Advertisement

Plant Cell Reports

, Volume 37, Issue 11, pp 1585–1595 | Cite as

Overexpressing heat-shock protein OsHSP50.2 improves drought tolerance in rice

  • Jianhua Xiang
  • Xinbo Chen
  • Wei Hu
  • Yanci Xiang
  • Mingli Yan
  • Jieming Wang
Original Article

Abstract

Key message

OsHSP50.2, an HSP90 family gene up-regulated by heat and osmotic stress treatments, positively regulates drought stress tolerance probably by modulating ROS homeostasis and osmotic adjustment in rice.

Abstract

Heat-shock proteins (HSPs) serve as molecular chaperones for a variety of client proteins in abiotic stress response and play pivotal roles in protecting plants against stress, but the molecular mechanism remains largely unknown. Here, we report an HSP90 family gene, OsHSP50.2, which acts as a positive regulator in drought stress tolerance in rice (Oryza sativa). OsHSP50.2 was ubiquitously expressed and its transcript level was up-regulated by heat and osmotic stress treatments. Overexpression of OsHSP50.2 in rice reduced water loss and enhanced the transgenic plant tolerance to drought and osmotic stresses. The OsHSP50.2-overexpressing plants exhibited significantly lower levels of electrolyte leakage and malondialdehyde (MDA) and less decrease of chlorophyll than wild-type plants under drought stress. Moreover, the OsHSP50.2-overexpressing plants had significantly higher SOD activity under drought stress compared with the wild type. These results imply that OsHSP50.2 positively regulates drought stress tolerance in rice, probably through the modulation of reactive oxygen species (ROS) homeostasis. Additionally, the OsHSP50.2-overexpressing plants accumulated significantly higher content of proline than the wild type under drought stress, which contributes to the improved protection ability from drought stress damage via osmotic adjustment. Our findings reveal that OsHSP50.2 plays a crucial role in drought stress response, and it may possess high potential usefulness in drought tolerance improvement of rice.

Keywords

Drought tolerance Reactive oxygen species Heat-shock protein OsHSP50.2 Oryza sativa 

Abbreviations

HSF

Heat-shock factor

HSP

Heat-shock protein

MDA

Malondialdehyde

MS

Murashige and Skoog

OE

Overexpression

PEG

Polyethylene glycol

qRT-PCR

Quantitative reverse transcription-polymerase chain reaction

ROS

Reactive oxygen species

RT

Reverse transcription

SOD

Superoxide dismutase

Notes

Acknowledgements

This study was supported by the National Natural Science Foundation of China (Grant Nos. 31401943 and 31671628), the Research Foundation of Education Bureau of Hunan Province, China (Grant No. 14C0453) and Southern Regional Collaborative Innovation Center for Grain and Oil Crops in China, Hunan Agricultural University.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

299_2018_2331_MOESM1_ESM.doc (29 kb)
Supplementary material 1 (DOC 29 KB)
299_2018_2331_MOESM2_ESM.doc (36 kb)
Supplementary material 2 (DOC 35 KB)

References

  1. Abraham E, Rigo G, Szekely G, Nagy R, Koncz C, Szabados L (2003) Light-dependent induction of proline biosynthesis by abscisic acid and salt stress is inhibited by brassinosteroid in Arabidopsis. Plant Mol Biol 51:363–372CrossRefGoogle Scholar
  2. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399CrossRefGoogle Scholar
  3. Boston RS, Viitanen PV, Vierling E (1996) Molecular chaperones and protein folding in plants. Plant Mol Biol 32:191–222CrossRefGoogle Scholar
  4. Breiman A (2014) Plant Hsp90 and its co-chaperones. Curr Protein Pept Sci 15:232–244CrossRefGoogle Scholar
  5. Du H, Wang N, Cui F, Li X, Xiao J, Xiong L (2010) Characterization of the β-carotene hydroxylase gene DSM2 conferring drought and oxidative stress resistance by increasing xanthophylls and abscisic acid synthesis in rice. Plant Physiol 154:1304–1318CrossRefGoogle Scholar
  6. Fang Y, Liao K, Du H, Xu Y, Song H, Li X, Xiong L (2015) A stress-responsive NAC transcription factor SNAC3 confers heat and drought tolerance through modulation of reactive oxygen species in rice. J Exp Bot 66:6803–6817CrossRefGoogle Scholar
  7. Hahn A, Bublak D, Schleiff E, Scharf KD (2011) Crosstalk between Hsp90 and Hsp70 chaperones and heat stress transcription factors in tomato. Plant Cell 23:741–755CrossRefGoogle Scholar
  8. Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6:271–282CrossRefGoogle Scholar
  9. Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300CrossRefGoogle Scholar
  10. Hu H, Xiong L (2014) Genetic engineering and breeding of drought-resistant crops. Annu Rev Plant Biol 65:715–741CrossRefGoogle Scholar
  11. Jiang C, Xu J, Zhang H, Zhang X, Shi J, Li M, Ming F (2009) A cytosolic class I small heat shock protein, RcHSP17.8, of Rosa chinensis confers resistance to a variety of stresses to Escherichia coli, yeast and Arabidopsis thaliana. Plant Cell Environ 32:1046–1059CrossRefGoogle Scholar
  12. Kadota Y, Shirasu K (2012) The HSP90 complex of plants. Biochim Biophys Acta 1823:689–697CrossRefGoogle Scholar
  13. Knudson LL, Tibbitts TW, Edwards GE (1977) Measurement of ozone injury by determination of leaf chlorophyll concentration. Plant Physiol 60:606–608CrossRefGoogle Scholar
  14. Li XM, Chao DY, Wu Y, Huang X, Chen K, Cui LG, Su L, Ye WW, Chen H, Chen HC, Dong NQ, Guo T, Shi M, Feng Q, Zhang P, Han B, Shan JX, Gao JP, Lin HX (2015) Natural alleles of a proteasome α2 subunit gene contribute to thermotolerance and adaptation of African rice. Nat Genet 47:827–833CrossRefGoogle Scholar
  15. Liu J, Zhu JK (1997) Proline accumulation and salt-stress-induced gene expression in a salt-hypersensitive mutant of Arabidopsis. Plant Physiol 114:591–596CrossRefGoogle Scholar
  16. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–∆∆CT Method. Methods 25:402–408CrossRefGoogle Scholar
  17. Lv Y, Guo Z, Li X, Ye H, Xiong L (2016) New insights into the genetic basis of natural chilling and cold shock tolerance in rice by genome-wide association analysis. Plant Cell Environ 39:556–570CrossRefGoogle Scholar
  18. Lv Y, Yang M, Hu D, Yang Z, Ma S, Li X, Xiong L (2017) The OsMYB30 transcription factor suppresses cold tolerance by interacting with a JAZ protein and suppressing β-amylase expression. Plant Physiol 173:1475–1491CrossRefGoogle Scholar
  19. Meiri D, Breiman A (2009) Arabidopsis ROF1 (FKBP62) modulates thermotolerance by interacting with HSP90.1 and affecting the accumulation of HsfA2-regulated sHSPs. Plant J 59:387–399CrossRefGoogle Scholar
  20. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410CrossRefGoogle Scholar
  21. Montero-Barrientos M, Hermosa R, Cardoza RE, Gutierrez S, Nicolas C, Monte E (2010) Transgenic expression of the Trichoderma harzianum hsp70 gene increases Arabidopsis resistance to heat and other abiotic stresses. J Plant Physiol 167:659–665CrossRefGoogle Scholar
  22. Moshe A, Gorovits R, Liu Y, Czosnek H (2016) Tomato plant cell death induced by inhibition of HSP90 is alleviated by Tomato yellow leaf curl virus infection. Mol Plant Pathol 17:247–260CrossRefGoogle Scholar
  23. O’Meara TR, Robbins N, Cowen LE (2017) The Hsp90 chaperone network modulates Candida virulence traits. Trends Microbiol 25:809–819CrossRefGoogle Scholar
  24. Park HS, Jeong WJ, Kim E, Jung Y, Lim JM, Hwang MS, Park EJ, Ha DS, Choi DW (2012) Heat shock protein gene family of the Porphyra seriata and enhancement of heat stress tolerance by PsHSP70 in Chlamydomonas. Mar Biotechnol (NY) 14:332–342CrossRefGoogle Scholar
  25. Pearl LH, Prodromou C (2006) Structure and mechanism of the Hsp90 molecular chaperone machinery. Annu Rev Biochem 75:271–294CrossRefGoogle Scholar
  26. Perez DE, Hoyer JS, Johnson AI, Moody ZR, Lopez J, Kaplinsky NJ (2009) BOBBER1 is a noncanonical Arabidopsis small heat shock protein required for both development and thermotolerance. Plant Physiol 151:241–252CrossRefGoogle Scholar
  27. Sato Y, Yokoya S (2008) Enhanced tolerance to drought stress in transgenic rice plants overexpressing a small heat-shock protein, sHSP17.7. Plant Cell Rep 27:329–334CrossRefGoogle Scholar
  28. Schopf FH, Biebl MM, Buchner J (2017) The HSP90 chaperone machinery. Nat Rev Mol Cell Biol 18:345–360CrossRefGoogle Scholar
  29. Song H, Zhao R, Fan P, Wang X, Chen X, Li Y (2009) Overexpression of AtHsp90.2. AtHsp90.5 and AtHsp90.7 in Arabidopsis thaliana enhances plant sensitivity to salt and drought stresses. Planta 229:955–964CrossRefGoogle Scholar
  30. Sun W, Bernard C, van de Cotte B, Van Montagu M, Verbruggen N (2001) At-HSP17.6A, encoding a small heat-shock protein in Arabidopsis, can enhance osmotolerance upon overexpression. Plant J 27:407–415CrossRefGoogle Scholar
  31. Swain DM, Sahoo RK, Srivastava VK, Tripathy BC, Tuteja R, Tuteja N (2017) Function of heterotrimeric G-protein gamma subunit RGG1 in providing salinity stress tolerance in rice by elevating detoxification of ROS. Planta 245:367–383CrossRefGoogle Scholar
  32. Taheri P, Kakooee T (2017) Reactive oxygen species accumulation and homeostasis are involved in plant immunity to an opportunistic fungal pathogen. J Plant Physiol 216:152–163CrossRefGoogle Scholar
  33. Taipale M, Jarosz DF, Lindquist S (2010) HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol 11:515–528CrossRefGoogle Scholar
  34. Trent JD (1996) A review of acquired thermotolerance, heat-shock proteins, and molecular chaperones in archaea. FEMS Microbiol Rev 18:249–258CrossRefGoogle Scholar
  35. Troll W, Lindsley J (1955) A photometric method for the determination of proline. J Biol Chem 215:655–660PubMedGoogle Scholar
  36. Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252CrossRefGoogle Scholar
  37. Wang R, Zhang Y, Kieffer M, Yu H, Kepinski S, Estelle M (2016) HSP90 regulates temperature-dependent seedling growth in Arabidopsis by stabilizing the auxin co-receptor F-box protein TIR1. Nat Commun 7:10269CrossRefGoogle Scholar
  38. Wang C, Lu G, Hao Y, Guo H, Guo Y, Zhao J, Cheng H (2017) ABP9, a maize bZIP transcription factor, enhances tolerance to salt and drought in transgenic cotton. Planta 246:453–469CrossRefGoogle Scholar
  39. Watanabe E, Mano S, Hara-Nishimura I, Nishimura M, Yamada K (2017) HSP90 stabilizes auxin receptor TIR1 and ensures plasticity of auxin responses. Plant Signal Behav 12:e1311439CrossRefGoogle Scholar
  40. Weng JK, Ye M, Li B, Noel JP (2016) Co-evolution of hormone metabolism and signaling networks expands plant adaptive plasticity. Cell 166:881–893CrossRefGoogle Scholar
  41. Whitlow TH, Bassuk NL, Ranney TG, Reichert DL (1992) An improved method for using electrolyte leakage to assess membrane competence in plant tissues. Plant Physiol 98:198–205CrossRefGoogle Scholar
  42. Xiang Y, Huang Y, Xiong L (2007) Characterization of stress-responsive CIPK genes in rice for stress tolerance improvement. Plant Physiol 144:1416–1428CrossRefGoogle Scholar
  43. Xiang J, Ran J, Zou J, Zhou X, Liu A, Zhang X, Peng Y, Tang N, Luo G, Chen X (2013) Heat shock factor OsHsfB2b negatively regulates drought and salt tolerance in rice. Plant Cell Rep 32:1795–1806CrossRefGoogle Scholar
  44. Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14(Suppl):S165–S183CrossRefGoogle Scholar
  45. Xu J, Xue C, Xue D, Zhao J, Gai J, Guo N, Xing H (2013) Overexpression of GmHsp90s, a heat shock protein 90 (Hsp90) gene family cloning from soybean, decrease damage of abiotic stresses in Arabidopsis thaliana. PLoS One 8:e69810CrossRefGoogle Scholar
  46. Yamada K, Fukao Y, Hayashi M, Fukazawa M, Suzuki I, Nishimura M (2007) Cytosolic HSP90 regulates the heat shock response that is responsible for heat acclimation in Arabidopsis thaliana. J Biol Chem 282:37794–37804CrossRefGoogle Scholar
  47. Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803CrossRefGoogle Scholar
  48. You J, Zong W, Hu H, Li X, Xiao J, Xiong L (2014) A stress-responsive NAC1-regulated protein phosphatase gene rice protein phosphatase18 modulates drought and oxidative stress tolerance through abscisic acid-independent reactive oxygen species scavenging in rice. Plant Physiol 166:2100–2114CrossRefGoogle Scholar
  49. Yue B, Xue W, Xiong L, Yu X, Luo L, Cui K, Jin D, Xing Y, Zhang Q (2006) Genetic basis of drought resistance at reproductive stage in rice: separation of drought tolerance from drought avoidance. Genetics 172:1213–1228CrossRefGoogle Scholar
  50. Zhang J, Liu B, Li J, Zhang L, Wang Y, Zheng H, Lu M, Chen J (2015a) Hsf and Hsp gene families in Populus: genome-wide identification, organization and correlated expression during development and in stress responses. BMC Genom 16:181CrossRefGoogle Scholar
  51. Zhang XC, Millet YA, Cheng Z, Bush J, Ausubel FM (2015b) Jasmonate signalling in Arabidopsis involves SGT1b-HSP70-HSP90 chaperone complexes. Nat Plants 1:15049CrossRefGoogle Scholar
  52. Zou J, Liu A, Chen X, Zhou X, Gao G, Wang W, Zhang X (2009) Expression analysis of nine rice heat shock protein genes under abiotic stresses and ABA treatment. J Plant Physiol 166:851–861CrossRefGoogle Scholar
  53. Zou J, Liu C, Liu A, Zou D, Chen X (2012) Overexpression of OsHsp17.0 and OsHsp23.7 enhances drought and salt tolerance in rice. J Plant Physiol 169:628–635CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute of Ecological Landscape RestorationHunan University of Science and TechnologyXiangtanChina
  2. 2.College of Bioscience and BiotechnologyHunan Agricultural UniversityChangshaChina
  3. 3.School of Life ScienceHunan University of Science and TechnologyXiangtanChina

Personalised recommendations