Skip to main content

Thank you for visiting 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.

Control of meristem determinacy by trehalose 6-phosphate phosphatases is uncoupled from enzymatic activity


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.

Your institute does not have access to this article

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Fig. 1: TPP4 acts as a redundant backup for RA3.
Fig. 2: TPP enzymatic activity does not correlate with ear branching phenotype.
Fig. 3: RA3 localizes to nuclear and cytoplasmic speckles.

Data availability

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


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

    CAS  Article  Google Scholar 

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

    Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

  21. Li, H. Preprint at (2013).

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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    Article  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    Google Scholar 

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

    CAS  Article  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  Article  Google Scholar 

Download references


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

Authors and Affiliations



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.

Corresponding author

Correspondence to David Jackson.

Ethics declarations

Competing interests

The authors declare no competing interests.

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.

Supplementary information

Supplementary Information

Supplementary Figures 1–7.

Reporting Summary

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Claeys, H., Vi, S.L., Xu, X. et al. Control of meristem determinacy by trehalose 6-phosphate phosphatases is uncoupled from enzymatic activity. Nat. Plants 5, 352–357 (2019).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:

Further reading


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