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Science 305 (5692): 1968-1971

Copyright © 2004 by the American Association for the Advancement of Science

Nitric Oxide Represses the Arabidopsis Floral Transition

Yikun He,1,2* Ru-Hang Tang,1* Yi Hao,1* Robert D. Stevens,3 Charles W. Cook,1 Sun M. Ahn,1 Liufang Jing,1 Zhongguang Yang,4 Longen Chen,4 Fangqing Guo,5 Fabio Fiorani,1{dagger} Robert B. Jackson,1 Nigel M. Crawford,5 Zhen-Ming Pei1{ddagger}

Abstract: The correct timing of flowering is essential for plants to maximize reproductive success and is controlled by environmental and endogenous signals. We report that nitric oxide (NO) repressed the floral transition in Arabidopsis thaliana. Plants treated with NO, as well as a mutant overproducing NO (nox1), flowered late, whereas a mutant producing less NO (nos1) flowered early. NO suppressed CONSTANS and GIGANTEA gene expression and enhanced FLOWERING LOCUS C expression, which indicated that NO regulates the photoperiod and autonomous pathways. Because NO is induced by environmental stimuli and constitutively produced, it may integrate both external and internal cues into the floral decision.

1 Department of Biology, Duke University, Durham, NC 27708, USA.
2 Department of Biology, Capital Normal University, Beijing 100037, China.
3 Mass Spectrometry Laboratory, Duke University Medical Center, Research Triangle Park, NC 27709, USA.
4 Orthopaedic Research Laboratory, Duke University Medical Center, Durham, NC 27710, USA.
5 Division of Biological Sciences, University of California, San Diego, La Jolla, CA 92093, USA.

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* These authors contributed equally to this work.

{dagger} Present address: Department of Plant Systems Biology, VIB-Ghent University, B-9052 Ghent, Belgium.

{ddagger} To whom correspondence should be addressed. E-mail: zpei{at}duke.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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