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First published online December 27, 2007; 10.1104/pp.107.113738

Plant Physiology 146:1368-1385 (2008)
© 2008 American Society of Plant Biologists

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DEVELOPMENT AND HORMONE ACTION

High Temperature-Induced Abscisic Acid Biosynthesis and Its Role in the Inhibition of Gibberellin Action in Arabidopsis Seeds1,2,[C],[W],[OA]

Shigeo Toh, Akane Imamura3, Asuka Watanabe, Kazumi Nakabayashi4, Masanori Okamoto, Yusuke Jikumaru, Atsushi Hanada, Yukie Aso, Kanako Ishiyama, Noriko Tamura5, Satoshi Iuchi, Masatomo Kobayashi, Shinjiro Yamaguchi, Yuji Kamiya, Eiji Nambara and Naoto Kawakami*

Department of Life Sciences, School of Agriculture, Meiji University, Kawasaki, Kanagawa 214–8571, Japan (S.T., A.I., A.W., N.T., N.K.); Growth Regulation Research Group, RIKEN Plant Science Center, Yokohama, Kanagawa 230–0045, Japan (K.N., M.O., Y.J., A.H., S.Y., Y.K., E.N.); and Experimental Plant Division, RIKEN Bioresource Center, Tsukuba, Ibaraki 305–0074, Japan (Y.A., K.I., S.I., M.K.)

Suppression of seed germination at supraoptimal high temperature (thermoinhibiton) during summer is crucial for Arabidopsis (Arabidopsis thaliana) to establish vegetative and reproductive growth in appropriate seasons. Abscisic acid (ABA) and gibberellins (GAs) are well known to be involved in germination control, but it remains unknown how these hormone actions (metabolism and responsiveness) are altered at high temperature. Here, we show that ABA levels in imbibed seeds are elevated at high temperature and that this increase is correlated with up-regulation of the zeaxanthin epoxidase gene ABA1/ZEP and three 9-cis-epoxycarotenoid dioxygenase genes, NCED2, NCED5, and NCED9. Reverse-genetic studies show that NCED9 plays a major and NCED5 and NCED2 play relatively minor roles in high temperature-induced ABA synthesis and germination inhibition. We also show that bioactive GAs stay at low levels at high temperature, presumably through suppression of GA 20-oxidase genes, GA20ox1, GA20ox2, and GA20ox3, and GA 3-oxidase genes, GA3ox1 and GA3ox2. Thermoinhibition-tolerant germination of loss-of-function mutants of GA negative regulators, SPINDLY (SPY) and RGL2, suggests that repression of GA signaling is required for thermoinibition. Interestingly, ABA-deficient aba2-2 mutant seeds show significant expression of GA synthesis genes and repression of SPY expression even at high temperature. In addition, the thermoinhibition-resistant germination phenotype of aba2-1 seeds is suppressed by a GA biosynthesis inhibitor, paclobutrazol. We conclude that high temperature stimulates ABA synthesis and represses GA synthesis and signaling through the action of ABA in Arabidopsis seeds.

1 This work was supported by the Japan Society for the Promotion of Science for Young Scientists (research fellowship to S.T.).

2 This article is dedicated to the memory of Akira Watanabe.

3 Present address: Space Station Engineering Department, Advanced Engineering Services Co., Chuoh-ku, Tokyo 103–0028, Japan.

4 Present address: Department of Plant Breeding and Genetics, Max Planck Institute for Plant Breeding Research, Cologne 50829, Germany.

5 Present address: Japan Turfgrass II, Inc., Taisei Corporation Technology Research Center, Yokohama, Kanagawa 245–0051, Japan.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Naoto Kawakami (kawakami{at}isc.meiji.ac.jp).

[C] Some figures in this article are displayed in color online but in black and white in the print edition.

[W] The online version of this article contains Web-only data.

[OA] Open Access articles can be viewed online without a subscription.

www.plantphysiol.org/cgi/doi/10.1104/pp.107.113738

* Corresponding author; e-mail kawakami{at}isc.meiji.ac.jp.

Received November 27, 2007; accepted December 18, 2007; published December 27, 2008.


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