Article

Arabidopsis NAC transcription factor JUB1 regulates GA/BR metabolism and signalling

  • Nature Plants 2, Article number: 16013 (2016)
  • doi:10.1038/nplants.2016.13
  • Download Citation
Received:
Accepted:
Published online:

Abstract

Gibberellins (GAs) and brassinosteroids (BRs) are important phytohormones that control plant development and responses to environmental cues by involving DELLA proteins and BRASSINAZOLE-RESISTANT1 (BZR1) respectively as key transcription factors. Here, we reveal a new role for JUNGBRUNNEN1 (JUB1) as a transcriptional regulator of GA/BR signalling in Arabidopsis thaliana. JUB1 directly represses the hormone biosynthesis genes GA3ox1 and DWARF4 (DWF4), leading to reduced levels of GAs and BRs and typical GA/BR deficiency phenotypes exhibiting short hypocotyls, dwarfism, late flowering and male sterility. JUB1 also directly represses PHYTOCHROME INTERACTING FACTOR4 (PIF4), a transcription factor connecting hormonal and environmental stimuli. On the other hand, JUB1 activates the DELLA genes GA INSENSITIVE (GAI) and RGA-LIKE 1 (RGL1). In addition, BZR1 and PIF4 act as direct transcriptional repressors upstream of JUB1, establishing a negative feedback loop. Thus, JUB1 forms the core of a robust regulatory module that triggers DELLA accumulation, thereby restricting cell elongation while concomitantly enhancing stress tolerance.

  • Subscribe to Nature Plants for full access:

    $62

    Subscribe

Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.

References

  1. 1.

    et al. Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nature Cell Biol. 14, 810–817 (2012).

  2. 2.

    et al. An interaction between BZR1 and DELLAs mediates direct signaling crosstalk between brassinosteroids and gibberellins in Arabidopsis. Sci. Signal. 5, ra72 (2012).

  3. 3.

    , , & Interaction of light and temperature signalling. J. Exp. Bot. 65, 2859–2871 (2014).

  4. 4.

    & Brassinosteroids: essential regulators of plant growth and development. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 427–451 (1998).

  5. 5.

    & A DELLAcate balance: the role of gibberellin in plant morphogenesis. Curr. Opin. Plant Biol. 8, 77–85 (2005).

  6. 6.

    , & Brassinosteroid signalling. Development 140, 1615–1620 (2013).

  7. 7.

    , , & Brassinosteroid transport. J. Exp. Bot. 59, 17–24 (2008).

  8. 8.

    & Biosynthesis and metabolism of brassinosteroids. Annu. Rev. Plant Biol. 54, 137–164 (2003).

  9. 9.

    & Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci. 5, 523–530 (2000).

  10. 10.

    , & Gibberellin signaling: biosynthesis, catabolism, and response pathways. Plant Cell 14, S61–S80 (2002).

  11. 11.

    , , , & A role for brassinosteroids in light-dependent development of Arabidopsis. Science 272, 398–401 (1996).

  12. 12.

    & Gibberellin biosynthesis: enzymes, genes and their regulation. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 431–460 (1997).

  13. 13.

    et al. The regulation of DWARF4 expression is likely a critical mechanism in maintaining the homeostasis of bioactive brassinosteroids in Arabidopsis. Plant Physiol. 140, 548–557 (2006).

  14. 14.

    , , & The CDG1 kinase mediates brassinosteroid signal transduction from BRI1 receptor kinase to BSU1 phosphatase and GSK3-like kinase BIN2. Mol. Cell 43, 561–571 (2011).

  15. 15.

    et al. PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1. Nature Cell Biol. 13, 124–131 (2011).

  16. 16.

    et al. BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 109, 181–191 (2002).

  17. 17.

    et al. Distinct and overlapping roles of two gibberellin 3-oxidases in Arabidopsis development. Plant J. 45, 804–818 (2006).

  18. 18.

    et al. Potential sites of bioactive gibberellin production during reproductive growth in Arabidopsis. Plant Cell 20, 320–336 (2008).

  19. 19.

    et al. GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437, 693–698 (2005).

  20. 20.

    et al. The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell 20, 2117–2129 (2008).

  21. 21.

    , , , & Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. Curr. Biol. 18, 656–660 (2008).

  22. 22.

    et al. Integration of plant responses to environmentally activated phytohormonal signals. Science 311, 91–94 (2006).

  23. 23.

    , , & The role of gibberellin signalling in plant responses to abiotic stress. J. Exp. Biol. 217, 67–75 (2014).

  24. 24.

    et al. A molecular framework for light and gibberellin control of cell elongation. Nature 451, 480–484 (2008).

  25. 25.

    et al. JUNGBRUNNEN1, a reactive oxygen species-responsive NAC transcription factor, regulates longevity in Arabidopsis. Plant Cell 24, 482–506 (2012).

  26. 26.

    Brassinosteroid-insensitive dwarf mutants of Arabidopsis accumulate brassinosteroids. Plant Physiol. 121, 743–752 (1999).

  27. 27.

    Arabidopsis mutants reveal multiple roles for sterols in plant development. Plant Cell 14, 1995–2000 (2002).

  28. 28.

    et al. NAC transcription factor speedy hyponastic growth regulates flooding-induced leaf movement in Arabidopsis. Plant Cell 25, 4941–4955 (2013).

  29. 29.

    et al. The Arabidopsis dwf7/ste1 mutant is defective in the delta7 sterol C-5 desaturation step leading to brassinosteroid biosynthesis. Plant Cell 11, 207–221 (1999).

  30. 30.

    et al. Della proteins and gibberellin-regulated seed germination and floral development in Arabidopsis. Plant Physiol. 135, 1008–1019 (2004).

  31. 31.

    et al. Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev. Cell 2, 505–513 (2002).

  32. 32.

    , & Arabidopsis NAC transcription factor JUNGBRUNNEN1 affects thermomemory-associated genes and enhances heat stress tolerance in primed and unprimed conditions. Plant Signal. Behav. 7, 1518–1521 (2012).

  33. 33.

    & Identification of a promoter region responsible for the senescence-specific expression of SAG12. Plant Mol. Biol. 41, 181–194 (1999).

  34. 34.

    et al. Biochemical insights on degradation of Arabidopsis DELLA proteins gained from a cell-free assay system. Plant Cell 21, 2378–2390 (2009).

  35. 35.

    et al. A genome-scale resource for the functional characterization of Arabidopsis transcription factors. Cell Rep. 8, 622–632 (2014).

  36. 36.

    , & Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nat. Cell Biol. 14, 802–809 (2012).

  37. 37.

    et al. Brassinosteroid regulates cell elongation by modulating gibberellin metabolism in rice. Plant Cell 26, 4376–4393 (2014).

  38. 38.

    et al. Brassinosteroids are master regulators of gibberellin biosynthesis in Arabidopsis. Plant Cell 27, 2261–2272 (2015).

  39. 39.

    & Gibberellin signaling in plants. Development 140, 1147–1151 (2013).

  40. 40.

    et al. Large-scale identification of gibberellin-related transcription factors defines group VII ETHYLENE RESPONSE FACTORS as functional DELLA partners. Plant Physiol. 166, 1022–1032 (2014).

  41. 41.

    , & GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193–195 (2002).

  42. 42.

    et al. DOF transcription factor AtDof1.1 (OBP2) is part of a regulatory network controlling glucosinolate biosynthesis in Arabidopsis. Plant J. 47, 10–24 (2006).

  43. 43.

    , & Transcription factors regulating leaf senescence in Arabidopsis thaliana. Plant Biol. (Stuttg). 10, 63–75 (2008).

  44. 44.

    , , & A quantitative RT-PCR platform for high-throughput expression profiling of 2500 rice transcription factors. Plant Methods 3, 7 (2007).

  45. 45.

    et al. Global analysis of della direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19, 3037–3057 (2007).

  46. 46.

    et al. Phytochrome-interacting transcription factors PIF4 and PIF5 induce leaf senescence in Arabidopsis. Nature Commun. 5, 4636 (2014).

  47. 47.

    et al. Darkness and gulliver2/phyB mutation decrease the abundance of phosphorylated BZR1 to activate brassinosteroid signaling in Arabidopsis. Plant J. 77, 737–747 (2014).

  48. 48.

    et al. Chromatin immunoprecipitation (ChIP) of plant transcription factors followed by sequencing (ChIP-SEQ) or hybridization to whole genome arrays (ChIP-CHIP). Nature Protoc. 5, 457–472 (2010).

  49. 49.

    , , , & Analysis of gibberellins as free acids by ultra performance liquid chromatography-tandem mass spectrometry. Talanta 112, 85–94 (2013).

  50. 50.

    et al. New techniques for the estimation of naturally occurring brassinosteroids. J. Plant Growth Regul. 26, 1–14 (2007).

  51. 51.

    & A new procedure for quantitative analysis by isotope dilution, with application to the determination of amino acids and fatty acids. J. Biol. Chem. 133, 737–744 (1940).

  52. 52.

    et al. Speeding cis-trans regulation discovery by phylogenomic analyses coupled with screenings of an arrayed library of Arabidopsis transcription factors. PLoS ONE 6, e21524 (2011).

  53. 53.

    & Tobacco rattle virus-based virus-induced gene silencing in Nicotiana benthamiana. Nature Protoc. 9, 1549–1562 (2014).

Download references

Acknowledgements

S.B. thanks the Deutsche Forschungsgemeinschaft for funding (grant no. BA 4769/2-1). The work on hormone measurements was funded by the Ministry of Education, Youth and Sports of the Czech Republic (National Program for Sustainability I Nr. LO1204 and the ‘Návrat’ programme LK21306) and by a Grant Agency of the Czech Republic (grant no. 14-34792S). Y.S. thanks the National Research Foundation of Korea (grant no. 500-20140212) for funding. We thank S. Choe (Seoul National University, Korea) for providing seeds of the 35S:BZR1–HA and DWF4prom:GUS lines, S. A. Kay (University of California, San Diego, La Jolla) for providing the Y1H library (made available through Pascal Falter-Braun, Technische Universität München), Karin Koehl and her team (MPI of Molecular Plant Physiology) for plant care and E. Maximova (MPI of Molecular Plant Physiology) for help with microscopy work. Support by the University of Potsdam and the MPI of Molecular Plant Physiology is gratefully acknowledged.

Author information

Affiliations

  1. University of Potsdam, Institute of Biochemistry and Biology, Karl-Liebknecht-Straße 24-25, Haus 20, 14476 Potsdam-Golm, Germany

    • Sara Shahnejat-Bushehri
    •  & Salma Balazadeh
  2. Max-Planck Institute of Molecular Plant Physiology, Am Mühlenberg 1, 14476 Potsdam-Golm, Germany

    • Sara Shahnejat-Bushehri
    •  & Salma Balazadeh
  3. Laboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany ASCR and Palacky University, v.v.i. Slechtitelu 11, CZ-783 71 Olomouc, Czech Republic

    • Danuse Tarkowska
  4. Department of Plant Science, Plant Genomics and Breeding Institute, Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul 151-921, Korea

    • Yasuhito Sakuraba

Authors

  1. Search for Sara Shahnejat-Bushehri in:

  2. Search for Danuse Tarkowska in:

  3. Search for Yasuhito Sakuraba in:

  4. Search for Salma Balazadeh in:

Contributions

S.B. conceived the idea for the study and supervised the work. S.S.-B. carried out the experiments. Y.S. did expression analysis of JUB1 in 35S:PIF4–myc and 35S:BZR1–HA lines, ChIP-qPCR assays to show binding of BZR1 and PIF4 to the JUB1 promoter, and Y2H experiments. D.T. performed the GA and BR analyses. S.B. and S.S.-B. wrote the manuscript; S.B. did the final editing.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Salma Balazadeh.

Supplementary information