Fructan metabolism in wheat under abiotic stress conditions
Subject Areas : Genetic
1 - Faculty of Agriculture, Mohaghegh Ardabili University, Meshginshahr, Iran.
Keywords: Drought stress, Wheat, Salt stress, Cold stress, fructan metabolism,
Abstract :
Accumulation of fructan in different organs of wheat plants is important physiological factor to cope with different environmental stresses. Fructans are fructose based oligo- and polysaccharides derived from sucrose. Depend on the linkage among frucosyle residues, different types of fructan molecules could be found in the plant species. In wheat stem, levan-type (containing β-(2,1) linkage) and graminan-type fructan (containing β-(2,1) and β-(2,6) linkages) are accumulated. Three different enzymes of 1-SST, 6-SFT, and 1-FFT are believed to be involved in wheat fructan biosynthesis. Since the fructan synthesis in wheat is complex, therefore various type and amount of fructan are found among wheat cultivars. Hydrolysis of fructans are catalyzed by 1-FEH and 6-FEH preferentially degrading β-(2,1) and β-(2,6) linked fructan, respectively. Wheat cultivar with greater fructan accumulation and mobilization in the stem are resistance to terminal heat and drought stresses. Fructans increases tolerance to salt stress by cell membrane stabilization, osmotic adjustment and preservation of current photosynthesis. During cold hardening, wheat seedling accumulates water soluble carbohydrates as well as fructan in their leaves and crown
Al-Sheikh Ahmed, S., Zhang, J., Farhan, H., Zhang, Y., Yu, Z., Islam, S., Chen, J., Cricelli, S., Foreman, A., Van den Ende, W., Ma, W. and Dell, B. (2020). Diurnal changes in water soluble carbohydrate components in leaves and sucrose associated TaSUT1 gene expression during grain development in wheat. International Journal of Molecular Science. 21:8276.
Aoki, N., Scofield, G.N., Wang, X.D., Patrick, J.W., Offler, C.E. and Furbank, R.T. (2004). Expression and localisation analysis of the wheat sucrose transporter TaSUT1 in vegetative tissues. Planta. 219: 176-184.
Aoki, N., Whitfeld, P., Hoeren, F., Scofield, G., Newell, K., Patrick, J., Offler, C., Clarke, B., Rahman, S. and Furbank, R.T. (2002). Three sucrose transporter genes are expressed in the developing grain of hexaploid wheat. Plant Molecular Biology. 50: 453–462.
Bagherikia, S., Pahlevani, M., Yamchi, A., Zaynalinezhad, K. and Mostafaie, A. (2019). Transcript profiling of genes encoding fructan and sucrose metabolism in wheat under terminal drought stress. Journal of Plant Growth Regulation. 38: 148-163.
Bancal, P. and Triboi, E. (1993). Temperature effect on fructan oligomer contents and fructan-related enzyme activities in stems of wheat (Triticum aestivum L.) during grain filling. New Phytologist. 123: 247-253.
Blum, A. (1998). Improving wheat grain filling under stress by stem reserve mobilization. Euphytica. 100: 77-83.
Chatterton, N.J. and Harrison, P.A. (1997). Fructan oligomers in Poa ampla. New Phytologist. 136: 3-10.
Goggin, D.E. and Setter, L. (2004). Fructosyl transferase activity and fructan accumulation during development in wheat exposed to terminal drought. Functional Plant Biology. 31: 11–21.
Hassaneian Khoshro, H., Taleei, A., Bihamta, M.R., Shahbazi, M., Abbasi, A. and Ramezanpour, S.S. (2014). Expression analysis of the genes involved in accumulation and remobilization of assimilates in wheat stem under terminal drought stress. Plant Growth Regulation. 74:165-176.
Hou, J., Huang, X., Sun, W., Du, C., Wang, C., Xie, Y., Ma, Y. and Ma, D. (2018). Accumulation of water-soluble carbohydrates and gene expression in what stems correlates with drought resistance. Journal of Plant Physiology. 231: 182-191.
Joudi, M., Ahmadi, A., Mohamadi, V., Abbasi, A., Vergauwen, R., Mohamadi, H. and Van den Ende W. (2012). Comparison of fructan dynamics in two wheat cultivars with different capacities of accumulation and remobilization under drought stress. Physiologia Plantarum. 144: 1-12.
Joudi, M. and Van den Ende, W. (2018). Genotypic variation in pre- and post-anthesis dry matter remobilization in Iranian wheat cultivars: Associations with stem characters and grain yield. Czech Journal of Genetic and Plant Breeding. 54, (3): 123–134.
Kawakami, A. and Yoshida, M. (2002). Molecular characterization of sucrose:sucrose 1-fructosyltransferase and sucrose:fructan 6-fructosyltransferase associated with fructan cccumulation in winter wheat during cold hardening. Bioscience, Biotechnology and Biochemistry. 66 (11): 2297-2305.
Kawakami, A. and Yoshida, M. (2012). Geraminan breakdown by fructan exohydrolase induced in winter wheat inoculated with snow mold. Journal of Plant Physiology. 169: 294-302.
Kawakami, A., Yoshida, M. and Van den Ende, W. (2005). Molecular cloning and functional analysis of a novel 6&1–FEH from wheat (Triticum aestivum L.) preferentially degrading small branched graminans like bifurcose. Gene. 358: 93–101.
Kerepesi, I. and Galiba, G. (2000). Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlings. Crop Science. 40: 482-487.
Liu, Y., Zhang, P., Li, M., Chang, L., Cheng, H. and Chai, S. (2020). Dynamic responses of accumulation and remobilization of water soluble carbohydrates in wheat stem to drought stress. Plant Physiology and Biochemistry. 155: 262-270.
Livingston, D.P. and Henson, C.A. (1998). Apoplastic sugars, fructan, fructan exohydrolase and invertase in winter oat: responses to second-phase cold hardening. Plant Physiology. 116: 403-408.
Livingston, D.P., Chatterton, N.J. and Harrison P.A. (1993). Structure and quantity of fructan oligomers in oat (Avena spp.). New Phytologist. 123: 725-734.
Livingston, D.P., Hincha, D.K. and Heyer, A. (2009). Fructan and its relationship to abiotic stress tolerance in plants. Cellular and Molecular Life Sciences. 66: 2007-2023.
Munns, R. and Tester M. (2008). Mechanisms of salinity tolerance. Annual Review of Plant Biology. 59:651-681.
Peshev, D., Vergauwen, R., Moglia, A., Hideg, E. and Van den Ende, W. (2013). Towards understanding vacuolar antioxidant mechanisms: a role for fructans? Journal of Experimental Botany. 64: 1025-1038.
Ritsema, T. and Smeekens, S. (2003). Fructans: beneficial for plants and humans. Current Opinion in Plant Biology. 6: 223-230.
Sharbatkhari, M., Shobbar, Z., Galeshi, S. and Nakhoda, B. (2016). Wheat stem reserves and salinity tolerance: molecular dissection of fructan biosynthesis and remobilization to grains. Planta. 244: 191-202.
Sharbatkhari, M., Shobbar, Z.S., Galeshi, S. and Nakhoda, B. (2016). Wheat stem reserves and salinity tolerance: molecular dissection of fructan biosynthesis and remobilization to grains. Planta. 244:191-202.
Simmen, U., Obenland, D., Boller, T. and Wiemken, A. (1993). Fructan synthesis in excised barley leaves. Identification of two sucrose: sucrose fructosyltransferases induced by light and their separation from constitutive invertase. Plant Physiology. 101: 459–468.
Tognetti, J.A., Salerno, G.L., Crespi, M.D. and Pontis, H.G. (1990). Sucrose and fructan metabolism of different wheat cultivars at chilling temperatures. Physiologia Plantarum. 78: 554-559.
Valluru, R. and Van den Ende, W. (2008). Plant fructans in stress environments: emerging concepts and future prospects. Journal of Experimental Botany. 59: 2905-2916.
Van den Ende, W. and Vallurum R. (2009). Sucrose, sucrosyl oligosaccharides and oxidative stress: scavenging and salvaging? Journal of Experimental Botany. 60: 9–18.
Van den Ende, W., Clerens, S., Vergauwen, R., Van Riet, L., Van Laere, A., Yoshida, M. and Kawakami, A. (2003). Fructan 1–exohydrolases. ß–(2,1)–trimmers during graminan biosynthesis in stems of wheat? Purification, characterization, mass mapping, and cloning of two fructan 1–exohydrolase isoforms. Plant Physiology. 131: 621–631.
Van den Ende, W., Coninck, B.D. and Van Laere, A. (2004). Plant fructan exohydrolase: a role in signaling and defense? Trends in Plant Science. 9(11): 523- 528.
Van Laere, A. and Van den Ende, W. (2002). Inulin metabolism in dicots: chicory as a model system. Plant, Cell and Environment. 25: 803-815.
Van Riet, L., Nagaraj, V., Van den Ende, W., Clerens, S., Wiemken, A. and Van Laere A. (2006). Purification, cloning and functional characterization of fructan 6–exohydrolase from wheat (Triticum aestivum L.). Journal of Experimental Botany. 57: 213–223.
Veenstra, L.D., Jannink, J.L. and Sorrells, M.E. (2017). Wheat fructan: A potential breeding target for nutritionally improved, climate-resilient varieties. Crop Science. 57: 1-17.
Vijn, I. and Smeekens, S. (1999). Fructan: More than a reserve carbohydrate? Plant Physiology. 120: 351-359.
Wang, N. and Fisher, D.B. (1994). Monitoring phloem unloading and post-phloem transport by microperfusion of attached wheat grains. Plant Physiology. 104: 7-16.
Wang, X., Cai, J., Liu, F., Jin, M., Yu H., Jiang, D., Wollenweber, B., Dai, T. and Cao, W. (2012). Pre-anthesis high temperature acclimation alleviates the negative effects of postanthesis heat stress on stem stored carbohydrates remobilization and grain starch accumulation in wheat. Journal of Cereal Science. 55: 331-336.
Yanez, A., Tapia, G., Guerra, F. and Del Pozo, A. (2017). Stem carbohydrates dynamics and expression of genes involved in fructan accumulation and remobilization during grain growth in wheat (Triticum aestivum L.) genotypes with contrasting tolerance to water stress. Plos One. 12(5): e0177667.
Yang, J., Zhang, J., Wang, Z., Zhu, Q. and Liu, L. (2004). Activities of fructan- and sucrose-metabolizing enzymes in wheat stems subjected to water stress during grain filling. Planta. 220: 331–343.
Yoshida, M. and Tamura, K. I. (2011). Sucrose and fructan metabolism of different wheat cultivars at chilling temperatures. Japan Agricultural Research Quartery. 45(1): 9-14.
Yoshida, M., Kawakami, A. and Van den Ende, W. (2007). Graminan metabolism in cereals: Wheat as a model system. In: Norio S., B. Noureddine, and O. Shuichi. eds. Recent advances in fructo-oligoaccharides research. Kerala, India: Research Signpost. 201–212.
Zhang, J., Chen, W., Dell, B., Vergauwen, R., Zhang, X., Mayer, J.E. and Van den Ende, W. (2015a). Wheat genotypic variation in dynamic fluxes of WSC components in different stem segments under drought during grain filling. Frontiers in Plant Science. 00624.
Zhang, J., Dell, B., Conocono, E., Waters, I., Setter, T. and Appels, R. (2009). Water deficits in wheat: fructan exohydrolase (1–FEH) mRNA expression and relationship to soluble carbohydrate concentrations in two varieties. New Phytologist. 181: 843–850.
Zhang, J., Xu, Y., Chen, W., Dell, B., Vergauwen, R., Biddulph, B., Khan, N., Luo, H. Appels, R. and Van den Ende, W. (2015b). A wheat 1-FEH w3 variant underlies enzyme activity for stem WSC remobilization to grain under drought. New Phytologist. 205: 293–305.
Zhang, P., Liu, Y., Li, M., Ma, J., Wang, C., Su, J. and Yang, D. (2020). Abscisic acid associated with key enzymes and gene involving in dynamic flux of water soluble carbohydrates in
wheat peduncle under terminal drought stress. Plant Physiology and Biochemistry. 151: 719-728.
Al-Sheikh Ahmed, S., Zhang, J., Farhan, H., Zhang, Y., Yu, Z., Islam, S., Chen, J., Cricelli, S., Foreman, A., Van den Ende, W., Ma, W. and Dell, B. (2020). Diurnal changes in water soluble carbohydrate components in leaves and sucrose associated TaSUT1 gene expression during grain development in wheat. International Journal of Molecular Science. 21:8276.
Aoki, N., Scofield, G.N., Wang, X.D., Patrick, J.W., Offler, C.E. and Furbank, R.T. (2004). Expression and localisation analysis of the wheat sucrose transporter TaSUT1 in vegetative tissues. Planta. 219: 176-184.
Aoki, N., Whitfeld, P., Hoeren, F., Scofield, G., Newell, K., Patrick, J., Offler, C., Clarke, B., Rahman, S. and Furbank, R.T. (2002). Three sucrose transporter genes are expressed in the developing grain of hexaploid wheat. Plant Molecular Biology. 50: 453–462.
Bagherikia, S., Pahlevani, M., Yamchi, A., Zaynalinezhad, K. and Mostafaie, A. (2019). Transcript profiling of genes encoding fructan and sucrose metabolism in wheat under terminal drought stress. Journal of Plant Growth Regulation. 38: 148-163.
Bancal, P. and Triboi, E. (1993). Temperature effect on fructan oligomer contents and fructan-related enzyme activities in stems of wheat (Triticum aestivum L.) during grain filling. New Phytologist. 123: 247-253.
Blum, A. (1998). Improving wheat grain filling under stress by stem reserve mobilization. Euphytica. 100: 77-83.
Chatterton, N.J. and Harrison, P.A. (1997). Fructan oligomers in Poa ampla. New Phytologist. 136: 3-10.
Goggin, D.E. and Setter, L. (2004). Fructosyl transferase activity and fructan accumulation during development in wheat exposed to terminal drought. Functional Plant Biology. 31: 11–21.
Hassaneian Khoshro, H., Taleei, A., Bihamta, M.R., Shahbazi, M., Abbasi, A. and Ramezanpour, S.S. (2014). Expression analysis of the genes involved in accumulation and remobilization of assimilates in wheat stem under terminal drought stress. Plant Growth Regulation. 74:165-176.
Hou, J., Huang, X., Sun, W., Du, C., Wang, C., Xie, Y., Ma, Y. and Ma, D. (2018). Accumulation of water-soluble carbohydrates and gene expression in what stems correlates with drought resistance. Journal of Plant Physiology. 231: 182-191.
Joudi, M., Ahmadi, A., Mohamadi, V., Abbasi, A., Vergauwen, R., Mohamadi, H. and Van den Ende W. (2012). Comparison of fructan dynamics in two wheat cultivars with different capacities of accumulation and remobilization under drought stress. Physiologia Plantarum. 144: 1-12.
Joudi, M. and Van den Ende, W. (2018). Genotypic variation in pre- and post-anthesis dry matter remobilization in Iranian wheat cultivars: Associations with stem characters and grain yield. Czech Journal of Genetic and Plant Breeding. 54, (3): 123–134.
Kawakami, A. and Yoshida, M. (2002). Molecular characterization of sucrose:sucrose 1-fructosyltransferase and sucrose:fructan 6-fructosyltransferase associated with fructan cccumulation in winter wheat during cold hardening. Bioscience, Biotechnology and Biochemistry. 66 (11): 2297-2305.
Kawakami, A. and Yoshida, M. (2012). Geraminan breakdown by fructan exohydrolase induced in winter wheat inoculated with snow mold. Journal of Plant Physiology. 169: 294-302.
Kawakami, A., Yoshida, M. and Van den Ende, W. (2005). Molecular cloning and functional analysis of a novel 6&1–FEH from wheat (Triticum aestivum L.) preferentially degrading small branched graminans like bifurcose. Gene. 358: 93–101.
Kerepesi, I. and Galiba, G. (2000). Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlings. Crop Science. 40: 482-487.
Liu, Y., Zhang, P., Li, M., Chang, L., Cheng, H. and Chai, S. (2020). Dynamic responses of accumulation and remobilization of water soluble carbohydrates in wheat stem to drought stress. Plant Physiology and Biochemistry. 155: 262-270.
Livingston, D.P. and Henson, C.A. (1998). Apoplastic sugars, fructan, fructan exohydrolase and invertase in winter oat: responses to second-phase cold hardening. Plant Physiology. 116: 403-408.
Livingston, D.P., Chatterton, N.J. and Harrison P.A. (1993). Structure and quantity of fructan oligomers in oat (Avena spp.). New Phytologist. 123: 725-734.
Livingston, D.P., Hincha, D.K. and Heyer, A. (2009). Fructan and its relationship to abiotic stress tolerance in plants. Cellular and Molecular Life Sciences. 66: 2007-2023.
Munns, R. and Tester M. (2008). Mechanisms of salinity tolerance. Annual Review of Plant Biology. 59:651-681.
Peshev, D., Vergauwen, R., Moglia, A., Hideg, E. and Van den Ende, W. (2013). Towards understanding vacuolar antioxidant mechanisms: a role for fructans? Journal of Experimental Botany. 64: 1025-1038.
Ritsema, T. and Smeekens, S. (2003). Fructans: beneficial for plants and humans. Current Opinion in Plant Biology. 6: 223-230.
Sharbatkhari, M., Shobbar, Z., Galeshi, S. and Nakhoda, B. (2016). Wheat stem reserves and salinity tolerance: molecular dissection of fructan biosynthesis and remobilization to grains. Planta. 244: 191-202.
Sharbatkhari, M., Shobbar, Z.S., Galeshi, S. and Nakhoda, B. (2016). Wheat stem reserves and salinity tolerance: molecular dissection of fructan biosynthesis and remobilization to grains. Planta. 244:191-202.
Simmen, U., Obenland, D., Boller, T. and Wiemken, A. (1993). Fructan synthesis in excised barley leaves. Identification of two sucrose: sucrose fructosyltransferases induced by light and their separation from constitutive invertase. Plant Physiology. 101: 459–468.
Tognetti, J.A., Salerno, G.L., Crespi, M.D. and Pontis, H.G. (1990). Sucrose and fructan metabolism of different wheat cultivars at chilling temperatures. Physiologia Plantarum. 78: 554-559.
Valluru, R. and Van den Ende, W. (2008). Plant fructans in stress environments: emerging concepts and future prospects. Journal of Experimental Botany. 59: 2905-2916.
Van den Ende, W. and Vallurum R. (2009). Sucrose, sucrosyl oligosaccharides and oxidative stress: scavenging and salvaging? Journal of Experimental Botany. 60: 9–18.
Van den Ende, W., Clerens, S., Vergauwen, R., Van Riet, L., Van Laere, A., Yoshida, M. and Kawakami, A. (2003). Fructan 1–exohydrolases. ß–(2,1)–trimmers during graminan biosynthesis in stems of wheat? Purification, characterization, mass mapping, and cloning of two fructan 1–exohydrolase isoforms. Plant Physiology. 131: 621–631.
Van den Ende, W., Coninck, B.D. and Van Laere, A. (2004). Plant fructan exohydrolase: a role in signaling and defense? Trends in Plant Science. 9(11): 523- 528.
Van Laere, A. and Van den Ende, W. (2002). Inulin metabolism in dicots: chicory as a model system. Plant, Cell and Environment. 25: 803-815.
Van Riet, L., Nagaraj, V., Van den Ende, W., Clerens, S., Wiemken, A. and Van Laere A. (2006). Purification, cloning and functional characterization of fructan 6–exohydrolase from wheat (Triticum aestivum L.). Journal of Experimental Botany. 57: 213–223.
Veenstra, L.D., Jannink, J.L. and Sorrells, M.E. (2017). Wheat fructan: A potential breeding target for nutritionally improved, climate-resilient varieties. Crop Science. 57: 1-17.
Vijn, I. and Smeekens, S. (1999). Fructan: More than a reserve carbohydrate? Plant Physiology. 120: 351-359.
Wang, N. and Fisher, D.B. (1994). Monitoring phloem unloading and post-phloem transport by microperfusion of attached wheat grains. Plant Physiology. 104: 7-16.
Wang, X., Cai, J., Liu, F., Jin, M., Yu H., Jiang, D., Wollenweber, B., Dai, T. and Cao, W. (2012). Pre-anthesis high temperature acclimation alleviates the negative effects of postanthesis heat stress on stem stored carbohydrates remobilization and grain starch accumulation in wheat. Journal of Cereal Science. 55: 331-336.
Yanez, A., Tapia, G., Guerra, F. and Del Pozo, A. (2017). Stem carbohydrates dynamics and expression of genes involved in fructan accumulation and remobilization during grain growth in wheat (Triticum aestivum L.) genotypes with contrasting tolerance to water stress. Plos One. 12(5): e0177667.
Yang, J., Zhang, J., Wang, Z., Zhu, Q. and Liu, L. (2004). Activities of fructan- and sucrose-metabolizing enzymes in wheat stems subjected to water stress during grain filling. Planta. 220: 331–343.
Yoshida, M. and Tamura, K. I. (2011). Sucrose and fructan metabolism of different wheat cultivars at chilling temperatures. Japan Agricultural Research Quartery. 45(1): 9-14.
Yoshida, M., Kawakami, A. and Van den Ende, W. (2007). Graminan metabolism in cereals: Wheat as a model system. In: Norio S., B. Noureddine, and O. Shuichi. eds. Recent advances in fructo-oligoaccharides research. Kerala, India: Research Signpost. 201–212.
Zhang, J., Chen, W., Dell, B., Vergauwen, R., Zhang, X., Mayer, J.E. and Van den Ende, W. (2015a). Wheat genotypic variation in dynamic fluxes of WSC components in different stem segments under drought during grain filling. Frontiers in Plant Science. 00624.
Zhang, J., Dell, B., Conocono, E., Waters, I., Setter, T. and Appels, R. (2009). Water deficits in wheat: fructan exohydrolase (1–FEH) mRNA expression and relationship to soluble carbohydrate concentrations in two varieties. New Phytologist. 181: 843–850.
Zhang, J., Xu, Y., Chen, W., Dell, B., Vergauwen, R., Biddulph, B., Khan, N., Luo, H. Appels, R. and Van den Ende, W. (2015b). A wheat 1-FEH w3 variant underlies enzyme activity for stem WSC remobilization to grain under drought. New Phytologist. 205: 293–305.
Zhang, P., Liu, Y., Li, M., Ma, J., Wang, C., Su, J. and Yang, D. (2020). Abscisic acid associated with key enzymes and gene involving in dynamic flux of water soluble carbohydrates in
wheat peduncle under terminal drought stress. Plant Physiology and Biochemistry. 151: 719-728.