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Over-expression of OsHsfA7 enhanced salt and drought tolerance in transgenic rice

  • Liu, Ai-Ling (Key Laboratory for Crop Germplasm Innovation and Utilization of Hunan Province, Hunan Agricultural University) ;
  • Zou, Jie (College of Bioscience and Biotechnology, Hunan Agricultural University) ;
  • Liu, Cui-Fang (College of Bioscience and Biotechnology, Hunan Agricultural University) ;
  • Zhou, Xiao-Yun (Key Laboratory for Crop Germplasm Innovation and Utilization of Hunan Province, Hunan Agricultural University) ;
  • Zhang, Xian-Wen (Key Laboratory for Crop Germplasm Innovation and Utilization of Hunan Province, Hunan Agricultural University) ;
  • Luo, Guang-Yu (College of Bioscience and Biotechnology, Hunan Agricultural University) ;
  • Chen, Xin-Bo (Key Laboratory for Crop Germplasm Innovation and Utilization of Hunan Province, Hunan Agricultural University)
  • Received : 2012.04.25
  • Accepted : 2012.08.15
  • Published : 2013.01.31

Abstract

Heat shock proteins play an important role in plant stress tolerance and are mainly regulated by heat shock transcription factors (Hsfs). In this study, we generated transgenic rice over-expressing OsHsfA7 and carried out morphological observation and stress tolerance assays. Transgenic plants exhibited less, shorter lateral roots and root hair. Under salt treatment, over-expressing OsHsfA7 rice showed alleviative appearance of damage symptoms and higher survival rate, leaf electrical conductivity and malondialdehyde content of transgenic plants were lower than those of wild type plants. Meanwhile, transgenic rice seedlings restored normal growth but wild type plants could not be rescued after drought and re-watering treatment. These findings indicate that over-expression of OsHsfA7 gene can increase tolerance to salt and drought stresses in rice seedlings.

INTRODUCTION

As sessile organism, plants have evolved a variety of mechanisms to rapidly respond to extreme environmental conditions by synthesizing increased amounts or new isoforms of diverse functional proteins. Among these proteins, heat shock proteins (Hsps, also known as heat stress proteins) are a group of proteins that function as molecular chaperones in regulating cellular homeostasis and promoting survival under stressful conditions (1,2). The induction of Hsps under stresses is primarily regulated by the heat shock transcription factors (Hsfs) that act by binding to the highly conserved heat shock element in the promoters of target genes (3). In many species, Hsfs are the terminal components of signal transduction chain mediating the activation of genes responsive to heat stress and a large number of chemical stressors (4-6).

Hsfs display a modular structure with an N-terminal DNA-binding domain characterized by a helix-turn-helix motif, an adjacent bipartite oligomerization domain composed of hydrophobic heptad repeats, a cluster of basic amino acid residues essential for nuclear import (the nuclear localization signal, or NLS) and a C-terminal activation domain (AHA motifs) (7,8). In plants, the Hsf system is more complex than in any other organisms investigated so far. Based on sequence homology and domain architecture, plant Hsfs have been divided into three conserved classes, A, B and C (8). The rice genome contains thirteen class A, eight class B and four class C Hsfs. Furthermore, AHA motifs are crucial for the activity of class A Hsfs which have been reported to play a central role in the induction of various genes involved in defense under stressful conditions (9).

Many researches suggested that HsfAs not only responded to high temperature but also to oxidative stress, high salinity, chilling and other stresses. Over-expression of HsfA1 genes enhanced thermotolerance in Arabidopsis, soybean and tomato (10-12). The transgenic Arabidopsis over-expressing OsHsfA2e exhibited tolerance to high salinity stress (13). Over-expression of AtHsfA1b improved resistance to chilling in transgenic tomato (14). It was reported that over-expression of HsfA2 conferred increased tolerance to high light, salt, oxidative, osmotic and anoxia stresses (15-18). Shim et al. (19) demonstrated that transgenic rice and wheat over-expressing HsfA4a enhanced Cd tolerance.

Rice is one of the most important crops in the world. The growth and productivity of rice are often threatened by environmental factors. In the last decade, many efforts have been undertaken to generate stress tolerant rice by manipulating the expression of stress-responsive genes (13,14,20-22). We previously demonstrated that the expression of rice OsHsfA7 gene can be induced by heat shock treatment and other abiotic stresses (23). In this study, we generated 35S::OsHsfA7 transgenic rice plants which exhibited different phenotype and higher survival rate under abiotic stresses compared with WT. Our results suggest that transgenic rice over-expressing HsfA7 can increase resistance to high salinity and drought stresses.

 

RESULTS

Bioinformatics analysis of OsHsfA7

The cDNA of OsHsfA7 with accession number AK064271 is composed of 1,209 bp, coding for a protein of 402 aa with a predicted molecular mass of 43.9 kDa (pI 7.05). Putative HsfA7 proteins were retrieved through a BLASTP search using rice OsHsfA7 (LOC_Os01g39020) as the query. Their putative protein sequences were aligned using the DNAMAN program. OsHsfA7 shares 31.7% and 62.3% identity at the amino acid level with HsfA7 of Medicago and Sorghum. Phylogenetic analysis revealed that genetic relationship between Oryza sativa and Sorghum was closer (Fig. S1).

Root morphology in OsHsfA7-OE transgenic rice

Eight independent T0 rice transgenic lines were obtained after selection on hygromycin media and analyzed by RT-PCR. All the subsequent T1 and T2 lines showed conformed over-expression and similar root morphology and stress responses. The two highly over-expressed T2 lines (OE-1 and OE-8) were used as representative for later characterization. Root morphology of the WT and OsHsfA7-OE transgenic plant seedlings was shown in Fig. 1. OsHsfA7-OE plants exhibited longer young roots (including primary root and adventitious root) (Fig. 1A) but shorter and less lateral roots (Fig. 1B) and root hair (Fig. 1C) compared with the WT. Average radicle length of 5 d OsHsfA7-OE seedling was 3.7 cm, and that of WT was only 1.5 cm (Fig. S2A), the results showed that the young roots of transgenic seedlings grew faster than the control. Moreover, the roots of OsHsfA7-OE at tillering stage were thicker, sparser, more wide distributed and almost no lateral roots compared with that of wild type.

Fig. 1.Root morphology of wild-type and OsHsfA7-OE transgenic plants. (A, B) Primary root, adventitious root and lateral root in wild type and T2 transformants. Plants were grown in MS medium and photographed at 5 d (A) and 15 d (B). (C) Root hair of 7 d rice seedlings was observed by stereoscope.

Fig. 2.Influence of high salt stress on rice seedlings. (A) Seedlings before treatment. Three-week-old OsHsfA7 transgenic plants and WT control plants were grown in soil in a tray. (B) Seedlings were subjected to 200 mM NaCl for 10 d. (C, D) Hydroponic seedling treatment. WT and OsHsfA7-OE grown in 1/2 MS liquid medium for 2 weeks were treated by 200 mM NaCl for 24 h, they were photographed after recovery for 4 d (C) and 10 d (D). (E, F) Assay of REC and MDA content. Three-week-old seedlings were treated with 200 mM NaCl for 10 d. The data are the means ± SD of three independent experiments. The values with significant differences according to t-tests are indicated by asterisks (*P < 0.05; **P < 0.01).

Enhanced salt and drought tolerance by over-expression of OsHsfA7

After irrigating with 200 mM NaCl for 10 d, leaf apex of WT plants became brown and dried, whereas over-expressing OsHsfA7 leaves remained green (Fig. 2B). Meanwhile, leaf REC and MDA content were lower in the transgenic lines than in the WT (Fig. 2E, F). In addition, hydroponic seedlings were treated with 200 mM NaCl for 24 h then transferred to 1/2 MS solution for recovery. After 4 d, leaves of WT were completely curled and wilted, while those of OsHsfA7-OE were rolled only in the tip part (Fig. 2C). After 10 d recovery, leaves of WT were withered and almost all plants were completely dead, while most of the transgenic plants remained alive and only the leaf tips scorched (Fig. 2D). The survival rates of the transgenic seedlings were 67.5% for OE-1 line and 70.8% for OE-8 line (Fig. S2B). These results indicate that over-expression of OsHsfA7 can improve salt resistance of transgenic rice.

To examine the tolerance to drought stress, three-week-old plants were withheld water for 10 d and then re-watered for additional 10 d. Both WT and transgenic plants suffered severe blast after un-watering (Fig. 3B), whereas there was remarkable difference after re-watering. While most of the WT plant leaves showed further withered and could not be rescued, the majority of OsHsfA7-OE plants restored normal growth (Fig. 3C). The survival rates of the transgenic seedlings were 77.4% for OE-1 line and 82.8% for OE-8 line (Fig. S2C).

Fig. 3.Phenotype of the OsHsfA7 over-expression transgenic plants in response to drought treatment. Threeweek-old OsHsfA7 transgenic plants and WT control plants were grown in soil in a tray. (A) Seedlings before treatment. (B) Seedlings were un-watered 10 d for drought treatment. (C) Seedlings were re-watered for 10 d after the treatment.

Fig. 4.Relative expression levels of OsHsfA7 and Hsp genes in WT and transgenic rice under normal conditions analyzed by real-time qPCR. OsUBQ5 was used as an internal control. The result is the average of three independent experiments and expression levels of these genes in WT were taken as 1, the error bars indicate ± SD. OsHsp80.2, OsHsp74.8 and OsHsp50.2 belong to Hsp90 family. OsHsp71.1, OsHsp58.7 and OsHsp23.7 belong to Hsp70 family. OsHsp26.7, OsHsp24.1 and OsHsp17.0 belong to sHsp family.

In addition, three-week-old seedlings of WT and transgenic plants with similar vigor were used for 47℃ high temperature treatments for 90 min. After treatment, leaf tips of both WT and transgenic plants were rolled or withered, no significant difference was observed. After recovery for 7 d, both transgenic plants and WT plants remained alive and new leaves grew out. Meanwhile, we tested the thermo-tolerance of transgenic and WT plants at booting stage, no significant difference was found in seed setting rate after treatment.

Expression of putative downstream genes regulated by OsHsfA7

To investigate the putative downstream genes regulated by OsHsfA7, nine Hsp genes from three major Hsp families (Hsp90s, Hsp70s and sHsps) were selected to detect their relative expressions in WT and OsHsfA7-OE plants under normal growth conditions by RT-PCR. It was found that only OsHsp24.1 was up-regulated in the OsHsfA7-OE plants, while expressions of the other eight Hsp genes showed no obvious difference between WT and transgenic rice (Fig. 4).

 

DISCUSSION

Individual Hsfs have unique functions during development. For example, HsfA9 was characterized as a specialized Hsf for embryogenesis and seed maturation in sunflower and Arabidopsis (24,25). HsfA5 transcripts are mainly found in pollen together with HsfA4 in Arabidopsis (26). A rice HsfA4d mutant (Spl7) showed spontaneous necrotic lesions in mature leaves (27). In the present study, transgenic rice plants over-expressing OsHsfA7 exhibited different root than WT. Noticeably, lateral roots and root hair of the OsHsfA7-OE rice were shorter and less than those of the WT at seedling stage. In the other hand, tap roots of OsHsfA7-OE rice were longer compared with WT. Our results indicate that OsHsfA7 has an important role in root growth and development.

There is increasing evidence that individual member of a Hsf family may play distinct role in response to various environmental stresses (9,13,15,19,28). The growth of OsHsfA7-OE seedlings in soil was unaffected under high salt stress, while the leaf apex of the control became scorched. Meanwhile, leaf REC and MDA content were lower in the transgenic lines than in the WT. Electrolyte leakage is an indirect measure of damage done to plant cell membranes, and lower REC indicates that less membrane damage occurred (29). MDA is one of the end products of lipid peroxidation damage from free radicals (30). Salt-tolerant plants have a more perfect defense mechanism to maintain low levels of MDA (31). These findings suggested that the changes of physiological index in plants are highly adapted to stress resistance. In addition, the transgenic rice plants over-expressing OsHsfA7 had increased tolerance to drought stress in our study. These results indicate that OsHsfA7 may play a role as a member of natural defense system against high salinity and drought stresses.

Over-expression of HsfA1 and HsfA2 genes in Arabidopsis, tomato and soybean have been reported to enhance plant heat stress resistance (14-16,32,33). Nevertheless, no obvious heat tolerance of OsHsfA7-OE transgenic plants was observed in our experiment. A recent investigation showed that over-expression of OsHsfC1b improved tolerance to salt in rice (34). In addition, HsfA3 was confirmed as part of drought stress signaling (35). These results indicated that a certain Hsf could be responsible for some specific kinds of abiotic stresses and different Hsfs could have diverse role in response to abiotic stresses.

Under abiotic stresses, different Hsfs can specifically bind to heat shock elements of some Hsps and subsequently activate their transcription (3-6). Almoguera et al. (24) found that the expression HaHsp17.6G1 and HaHsp17.7G4 were regulated by sunflower HsfA9. Busch et al. (36) demonstrated HsfA1a and (or) HsfA1b regulated the expression of Hsp70 and Hsp101 in double mutants. Over-expression of LlHsfA2 activated the downstream genes including Hsp101, Hsp70 and Hsp25.3 (37). We have checked the expression of nine OsHsp genes in OsHsfA7-OE transgenic plants and only OsHsp24.1 was highly expressed in comparison with WT. It is likely that OsHsp24.1 was potential target gene of OsHsfA7 and involved in the adaptation to high salinity or drought stress in transgenic rice.

 

MATERIALS AND METHODS

Phylogenetic analysis

OsHsfA7 homolog protein sequences from various plant species were retrieved from GenBank through a BLASTP search. OsHsfA7 and these homolog Hsfs protein sequences were aligned by DNAMAN software with default gap penalties. The phylogenetic tree was constructed by MEGA4 with the neighbor-joining algorithm using default settings. A bootstrap analysis of 1,000 replicates was performed.

Plasmid construction and rice transformation

The complete ORF of OsHsfA7 was obtained from full-length cDNA clone AK064271 (National Institute of Agrobiological Sciences, Tsukuba, Japan) by Kpn I and Pst I digestion. Then the ORF fragment was cloned into Kpn I and Pst I digested pCAMBIA1301-Multi (modifiedfrompCAMBIA1301) under the control of the CaMV 35S promoter. The construct was transformed into rice (Oryza sativa ssp. japanica var. Nipponbare) according to the rice genetic transformation method (38).

RNA isolation and real-time qPCR analysis

OsHsfA7-OE and WT were planted according to Liu et al. (23). After 3 weeks, rice leaf samples were collected for expression analysis of OsHsfA7 and 9 OsHsp genes (primerslistedinTableS1). Total RNA extraction, reverse transcription into cDNA and real-time quantitative PCR was performed according to Zou et al. (39). All cDNA samples were analyzed in triplicate from three sets of independent plants. The relative changes in gene expression were quantified using the 2-△△Ct method. The data were expressed as mean ± standard error.

Drought, salt and heat stress treatments

T2 generation seeds of OsHsfA7-OE homozygous plants were used for stress treatments. After one week germination on 1/2 MS solid medium, the seedlings were transferred to nutritious soil in plastic pots and placed in a growth chamber (14-h-light/10-h-dark cycles) at 30℃ and 75% relative humidity. After two weeks, the seedlings were used for the following abiotic stress treatments. For drought tolerance treatment, seedling plants were withheld water for 10 d, and then re-watered for 10 d. For high-salt stress treatment, seedlings were irrigated with 200 mM NaCl solution for 10 d. For heat stress treatment, plants were exposed to 47℃ for 90 min. In addition, salt tolerance at seedling stage was evaluated under another stress conditions. After germination on 1/2 MS solid medium for one week, hydroponic seedlings were cultured with 1/2 MS liquid medium for 1 week, and followed by 24 h treatment in 1/2 MS solution containing 200 mM NaCl, and then transferred back to 1/2 MS solution for 4 d and 10 d recovery, respectively. The seedlings were evaluated for their survival percentage based on observations that actively growing seedlings as survivors and the non-growing and wilted seedlings were as non-survivors. All above experiments were repeated three times. The phenotype of OsHsfA7 transgenic plants and the WT under different treatments was observed and photographed.

Assay for relative electrical conductivity (REC) and malondialdehyde (MDA)

Three-week-old seedlings were treated with 200 mM NaCl for 10 d and the leaf REC and MDA were assayed. The leaf REC was measured at the beginning and at the end of salt treatment as the method described by Yu et al. (40). Five seedling shoots were harvested before and after the treatment and finely ground in liquid nitrogen using a mortar and pestle previously chilled with liquid nitrogen and the frozen powder was immediately used for MDA assay. MDA content was measured for salt treatment according to Kuk et al. (41). The mean values of REC and MDA were taken from the measurements of three replicates and ‘Standard Error’ of the means was calculated. Data were analyzed by Excel using t test to assess the significance of differences among the means.

References

  1. Haslbeck, M. (2002) sHsps and their role in the chaperone network. Cell Mol. Life Sci. 59, 1649-1657. https://doi.org/10.1007/PL00012492
  2. Hartl, F. U. and Hayer-Hartl, M. (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295, 1852-1858. https://doi.org/10.1126/science.1068408
  3. Baniwal, S. K., Bharti, K., Chan, K. Y., Fauth, M., Ganguli, A., Kotak, S., Mishra, S. K., Nover, L., Port, M., Scharf, K. D., Tripp, J., Weber, C., Zielinski, 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. J. Biosci. 29, 471-487. https://doi.org/10.1007/BF02712120
  4. Morimoto, R. I. (1998) Regulation of the heat stress transcriptional response: cross talk between family of heat stress factors, molecular chaperones, and negative regulators. Genes Dev. 12, 3788-3796. https://doi.org/10.1101/gad.12.24.3788
  5. Schöffl, F., Prändl, R. and Reindl, A. (1998) Regulation of the heat shock response. Plant Physiol. 117, 1135-1141. https://doi.org/10.1104/pp.117.4.1135
  6. Wu, C. (1995) Heat shock transcription factors: structure and regulation. Annu. Rev. Cell Dev. Biol. 11, 441-469. https://doi.org/10.1146/annurev.cb.11.110195.002301
  7. Döring, P., Treuter, E., Kistner, C., Lyck, R., Chen, A. and Nover, L. (2000) The role of AHA motifs in the activator function of tomato heat stress transcription factors HsfA1 and HsfA2. Plant. Cell 12, 265-278. https://doi.org/10.1105/tpc.12.2.265
  8. Nover, L., Bharti, K., Döring, P., Mishra, S. K., Ganguli, A. and Scharf, K. D. (2001) Arabidopsis and the Hsf world: How many heat stress transcription factors do we need? Cell Stress Chaperones. 6, 177-189. https://doi.org/10.1379/1466-1268(2001)006<0177:AATHST>2.0.CO;2
  9. Chauhan, H., Khurana, N., Agarwal, P. and Khurana, P. (2011) Heat shock factors in rice (Oryza sativa L.): genome- wide expression analysis during reproductive development and abiotic stress. Mol. Genet. Genomics. 286, 171-187. https://doi.org/10.1007/s00438-011-0638-8
  10. Lohmann. C., Eggers-Schumacher, G., Wunderlich, M. and Schoffl, F. (2004) Two different heat shock factors regulate immediate early expression of stress genes in Arabidopsis. Mol. Genet. Genomics. 271, 11-21. https://doi.org/10.1007/s00438-003-0954-8
  11. Mishra, S. K., Tripp, J., Winkelhaus, S., Tschiersch, B., Theres, K., Nover, L. and Scharf, K. D. (2002) In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato. Genes Dev. 16, 1555-1567. https://doi.org/10.1101/gad.228802
  12. Zhu, B., Ye, C., Lü, H., Chen, X., Chai, G., Chen, J. and Wang, C. (2006) Identification and characterization of a novel heat shock transcription factor gene, GmHsfA1, in soybeans (Glycine max). J. Plant Res. 119, 247-256. https://doi.org/10.1007/s10265-006-0267-1
  13. 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. https://doi.org/10.1007/s00425-007-0670-4
  14. Li, H. Y., Chang, C. S., Lu, L. S., Liu, C. A., Chan, M. T. and Charng, Y. Y. (2003) Over-expression of Arabidopsis thaliana heat shock factor gene (AtHsfA1b) enhances chilling tolerance in transgenic tomato. Bot. Bull. Acad. Sin. 44, 129-140.
  15. Banti, V., Mafessoni, F., Loreti, E., Alpi, A. and Perata, P. (2010) The heat-inducible transcription factor HsfA2 enhances anoxia tolerance in Arabidopsis. Plant Physiol. 152, 1471-1483. https://doi.org/10.1104/pp.109.149815
  16. Li, C. G., Chen, Q. J., Gao, X. Q., Qi, B. S., Chen, N. Z., Xu, S. M., Chen, J. and Wang, X. C. (2005) AtHsfA2 modulates expression of stress responsive genes and enhances tolerance to heat and oxidative stress in Arabidopsis. Sci. China C. Life Sci. 48, 540-550. https://doi.org/10.1360/062005-119
  17. Nishizawa, A., Yabuta, Y., Yoshida, E., Maruta, T., Yoshimura, K. and Shigeoka, S. (2006) Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J. 48, 535-547. https://doi.org/10.1111/j.1365-313X.2006.02889.x
  18. Ogawa, D., Yamaguchi, K. and Nishiuchi, T. (2007) High-level overexpression of the Arabidopsis HsfA2 gene confers not only increased themotolerance but also salt/osmotic stress tolerance and enhanced callus growth. J. Exp. Bot. 58, 3373-3383. https://doi.org/10.1093/jxb/erm184
  19. Shim, D., Hwang, J. U., Lee, J., Lee, S., Choi, Y., An, G., Martinoia, E. and Lee, Y. (2009) Orthologs of the class A4 heat shock transcription factor HsfA4a confer cadmium tolerance in wheat and rice. Plant Cell. 21, 4031-4043. https://doi.org/10.1105/tpc.109.066902
  20. Huang, C., Ding, S., Zhang, H., Du, H. and An, L. (2011) CIPK7 is involved in cold response by interacting with CBL1 in Arabidopsis thaliana. Plant Sci. 181, 57-64. https://doi.org/10.1016/j.plantsci.2011.03.011
  21. Tripathi, V., Parasuraman, B., Laxmi, A. and Chattopadhyay, D. (2009) CIPK6, a CBL-interacting protein kinase is required for development and salt tolerance in plants. Plant J. 58, 778-790. https://doi.org/10.1111/j.1365-313X.2009.03812.x
  22. Wang, Y., Wan, L., Zhang, L., Zhang, Z., Zhang, H., Quan, R., Zhou, S. and Huang, R. F. (2012) An ethylene response factor OsWR1 responsive to drought stress transcriptionally activates wax synthesis related genes and increases wax production in rice. Plant Mol. Biol. 78, 275-288. https://doi.org/10.1007/s11103-011-9861-2
  23. Liu, A. L., Zou, J., Zhang, X. W., Zhou, X. Y., 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 J. Plant Biol. 53, 142-149. https://doi.org/10.1007/s12374-010-9099-6
  24. Almoguera, C., Rojas, A., Díaz-Martín, J., Prieto-Dapena, P., Carranco, R. and Jordano, J. (2002) A seed-specific heat-shock transcription factor involved in developmental regulation during embryogenesis in sunflower. J. Biol. Chem. 277, 43866-43872. https://doi.org/10.1074/jbc.M207330200
  25. Kotak, S., Vierling, E., Bäumlein, H. and von Koskull- Doring, P. (2007) A novel transcriptional cascade regulating expression of heat stress proteins during seed development of Arabidopsis. Plant Cell 19, 182-195. https://doi.org/10.1105/tpc.106.048165
  26. Baniwal, S. K., Chan, K. Y., Scharf, K. D. and Nover, L. (2007) Role of heat stress transcription factor HsfA5 as specific repressor of HsfA4. J. Biol. Chem. 282, 3605-3613.
  27. Yamanouchi, U., Yano, M., Lin, H., Ashikari, M. and Yamada, K. (2002) A rice spotted leaf gene, Sp l7, encodes a heat stress transcription factor protein. Proc. Natl. Acad. Sci. U. S. A. 99, 7530-7535. https://doi.org/10.1073/pnas.112209199
  28. Liu, H. C., Liao, H. T. and Charng, Y. Y. (2011) The role of class A1 heat shock factors (HSFA1s) in response to heat and other stresses in Arabidopsis. Plant. Cell Environ. 34, 738-751. https://doi.org/10.1111/j.1365-3040.2011.02278.x
  29. Bajji, M., Kinet, J. and Lutts, S. (2002) The use of the electrolyte leakage method for assessing cell membrane stability as a water stress tolerance test in durum wheat. Plant Growth Regul. 36, 61-70. https://doi.org/10.1023/A:1014732714549
  30. Marnett, L. J. (1999) Lipid peroxidation-DNA damage by malondialdehyde. Mutat. Res-Fund Mol. M. 424, 83-95. https://doi.org/10.1016/S0027-5107(99)00010-X
  31. Xie, Z., Duan, L., Tian, X., Wang, B., Eneji, A. E. and Li, Z. (2008) Coronatine alleviates salinity stress in cotton by improving the antioxidative defense system and radical- scavenging activity. Plant Physiol. 165, 375-384. https://doi.org/10.1016/j.jplph.2007.06.001
  32. Charng, Y. Y., Liu, H. C., Liu, N. Y., Chi, W. T., Wang, C. N., Chang, S. H. and Wang, T. T. (2007) A heat-inducible transcription factor, HsfA2, is required for extension of acquired thermotolerance in Arabidopsis. Plant Physiol. 143, 251-262.
  33. Liu, J. G., Qin, Q. L., Zhang, Z., Peng, R. H., Xiong, A. S., Chen, J. M. and Yao, Q. H. (2009) OsHSF7 gene in rice, Oryza sativa L., encodes a transcription factor that functions as a high temperature receptive and responsive factor. BMB Rep. 42, 16-21. https://doi.org/10.5483/BMBRep.2009.42.1.016
  34. Schmidt, R., Schippers, J. H., Welker, A., Mieulet, D., Guiderdoni, E. and Mueller-Roeber, B. (2012) Transcription factor OsHsfC1b regulates salt tolerance and development in Oryza sativa ssp. japonica. AoB Plants. doi:10. 1093/aobpla/pls011. https://doi.org/10.1093/aobpla/pls011
  35. Scharf, K. D., Berberich, T., Ebersberger, I. and Nover, L. (2012) The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim. Biophys. Acta. 1819, 104-119. https://doi.org/10.1016/j.bbagrm.2011.10.002
  36. Busch, W., Wunderlich, M. and Schoffl, F. (2005) Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. Plant J. 41, 1-14.
  37. Xin, H., Zhang, H., Chen, L., Li, X., Lian, Q., Yuan, X., Hu, X., Cao, L., He, X. and Yi, M. (2010) Cloning and characterization of HsfA2 from Lily (Lilium longiflorum). Plant Cell Rep. 29, 875-885. https://doi.org/10.1007/s00299-010-0873-1
  38. Toki, S., Hara, N., Ono, K., Onodera, H., Tagiri, A., Oka, S. and Tanaka, H. (2006) Early infection of scutellum tissue with Agrobacterium allows high speed transformation of rice. Plant J. 47, 969-976. https://doi.org/10.1111/j.1365-313X.2006.02836.x
  39. Zou, J., Liu, C. F., Liu, A. L., Zou, D. and Chen, X. B. (2012) Overexpression of OsHsp17.0 and OsHsp23.7 enhances drought and salt tolerance in rice. J. Plant. Physiol. 169, 628-635. https://doi.org/10.1016/j.jplph.2011.12.014
  40. Yu, X., Peng, Y. H., Zhang, M. H., Shao, Y. J., Su, W. A. and Tang, Z. C. (2006) Water relations and an expression analysis of plasma membrane intrinsic proteins in sensitive and tolerant rice during chilling and recovery. Cell Res. 16, 599-608. https://doi.org/10.1038/sj.cr.7310077
  41. Kuk, Y. I., Shin, J. S., Burgos, N. R., Hwang, T. E., Han, O., Cho, B. H., Jung, S. and Guh, J. O. (2003) Antioxidative enzymes offer protection from chilling damage in rice plants. Crop. Sci. 43, 2109-2117. https://doi.org/10.2135/cropsci2003.2109

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  2. Challenges of modifying root traits in crops for agriculture vol.19, pp.12, 2014, https://doi.org/10.1016/j.tplants.2014.08.005
  3. Integrating Classical with Emerging Concepts for Better Understanding of Salinity Stress Tolerance Mechanisms in Rice vol.5, 2017, https://doi.org/10.3389/fenvs.2017.00042
  4. Sub-Functionalization in Rice Gene Families with Regulatory Roles in Abiotic Stress Responses vol.35, pp.4, 2016, https://doi.org/10.1080/07352689.2016.1265357
  5. Transgenic cereals: Current status and future prospects vol.59, pp.3, 2014, https://doi.org/10.1016/j.jcs.2013.08.008
  6. Simultaneous expression of regulatory genes associated with specific drought-adaptive traits improves drought adaptation in peanut vol.14, pp.3, 2016, https://doi.org/10.1111/pbi.12461
  7. Over-expression of BvMTSH, a fusion gene for maltooligosyltrehalose synthase and maltooligosyltrehalose trehalohydrolase, enhances drought tolerance in transgenic rice vol.47, pp.1, 2014, https://doi.org/10.5483/BMBRep.2014.47.1.064
  8. Understanding salinity responses and adopting ‘omics-based’ approaches to generate salinity tolerant cultivars of rice vol.6, 2015, https://doi.org/10.3389/fpls.2015.00712
  9. Over-expression of heat shock factor gene (AtHsfA1d) from Arabidopsis thaliana confers formaldehyde tolerance in tobacco vol.36, pp.6, 2014, https://doi.org/10.1007/s11738-014-1523-y
  10. Heat shock factor OsHsfB2b negatively regulates drought and salt tolerance in rice vol.32, pp.11, 2013, https://doi.org/10.1007/s00299-013-1492-4
  11. Hsp transcript induction is correlated with physiological changes under drought stress in Indian mustard vol.21, pp.3, 2015, https://doi.org/10.1007/s12298-015-0305-3
  12. Genetic improvement of rice crop under high temperature stress: bridging plant physiology with molecular biology vol.21, pp.4, 2016, https://doi.org/10.1007/s40502-016-0255-y
  13. Forward and reverse genetics approaches for combined stress tolerance in rice pp.0974-0252, 2018, https://doi.org/10.1007/s40502-018-0418-0
  14. Identification of QTN and candidate genes for Salinity Tolerance at the Germination and Seedling Stages in Rice by Genome-Wide Association Analyses vol.8, pp.1, 2018, https://doi.org/10.1038/s41598-018-24946-3
  15. Overexpression of Rice Rab7 Gene Improves Drought and Heat Tolerance and Increases Grain Yield in Rice (Oryza sativa L.) vol.10, pp.1, 2019, https://doi.org/10.3390/genes10010056
  16. Genome-Wide Analysis and Expression Profiling of the Heat Shock Factor Gene Family in Phyllostachys edulis during Development and in Response to Abiotic Stresses vol.10, pp.2, 2019, https://doi.org/10.3390/f10020100