Skip to main content
SpringerLink
Log in

Overexpression of the receptor-like kinase gene OsNRRB enhances drought-stress tolerance in rice

  • Review
  • Published:
Euphytica Aims and scope Submit manuscript

Abstract

Receptor-like kinases (RLKs) play essential roles in plant growth, development and responses to environmental stresses. Here, we report that a putative RLK gene OsNRRB (Os10g40100.2), which encodes OsNRRB protein with a kinase domain and a U-box domain, is cloned and characterized in rice (Oryza sativa L.). Tissue-specific expression of OsNRRB tested by qRT-PCR and promoter-GUS assays shows that OsNRRB is widely expressed in rice, including internodes, roots, leaves and developing seeds. Expression profile analysis showed that OsNRRB had different transcriptional responses to drought, salt and oxidative (H2O2) stresses, as well as ABA, SA and GA3 treatments. Furthermore, OsNRRB protein is located at the surface of protoplast cells by transient expressing OsNRRB-GFP (green fluorescent protein) fusion construct in rice protoplasts. Moreover, the transgenic seedlings with overexpressed OsNRRB show better tolerance to drought stress compared to wild-type seedlings. On the contrary, the RNAi transgenic seedlings are more sensitive to drought stress. OsNRRB may positively regulate drought stress tolerance through upregulating these stress-responsive genes in rice. Indeed, the expression of stress-responsive genes of OsbZIP23, OsDREB2A, OsP5CS and OsLea3 are upregulated by overexpression of OsNRRB, which in turn increasing drought tolerance in rice.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Barrs HD, Weatherley PE (1962) A re-examination of relative turgidity for estimating water deficit in leaves. Aust J Biol Sci 15:413–428

    Article  Google Scholar 

  • Boyd LA, Ridout C, Sullivan DMO (2013) Plant–pathogen interactions: disease resistance in modern agriculture. Trends Genet 29:233–240

  • Chen W, Yao XQ, Cai KZ, Chen J (2011) Silicon alleviates drought stress of rice plants by improving plant water status, photosynthesis and mineral nutrient absorption. Biol Trace Elem Res 142:67–76

    Article  CAS  PubMed  Google Scholar 

  • Chugh V, Kaur N, Gupta AK (2011) Evaluation of oxidative stress tolerance in maize (Zea mays L.) seedlings in response to drought. Indian J Biochem Biophys 48:47–53

    CAS  PubMed  Google Scholar 

  • Ciftci-Yilmaz S, Mittler R (2008) The zine finger network of plants. Cell Mol Life Sci 65:1150–1160

    Article  CAS  PubMed  Google Scholar 

  • Du BG, Nian H, Zhang ZS, Yang CY (2010) Effects of aluminum on superoxide dismutase and peroxidase activities, and lipid peroxidation in the roots and calluses of soybeans differing in aluminum tolerance. Acta Physiol Plant 32:883–890

    Article  CAS  Google Scholar 

  • Einhellig F, Rasmussen J (1979) Effects of three phenolic acids on chlorophyll content and growth of soybean and grain sorghum seedlings. J Chem Ecol 5(5):815–824

    Article  CAS  Google Scholar 

  • FAO (2010) The state of food insecurity in the world: addressing food insecurity in protracted crises. Rome

  • Golldack D, Li C, Mohan H, Probst N (2014) Tolerance to drought and salt stress in plants: unraveling the signaling networks. Front Plant Sci 5:151

    Article  PubMed  PubMed Central  Google Scholar 

  • Ha CV, Leyva-Gonzalez MA, Osakabe Y, Tran UT, Nishiyama R, Watanabe Y, Tanaka M, Seki M, Yamaguchi S, Dong NV, Yamaguchi-Shinozaki K, Shinozaki K, Herrera-Estrella L, Tran LS (2013) Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proc Natl Acad Sci 111:851–856

    Article  PubMed  PubMed Central  Google Scholar 

  • Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J 61:1041–1052

    Article  CAS  PubMed  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions β-glucuronidase as a sensitive and versatile gene fusionmarker in higher plants. EMBO J 6(13):3901–3907

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kilian J, Whitehead D, Horak J, Wanke D, Weinl S, Batistic O, D’Angelo C, Bornberg-Bauer E, Kudla J, Harter K (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J 50:347–363

    Article  CAS  PubMed  Google Scholar 

  • Kuo MC, Kao CH (2003) Aluminum effects on lipid peroxidation and antioxidative enzyme activities in rice leaves. Biol Plant 46(1):149–152

    Article  CAS  Google Scholar 

  • Lata C, Prasad M (2011) Role of DREBs in regulation of abiotic stress responses in plants. J Exp Bot 62:4731–4748

    Article  CAS  PubMed  Google Scholar 

  • Lata C, Jha S, Dixit V, Sreenivasulu N, Prasad M (2011) Differential antioxidative responses to dehydration-induced oxidative stress in core set of foxtail millet cultivars [Setaria italica (L.)]. Protoplasma 248:817–828

    Article  CAS  PubMed  Google Scholar 

  • Li QF, Ma CC, Ji J (2009) Effect of silicon on water metabolism in maize plants under drought stress. Acta Ecol Sin 29:4163–4168

    CAS  Google Scholar 

  • Li DX, Li CD, Sun HC, Wang WX, Liu LT, Zhang YJ (2010) Effects of drought on soluble protein content and protective enzyme system in cotton leaves. Front Agric China 4:56–62

    Article  Google Scholar 

  • Lin WW, Ma XY, Shan LB, He P (2013) Big roles of small kinases: the complex functions of receptor-like cytoplasmic kinases in plant immunity and development. J Integr Plant Biol 55:1188–1197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin GB, Bogdanove AJ, Sessa G (2003) Understanding the functions of plant disease resistance proteins. Annu Rev Plant Biol 54:23–61

    Article  CAS  PubMed  Google Scholar 

  • Moussa HR, Abdel Aziz M (2008) Comparative response of drought tolerant and drought sensitive maize genotypes to water stress. Aust J Crop Sci 1:31–36

    Google Scholar 

  • Osakabe Y, Mizuno S, Tanaka H, Maruyama K, Osakabe K, Todaka D, Fujita Y, Kobayashi M, Shinozaki K, Yamaguchi-Shinozaki K (2010) Overproduction of the membrane-bound receptor-like protein kinase 1, RPK1, enhances abiotic stress tolerance in Arabidopsis. J Biol Chem 285:9190–9201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ouyang SQ, Liu YF, Liu P, Lei G, He SJ, Ma B, Zhang WK, Zhang JS, Chen SY (2010a) Receptor-like kinase OsSIK1 improves drought and salt stress tolerance in rice (Oryza sativa) plants. Plant J 62:316–329

    Article  CAS  PubMed  Google Scholar 

  • Ouyang Shou-Qiang, Liu Yun-Feng, Liu Peng, Lei Gang, He Si-Jie, Ma Biao, Zhang Wan-Ke, Zhang Jin-Song, Chen Shou-Yi (2010b) Receptor-like kinase OsSIK1 improves drought and salt stress tolerance in rice (Oryza sativa) plants. Plant J 62(2):316–329

    Article  CAS  PubMed  Google Scholar 

  • Read SM, Northcote DH (1981) Minimization of variation in the response to different protein of the Coomassic Blue G dye binding assay for protein. Anal Biochem 116:53–64

    Article  CAS  PubMed  Google Scholar 

  • Sajedi NA, Ferasat M, Mirzakhani M, Mashhadi Akbar Boojar M (2012) Impact of water deficit stress on biochemical characteristics of safflower cultivars. Physiol Mol Biol Plants 18:323–329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006a) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18:1292–1309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakuma Y, Maruyama K, Qin F, Osakabe Y, Shinozaki K, YamaguchiShinozaki K (2006b) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci USA 103:18822–18827

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method, vol 3. Nature Protocols, England

    Google Scholar 

  • Shiu SH, Karlowski WM, Pan RS, Tzeng YH, Mayer KX, Li H (2004) Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell Online 16:1220–1234

    Article  CAS  Google Scholar 

  • Song WY, Wang GL, Chen LL, Kim HS, Pi LY, Holsten T, Gardner J, Wang B, Zhai WX, Zhu LH, Fauquet C, Ronald P (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804–1806

    Article  CAS  PubMed  Google Scholar 

  • Tanaka H, Osakabe Y, Katsura S, Mizuno S, Maruyama K, Kusakabe K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) Abiotic stress-inducible receptor-like kinases negatively control ABA signaling in Arabidopsis. Plant J 70:599–613

  • Tang N, Zhang H, Li XH, Xiao JH, Xiong LZ (2012) Constitutive activation of transcription factor OsbZIP46 improves drought tolerance in rice. Plant Physiol 158:1755–1768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trontin C, Kiani S, Corwin JA, Hématy K, Yansouni J, Kliebenstein DJ, Loudet O (2014) A pair of receptor-like kinases is responsible for natural variation in shoot growth response to mannitol treatment in Arabidopsis thaliana. Plant J 78:121–133

    Article  CAS  PubMed  Google Scholar 

  • Vij S, Giri J, Dansana PK, Kapoor S, Tyagi AK (2008) The receptor-like cytoplasmic kinase (OsRLCK) gene family in rice: organization, phylogenetic relationship, and expression during development and stress. Mol Plant 1:732–750

    Article  CAS  PubMed  Google Scholar 

  • Xiao J, Cheng H, Li X, Xiao J, Xu C, Wang S (2013) Rice WRKY13 regulates cross talk between abiotic and biotic stress signaling pathways by selective binding to different cis-elements. Plant Physiol 163(4):1868–1882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu R, Song F, Zheng Z (2006) OsBISAMT1, a gene encoding S-adenosyl-l-methionine:salicylic acid carboxyl methyltransferase, is differentially expressed in rice defense responses. Mol Biol Rep 33:223–231

    Article  CAS  PubMed  Google Scholar 

  • Yue B, Xue W, Xiong L, Yu X, Luo L, Cui K, Jin D, Xing Y, Zhang Q (2005) Genetic basis of drought resistance at reproductive stage in rice: separation of drought tolerance from drought avoidance. Genetics 172:1213–1228

    Article  PubMed  Google Scholar 

  • Zhang M, Wu YH, Lee MK, Liu YH, Rong Y, Santos TS, Wu C, Xie F, Nelson RL, Zhang HB (2010) Numbers of genes in the NBS and RLK families vary by more than four-fold within a plant species and are regulated by multiple factors. Nucleic Acids Res 38:6513–6525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou HL, He SJ, Cao YR, Chen T, Du BX, Chu CC, Zhang JS, Chen SY (2006) OsGLU1, A putative membrane-bound Endo-1,4-ß-D-glucanase from rice, affects plant internode elongation. Plant Mol Biol 60:137–151

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the National key research and development program of China (2016YFD0100600), (2016YFD0100903), and the National Natural Science Foundation of China (Grant No. 31560297).

Author information

Authors and Affiliations

  1. Xiamen Key Laboratory for Plant Genetics, School of Life Sciences, Xiamen University, Xiamen, 361102, People’s Republic of China

    Y. X. Zhang & L. Chen

Authors
  1. Y. X. Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L. Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to L. Chen.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 122 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, Y.X., Chen, L. Overexpression of the receptor-like kinase gene OsNRRB enhances drought-stress tolerance in rice. Euphytica 213, 86 (2017). https://doi.org/10.1007/s10681-017-1854-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10681-017-1854-z

Keywords

Search

Navigation