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.

  • Article
  • Published:

OsFTIP7 determines auxin-mediated anther dehiscence in rice

Nature Plants volume 4, pages 495–504 (2018)Cite this article

Subjects

An Author Correction to this article was published on 02 November 2018

This article has been updated

Abstract

Anther dehiscence determines successful sexual reproduction of flowering plants through timely release of pollen grains for pollination and fertilization. Downregulation of auxin levels during pollen mitosis is essential for promoting anther dehiscence along with pollen maturation. How this key transition of auxin levels is regulated in male organs remains elusive. Here, we report that the rice FT-INTERACTING PROTEIN 7 is highly expressed in anthers before pollen mitotic divisions and facilitates nuclear translocation of a homeodomain transcription factor, Oryza sativa homeobox 1, which directly suppresses a predominant auxin biosynthetic gene, OsYUCCA4, during the late development of anthers. This confers a key switch of auxin levels between meiosis of microspore mother cells and pollen mitotic divisions, thus controlling the timing of anther dehiscence during rice anthesis. Our findings shed light on the mechanism of hormonal control of anther dehiscence, and provide a new avenue for creating hormone-sensitive male sterile lines for hybrid plant breeding.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Fig. 1: Osftip7 mutants are male sterile.
Fig. 2: Expression patterns of OsFTIP7.
Fig. 3: OsFTIP7 affects auxin biosynthesis during anther development.
Fig. 4: OsFTIP7 interacts with OSH1.
Fig. 5: OSH1 regulates auxin biosynthesis in anthers via directly repressing OsYUCCA4.
Fig. 6: OsFTIP7 mediates nucleocytoplasmic distribution of OSH1 in anthers.

Similar content being viewed by others

Change history

  • 02 November 2018

    In the version of this Article originally published, an incorrect immunoblot was used in the left, middle panel of Fig. 6a, which describes α-tubulin expression in whole-cell extracts. This panel, and the corresponding quantitative result shown in Supplementary Fig. 11e, have now been corrected in the Article. This does not affect the results or conclusions of this work.

References

  1. Wilson, Z. A., Song, J., Taylor, B. & Yang, C. The final split: the regulation of anther dehiscence. J. Exp. Bot. 62, 1633–1649 (2011).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  3. Ishiguro, S., Kawai-Oda, A., Ueda, J., Nishida, I. & Okada, K. The DEFECTIVE IN ANTHER DEHISCENCE1 gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell 13, 2191–2209 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Sanders, P. M. et al. The Arabidopsis DELAYED DEHISCENCE1 gene encodes an enzyme in the jasmonic acid synthesis pathway. Plant Cell 12, 1041–1061 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Stintzi, A. The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proc. Natl Acad. Sci. USA 97, 10625–10630 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Devoto, A. et al. COI1 links jasmonate signalling and fertility to the SCF ubiquitin–ligase complex in Arabidopsis. Plant J. 32, 457–466 (2002).

    Article  CAS  PubMed  Google Scholar 

  7. Xie, D.-X., Feys, B. F., James, S., Nieto-Rostro, M. & Turner, J. G. COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280, 1091–1094 (1998).

    Article  CAS  PubMed  Google Scholar 

  8. Sanders, P. M. et al. Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex. Plant Reprod. 11, 297–322 (1999).

    Article  CAS  Google Scholar 

  9. Nagpal, P. et al. Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132, 4107–4118 (2005).

    Article  CAS  PubMed  Google Scholar 

  10. Cheng, Y., Dai, X. & Zhao, Y. Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev. 20, 1790 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Cecchetti, V., Altamura, M. M., Falasca, G., Costantino, P. & Cardarelli, M. Auxin regulates Arabidopsis anther dehiscence, pollen maturation, and filament elongation. Plant Cell 20, 1760–1774 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Tabata, R. et al. Arabidopsis AUXIN RESPONSE FACTOR6 and 8 regulate jasmonic acid biosynthesis and floral organ development via repression of class 1 KNOX genes. Plant Cell Physiol. 51, 164–175 (2010).

    Article  CAS  PubMed  Google Scholar 

  13. Cecchetti, V. et al. Auxin controls Arabidopsis anther dehiscence by regulating endothecium lignification and jasmonic acid biosynthesis. Plant J. 74, 411–422 (2013).

    Article  CAS  PubMed  Google Scholar 

  14. Cecchetti, V. et al. An auxin maximum in the middle layer controls stamen development and pollen maturation in Arabidopsis. New Phytol. 213, 1194–1207 (2017).

    Article  CAS  PubMed  Google Scholar 

  15. Zhao, Z. et al. A role for a dioxygenase in auxin metabolism and reproductive development in rice. Dev. Cell 27, 113–122 (2013).

    Article  CAS  PubMed  Google Scholar 

  16. Liu, L., Zhu, Y., Shen, L. & Yu, H. Emerging insights into florigen transport. Curr. Opin. Plant Biol. 16, 607–613 (2013).

    Article  CAS  PubMed  Google Scholar 

  17. Liu, L., Li, C., Liang, Z. & Yu, H. Characterization of multiple C2 domain and transmembrane region proteins in Arabidopsis. Plant Physiol. 176, 2119–2132 (2018).

    Article  CAS  PubMed  Google Scholar 

  18. Feng, Z. et al. Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proc. Natl Acad. Sci. USA 111, 4632–4637 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Song, S. et al. OsFTIP1-mediated regulation of florigen transport in rice is negatively regulated by the ubiquitin-like domain kinase OsUbDKγ4. Plant Cell 29, 491–507 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Liu, L. et al. FTIP1 is an essential regulator required for florigen transport. PLoS Biol. 10, e1001313 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Zhang, D. & Wilson, Z. A. Stamen specification and anther development in rice. Chin. Sci. Bull. 54, 2342–2353 (2009).

    Article  CAS  Google Scholar 

  22. Zhang, D., Luo, X. & Zhu, L. Cytological analysis and genetic control of rice anther development. J. Genet. Genom. 38, 379–390 (2011).

    Article  CAS  Google Scholar 

  23. Giordano, F. et al. PI(4,5)P(2)-dependent and Ca2+-regulated ER-PM interactions mediated by the extended synaptotagmins. Cell 153, 1494–1509 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Zhao, Y. Auxin biosynthesis and its role in plant development. Annu. Rev. Plant Biol. 61, 49–64 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Korasick, D. A., Enders, T. A. & Strader, L. C. Auxin biosynthesis and storage forms. J. Exp. Bot. 64, 2541–2555 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Yamamoto, Y., Kamiya, N., Morinaka, Y., Matsuoka, M. & Sazuka, T. Auxin biosynthesis by the YUCCA genes in rice. Plant Physiol. 143, 1362–1371 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Ulmasov, T., Murfett, J., Hagen, G. & Guilfoyle, T. J. Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9, 1963–1971 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Tsuda, K., Ito, Y., Sato, Y. & Kurata, N. Positive autoregulation of a KNOX gene is essential for shoot apical meristem maintenance in rice. Plant Cell 23, 4368–4381 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Burglin, T. R. Analysis of TALE superclass homeobox genes (MEIS, PBC, KNOX, Iroquois, TGIF) reveals a novel domain conserved between plants and animals. Nucleic Acids Res. 25, 4173–4180 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Sentoku, N., Sato, Y. & Matsuoka, M. Overexpression of rice OSH genes induces ectopic shoots on leaf sheaths of transgenic rice plants. Dev. Biol. 220, 358–364 (2000).

    Article  CAS  PubMed  Google Scholar 

  31. Tsuda, K., Kurata, N., Ohyanagi, H. & Hake, S. Genome-wide study of KNOX regulatory network reveals brassinosteroid catabolic genes important for shoot meristem function in rice. Plant Cell 26, 3488–3500 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Bolduc, N. & Hake, S. The maize transcription factor KNOTTED1 directly regulates the gibberellin catabolism gene ga2ox1. Plant Cell 21, 1647–1658 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Goldberg, R. B., Beals, T. P. & Sanders, P. M. Anther development: basic principles and practical applications. Plant Cell 5, 1217 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Reeves, P. H. et al. A regulatory network for coordinated flower maturation. PLoS Genet. 8, e1002506 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Cole, M., Nolte, C. & Werr, W. Nuclear import of the transcription factor SHOOT MERISTEMLESS depends on heterodimerization with BLH proteins expressed in discrete sub-domains of the shoot apical meristem of Arabidopsis thaliana. Nucleic Acids Res. 34, 1281–1292 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Rutjens, B. et al. Shoot apical meristem function in Arabidopsis requires the combined activities of three BEL1-like homeodomain proteins. Plant J. 58, 641–654 (2009).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  38. Kuroda, M., Kimizu, M. & Mikami, C. A simple set of plasmids for the production of transgenic plants. Biosci. Biotechnol. Biochem. 74, 2348–2351 (2010).

    Article  CAS  PubMed  Google Scholar 

  39. Toki, S. et al. Early infection of scutellum tissue with Agrobacterium allows high‐speed transformation of rice. Plant J. 47, 969–976 (2006).

    Article  CAS  PubMed  Google Scholar 

  40. Liu, C. et al. Specification of Arabidopsis floral meristem identity by repression of flowering time genes. Development 134, 1901–1910 (2007).

    Article  CAS  PubMed  Google Scholar 

  41. Li, D. et al. A repressor complex governs the integration of flowering signals in Arabidopsis. Dev. Cell 15, 110–120 (2008).

    Article  CAS  PubMed  Google Scholar 

  42. Saleh, A., Alvarez-Venegas, R. & Avramova, Z. An efficient chromatin immunoprecipitation (ChIP) protocol for studying histone modifications in Arabidopsis plants. Nat. Protoc. 3, 1018–1025 (2008).

    Article  CAS  PubMed  Google Scholar 

  43. Liu, S., Chen, W., Qu, L., Gai, Y. & Jiang, X. Simultaneous determination of 24 or more acidic and alkaline phytohormones in femtomole quantities of plant tissues by high-performance liquid chromatography–electrospray ionization–ion trap mass spectrometry. Anal. Bioanal. Chem. 405, 1257–1266 (2013).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Z. He and J.-K. Zhu for providing the BAC clone and psgR-CAS9-Os vector, and members of the Yu lab for discussion and comments on the manuscript. This work was supported by the Singapore National Research Foundation Investigatorship Programme (NRF-NRFI2016-02), the National Natural Science Foundation of China (grant no. 31529001), the Ministry of Education and Bureau of Foreign Experts of China (grant B14027), and the intramural research support from National University of Singapore and Temasek Life Sciences Laboratory.

Author information

Author notes

  1. These authors contributed equally: Shiyong Song, Ying Chen.

Authors and Affiliations

  1. Department of Biological Sciences and Temasek Life Sciences Laboratory, National University of Singapore, Singapore, Singapore

    Shiyong Song, Ying Chen, Lu Liu, Yen How Benjamin See & Hao Yu

  2. College of Life Science, Zhejiang University, Hangzhou, China

    Chuanzao Mao

  3. College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, China

    Yinbo Gan

Authors
  1. Shiyong Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ying Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lu Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yen How Benjamin See
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chuanzao Mao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yinbo Gan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hao Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

S.S., Y.C. and H.Y. conceived the project; S.S. and Y.C. performed most of the experiments; L.L. participated in investigating the link between OsFTIP7 and OSH1; Y.H.B.S. conducted part of the rice transformation. S.S. and Y.C. conducted all statistical analyses; S.S., Y.C., C.M., Y.G. and H.Y. analysed data; S.S., Y.C. and H.Y. wrote the paper.

Corresponding author

Correspondence to Hao Yu.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

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

Supplementary information

Supplementary Information

Supplementary Figures 1–13 and Supplementary 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

Song, S., Chen, Y., Liu, L. et al. OsFTIP7 determines auxin-mediated anther dehiscence in rice. Nature Plants 4, 495–504 (2018). https://doi.org/10.1038/s41477-018-0175-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41477-018-0175-0

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