Distinct and overlapping roles of two gibberellin 3-oxidases in Arabidopsis development

doi:10.1111/j.1365-313X.2005.02642.x

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Wiley InterScience

The Plant Journal

Volume 45 Issue 5, Pages 804 - 818

Published Online: 31 Jan 2006

Published in association with the Society for Experimental Biology

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Distinct and overlapping roles of two gibberellin 3-oxidases in Arabidopsis development

Melissa G. Mitchum ^1,†,‡ , Shinjiro Yamaguchi ^2,† , Atsushi Hanada ² , Ayuko Kuwahara ² , Yasushi Yoshioka ³ , Tomohiko Kato ⁴ , Satoshi Tabata ⁴ , Yuji Kamiya ² and Tai-ping Sun ^1,*

¹ Developmental, Cell, and Molecular Biology Group, Department of Botany, Box 91000, Duke University, Durham, NC 27708-1000, USA , ² RIKEN Plant Science Center, Suehiro-cho 1-7-22, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan , ³ Division of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, 464-8602, Japan , and ⁴ Kazusa DNA Research Institute, Kisarazu, Chiba 292-081, Japan

Correspondence to *(fax +1 919 613 8177; e-mail tps@duke.edu).

^† These authors contributed equally to this work.

^‡ Present address: Division of Plant Sciences, Integrative Plant Biology Group, University of Missouri-Columbia, 371H Life Sciences Center, Columbia, MO 65211, USA. E-mail: goellnerm@missouri.edu

KEYWORDS

gibberellin • biosynthesis • GA 3-oxidases • GA mutants • developmental regulation • Arabidopsis

ABSTRACT

Gibberellin (GA) 3-oxidase, a class of 2-oxoglutarate-dependent dioxygenases, catalyzes the conversion of precursor GAs to their bioactive forms, thereby playing a direct role in determining the levels of bioactive GAs in plants. Gibberellin 3-oxidase in Arabidopsis is encoded by a multigene family consisting of at least four members, designated AtGA3ox1 to AtGA3ox4. It has yet to be investigated how each AtGA3ox gene contributes to optimizing bioactive GA levels during growth and development. Using quantitative real-time PCR analysis, we have shown that each AtGA3ox gene exhibits a unique organ-specific expression pattern, suggesting distinct developmental roles played by individual AtGA3ox members. To investigate the sites of synthesis of bioactive GA in plants, we generated transgenic Arabidopsis that carried AtGA3ox1–GUS and AtGA3ox2–GUS fusions. Comparisons of the GUS staining patterns of these plants with that of AtCPS–GUS from previous studies revealed the possible physical separation of the early and late stages of the GA pathway in roots. Phenotypic characterization and quantitative analysis of the endogenous GA content of ga3ox1 and ga3ox2 single and ga3ox1/ga3ox2 double mutants revealed distinct as well as overlapping roles of AtGA3ox1 and AtGA3ox2 in Arabidopsis development. Our results show that AtGA3ox1 and AtGA3ox2 are responsible for the synthesis of bioactive GAs during vegetative growth, but that they are dispensable for reproductive development. The stage-specific severe GA-deficient phenotypes of the ga3ox1/ga3ox2 mutant suggest that AtGA3ox3 and AtGA3ox4 are tightly regulated by developmental cues; AtGA3ox3 and AtGA3ox4 are not upregulated to compensate for GA deficiency during vegetative growth of the double mutant.