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

Nature Plants volume 2, Article number: 16013 (2016) Cite this article

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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.

The plant hormones GAs and BRs, often acting cooperatively, play a central role in many aspects of plant growth, development and adaptation to environmental cues, such as light and temperature1–3. Mutants deficient in either GAs or BRs exhibit a variety of growth defects, including short hypocotyls, dwarfism, dark-green curly leaves, delayed flowering and male sterility4,5. Therefore, optimum levels of cellular GAs and BRs, controlled by biosynthesis, transport, perception and signalling, are essential for plant growth and responses to the environment6–12.

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Figure 1: Plants overexpressing JUB1 exhibit a typical phenotype of GA- and/or BR-deficient mutants.
Figure 2: JUB1 regulation of GA- and BR-associated genes.
Figure 3: GA/BR-related growth phenotypes of JUB1-OX plants are fully rescued by overexpression of GA3ox1 and DWF4.
Figure 4: Suppression of growth by JUB1 requires DELLA proteins.
Figure 5: PIF4 and BZR1 directly repress JUB1 transcription.
Figure 6: A model for JUB1 function in the regulation of cell elongation and stress responses.

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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.

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Authors and 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

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  1. Sara Shahnejat-Bushehri
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  3. Yasuhito Sakuraba
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  4. Salma Balazadeh
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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.

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Correspondence to Salma Balazadeh.

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Shahnejat-Bushehri, S., Tarkowska, D., Sakuraba, Y. et al. Arabidopsis NAC transcription factor JUB1 regulates GA/BR metabolism and signalling. Nature Plants 2, 16013 (2016). https://doi.org/10.1038/nplants.2016.13

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