Abstract

Meristem fate is regulated by trehalose 6-phosphate phosphatases (TPPs), but their mechanism of action remains mysterious. Loss of the maize TPPs RAMOSA3 and TPP4 leads to reduced meristem determinacy and more inflorescence branching. However, analysis of an allelic series revealed no correlation between enzymatic activity and branching, and a catalytically inactive version of RA3 complements the ra3 mutant. Together with their nuclear localization, these findings suggest a moonlighting function for TPPs.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Data availability

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

Additional information

Journal peer review information: Nature Plants thanks Yuling Jiao and 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.

References

  1. 1.

    Tanaka, W., Pautler, M., Jackson, D. & Hirano, H.-Y. Plant Cell Physiol. 54, 313–324 (2013).

  2. 2.

    van Dijken, A. J. H., Schluepmann, H. & Smeekens, S. C. M. Plant Physiol. 135, 969–977 (2004).

  3. 3.

    Satoh-Nagasawa, N., Nagasawa, N., Malcomber, S., Sakai, H. & Jackson, D. Nature 441, 227–230 (2006).

  4. 4.

    Figueroa, C. M. & Lunn, J. E. Plant Physiol. 172, 7–27 (2016).

  5. 5.

    Nunes, C. et al. Plant Physiol. 162, 1720–1732 (2013).

  6. 6.

    Figueroa, C. M. et al. Plant J. 85, 410–423 (2016).

  7. 7.

    Nuccio, M. L. et al. Nat. Biotechnol. 33, 862–869 (2015).

  8. 8.

    Griffiths, C. A. et al. Nature 540, 574–578 (2016).

  9. 9.

    Eveland, A. L. et al. Genome Res. 24, 431–443 (2014).

  10. 10.

    Kafri, R., Levy, M. & Pilpel, Y. Proc. Natl Acad. Sci. USA 103, 11653–11658 (2006).

  11. 11.

    De Virgilio, C. et al. Eur. J. Biochem. 212, 315–323 (1993).

  12. 12.

    Vandesteene, L. et al. Plant Physiol. 160, 884–896 (2012).

  13. 13.

    Kretzschmar, T. et al. Nat. Plants 1, 15124 (2015).

  14. 14.

    Copley, S. D. Bioessays 34, 578–588 (2012).

  15. 15.

    Cho, Y.-H., Yoo, S. D. & Sheen, J. Cell 127, 579–589 (2006).

  16. 16.

    Cho, Y.-H. & Yoo, S.-D. PLoS Genet. 7, e1001263 (2011).

  17. 17.

    Spector, D. L. & Lamond, A. I. Cold Spring Harb. Perspect. Biol. 3, a000646 (2011).

  18. 18.

    Brown, P. J. et al. PLoS Genet. 7, e1002383 (2011).

  19. 19.

    Hufford, M. B. et al. Nat. Genet. 44, 808–811 (2012).

  20. 20.

    Freeling, M. & Walbot, V. The Maize Handbook (Springer, 1994).

  21. 21.

    Li, H. Preprint at https://arxiv.org/abs/1303.3997 (2013).

  22. 22.

    McKenna, A. et al. Genome Res. 20, 1297–1303 (2010).

  23. 23.

    Lei, Y. et al. Mol. Plant 7, 1494–1496 (2014).

  24. 24.

    Wu, Q., Regan, M., Furukawa, H. & Jackson, D. PLoS Genet. 14, e1007374 (2018).

  25. 25.

    Char, S. N. et al. Plant Biotechnol. J. 15, 257–268 (2017).

  26. 26.

    Kim, D., Langmead, B. & Salzberg, S. L. Nat. Methods 12, 357–360 (2015).

  27. 27.

    Anders, S., Pyl, P. T. & Huber, W. Bioinformatics 31, 166–169 (2015).

  28. 28.

    Robinson, M. D., McCarthy, D. J. & Smyth, G. K. Bioinformatics 26, 139–140 (2010).

  29. 29.

    Zhou, M.-L. et al. J. Plant Growth Regul. 33, 256–271 (2014).

  30. 30.

    Jackson, D., Veit, B. & Hake, S. Development 120, 405–413 (1994).

  31. 31.

    Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N. & Sternberg, M. J. E. Nat. Protoc. 10, 845–858 (2015).

  32. 32.

    Shan, S., Min, H., Liu, T., Jiang, D. & Rao, Z. FASEB J. 30, 3989–3996 (2016).

  33. 33.

    Miao, Y. et al. Proc. Natl Acad. Sci. USA 113, 7148–7153 (2016).

  34. 34.

    Miao, Y. et al. mBio 8, e00643-17 (2017).

  35. 35.

    Asención Diez, M. D. et al. J. Biol. Chem. 292, 945–954 (2017).

  36. 36.

    Karimi, M., Inzé, D. & Depicker, A. Trends Plant Sci. 7, 193–195 (2002).

  37. 37.

    Xu, F., Copeland, C. & Li, X. Bio-protocol 5, e1520 (2015).

  38. 38.

    Voinnet, O., Rivas, S., Mestre, P. & Baulcombe, D. Plant J. 33, 949–956 (2003).

  39. 39.

    Smith, L. G., Greene, B., Veit, B. & Hake, S. Development 116, 21–30 (1992).

  40. 40.

    Turner, B. M. & Franchi, L. J. Cell Sci. 87, 269–282 (1987).

  41. 41.

    Fang, Y., Hearn, S. & Spector, D. L. Mol. Biol. Cell 15, 2664–2673 (2004).

Download references

Acknowledgements

We thank P. Van Dijck for sharing the pYX212 vector, K. Rao for discussion of RA3 protein structure, T. Mulligan for plant care, and S. Pouzet, G. Carver and all other Jackson lab summer students for their enthusiastic involvement in some of this work. This work was supported by funding from the National Science Foundation (IOS-1238202 and IOS-1755141), a collaborative agreement with Dupont Pioneer, the European Molecular Biology Organization (Long-Term Fellowship to H.C.) and the Vietnam National Foundation for Science and Technology Development (under grant number 106-NN.01-2014.48 to S.L.V.). The metabolite analysis was supported by the Max Planck Society (R.F. and J.E.L.).

Author information

Author notes

    • Son Lang Vi

    Present address: Agricultural Genetics Institute, Hanoi, Vietnam

    • Namiko Satoh-Nagasawa

    Present address: Akita Prefectural University, Akita, Japan

    • Alexander Goldshmidt

    Present address: Institute of Plant Sciences, Agricultural Research Organization, Volcani Center, Bet Dagan, Israel

    • Hajime Sakai

    Present address: Napigen, Wilmington, DE, USA

Affiliations

  1. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, NY, USA

    • Hannes Claeys
    • , Son Lang Vi
    • , Xiaosa Xu
    • , Namiko Satoh-Nagasawa
    • , Alexander Goldshmidt
    •  & David Jackson
  2. DuPont Pioneer, Wilmington, DE, USA

    • Namiko Satoh-Nagasawa
    •  & Hajime Sakai
  3. Donald Danforth Plant Science Center, St Louis, MO, USA

    • Andrea L. Eveland
  4. Max Planck Institute of Molecular Plant Physiology, Potsdam, Germany

    • Regina Feil
    •  & John E. Lunn
  5. Duke University, Durham, NC, USA

    • Grace A. Beggs
    •  & Richard G. Brennan

Authors

  1. Search for Hannes Claeys in:

  2. Search for Son Lang Vi in:

  3. Search for Xiaosa Xu in:

  4. Search for Namiko Satoh-Nagasawa in:

  5. Search for Andrea L. Eveland in:

  6. Search for Alexander Goldshmidt in:

  7. Search for Regina Feil in:

  8. Search for Grace A. Beggs in:

  9. Search for Hajime Sakai in:

  10. Search for Richard G. Brennan in:

  11. Search for John E. Lunn in:

  12. Search for David Jackson in:

Contributions

H.C. performed all experimental procedures except for those listed below, prepared figures and co-wrote the manuscript. A.G. and S.L.V. isolated and fine-mapped tpp4-1. A.L.E. analysed the tpp4-1 whole-genome sequencing data. X.X. mapped tpp4-3 and tpp4-4. N.S.-N. performed immunolocalizations, under the supervision of H.S. R.F. performed metabolite measurements, under the supervision of J.E.L., who also co-wrote the manuscript. G.A.B. performed modelling of the TPP4 structure, supervised by R.G.B. D.J. supervised the research, assisted with mutant screening and co-wrote the manuscript.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to David Jackson.

Supplementary information

  1. Supplementary Information

    Supplementary Figures 1–7.

  2. Reporting Summary

About this article

Publication history

Received

Accepted

Published

Issue Date

DOI

https://doi.org/10.1038/s41477-019-0394-z