Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Slowing development restores the fertility of thermo-sensitive male-sterile plant lines

Nature Plants volume 6, pages 360–367 (2020)Cite this article

Subjects

Abstract

Temperature-sensitive genic male sterility (TGMS) lines are widely used in the breeding of hybrid crops1,2, but by what means temperature as a general environmental factor reverses the fertility of different TGMS lines remains unknown. Here, we identified an Arabidopsis TGMS line named reversible male sterile (rvms) that is fertile at low temperature (17 °C) and encodes a GDSL lipase. Cytological observations and statistical analysis showed that low temperature slows pollen development. Further screening of restorers of rvms, as well as crossing with a slow-growth line at normal temperature (24 °C), demonstrate that slowing of development overcomes the defects of rvms microspores and allows them to develop into functional pollen. Several other Arabidopsis TGMS lines were identified, and their fertility was also restored by slowing of development. Given that male reproductive development is conserved3, we propose that slowing of development is a general mechanism applicable to the sterility–fertility conversion of TGMS lines from different plant species.

Access through your institution
Buy or subscribe

This is a preview of subscription content, access via your institution

Access options

Access through your institution

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: rvms, a mutant of a GDSL lipase, displays temperature-dependent male sterility.
Fig. 2: Pollen development is slower at low temperature.
Fig. 3: res1 exhibits delayed and asynchronous cell division during meiosis in the restoration of rvms fertility.
Fig. 4: Slow pollen development is a general mechanism capable of restoring fertility in other Arabidopsis TGMS mutants.

Similar content being viewed by others

Data availability

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

References

  1. Chen, L. & Liu, Y. G. Male sterility and fertility restoration in crops. Annu. Rev. Plant Biol. 65, 579–606 (2014).

    Article  CAS  Google Scholar 

  2. Virmani, S. S. & Ilyas-Ahmed, M. Environment-sensitive genic male sterility (EGMS) in crops. Adv. Agron. 72, 139–195 (2001).

    Article  CAS  Google Scholar 

  3. Gómez, J. F., Talle, B. & Wilson, Z. A. Anther and pollen development: a conserved developmental pathway. J. Integr. Plant Biol. 57, 876–891 (2015).

    Article  Google Scholar 

  4. Hochholdinger, F. & Hoecker, N. Towards the molecular basis of heterosis. Trends Plant Sci. 12, 427–432 (2007).

    Article  CAS  Google Scholar 

  5. Tester, M. & Langridge, P. Breeding technologies to increase crop production in a changing world. Science 327, 818–822 (2010).

    Article  CAS  Google Scholar 

  6. Zhang, Q. et al. Using bulked extremes and recessive class to map genes for photoperiod-sensitive genic male sterility in rice. Proc. Natl Acad. Sci. USA 91, 8675–8679 (1994).

    Article  CAS  Google Scholar 

  7. Wang, H. et al. The Arabidopsis U-box/ARM repeat E3 ligase AtPUB4 influences growth and degeneration of tapetal cells, and its mutation leads to conditional male sterility. Plant J. 74, 511–523 (2013).

    Article  CAS  Google Scholar 

  8. Millar, A. A. & Gubler, F. The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell 17, 705–721 (2005).

    Article  CAS  Google Scholar 

  9. Zhou, H. et al. Photoperiod- and thermo-sensitive genic male sterility in rice are caused by a point mutation in a novel noncoding RNA that produces a small RNA. Cell Res. 22, 649–660 (2012).

    Article  CAS  Google Scholar 

  10. Ding, J. et al. A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice. Proc. Natl Acad. Sci. USA 109, 2654–2659 (2012).

    Article  CAS  Google Scholar 

  11. Fan, Y. et al. PMS1T, producing phased small-interfering RNAs, regulates photoperiod-sensitive male sterility in rice. Proc. Natl Acad. Sci. USA 113, 15144–15149 (2016).

    Article  CAS  Google Scholar 

  12. Zhou, H. et al. RNase ZS1 processes Ub L40 mRNAs and controls thermosensitive genic male sterility in rice. Nat. Commun. 5, 4884 (2014).

    Article  CAS  Google Scholar 

  13. Chen, R. Z. et al. Rice UDP-glucose pyrophosphorylase1 is essential for pollen callose deposition and its cosuppression results in a new type of thermosensitive genic male sterility. Plant Cell 19, 847–861 (2007).

    Article  CAS  Google Scholar 

  14. Yu, J. et al. Two rice receptor-like kinases maintain male fertility under changing temperatures. Proc. Natl Acad. Sci. USA 114, 12327–12332 (2017).

    Article  CAS  Google Scholar 

  15. Shi, J., Cui, M., Yang, L., Kim, Y. J. & Zhang, D. Genetic and biochemical mechanisms of pollen wall development. Trends Plant Sci. 20, 741–753 (2015).

    Article  CAS  Google Scholar 

  16. Akoh, C. C., Lee, G. C., Liaw, Y. C., Huang, T. H. & Shaw, J. F. GDSL family of serine esterases/lipases. Prog. Lipid Res. 43, 534–552 (2004).

    Article  CAS  Google Scholar 

  17. Ma, H. Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu. Rev. Plant Biol. 56, 393–434 (2005).

    Article  CAS  Google Scholar 

  18. Iwakawa, H., Shinmyo, A. & Sekine, M. Arabidopsis CDKA;1, a cdc2 homologue, controls proliferation of generative cells in male gametogenesis. Plant J. 45, 819–831 (2006).

    Article  CAS  Google Scholar 

  19. Wijnker, E. et al. The Cdk1/Cdk2 homolog CDKA;1 controls the recombination landscape in Arabidopsis. Proc. Natl Acad. Sci. USA 116, 12534–12539 (2019).

    Article  CAS  Google Scholar 

  20. Magnard, J. L., Yang, M., Chen, Y. C., Leary, M. & McCormick, S. The Arabidopsis gene tardy asynchronous meiosis is required for the normal pace and synchrony of cell division during male meiosis. Plant Physiol. 127, 1157–1166 (2001).

    Article  CAS  Google Scholar 

  21. Wang, Y., Magnard, J. L., McCormick, S. & Yang, M. Progression through meiosis I and meiosis II in Arabidopsis anthers is regulated by an A-type cyclin predominately expressed in prophase I. Plant Physiol. 136, 4127–4135 (2004).

    Article  CAS  Google Scholar 

  22. Cromer, L. et al. OSD1 promotes meiotic progression via APC/C inhibition and forms a regulatory network with TDM and CYCA1;2/TAM. PLoS Genet. 8, e1002865 (2012).

    Article  CAS  Google Scholar 

  23. Verkest, A. et al. The cyclin-dependent kinase inhibitor KRP2 controls the onset of the endoreduplication cycle during Arabidopsis leaf development through inhibition of mitotic CDKA;1 kinase complexes. Plant Cell 17, 1723–1736 (2005).

    Article  CAS  Google Scholar 

  24. Cao, Z. L. et al. Mapping and analysis of a yellow mutant chlm-4 of Arabidopsis thaliana. Acta Bot. Yunnan. 32, 134–140 (2010).

    Article  CAS  Google Scholar 

  25. Dong, X., Hong, Z., Sivaramakrishnan, M., Mahfouz, M. & Verma, D. P. Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis. Plant J. 42, 315–328 (2005).

    Article  CAS  Google Scholar 

  26. Guan, Y. F. et al. RUPTURED POLLEN GRAIN1, a member of the MtN3/saliva gene family, is crucial for exine pattern formation and cell integrity of microspores in Arabidopsis. Plant Physiol. 147, 852–863 (2008).

    Article  CAS  Google Scholar 

  27. de Azevedo, S. C. et al. A novel fatty Acyl-CoA synthetase is required for pollen development and sporopollenin biosynthesis in Arabidopsis. Plant Cell 21, 507–525 (2009).

    Article  Google Scholar 

  28. Morant, M. et al. CYP703 is an ancient cytochrome P450 in land plants catalyzing in-chain hydroxylation of lauric acid to provide building blocks for sporopollenin synthesis in pollen. Plant Cell 19, 1473–1487 (2007).

    Article  CAS  Google Scholar 

  29. Quilichini, T. D., Friedmann, M. C., Samuels, A. L. & Douglas, C. J. ATP-binding cassette transporter G26 is required for male fertility and pollen exine formation in Arabidopsis. Plant Physiol. 154, 678–690 (2010).

    Article  CAS  Google Scholar 

  30. Cassidy, J. J. et al. Repressive gene regulation synchronizes development with cellular metabolism. Cell 178, 980–992 (2019).

    Article  CAS  Google Scholar 

  31. Yi, J. et al. Genetic and mapping analysis of Arabidopsis thaliana male sterile mutant m1502. Acta Bot. Yunnan. 28, 283–288 (2006).

    CAS  Google Scholar 

  32. Zhang, Z. B. et al. Transcription factor AtMYB103 is required for anther development by regulating tapetum development, callose dissolution and exine formation in Arabidopsis. Plant J. 52, 528–538 (2007).

    Article  CAS  Google Scholar 

  33. Lou, Y. et al. The tapetal AHL family protein TEK determines nexine formation in the pollen wall. Nat. Commun. 5, 3855 (2014).

    Article  CAS  Google Scholar 

  34. Lou, Y. et al. Positive regulation of AMS by TDF1 and the formation of a TDF1-AMS complex are required for anther development in Arabidopsis thaliana. New Phytol. 217, 378–391 (2018).

    Article  CAS  Google Scholar 

  35. Huang, X. Y. et al. CYCLIN-DEPENDENT KINASE G1 is associated with the spliceosome to regulate CALLOSE SYNTHASE5 splicing and pollen wall formation in Arabidopsis. Plant Cell 25, 637–648 (2013).

    Article  CAS  Google Scholar 

  36. Wang, S. et al. Dissecting a heterotic gene through GradedPool-Seq mapping informs a rice-improvement strategy. Nat. Commun. 10, 2982 (2019).

    Article  Google Scholar 

Download references

Acknowledgements

We thank H. Huang, L. Xu, J.-D. Rochaix, S. McCormick, J. Xu, L.-W. Peng and L. Zhang for discussions about this manuscript. This work was supported by grants from the National Key Research and Development Program of China (no. 2016YFD0100902), National Science Foundation of China (nos. 31770348 and 31600243), Science and Technology Commission of Shanghai Municipality (nos. 18DZ2260500 and 17DZ2252700) and the Innovation Program of Shanghai Municipal Education Commission (no. 2019-01-07-00-02-E00006).

Author information

Author notes

  1. These authors contributed equally: Jun Zhu, Yue Lou, Qiang-Sheng Shi and Sen Zhang.

Authors and Affiliations

  1. Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, China

    Jun Zhu, Yue Lou, Qiang-Sheng Shi, Sen Zhang, Wen-Tao Zhou, Jun Yang, Cheng Zhang, Xiao-Zhen Yao, Te Xu, Jia-Li Liu, Lei Zhou, Jian-Qiao Hou, Jia-Qi Wang, Shui Wang, Xue-Hui Huang & Zhong-Nan Yang

Authors
  1. Jun Zhu
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Yue Lou
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Qiang-Sheng Shi
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Sen Zhang
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. Wen-Tao Zhou
    View author publications

    You can also search for this author inPubMed Google Scholar

  6. Jun Yang
    View author publications

    You can also search for this author inPubMed Google Scholar

  7. Cheng Zhang
    View author publications

    You can also search for this author inPubMed Google Scholar

  8. Xiao-Zhen Yao
    View author publications

    You can also search for this author inPubMed Google Scholar

  9. Te Xu
    View author publications

    You can also search for this author inPubMed Google Scholar

  10. Jia-Li Liu
    View author publications

    You can also search for this author inPubMed Google Scholar

  11. Lei Zhou
    View author publications

    You can also search for this author inPubMed Google Scholar

  12. Jian-Qiao Hou
    View author publications

    You can also search for this author inPubMed Google Scholar

  13. Jia-Qi Wang
    View author publications

    You can also search for this author inPubMed Google Scholar

  14. Shui Wang
    View author publications

    You can also search for this author inPubMed Google Scholar

  15. Xue-Hui Huang
    View author publications

    You can also search for this author inPubMed Google Scholar

  16. Zhong-Nan Yang
    View author publications

    You can also search for this author inPubMed Google Scholar

Contributions

The project leader is Z.-N.Y. Z.-N.Y. and J.Z. conceived the experiments. J.Z. and Y.L. performed thermo-sensitive phenotype analysis. Q.-S.S. and J.Z. performed statistical analysis of microspore development. Q.-S.S. contributed to analysis of restorers of rvms-2. S.Z. contributed fine mapping of RVMS. W.-T.Z. contributed enzyme activity assays. J.Y. and Y.L. performed genetic complementation. J.-Q.H. and J.-Q.W. detected the expression of RES1. C.Z., T.X., J.-L.L. and L.Z. analysed fertility restoration of pollen-wall-related mutants. X.-H.H contributed BAS-seq analysis. J.Z. and Y.L. wrote the paper with input from Z.-N.Y. S.W. and X.-Z.Y. revised the manuscript. All authors discussed the results and commented on the manuscript.

Corresponding author

Correspondence to Zhong-Nan Yang.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Nature Plants thanks Danny Geelen, Yidan Ouyang, Dabing Zhang and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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

Supplementary information

Supplementary Information

Supplementary Figs. 1–26 and Tables 1–3.

Reporting Summary

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhu, J., Lou, Y., Shi, QS. et al. Slowing development restores the fertility of thermo-sensitive male-sterile plant lines. Nat. Plants 6, 360–367 (2020). https://doi.org/10.1038/s41477-020-0622-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41477-020-0622-6

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing