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:

NINJA connects the co-repressor TOPLESS to jasmonate signalling

Abstract

Jasmonoyl-isoleucine (JA-Ile) is a plant hormone that regulates a broad array of plant defence and developmental processes1,2,3,4,5. JA-Ile-responsive gene expression is regulated by the transcriptional activator MYC2 that interacts physically with the jasmonate ZIM-domain (JAZ) repressor proteins. On perception of JA-Ile, JAZ proteins are degraded and JA-Ile-dependent gene expression is activated6,7. The molecular mechanisms by which JAZ proteins repress gene expression remain unknown. Here we show that the Arabidopsis JAZ proteins recruit the Groucho/Tup1-type co-repressor TOPLESS (TPL)8 and TPL-related proteins (TPRs) through a previously uncharacterized adaptor protein, designated Novel Interactor of JAZ (NINJA). NINJA acts as a transcriptional repressor whose activity is mediated by a functional TPL-binding EAR repression motif. Accordingly, both NINJA and TPL proteins function as negative regulators of jasmonate responses. Our results point to TPL proteins as general co-repressors that affect multiple signalling pathways through the interaction with specific adaptor proteins. This new insight reveals how stress-related and growth-related signalling cascades use common molecular mechanisms to regulate gene expression in plants.

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

Access options

Buy this article

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

Figure 1: NINJA interacts with JAZ proteins.
Figure 2: NINJA negatively regulates JA signalling.
Figure 3: NINJA interacts with TPL and functions as a transcriptional repressor.
Figure 4: Model for a general function of TPL proteins in plant hormone signalling.

Similar content being viewed by others

Accession codes

Primary accessions

Gene Expression Omnibus

Data deposits

The Arabidopsis Genome Initiative accession number for NINJA is At4g28910. All microarray data are deposited in GEO under accession numbers GSM484805 to GSM484812.

References

  1. Browse, J. Jasmonate passes muster: A receptor and targets for the defense hormone. Annu. Rev. Plant Biol. 60, 183–205 (2009)

    Article  CAS  Google Scholar 

  2. Kazan, K. & Manners, J. M. Jasmonate signaling: toward an integrated view. Plant Physiol. 146, 1459–1468 (2008)

    Article  CAS  Google Scholar 

  3. Wasternack, C. Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann. Bot. (Lond.) 100, 681–697 (2007)

    Article  CAS  Google Scholar 

  4. Browse, J. & Howe, G. A. New weapons and a rapid response against insect attack. Plant Physiol. 146, 832–838 (2008)

    Article  CAS  Google Scholar 

  5. Pauwels, L., Inzé, D. & Goossens, A. Jasmonate-inducible gene: what does it mean? Trends Plant Sci. 14, 87–91 (2009)

    Article  CAS  Google Scholar 

  6. Chini, A. et al. The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448, 666–671 (2007)

    Article  ADS  CAS  Google Scholar 

  7. Thines, B. et al. JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448, 661–665 (2007)

    Article  ADS  CAS  Google Scholar 

  8. Szemenyei, H., Hannon, M. & Long, J. A. TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319, 1384–1386 (2008)

    Article  ADS  CAS  Google Scholar 

  9. 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  Google Scholar 

  10. Fonseca, S. et al. (+)-7-iso-Jasmonoyl-l-isoleucine is the endogenous bioactive jasmonate. Nature Chem. Biol. 5, 344–350 (2009)

    Article  CAS  Google Scholar 

  11. Katsir, L., Schilmiller, A. L., Staswick, P. E., He, S. Y. & Howe, G. A. COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc. Natl Acad. Sci. USA 105, 7100–7105 (2008)

    Article  ADS  CAS  Google Scholar 

  12. Lorenzo, O., Chico, J. M., Sánchez-Serrano, J. J. & Solano, R. JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16, 1938–1950 (2004)

    Article  CAS  Google Scholar 

  13. Pauwels, L. et al. Mapping methyl jasmonate-mediated transcriptional reprogramming of metabolism and cell cycle progression in cultured Arabidopsis cells. Proc. Natl Acad. Sci. USA 105, 1380–1385 (2008)

    Article  ADS  CAS  Google Scholar 

  14. Van Leene, J., Witters, E., Inzé, D. & De Jaeger, G. Boosting tandem affinity purification of plant protein complexes. Trends Plant Sci. 13, 517–520 (2008)

    Article  CAS  Google Scholar 

  15. Grunewald, W. et al. Expression of the Arabidopsis jasmonate signalling repressor JAZ1/TIFY10A is stimulated by auxin. EMBO Rep. 10, 923–928 (2009)

    Article  CAS  Google Scholar 

  16. Chini, A., Fonseca, S., Chico, J. M., Fernández-Calvo, P. & Solano, R. The ZIM domain mediates homo- and heteromeric interactions between Arabidopsis JAZ proteins. Plant J. 59, 77–87 (2009)

    Article  CAS  Google Scholar 

  17. Chung, H. S. & Howe, G. A. A critical role for the TIFY motif in repression of jasmonate signaling by a stabilized splice variant of the JASMONATE ZIM-domain protein JAZ10 in Arabidopsis . Plant Cell 21, 131–145 (2009)

    Article  CAS  Google Scholar 

  18. Garcia, M. E., Lynch, T., Peeters, J., Snowden, C. & Finkelstein, R. A small plant-specific protein family of ABI five binding proteins (AFPs) regulates stress response in germinating Arabidopsis seeds and seedlings. Plant Mol. Biol. 67, 643–658 (2008)

    Article  CAS  Google Scholar 

  19. Goossens, A. et al. A functional genomics approach toward the understanding of secondary metabolism in plant cells. Proc. Natl Acad. Sci. USA 100, 8595–8600 (2003)

    Article  ADS  CAS  Google Scholar 

  20. Vanholme, B., Grunewald, W., Bateman, A., Kohchi, T. & Gheysen, G. The tify family previously known as ZIM. Trends Plant Sci. 12, 239–244 (2007)

    Article  CAS  Google Scholar 

  21. Yan, Y. et al. A downstream mediator in the growth repression limb of the jasmonate pathway. Plant Cell 19, 2470–2483 (2007)

    Article  CAS  Google Scholar 

  22. Kazan, K. Negative regulation of defence and stress genes by EAR-motif-containing repressors. Trends Plant Sci. 11, 109–112 (2006)

    Article  CAS  Google Scholar 

  23. Long, J. A., Woody, S., Poethig, S., Meyerowitz, E. M. & Barton, M. K. Transformation of shoots into roots in Arabidopsis embryos mutant at the TOPLESS locus. Development 129, 2297–2306 (2002)

    Google Scholar 

  24. Chico, J. M., Chini, A., Fonseca, S. & Solano, R. JAZ repressors set the rhythm in jasmonate signaling. Curr. Opin. Plant Biol. 11, 486–494 (2008)

    Article  CAS  Google Scholar 

  25. Gray, W. M., Kepinski, S., Rouse, D., Leyser, O. & Estelle, M. Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature 414, 271–276 (2001)

    Article  ADS  CAS  Google Scholar 

  26. White, D. W. R. PEAPOD regulates lamina size and curvature in Arabidopsis . Proc. Natl Acad. Sci. USA 103, 13238–13243 (2006)

    Article  ADS  CAS  Google Scholar 

  27. Van Leene, J. et al. A tandem affinity purification-based technology platform to study the cell cycle interactome in Arabidopsis thaliana . Mol. Cell. Proteomics 6, 1226–1238 (2007)

    Article  CAS  Google Scholar 

  28. Clough, S. J. & Bent, A. F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana . Plant J. 16, 735–743 (1998)

    Article  CAS  Google Scholar 

  29. De Sutter, V. et al. Exploration of jasmonate signalling via automated and standardized transient expression assays in tobacco cells. Plant J. 44, 1065–1076 (2005)

    Article  CAS  Google Scholar 

  30. Karimi, M., Inzé, D. & Depicker, A. GATEWAY™ vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193–195 (2002)

    Article  CAS  Google Scholar 

  31. Karimi, M., Depicker, A. & Hilson, P. Recombinational cloning with plant Gateway vectors. Plant Physiol. 145, 1144–1154 (2007)

    Article  CAS  Google Scholar 

  32. Salmon, J., Ramos, J. & Callis, J. Degradation of the auxin response factor ARF1. Plant J. 54, 118–128 (2008)

    Article  CAS  Google Scholar 

  33. Dreher, K. A., Brown, J., Saw, R. E. & Callis, J. The Arabidopsis Aux/IAA protein family has diversified in degradation and auxin responsiveness. Plant Cell 18, 699–714 (2006)

    Article  CAS  Google Scholar 

  34. Swarbreck, D. et al. The Arabidopsis Information Resource (TAIR): gene structure and function annotation. Nucleic Acids Res. 36, D1009–D1014 (2008)

    Article  CAS  Google Scholar 

  35. Hilson, P. et al. Versatile gene-specific sequence tags for Arabidopsis functional genomics: transcript profiling and reverse genetics applications. Genome Res. 14, 2176–2189 (2004)

    Article  CAS  Google Scholar 

  36. Harrison, S. J. et al. A rapid and robust method of identifying transformed Arabidopsis thaliana seedlings following floral dip transformation. Plant Methods 2, 19.1–19.7 (2006)

    Article  Google Scholar 

  37. Adie, B. A. T. et al. ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis . Plant Cell 19, 1665–1681 (2007)

    Article  CAS  Google Scholar 

  38. Goda, H. et al. The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access. Plant J. 55, 526–542 (2008)

    Article  CAS  Google Scholar 

  39. Breitling, R., Armengaud, P., Amtmann, A. & Herzyk, P. Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Lett. 573, 83–92 (2004)

    Article  CAS  Google Scholar 

  40. Hong, F. et al. RankProd: a bioconductor package for detecting differentially expressed genes in meta-analysis. Bioinformatics 22, 2825–2827 (2006)

    Article  CAS  Google Scholar 

  41. Ohta, M., Ohme-Takagi, M. & Shinshi, H. Three ethylene-responsive transcription factors in tobacco with distinct transactivation functions. Plant J. 22, 29–38 (2000)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank F. Lammertyn and all colleagues of the Functional Proteomics group at VIB and Ecophysiology–Biochemistry–Toxicology, Centre for Proteome Analysis and Mass Spectrometry (EBT-CEPROMA) at Antwerp University for technical assistance; M. I. Puga and J. Paz-Ares for providing the prey cDNA library for Y2H screens; V. Storme for help with statistical analysis; J. Van Leene and M. Karimi for discussions; and M. De Cock for help in preparing the manuscript. This work was supported by the Research Foundation–Flanders (predoctoral fellowship to L.P.), the Agency for Innovation by Science and Technology in Flanders (‘Generisch Basisonderzoek aan de Universiteiten’, and predoctoral fellowships to S.T. and J.G.), the Special Research Fund of Ghent University (postdoctoral fellowship to W.G.), the National Institutes of Health (to J.L.) and the Spanish Ministerio de Ciencia y Tecnología and the Comunidad de Madrid (to R.S.).

Author Contributions L.P., G.F.B., J.G., S.T., W.G., A.C.P., J.M.C., R.V.B., J.S., E.G, G.G.-C. and J.A.L. performed experiments and analysed the results. L.P., W.G., E.W., J.A.L., G.D.J., R.S. and A.G. planned experiments and analyses. L.P., D.I., J.A.L., R.S. and A.G. wrote the manuscript. All authors commented on the results and the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alain Goossens.

Supplementary information

Supplementary Information

This file contains Supplementary Figures 1-10 with legends and Supplementary Tables 1-5. (PDF 2322 kb)

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pauwels, L., Barbero, G., Geerinck, J. et al. NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 464, 788–791 (2010). https://doi.org/10.1038/nature08854

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature08854

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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