Skip to main content
Log in

Functional Analysis of Wheat TaPaO1 Gene Conferring Pollen Sterility Under Low Temperature

  • Original Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Thermosensitive male sterility plays an important role in wheat fertility and production. As a key enzyme for chlorophyll degradation, pheophorbide a oxygenase (PaO) can suppress cell death in plants. We cloned the wheat gene TaPaO1 from the thermosensitive genetic male sterile (TGMS) line BS366; it encodes a typical PaO protein, containing a conserved Rieske [2Fe-2S] iron–sulphur motif, a mononuclear non-heme iron-binding motif, and a C-terminal CxxC motif. TaPaO1 was expressed in all tissues and was upregulated during the meiosis stage of BS366 anthers under low temperature. Subcellular localization of TaPaO1 specifically labelled the surrounding of chloroplasts. TaPaO1 regulated by RD29A promoter which responded to low temperature led to pollen sterility in transgenic tobacco. Expression analysis showed that TaPaO1 exhibited a higher level of expression in the anther than in other tissues in transgenic tobacco plants during low temperature treatment. We propose that the higher senescence-related activity of TaPaO1 may lead to the cell death of anthers, which happens at an early developmental stage under low temperature. These results provide new insights into the function of PaO during the early developmental stage of anthers. PaO is closely related to cell death regardless of whether it exhibits increased activity or inactive.

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.

Similar content being viewed by others

References

  • Buchanan-Wollaston V (1997) The molecular of leaf senescence. J Exp Bot 48:181–199

    Article  Google Scholar 

  • Chen L, Liu YG (2014) Male Sterility and Fertility Restoration in Crops. Annu. Rev. Plant Bio l65:579–606

    Article  Google Scholar 

  • Gray J, Buckner DJ, Buckner B, Close PS, Johal GS (2002) Lightdependent death of maize lls1 cells is mediated by mature chloroplasts. Plant Physiol 130:1894–1907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gray J, Close PS, Briggs SP, Johal GS (1997) A novel suppressor of cell death in plants encoded by the Lls1 gene of maize. Cell 89: 25–31

    Article  CAS  PubMed  Google Scholar 

  • Greenberg JT, Ausubel FM (1993) Arabidopsis mutants compromised for the control of cellular damage during pathogenesis and aging. Plant J 4:327–341

    Article  CAS  PubMed  Google Scholar 

  • Guttman M, Rinn JL (2012) Modular regulatory principles of large non-coding RNAs. Nature 482:339–346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hörtensteiner S, Kra¨utler B (2011) Chlorophyll breakdown in higher plants. Biochim. Biophys. Acta 1807:977–988

    Google Scholar 

  • Hörtensteiner S (1999) Chlorophyll breakdown in higher plants and algae. Cell Mol Life Sci 56:330–347

    Article  PubMed  Google Scholar 

  • Hörtensteiner S, Rodoni S, Schellenberg M, Vicentini F, Nandi OI, Qiu YL, Matil P (2000) Evolution of chlorophyll degradation: the significance of RCC reductase. Plant Biol 2:63–67

    Article  Google Scholar 

  • Hörtensteiner S, Wüthrich KL, Matile P, Ongania KH, Kräutler B (1998) The key step in chlorophyll breakdown in higher plants. Cleavage of pheophorbide a macrocycle by a monooxygenase. J Biol Chem 273:15335–15339

    Article  PubMed  Google Scholar 

  • Joyard J, Ferro M, Masselon C, Seigneurin-Berny D, Salvi D, Garin J, and Rolland N. (2009) Chloroplast proteomics and the compartmentation of plastidial isoprenoid biosynthetic pathways. Mol. Plant 2:1154–1180

    CAS  Google Scholar 

  • Li P, Ma Y, Li X, Zhang L, Wang Y, Wang N (2006) Cloning and expressional characterization of soybean GmLls1 gene. Chin Sci Bull 51:1210–1218

    Article  CAS  Google Scholar 

  • Mach JM, Castillo AR, Hoogstraten R, Greenberg JT (2001) The Arabidopsis-accelerated cell death gene ACD2 encodes red chlorophyll catabolite reductase and suppresses the spread of disease symptoms. Proc. Natl. Acad. Sci. USA. 98:771–776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma N, Ma X, Li AF, Cao XC, Kong LR (2012) Cloning and expression analysis of wheat pheophorbide a oxygenase gene TaPaO. Plant MolBiol Rep 30:1237–1245

    Article  CAS  Google Scholar 

  • Matile, P and Schellenberg, M (1996) The cleavage of pheophorbide a is located in the envelope of barley gerontoplasts. Plant Physiol.Biochem 34:55–59

    CAS  Google Scholar 

  • Murray M, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakashima K, Fujita Y, Katsura K, Maruyama K, Narusaka Y, Seki M, Yamaguchi-Shinozaki K (2006) Transcriptional regulation of ABI3-and ABA-responsive genes including RD29B and RD29A in seeds, germinating embryos, and seedlings of Arabidopsis. Plant Mol Biol 60:51–68

    Article  CAS  PubMed  Google Scholar 

  • Peterson R, Slovin JP, Chen CB (2010) A simplifed method for differential staining of aborted and non-aborted pollen grains. Internation of Plant Biology 1: e13

    Article  Google Scholar 

  • Pruźinská A, Tanner G, Anders I, Roca M, Hörtensteiner S (2003) Chlorophyll breakdown: Pheophorbide a oxygenase is a Riesketype iron-sulfur protein, encoded by the accelerated cell death 1 gene. Proc. Natl. Acad. Sci. USA. 100: 15259–15264

    Article  PubMed  PubMed Central  Google Scholar 

  • Pruźinská A, Tanner G, Aubry S, Anders I, Moser S, Müller T, Ongania KH, Kraütler B, Youn JY, Liljegren SJ, and Hörtensteiner S (2005) Chlorophyll breakdown in senescent Arabidopsis leaves. Characterization of chlorophyll catabolites and of chlorophyll catabolic enzymes involved in the degreening reaction. Plant Physiol 139:52–63

    Article  PubMed  PubMed Central  Google Scholar 

  • Sakuraba Y, Schelbert S, Park SY, Han SH, Lee BD, Andrès CB, Kessler F, Hörtensteiner S and Paek NC (2012) Stay-green and chlorophyll catabolic enzymes interact at light-harvesting complex II for chlorophyll detoxification during leaf senescence in Arabidopsis. Plant Cell 24:507–518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spassieva S, Hille J (2002) A lesion mimic phenotype in tomato obtained by isolating and silencing an Lls1 homologue. Plant Sci 162:543–549

    Article  CAS  Google Scholar 

  • Tanaka R, Hirashima M, Satoh S, Tanaka A (2003) The Arabidopsis-accelerated cell death gene ACD1 is involved in oxygenation of pheophorbide a: inhibition of pheophorbide a oxygenase activity does not lead to the “stay-green” phenotype in Arabidopsis. Plant Cell Physiol 44:1266–1274

    Article  CAS  PubMed  Google Scholar 

  • Tang Y, Li M, Chen Y, Wu P, Wu G, Jiang H (2011) Knockdown of OsPAO and OsRCCR1 cause different plant death phenotypes in rice. J Plant Physiol 168:1952–1959

    Article  CAS  PubMed  Google Scholar 

  • Tang Z, Zhang L, Yang D, Zhao C, Zheng Y (2011) Cold stress contributes to aberrant cytokinesis during male meiosis I in a wheat thermosensitive genic male sterile line. Plant Cell Environ 34:389–405

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki K, Koisumi M, Urao S, Shinozaki K (1992) Molecular cloning and characterization of 9 cDNAs genes that are responsive to desiccation in Arabidopsis thaliana: sequence analysis of one cDNA clone that encodes a putative transmembrane channel protein. Plant Cell Physiol 33:217–224

    Article  CAS  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (1993a) Arabidopsis DNA encoding two desiccation-responsive rd29 genes. Plant Physiol 101:1119–1120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (1993b) Characterization of the expression of a desiccation-responsive rd29 gene of Arabidopsis thaliana and analysis of its promoter in transgenic plants. Mol Gen Genet 236:331–340

    Article  CAS  PubMed  Google Scholar 

  • Yang M, Wardzala E, Johal GS, Gray J (2004) The wound-inducible Lls1 gene from maize is an orthologue of the Arabidopsis Acd1 gene, and the LLS1 protein is present in non-photosynthstic tissues. Plant Mol Biol 54:175–191

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Li J, Liu A, Zou J, Zhou X, Xiang J, Rerksiri W, Peng Y, Xiong X, Chen X (2012) Expression profile in rice panicle: insights into heat response mechanism at reproductive stage. PLoS One 7: e49652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Liping Zhang or Changping Zhao.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yuan, G., Wang, Y., Yuan, S. et al. Functional Analysis of Wheat TaPaO1 Gene Conferring Pollen Sterility Under Low Temperature. J. Plant Biol. 61, 25–32 (2018). https://doi.org/10.1007/s12374-017-0269-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-017-0269-7

Keywords

Navigation