Skip to main content
SpringerLink
Log in

The transcription factor OsbHLH138 regulates thermosensitive genic male sterility in rice via activation of TMS5

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

Abstract

Thermosensitive genic male sterile (TGMS) lines favored heterosis exploitation in two-line hybrid rice. TMS5, a member of RNase Z cleavages the UbL40 mRNAs, plays an important role in two-line hybrid rice. Here, we identified a new TGMS mutant 93-11s, which lost two amino acids in the first exon of TMS5 gene and caused thermosensitive genic male sterility in rice. The tms5-2 cannot process mRNAs of the ubiquitin fusion ribosomal protein L40 (UbL40) and hence cause the mRNAs accumulation in restrictive temperature. Further, we identified a nucleus-localized bHLH transcription factor OsbHLH138, which can form the basic helix–loop–helix structure and bind the core region of tms5-2 promoter sequences by bHLH domain, and activate expression of tms5-2 by the acidic amino acid-rich domain. These results indicate a novel mechanism for the tms5-2 regulating thermosensitive male sterility of rice. By altering expression of OsbHLH138, we can regulate the expression level of TMS5 and the accumulation of UbL40 mRNAs to command the male fertility in different temperatures. The identification of OsbHLH138 provides breeders a new choice for development of TGMS rice lines, which will favor the sustainable development of two-line hybrid 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
Fig. 7

Similar content being viewed by others

Abbreviations

TGMS:

Thermosensitive genic male sterile

UbL40 :

Ubiquitin fusion ribosomal protein L40

RNase Z:

Ribonuclease Z

bHLH:

Basic helix–loop–helix

PIF:

Phytochrome-interacting factor

APA:

Active phytochrome A

APB:

Active phytochrome B

MBL:

Metal beta-lactamase

DDO:

SD/-Trp/-Leu

TDO:

SD/-Trp/-Leu/-His

References

  • Atchley WR, Fitch WM (1997) A natural classification of the basic helix-loop-helix class of transcription factors. Proc Natl Acad Sci U S A 94:5172–5176

    Article  CAS  PubMed  PubMed Central  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 

  • Bailey PC, Martin C, Toledo-Ortiz G, Quail PH, Huq E, Heim MA, Jakoby M, Werber M, Weisshaar B (2003) Update on the basic helix-loop-helix transcription factor gene family in Arabidopsis thaliana. Plant Cell 15:2497–2502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brzezniak LK, Bijata M, Szczesny RJ, Stepien PP (2011) Involvement of human ELAC2 gene product in 3′ end processing of mitochondrial tRNAs. RNA Biol 8:616–626

    Article  CAS  PubMed  Google Scholar 

  • Cao H, Huang P, Yan Y, Shi Y, Dong B, Liu X, Ye L, Lin F, Lu J (2018) The basic helix-loop-helix transcription factor Crf1 is required for development and pathogenicity of the rice blast fungus by regulating carbohydrate and lipid metabolism. Environ Microbiol 20:3427–3441

    Article  CAS  PubMed  Google Scholar 

  • Chen HC, Cheng WH, Hong CY, Chang YS, Chang MC (2018) The transcription factor OsbHLH035 mediates seed germination and enables seedling recovery from salt stress through ABA-dependent and ABA-independent pathways, respectively. Rice 11:50

    Article  PubMed  PubMed Central  Google Scholar 

  • Cheng X, Zhu L, He G (2013) Towards understanding of molecular interactions between rice and the brown planthopper. Mol Plant 6:621–634

    Article  CAS  PubMed  Google Scholar 

  • Ding J, Lu Q, Ouyang Y, Mao H, Zhang P, Yao J, Xu C, Li X, Xiao J, Zhang Q (2012) A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice. Proc Natl Acad Sci U S A 109:2654–2659

    Article  PubMed  PubMed Central  Google Scholar 

  • Fan Y, Zhang Q (2018) Genetic and molecular characterization of photoperiod and thermo-sensitive male sterility in rice. Plant Reprod 31:3–14

    Article  CAS  PubMed  Google Scholar 

  • Fan L, Wang Z, Liu J, Guo W, Yan J, Huang Y (2011) A survey of green plant tRNA 3′-end processing enzyme tRNase Zs, homologs of the candidate prostate cancer susceptibility protein ELAC2. BMC Evol Biol 11:219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fisher A, Caudy M (1998) The function of hairy-related bHLH repressor proteins in cell fate decisions. BioEssays 20:298–306

    Article  CAS  PubMed  Google Scholar 

  • Geng J, Liu JH (2018) The transcription factor CsbHLH18 of sweet orange functions in modulation of cold tolerance and homeostasis of reactive oxygen species by regulating the antioxidant gene. J Exp Bot 69:2677–2692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goding CR (2000) Mitf from neural crest to melanoma: signal transduction and transcription in the melanocyte lineage. Genes Dev 14:1712–1728

    CAS  PubMed  Google Scholar 

  • Heim MA, Jakoby M, Werber M, Martin C, Weisshaar B, Bailey PC (2003) The basic helix-loop-helix transcription factor family in plants: a genome-wide study of protein structure and functional diversity. Mol Biol Evol 20:735–747

    Article  CAS  PubMed  Google Scholar 

  • Hellens RP, Allan AC, Friel EN, Bolitho K, Grafton K, Templeton MD, Karunairetnam S, Gleave AP, Laing WA (2005) Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods 1:13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Henriksson M, Luscher B (1996) Proteins of the Myc network: essential regulators of cell growth and differentiation. Adv Cancer Res 68:109–182

    Article  CAS  PubMed  Google Scholar 

  • Huai J, Zhang X, Li J, Ma T, Zha P, Jing Y, Lin R (2018) SEUSS and PIF4 coordinately regulate light and temperature signaling pathways to control plant growth. Mol Plant 11:928–942

    Article  CAS  PubMed  Google Scholar 

  • Huq E, Quail PH (2002) PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis. EMBO J 21:2441–2450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kay S, Hahn S, Marois E, Hause G, Bonas U (2007) A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science 318:648–651

    Article  CAS  PubMed  Google Scholar 

  • Li de la Sierra-Gallay I, Pellegrini O, Condon C (2005) Structural basis for substrate binding, cleavage and allostery in the tRNA maturase RNase Z. Nature 433:657–661

    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, Ma H, Wang J, Zhang D (2006) Genome-wide analysis of basic/helix-loop-helix transcription factor family in rice and Arabidopsis. Plant Physiol 141:1167–1184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Massari ME, Murre C (2000) Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol Cell Biol 20:429–440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Minagawa A, Takaku H, Takagi M, Nashimoto M (2004) A novel endonucleolytic mechanism to generate the CCA 3′ termini of tRNA molecules in Thermotoga maritima. J Biol Chem 279:15688–15697

    Article  CAS  PubMed  Google Scholar 

  • Poirier BC, Feldman MJ, Lange BM (2018) bHLH093/NFL and bHLH061 are required for apical meristem function in Arabidopsis thaliana. Plant Signal Behav 13:e1486146

    Article  CAS  PubMed  Google Scholar 

  • Shi Q, Zhang H, Song X, Jiang Y, Liang R, Li G (2017) Functional characterization of the maize phytochrome-interacting factors PIF4 and PIF5. Front Plant Sci 8:2273

    Article  PubMed  Google Scholar 

  • Steidl C, Leimeister C, Klamt B, Maier M, Nanda I, Dixon M, Clarke R, Schmid M, Gessler M (2000) Characterization of the human and mouse HEY1, HEY2, and HEYL genes: cloning, mapping, and mutation screening of a new bHLH gene family. Genomics 66:195–203

    Article  CAS  PubMed  Google Scholar 

  • Sun X, Wang Y, Sui N (2018) Transcriptional regulation of bHLH during plant response to stress. Biochem Biophys Res Commun 503:397–401

    Article  CAS  PubMed  Google Scholar 

  • Weng J, Gu S, Wan X, Gao H, Guo T, Su N, Lei C, Zhang X, Cheng Z, Guo X, Wang J, Jiang L, Zhai H, Wan J (2008) Isolation and initial characterization of GW5, a major QTL associated with rice grain width and weight. Cell Res 18:1199–1209

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Ren Y, Cai Y, Niu M, Feng Z, Jing R, Mou C, Liu X, Xiao L, Zhang X, Wu F, Guo X, Jiang L, Wan J (2018) Overexpression of OsbHLH107, a member of the basic helix-loop-helix transcription factor family, enhances grain size in rice (Oryza sativa L.). Rice (N Y) 11:41

    Article  Google Scholar 

  • Zhang H, Xu C, He Y, Zong J, Yang X, Si H, Sun Z, Hu J, Liang W, Zhang D (2013) Mutation in CSA creates a new photoperiod-sensitive genic male sterile line applicable for hybrid rice seed production. Proc Natl Acad Sci U S A 110:76–81

    Article  PubMed  Google Scholar 

  • Zhou H, Zhou M, Yang Y, Li J, Zhu L, Jiang D, Dong J, Liu Q, Gu L, Zhou L, Feng M, Qin P, Hu X, Song C, Shi J, Song X, Ni E, Wu X, Deng Q, Liu Z, Chen M, Liu YG, Cao X, Zhuang C (2014) RNase ZS1 processes Ub L40 mRNAs and controls thermosensitive genic male sterility in rice. Nat Commun 5:4884

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was partly granted from the National Transgenic Research Program (2016ZX08001004-001-002), National Key Research and Development Program (2016YFD0100903) of China and Huanghe Patent Program of Wuhan City.

Author information

Authors and Affiliations

  1. State Key Laboratory of Hybrid Rice, Key Laboratory for Research and Utilization of Heterosis in Indica Rice of Ministry of Agriculture, Engineering Research Center for Plant Biotechnology and Germplasm Utilization of Ministry of Education, College of Life Science, Wuhan University, Wuhan, 430072, China

    Jianyu Wen, Liuting Wang, Jie Wang, Yafei Zeng, Yanghong Xu & Shaoqing Li

Authors
  1. Jianyu Wen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Liuting Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jie Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yafei Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yanghong Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shaoqing Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shaoqing Li.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Jianbing Yan.

Publisher's Note

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

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wen, J., Wang, L., Wang, J. et al. The transcription factor OsbHLH138 regulates thermosensitive genic male sterility in rice via activation of TMS5. Theor Appl Genet 132, 1721–1732 (2019). https://doi.org/10.1007/s00122-019-03310-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-019-03310-7

Search

Navigation