Skip to main content
Log in

OsMAPK6 positively regulates rice cold tolerance at seedling stage via phosphorylating and stabilizing OsICE1 and OsIPA1

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Rice is a chilling-sensitive plant, and extremely low temperatures seriously decrease rice production. Several genes involved in chilling stress have been reported in rice; however, the chilling signaling in rice remains largely unknown. Here, we investigated the chilling tolerance phenotype of overexpression of constitutive active OsMAPK6 (CAMAPK6-OE) and OsMAPK6 mutant dsg1, and demonstrated that OsMAPK6 positively regulated rice chilling tolerance. It was shown that, under cold stress, the survival rate of dsg1 was significantly lower than that of WT, whereas CAMAPK6-OE display higher survival rate than WT. Physiological assays indicate that ion leakage and dead cell in dsg1 was much more severe than those in WT and CAMAPK6-OE. Consistently, expression of chilling responsive genes in dsg1, including OsCBFs and OsTPP1, was significantly lower than that of in WT and CAMAPK6-OE. Biochemical analyses revealed that chilling stress promotes phosphorylation of OsMAPK6. Besides, we found that OsMAPK6 interacts with and phosphorylates two key regulators in rice cold signaling, OsIPA1 and OsICE1, and then enhance their protein stability. Overall, our results revealed a cold-induced OsMAPK6-OsICE1/OsIPA1 signaling cascade by which OsMAPK6 was involved in rice chilling tolerance, which provides novel insights to understand rice cold response at seedling stage.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data availability

The data used to support the findings of this study are available from the corresponding author upon request.

References

  • Bowling SA, Clarke JD, Liu YD, Klessig DF, Dong XN (1997) The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. The Plant cell 9:1573–1584

    CAS  PubMed  PubMed Central  Google Scholar 

  • Budhagatapalli N, Narasimhan R, Rajaraman J, Viswanathan C, Nataraja KN (2016) Ectopic expression of AtICE1 and OsICE1 transcription factor delays stress-induced senescence and improves tolerance to abiotic stresses in tobacco. J Plant Biochem Biotechnol 25:285–293

    Article  CAS  Google Scholar 

  • Chander S, Almeida DM, Serra TS, Jardim-Messeder D, Barros PM, Lourenco TF, Figueiredo DD, Margis-Pinheiro M, Costa JM, Oliveira MM, Saibo NJM (2018) OsICE1 transcription factor improves photosynthetic performance and reduces grain losses in rice plants subjected to drought. Environ Exp Bot 150:88–98

    Article  CAS  Google Scholar 

  • Chen XX, Ding YL, Yang YQ, Song CP, Wang BS, Yang SH, Guo Y, Gong ZZ (2021) Protein kinases in plant responses to drought, salt, and cold stress. J Integr Plant Biol 63:53–78

    Article  CAS  PubMed  Google Scholar 

  • Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong XH, Agarwal M, Zhu JK (2003) ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev 17:1043–1054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chujo T, Miyamoto K, Ogawa S, Masuda Y, Shimizu T, Kishi-Kaboshi M, Takahashi A, Nishizawa Y, Minami E, Nojiri H, Yamane H, Okada K (2014) Overexpression of phosphomimic mutated OsWRKY53 leads to enhanced blast resistance in rice. PLoS ONE 9:e98737

    Article  PubMed  PubMed Central  ADS  Google Scholar 

  • Ding YL, Li H, Zhang XY, Xie Q, Gong ZZ, Yang SH (2015) OST1 Kinase modulates freezing tolerance by enhancing ICE1 stability in arabidopsis. Dev Cell 32:278–289

    Article  CAS  PubMed  Google Scholar 

  • Evrard A, Kumar M, Lecourieux D, Lucks J, von Koskull-Doring P, Hirt H (2013) Regulation of the heat stress response in Arabidopsis by MPK6-targeted phosphorylation of the heat stress factor HsfA2. PeerJ 1:e59

    Article  PubMed  PubMed Central  Google Scholar 

  • Guo X, Liu D, Chong K (2018) Cold signaling in plants: Insights into mechanisms and regulation. J Integr Plant Biol 66:745–756

    Article  Google Scholar 

  • Guo T, Lu Z-Q, Shan J-X, Ye W-W, Dong N-Q, Lin H-X (2020) ERECTA1 acts upstream of the OsMKKK10-OsMKK4-OsMPK6 Cascade to control spikelet number by regulating cytokinin metabolism in rice. Plant Cell 32:2763–2779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jai SR, Yinong Y (2007) Rice mitogen-activated protein kinase gene family and its role in biotic and abiotic stress respon. J Integr Plant Biol 49:751–759

    Article  Google Scholar 

  • Jia MR, Luo N, Meng XB, Song XG, Jing YH, Kou LQ, Liu GF, Huang XH, Wang YC, Li JY, Wang B, Yu H (2022) OsMPK4 promotes phosphorylation and degradation of IPA1 in response to salt stress to confer salt tolerance in rice. J Gen Genom 49:766–775

    Article  CAS  Google Scholar 

  • Jiao YQ, Wang YH, Xue DW, Wang J, Yan MX, Liu GF, Dong GJ, Zeng DL, Lu ZF, Zhu XD, Qian Q, Li JY (2010) Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 42:541-U536

    Article  CAS  PubMed  Google Scholar 

  • Kawarazaki T, Kimura S, Iizuka A, Hanamata S, Nibori H, Michikawa M, Imai A, Abe M, Kaya H, Kuchitsu K (2013) A low temperature-inducible protein AtSRC2 enhances the ROS-producing activity of NADPH oxidase AtRbohF. BBA-Mol Cell Res 1833:2775–2780

    CAS  Google Scholar 

  • Kim SH, Oikawa T, Kyozuka J, Wong HL, Umemura K, Kishi-Kaboshi M, Takahashi A, Kawano Y, Kawasaki T, Shimamoto K (2012) The bHLH Rac immunity1 (RAI1) is activated by OsRac1 via OsMAPK3 and OsMAPK6 in rice immunity. Plant Cell Physiol 53:740–754

    Article  CAS  PubMed  Google Scholar 

  • Li H, Ding YL, Shi YT, Zhang XY, Zhang SQ, Gong ZZ, Yang SH (2017) MPK3-and MPK6-Mediated ICE1 phosphorylation negatively regulates ICE1 stability and freezing tolerance in arabidopsis. Dev Cell 43:630–642

    Article  CAS  PubMed  Google Scholar 

  • Liu SY, Hua L, Dong SJ, Chen HQ, Zhu XD, Jiang JE, Zhang F, Li YH, Fang XH, Chen F (2015) OsMAPK6, a mitogen-activated protein kinase, influences rice grain size and biomass production. Plant J 84:672–681

    Article  CAS  PubMed  Google Scholar 

  • Liu MM, Shi ZY, Zhang XH, Wang MX, Zhang L, Zheng KZ, Liu JY, Hu XM, Di CR, Qian Q, He ZH, Yang DL (2019) Inducible overexpression of Ideal Plant Architecture1 improves both yield and disease resistance in rice. Nat Plants 5:389–400

    Article  CAS  PubMed  Google Scholar 

  • Lou Q, Guo H, Li J, Han S, Khan NU, Gu Y, Zhao W, Zhang Z, Zhang H, Li Z, Li J (2022) Cold-adaptive evolution at the reproductive stage in Geng japonica subspecies reveals the role of OsMAPK3 and OsLEA9. Plant J 111:1032–1051

    Article  CAS  PubMed  Google Scholar 

  • Lourenço T, Sapeta H, Figueiredo DD, Rodrigues M, Cordeiro A, Abreu IA, Saibo NJM, Oliveira MM (2013) Isolation and characterization of rice (Oryza sativa L.) E3-ubiquitin ligase OsHOS1 gene in the modulation of cold stress response. Plant Mol Biol 83:351–363

    Article  PubMed  Google Scholar 

  • Miura K, Ikeda M, Matsubara A, Song XJ, Ito M, Asano K, Matsuoka M, Kitano H, Ashikari M (2010) OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat Genet 42:545-U102

    Article  CAS  PubMed  Google Scholar 

  • Singh R, Lee MO, Lee JE, Choi J, Park JH, Kim EH, Yoo RH, Cho JI, Jeon JS, Rakwal R, Agrawal GK, Moon JS, Jwa NS (2012) Rice mitogen-activated protein kinase interactome analysis using the yeast two-hybrid system. Plant Physiol 160:477–487

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian XJ, Li XF, Zhou WJ, Ren YK, Wang ZY, Liu ZQ, Tang JQ, Tong HN, Fang J, Bu QY (2017) Transcription Factor OsWRKY53 positively regulates brassinosteroid signaling and plant architecture. Plant Physiol 175:1337–1349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian XJ, He ML, Mei EY, Zhang BW, Tang JQ, Xu M, Liu JL, Li XF, Wang ZY, Tang WQ, Guan QJ, Bu QY (2021) WRKY53 integrates classic brassinosteroid signaling and the mitogen-activated protein kinase pathway to regulate rice architecture and seed size. Plant Cell 33:2753–2775

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang J, Yu H, Xiong GS, Lu ZF, Jiao YQ, Meng XB, Liu GF, Chen XW, Wang YH, Li JY (2017) Tissue-Specific Ubiquitination by IPA1 INTERACTING PROTEIN1 Modulates IPA1 protein levels to regulate plant architecture in rice. Plant Cell 29:697–707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Zhou L, Shi H, Chern M, Yu H, Yi H, He M, Yin JJ, Zhu XB, Li Y, Li WT, Liu JL, Wang JC, Chen XQ, Qing H, Wang YP, Liu GF, Wang WM, Li P, Wu XJ, Zhu LH, Zhou JM, Ronald PC, Li SG, Li JY, Chen XW (2018) A single transcription factor promotes both yield and immunity in rice. Science 361:1026–1028

    Article  CAS  PubMed  ADS  Google Scholar 

  • Wankhede DP, Misra M, Singh P, Sinha AK (2013) Rice mitogen activated protein kinase kinase and mitogen activated protein kinase interaction network revealed by In-Silico docking and yeast two-hybrid approaches. PLoS ONE 8:e65011

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Xia CX, Gong YS, Chong K, Xu YY (2021) Phosphatase OsPP2C27 directly dephosphorylates OsMAPK3 and OsbHLH002 to negatively regulate cold tolerance in rice. Plant Cell Environ 44:491–505

    Article  CAS  PubMed  Google Scholar 

  • Xie GS, Kato F, Imai R (2012) Biochemical identification of the OsMKK6-OsMPK3 signalling pathway for chilling stress tolerance in rice. Biochem J 443:95–102

    Article  CAS  PubMed  Google Scholar 

  • Xiong LZ, Yang YN (2003) Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase. Plant Cell 15:745–759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu R, Duan PG, Yu HY, Zhou ZK, Zhang BL, Wang RC, Li J, Zhang GZ, Zhuang SS, Lyu J, Li N, Chai TY, Tian ZX, Yao SG, Li YH (2018) Control of grain size and weight by the OsMKKK10-OsMKK4-OsMAPK6 signaling pathway in rice. Mol Plant 11:860–873

    Article  CAS  PubMed  Google Scholar 

  • Yang HB, Shi YT, Liu JY, Guo L, Zhang XY, Yang SH (2010) A mutant CHS3 protein with TIR-NB-LRR-LIM domains modulates growth, cell death and freezing tolerance in a temperature-dependent manner in Arabidopsis. Plant J 63:283–296

    Article  CAS  PubMed  Google Scholar 

  • Yi J, Lee YS, Lee DY, Cho MH, Jeon JS, An G (2016) OsMPK6 plays a critical role in cell differentiation during early embryogenesis in Oryza sativa. J Exp Bot 67:2425–2437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu LJ, Nie JN, Cao CY, Jin YK, Yan M, Wang FZ, Liu J, Xiao Y, Liang YH, Zhang WH (2010) Phosphatidic acid mediates salt stress response by regulation of MPK6 in Arabidopsis thaliana. New Phytol 188:762–773

    Article  CAS  PubMed  Google Scholar 

  • Yu J, Zhu CS, Xuan W, An HZ, Tian YL, Wang BX, Chi WC, Chen GM, Ge YW, Li J, Dai ZY, Liu Y, Sun ZG, Xu DY, Wang CM, Wan JM (2023) Genome-wide association studies identify OsWRKY53 as a key regulator of salt tolerance in rice. Nat Commun 14:3550

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Yuan PG, Yang TB, Poovaiah BW (2018) Calcium signaling-mediated plant response to cold stress. Int J Mol Sci 19:3896

    Article  PubMed  PubMed Central  Google Scholar 

  • Zeng DL, Tian ZX, Rao YC, Dong GJ, Yang YL, Huang LC, Leng YJ, Xu J, Sun C, Zhang GH, Hu J, Zhu L, Gao ZY, Hu XM, Guo LB, Xiong GS, Wang YH, Li JY, Qian Q (2017) Rational design of high-yield and superior-quality rice. Nat Plants 3:17031

    Article  PubMed  Google Scholar 

  • Zhang Z, Li J, Li F, Liu H, Yang W, Chong K, Xu Y (2017) OsMAPK3 phosphorylates OsbHLH002/OsICE1 and inhibits its ubiquitination to activate OsTPP1 and enhances rice chilling tolerance. Dev Cell 43:731-743.e735

    Article  CAS  PubMed  Google Scholar 

  • Zhang D, Guo X, Xu Y, Li H, Ma L, Yao X, Weng Y, Guo Y, Liu C, Chong K (2019) OsCIPK7 point-mutation leads to conformation and kinase-activity change for sensing cold response. J Integr Plant Biol 61:1194–1200

    Article  CAS  PubMed  Google Scholar 

  • Zhao CZ, Zhang ZJ, Xie SJ, Si T, Li YY, Zhu JK (2016) Mutational evidence for the critical role of CBF transcription factors in cold acclimation in arabidopsis. Plant Physiol 171:2744–2759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao CZ, Wang PC, Si T, Hsu CC, Wang L, Zayed O, Yu ZP, Zhu YF, Dong J, Tao WA, Zhu JK (2017) MAP kinase cascades regulate the cold response by modulating ICE1 protein stability. Dev Cell 43:618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu MH, He YG, Zhu MQ, Ahmad A, Xu S, He ZJ, Jiang S, Huang JQ, Li ZH, Liu SJ, Hou X, Zhang ZH (2022) ipa1 improves rice drought tolerance at seedling stage mainly through activating abscisic acid pathway. Plant Cell Rep 41:221–232

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank Prof. Yunhai Li for providing the mutant of dsg1 and CAMAPK6-OE. This study was supported by Natural Science Foundation of Heilongjiang (Grant No. YQ2022CO38), Youth Innovation Promotion Association CAS (Grant No. 2021229), Heilongjiang Key Research and Development Program (Grant No. 2022ZX02B03), Young Scientist Group Project of Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences (Grant No. 2023QNXZ02).

Funding

The authors have not disclosed any funding.

Author information

Authors and Affiliations

Authors

Contributions

XT and QB conceived and designed the experiments. JL and JL performed most of the experiments, and MH, YL, XL, ZW assisted the experiments. XT and JL analyzed the data and wrote the article, and XT, QB, CZ, XJ, JS and WZ revised the manuscript. All authors read and approved the manuscript.

Corresponding authors

Correspondence to Qingyun Bu or Xiaojie Tian.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest.

Additional information

Communicated by Peter Langridge.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOC 63 KB)

Supplementary file2 (PDF 1500 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, J., Liu, J., He, M. et al. OsMAPK6 positively regulates rice cold tolerance at seedling stage via phosphorylating and stabilizing OsICE1 and OsIPA1. Theor Appl Genet 137, 10 (2024). https://doi.org/10.1007/s00122-023-04506-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00122-023-04506-8

Navigation