Althan and E. Pressman, “Pollen Grains of Heat Tolerant Tomato Cultivars Retain Higher Carbohydrate Concentration Under Heat Stress Conditions,” Scientia Horticulturae, Vol. 109, No. 3, 2006, pp. 212-217. doi:10.1016/j.scienta.2006.03.007
[34] M. Jain , P. V. Prasad , K. J. Boote , A. L. Hartwell Jr. and P. S. Chourey, “Effects of Season-Long High Temperature Growth Conditions on Sugar-to-Starch Metabolism in Developing Microspores of Grain Sorghum (Sorghum bicolor L. Moench),” Planta, Vol. 227, No. 1, 2007, pp. 67-79. doi:10.1007/s00425-007-0595-y
[35] F. A. Hoekstra and T. van Roekel, “Dessication Tolerance of Papaver-dubium Pollen during Its Development in the Anther—Possible Role of Phospholipid Composition and Sucrose Content,” Plant Physiology, Vo. 88, No. 3, 1988, pp. 626-632. doi:10.1104/pp.88.3.626
[36] S. A. Reznickova and H. G. Dickinson, “Ultrastructural Aspects of Storage Lipid Mobilization in the Tapetum of Lilium hybrida var. Enchantment,” Planta, Vol. 155, No. 5, 1982, pp. 400-408. doi:10.1007/BF00394468
[37] J. Hirsche, T. Engelke, D. V?ller, M. G?tz and T. Roitsch, “Interspecies Compatibility of the Anther Specific Cell Wall Invertase Promoters from Arabidopsis and Tobacco for Generating Male Sterile Plants,” Theoretical and Applied Genetics, Vol. 118, No. 2, 2009, pp. 235-245. doi:10.1007/s00122-008-0892-2
[38] T. Engelke, J. Hirsche and T. Roitsch, “Metabolically Engineered Male Sterility in Rapeseed (Brassica napus L.),” Theoretical and Applied Genetics, Vol. 122, No. 1, 2010, pp. 163-174. doi:10.1007/s00122-010-1432-4
[39] M. Goetz, D. E. Godt, A. Guivarc’h, U. Kahmann, D. Chriqui and T. Roitsch, “Induction of Male Sterility in Plants by Metabolic Engineering of the Carbohydrate Supply,” Proceedings of the National Academy of Sciences USA, Vol. 98, No. 11, 2001, pp. 6522-6527. doi:10.1073/pnas.091097998
[40] R. K. Proels, M.C. Gonzalez and T. Roitsch, “Gibberellin-Dependent Induction of Tomato Extracellular Invertase Lin7 Is Required for Pollen Development,” Functional Plant Biology, Vol. 33, No. 6, 2006, pp. 547-554. doi:10.1071/FP04146
[41] L. Karni and B. Aloni, “Fructokinase and Hexokinase from Pollen Grains of Bell Pepper (Capsicum annum L.): Possible Role in Pollen Germination under Conditions of High Temperature and CO2 Enrichment,” Annals of Botany, Vol. 90, No. 5, 2002, pp. 607-612. doi:10.1093/aob/mcf234
[42] M. Seki, T. Umezawa, K. Urano and K. Shinizaki, “Regulatory Metabolic Networks in Drought Stress Responses,” Current Opinion in Plant Biology, Vol. 10, No. 3, 2007, pp. 296-302. doi:10.1016/j.pbi.2007.04.014
[43] A. Mukaiyama, Y. Koga, K. Takano and S. Kayana, “Osmolyte Effect on the Stability and Folding of a Hyperthermophilic Protein, Proteins: Structure,” Function and Genetics, Vol. 71, No. 1, 2008, pp. 110-118. doi:10.1002/prot.21660
[44] E. Pacini, M. Guarnieri and M. Nepi, “Pollen Carbohydrates and Water Content during Development, Presentation, and Dispersal: A Short Review,” Protoplasma, Vol. 228, No. 1-3, 2006, pp. 73-77. doi:10.1007/s00709-006-0169-z
[45] A. Speranza, G. L. Calzoni and E. Pacini, “Occurrence of Mono- or Disaccharides and Polysaccharide Reserves in Mature Pollen Grains,” Sexual Plant Reproduction, Vol. 10, No. 2, 1997, pp. 110-115. doi:10.1007/s004970050076
[46] J. Buitink and O. Leprince, “Glass Formation in Plant Anhydrobiotes: Survival in the Dry State,” Cryobiology, Vol. 48, No. 3, 2004, pp. 215-228. doi:10.1016/j.cryobiol.2004.02.011
[47] J. L. Vesprini, M. Nepi, L. Cresti, M. Guarnieri and E. Pacini, “Changes in Cytoplasmic Carbohydrate Content During Helleborus Pollen Presentation,” Grana, Vol. 41, No. 1, 2002, pp. 16-20. doi:10.1080/00173130260045459

Copyright © 2023 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.