Hsp90 and reactive oxygen species regulate thermotolerance of rice seedlings via induction of heat shock factor A2 (OsHSFA2) and galactinol synthase 1 (OsGolS1)

Nong Thi Hue, Huong Thi Tran, Thuy Phan, Junya Nakamura, Tomoe Iwata, Keisuke Harano, Yushi Ishibashi, Takashi Yuasa, Mari Iwaya-Inoue

Department of Bioresource Sciences, Faculty of Agriculture, Kyushu University, Fukuoka, Japan..
Graduate School of Bioresource and Bioenvironmental Sciences, Kyushu University, Fukuoka, Japan.
Graduate School of Bioresource and Bioenvironmental Sciences, Kyushu University, Fukuoka, Japan..
School of Agriculture, Kyushu University, Fukuoka, Japan..

DOI: 10.4236/as.2013.43023                

Abstract

Heat stress induces expression of a set of thermotolerance-related genes in plants. We focused on rice (Oryza sativa L.) homologs of the gene family that encodes galactinol synthase (OsGolS), which is closely related to the Arabidopsis thaliana galactinol synthase (AtGolS) family whose expression is induced under various stresses. OsGolS1 was highly up-regulated compare to the level of OsGolS2 in re- sponse to heat stress. Interestingly, OsGolS1 was also up-regulated by treatment with the Hsp90 inhibitor, geldanamycin (GDA). Expression profiles of OsGolS1 were correlated to those of OsHsfA2 under the GDA treatments. Treatment with GDA increased expression of OsHsfA2, but marginally increased or did not change OsHsfA1 expression. Notably, gel shift assay indicated that OsHsfA2 binds directly to OsGolS1 promoter region and that OsHsfA1 also binds to the promoter regions of OsHsfA2. Both OsHsfA2 and OsGolS1 were dramatically induced in response to heat stress. Accordingly, galactinol and raffinose contents in rice seedlings increased significantly following the induction of OsGolS1. Pre-treatment of rice seedlings with raffinose or GDA improved their thermotolerance. These results suggest that OsGolS1 plays an important role in response to heat stress, possibly via the transcription cascade of OsHsfA1-OsHsfA2 that leads to galactinol and raffinose accumulation, and that the increased content of these carbohydrates is a

key response factor for rice seedlings to enhance thermotolerance.

Keywords

Galactinol Synthase; Geldanamycin; Heat Shock Factor; Heat Shock Protein; Oryza sativa

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	Baniwal, S.K., Bharti, K., Chan, K.Y., Fauth, K., Ganguli, A., Kotak, S., Mishra, S.K., Nover, L., Port, M., Scharf, A.D., Tripp, J., Weber, C., Zielinsky, D. and von Koskull-Doring, P. (2004) Heat stress response in plants: A complex game with chaperones and more than twenty heat stress transcription factors. Journal of Biosciences, 29, 471-487. doi:10.1007/BF02712120
[2]	Lee, B., Won, S. and Lee, H. (2000) Expression of chloroplast-localized small heat shock protein by oxidative stress in rice. Gene, 245, 283-290. doi:10.1016/S0378-1119(00)00043-3
[3]	Maestri, E., Klueva, N. and Perrotta, C. (2002) Molecular of heat shock proteins in cereals. Plant Molecular Biology, 48, 667-681. doi:10.1023/A:1014826730024
[4]	McLellan, C. and Turbyville, T. (2007) A rhizosphere fungus enhances Arabidopsis thermotolerance through production of an Hsp90 inhibitor. Plant Physiology, 145, 174-182. doi:10.1104/pp.107
[5]	Nishizawa, A., Yabuta, Y. and Shigeoka, S. (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiology, 147, 1251-1263. doi:10.1104/pp.108
[6]	Liu, J.-J., Krenz, D.C., Galvez, A.F. and de Lumen, B.D. (1998) Galactinol synthase (GS): Increased enzyme activity and levels of mRNA due to cold and desication. Plant Science, 134, 11-20. doi:10.1016/S0168-9452(98)00042-9
[7]	Saravitz, D.M., Pharr, D.M. and Carter, T.E. (1987) Galactinol synthase activity and soluble sugars in developing seeds of four soybean genotypes. Plant Physiology, 83, 185-189. doi:10.1104/pp.83.1.185
[8]	Nishizawa, A., Yabuta, Y. and Yoshida, E. (2006) Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant Journal, 48, 535-547. doi:10.1111/j.1365-313X.2006.02889.x
[9]	Nishizawa, A., Tainaka, H., Yoshida, E., Tamoi, M., Yabuta, Y. and Shigeoka, S. (2010) The 26S proteasome function and Hsp90 activity involved in the regulation of HsfA2 expression in response to oxidative stress. Plant and Cell Physiology, 51, 486-496. doi:10.1093/pcp/pcq015
[10]	Panikulangara, T.J., Eggers-Schumacher, G. and Wunderlich, M. (2004) Galactinol synthase 1. A novel heat shock factor target gene responsible for heat-induced synthesis of raffinose family oligosaccharides in Arabidopsis. Plant Physiology, 136, 3148-3158. doi:10.1104/pp.104
[11]	Phan, T., Ishibashi, Y., Yuasa, T. and Iwaya-Inoue, M. (2010) Chilling stress induces galactinol synthase (OsGolS1) in rice seedlings. Cryobiology and Cryotechnology, 56, 139- 146.
[12]	Yuasa, T., Ishibashi, Y. and Iwaya-Inoue, M. (2012) A flower specific calcineurin B-like molecule (CBL)-interacting protein kinase (CIPK) homolog in yomato cultivar Micro-Tom (Solanum lycopersicum L.). American Journal of Plant Sciences, 3, 753-763. doi:10.4236/ajps.2012.36091
[13]	Nakamura, J., Yuasa, T., Huong, T.T., Harano, K., Tanaka, S., Iwata, T., Phan, T. and Iwaya-Inoue, M. (2011) Rice homologs of inducer of CBF expression (OsICE) are involved in cold acclimation. Plant Biotechnology, 28, 303-309. doi:10.5511/plantbiotechnology.11.0421a
[14]	Storozhenko, S., Pauw, P.D., Motagu, M.V., Inze, D. and Kushnir, S. (1998) The heat-shock element is a functional component of the Arabidopsis APX1 gene promoter. Plant Physiology, 118, 1005-1014. doi:10.1104/pp.118.3.1005
[15]	Liu, A.L., Zou, J., Zhang, X.W., Wang, W.F., Xiong, X.Y., Chen, L.Y. and Chen, X.B. (2010) Expression profiles of class A rice heat shock transcription factor genes under abiotic stresses. Journal of Plant Biology, 53, 142-149. doi:10.1007/s12374-010-9099-6
[16]	Veljovic-Jovanovic, S., Noctor, G. and Foyer, C.H. (2002) Are leaf hydrogen peroxide concentrations commonly overestimated? The potential influence of artefactual interference by tissue phenolics and ascorbate. Plant Physiology and Biochemistry, 40, 501-507. doi:10.1016/S0981-9428(02)01417-1
[17]	Ishibashi, Y., Yamaguchi, H., Yuasa, T., Iwaya-Inoue, M., Arima, S. and Zheng, S.H. (2011) Hydrogen peroxide spraying alleviates drought stress in soybean plants. Journal of Plant Physiology, 168, 1562-1567. doi:10.1016/j.jplph.2011.02.003
[18]	Yamada, K., Uchida, A., Fukao, Y., Hayashi, M., Fukazawa, M., Suzuki, I. and Nishimura, M. (2007) Cytosolic HSP90 regulates the heat shock response that is responsible for heat acclimation in Arabidopsis thaliana. Journal of Biological Chemistry, 282, 37794-37804. doi:10.1074/jbc.M707168200
[19]	Schoffl, F., Prandl, R. and Reindl, A. (1998) Regulation of the heat-shock response. Plant Physiology, 117, 1135-1141. doi:10.1104/pp.117.4.1135
[20]	Asada, K. (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiology, 141, 391-396. doi:10.1104/pp.106.082040
[21]	Kotak, S., Larkindale, J., Lee, U., von Koskull-Doring, P., Vierling, E. and Scharf, K.D. (2007) Complexity of the heat stress responses in plants. Current Opinion in Plant Biology, 10, 310-316. doi:10.1016/j.pbi.2007.04.011
[22]	Mittal, D., Chakrabarti, S., Sarkara, A., Singh, A. and Grover, A. (2009) Heat shock factor gene family in rice: Genomic organization and transcript expression profiling in response to high temperature, low temperature and oxidative stresses. Plant Physiology and Biochemistry, 47, 785-795. doi:10.1016/j.plaphy.2009.05.003
[23]	Nishizawa, A., Yoshida, E., Yabuta, Y. and Shigeoka, S. (2009) Analysis of the regulation of target gene by and Arabidopsis heat shock transcription factor, HsfA2. Bioscience, Biothechnology, and Biochemistry, 73, 890-895. doi:10.1271/bbb.80809
[24]	Nishizawa-Yokoi, A., Nosaka, R., Hayashi, H., Tainaka, H., Maruta, T., Tamoi, M., Ikeda, M., Ohme-Takagi, M., Yoshimura, K., Yabuta, Y. and Shigeoka, S. (2011) Hsf-A1d and HsfA1e involved in the transcriptional regulation of HsfA2 function as key regulators for the Hsf signaling network in response to environmental stress. Plant and Cell Physiology, 52, 933-945. doi:10.1093/pcp/pcr045
[25]	Van den Ende, W. and Valluru, R. (2009) Sucrose, sucrosyl oligosaccharides, and oxidative stress: Scavenging and salvaging? Journal of Experimental Botany, 60, 9-18. doi:10.1093/jxb/ern297
[26]	Boonyaritthongchai, P., Manuwong, S., Kanlayanarat, S., Nakamura, Y., Okamoto, S. and Matsuo, T. (2008) Acceleration of senescence by high temperature treatment in Lycoris (L. traubii × L. sanguinea) leaf sections. Journal of the Japanese Society for Horticulture Science, 77, 431-439. doi:10.2503/jjshs1.77.431
[27]	Taji, T., Ohsumi, C., Iuchi, S., Seki, M., Kasuga, M., Kobayashi, M., Yamaguchi-Shinozaki, K. and Shinozaki, K. (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant Journal, 29, 417-426. doi:10.1046/j.0960-7412.2001.01227.x
[28]	Yokotani, N., Ichikawa, T., Kondou, Y., Matsui, M., Hirochika, H., Iwabuchi, M. and Oda, K. (2008) Expression of rice heat stress transcription factor OsHsfA2e enhances tolerance to environmental stresses in transgenic Arabidopsis. Planta, 227, 957-967. doi:10.1007/s00425-007-0670-4