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BZR1 Is a Transcriptional Repressor with Dual Roles in Brassinosteroid Homeostasis and Growth Responses
Jun-Xian He,1*
Joshua M. Gendron,1,2*
Yu Sun,1
Srinivas S. L. Gampala,1
Nathan Gendron,1
Catherine Qing Sun,1
Zhi-Yong Wang1
Abstract:
Brassinosteroid (BR) homeostasis and signaling are crucial fornormal growth and development of plants. BR signaling throughcell-surface receptor kinases and intracellular components leadsto dephosphorylation and accumulation of the nuclear proteinBZR1. How BR signaling regulates gene expression, however, remainsunknown. Here we show that BZR1 is a transcriptional repressorthat has a previously unknown DNA binding domain and binds directlyto the promoters of feedback-regulated BR biosynthetic genes.Microarray analyses identified additional potential targetsof BZR1 and illustrated, together with physiological studies,that BZR1 coordinates BR homeostasis and signaling by playingdual roles in regulating BR biosynthesis and downstream growthresponses.
1 Department of Plant Biology, Carnegie Institution, Stanford, CA 94305, USA. 2 Department of Biological Sciences, Stanford University, Stanford, CA 94305, USA.
* These authors contributed equally to this work.
To whom correspondence should be addressed. E-mail: zywang24{at}stanford.edu
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|Abstract »|Full Text »|PDF »
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|Abstract »|Full Text »|PDF »
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|Abstract »|Full Text »|PDF »
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|Abstract »|Full Text »|PDF »
Brassinosteroid transport.
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|Abstract »|Full Text »|PDF »
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|Abstract »|Full Text »|PDF »
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|Abstract »|Full Text »|PDF »
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|Abstract »|Full Text »|PDF »
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|Abstract »|Full Text »|PDF »
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|Abstract »|Full Text »|PDF »
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|Abstract »|Full Text »|PDF »
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133, 1857-1869
|Abstract »|Full Text »|PDF »
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S. Bancos, A.-M. Szatmari, J. Castle, L. Kozma-Bognar, K. Shibata, T. Yokota, G. J. Bishop, F. Nagy, and M. Szekeres (2006)
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|Abstract »|Full Text »|PDF »
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|Abstract »|Full Text »|PDF »
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