Skip to main content
Log in

OsMPK3 is a TEY-type rice MAPK in Group C and phosphorylates OsbHLH65, a transcription factor binding to the E-box element

  • Original Paper
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

OsMPK3 is a TEY-type rice MAPK belonging to Group C and directly phosphorylates OsbHLH65 in the nucleus. OsMPK3 and OsbHLH65 are induced by biotic stress and defense-related hormones.

Abstract

Mitogen-activated protein kinases (MAPKs) are involved in the majority of signaling pathways that regulate plant development and stress tolerance via the phosphorylation of target molecules. Plant MAPKs are classified into two subtypes, TEY and TDY, according to the TxY (x = E or D) motif in their activation loop, and the TDY motif is unique to plant MAPKs. In rice, 17 MAPKs have been classified into six groups. To date, the functions of many TDY-type rice MAPKs have been characterized, but little is known of the TEY-type MAPKs in Group C and their possible target substrates. In the study reported here, we determined that a TEY-type rice MAPK belonging to subgroup C, named OsMPK3, phosphorylates its substrate OsbHLH65 in the nucleus. Our electrophoresis mobility shift assay results revealed that OsbHLH65 specifically binds to the E-box cis-element, but not to the G-box. Both OsMPK3 and OsbHLH65 were induced by treatments with rice blast (Magnaporthe grisea), brown planthopper (Nilaparvata lugens), and defense-related hormones, such as methyl jasmonic acid and salicylic acid. Our results suggest the possibility that OsMPK3 contributes to the defense signal transduction by phosphorylating the basic helix–loop–helix transcription factor.

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

Similar content being viewed by others

Abbreviations

MAPK (MPK):

Mitogen-activated protein kinase

BPH:

Brown planthopper

ERK:

Extracellular signal-regulated kinase

CD:

Common docking site

TF:

Transcription factor

bHLH:

Basic helix–loop–helix

References

  • Agrawal GK, Rakwal R, Iwahashi H (2002) Isolation of novel rice (Oryza sativa L.) multiple stress responsive MAP kinase gene, OsMSRMK2, whose mRNA accumulates rapidly in response to environmental cues. Biochem Biophys Res Commun 294:1009–1016

    Article  CAS  PubMed  Google Scholar 

  • Agrawal GK, Agrawal SK, Shibato J, Iwahashi H, Rakwal R (2003) Novel rice MAP kinases OsMSRMK3 and OsWJUMK1 involved in encountering diverse environmental stresses and developmental regulation. Biochem Biophys Res Commun 300:775–783

    Article  CAS  PubMed  Google Scholar 

  • Atchley WR, Terhalle W, Dress A (1999) Positional dependence, cliques, and predictive motifs in the bHLH protein domain. J Mol Evol 48:501–516

    Article  CAS  PubMed  Google Scholar 

  • Carretero-Paulet L, Galstyan A, Roig-Villanova I, Martínez-García JF, Bilbao-Castro JR, Robertson DL (2010) Genome-wide classification and evolutionary analysis of the bHLH family of transcription factors in Arabidopsis, poplar, rice, moss, and algae. Plant Physiol 153:1398–1412

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cho S, Jung K, Jeung J, Kang K, Shim K, You M, Yoo K, Ok S, Shin J (2005) Analysis of differentially expressed transcripts from planthopper-infested wild rice (Oryza minuta). Plant Cell Rep 24:59–67

    Article  CAS  PubMed  Google Scholar 

  • Cristina MS, Petersen M, Mundy J (2010) Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol 61:621–649

    Article  Google Scholar 

  • Dóczi R, Ökrész L, Romero AE, Paccanaro A, Bögre L (2012) Exploring the evolutionary path of plant MAPK networks. Trends Plant Sci 17:518–525

    Article  PubMed  Google Scholar 

  • Fernández-Calvo P, Chini A, Fernández-Barbero G, Chico J-M, Gimenez-Ibanez S, Geerinck J, Eeckhout D, Schweizer F, Godoy M, Franco-Zorrilla JM (2011) The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. Plant Cell 23:701–715

    Article  PubMed Central  PubMed  Google Scholar 

  • Fu S-F, Chou W-C, Huang D-D, Huang H-J (2002) Transcriptional regulation of a rice mitogen-activated protein kinase gene, OsMAPK4, in response to environmental stresses. Plant Cell Physiol 43:958–963

    Article  CAS  PubMed  Google Scholar 

  • Gan PH, Dodds PN, Hardham AR (2012) Plant infection by biotrophic fungal and oomycete pathogens. In: Signal commun plant symbiosis. Springer, Berlin, pp 183–212

  • Hamel L-P, Nicole M-C, Sritubtim S, Morency M-J, Ellis M, Ehlting J, Beaudoin N, Barbazuk B, Klessig D, Lee J (2006) Ancient signals: comparative genomics of plant MAPK and MAPKK gene families. Trends Plant Sci 11:192–198

    Article  CAS  PubMed  Google Scholar 

  • Ichimura K, Shinozaki K, Tena G, Sheen J, Henry Y, Champion A, Kreis M, Zhang S, Hirt H, Wilson C (2002) Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci 7:301–308

    Article  CAS  Google Scholar 

  • Jeong H-J, Shin JS, Ok SH (2011) Barley DNA-binding methionine aminopeptidase, which changes the localization from the nucleus to the cytoplasm by low temperature, is involved in freezing tolerance. Plant Sci 180:53–60

    Article  CAS  PubMed  Google Scholar 

  • Kim S-H, 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 X, Duan X, Jiang H, Sun Y, Tang Y, Yuan Z, Guo J, Liang W, Chen L, Yin J (2006) Genome-wide analysis of basic/helix-loop-helix transcription factor family in rice and Arabidopsis. Plant Physiol 141:1167–1184

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liu Q, Xue Q (2007) Computational identification and phylogenetic analysis of the MAPK gene family in Oryza sativa. Plant Physiol Biochem 45:6–14

    Article  CAS  PubMed  Google Scholar 

  • Miyamoto K, Shimizu T, Lin F, Sainsbury F, Thuenemann E, Lomonossoff G, Nojiri H, Yamane H, Okada K (2012) Identification of an E-box motif responsible for the expression of jasmonic acid-induced chitinase gene OsChia4a in rice. J Plant Physiol 169:621–627

    Article  CAS  PubMed  Google Scholar 

  • Pires N, Dolan L (2010) Origin and diversification of basic-helix-loop-helix proteins in plants. Mol Biol Evol 27:862–874

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Reyna NS, Yang Y (2006) Molecular analysis of the rice MAP kinase gene family in relation to Magnaporthe grisea infection. Mol Plant Microbe Interact 19:530–540

    Article  CAS  PubMed  Google Scholar 

  • Rohila JS, Yang Y (2007) Rice mitogen-activated protein kinase gene family and its role in biotic and abiotic stress response. J Integr Plant Biol 49:751–759

    Article  CAS  Google Scholar 

  • Sailsbery JK, Dean RA (2012) Accurate discrimination of bHLH domains in plants, animals, and fungi using biologically meaningful sites. BMC Evol Biol 12:154

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sharrocks AD, Yang S-H, Galanis A (2000) Docking domains and substrate-specificity determination for MAP kinases. Trends Biochem Sci 25:448–453

    Article  CAS  PubMed  Google Scholar 

  • Shim K, Cho S, Jeung J, Jung K, You M, Ok S, Chung Y, Kang K, Hwang H, Choi H (2004) Identification of fungal (Magnaporthe grisea) stress-induced genes in wild rice (Oryza minuta). Plant Cell Rep 22:599–607

    Article  CAS  PubMed  Google Scholar 

  • Singh R, Lee M-O, Lee J-E, Choi J, Park JH, Kim EH, Yoo RH, Cho J-I, Jeon J-S, Rakwal R (2012) Rice mitogen-activated protein kinase interactome analysis using the yeast two-hybrid system. Plant Physiol 160:477–487

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Song F, Goodman RM (2002) OsBIMK1, a rice MAP kinase gene involved in disease resistance responses. Planta 215:997–1005

    Article  CAS  PubMed  Google Scholar 

  • Song D, Chen J, Song F, Zheng Z (2006) A novel rice MAPK gene, OsBIMK2, is involved in disease-resistance responses. Plant Biol 8:587–596

    Article  CAS  PubMed  Google Scholar 

  • Walter M, Chaban C, Schütze K, Batistic O, Weckermann K, Näke C, Blazevic D, Grefen C, Schumacher K, Oecking C (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J 40:428–438

    Article  CAS  PubMed  Google Scholar 

  • Wang Q, Li J, Hu L, Zhang T, Zhang G, Lou Y (2013) OsMPK3 positively regulates the JA signaling pathway and plant resistance to a chewing herbivore in rice. Plant Cell Rep 32:1075–1084

    Article  PubMed  Google Scholar 

  • Xiong L, Yang Y (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 Central  PubMed  Google Scholar 

  • You MK, Oh S, Ok SH, Cho SK, Shin HY, Jeung JU, Shin JS (2007) Identification of putative MAPK kinases in Oryza minuta and O. sativa responsive to biotic stresses. Mol Cell 23:108

    CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by a Grant (2011-0015848) from the National Research Foundation of Korea (NRF) funded by the Ministry of Science and Technology and by a Grant (PJ008160) from the Next-Generation BioGreen 21 Program funded by the Rural Development Administration, Republic of Korea.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jeong Sheop Shin.

Additional information

Communicated by Y.-I. Park.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 246 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shin, HY., You, M.K., Jeung, J.U. et al. OsMPK3 is a TEY-type rice MAPK in Group C and phosphorylates OsbHLH65, a transcription factor binding to the E-box element. Plant Cell Rep 33, 1343–1353 (2014). https://doi.org/10.1007/s00299-014-1620-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-014-1620-9

Keywords

Navigation