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ENVIRONMENTAL STRESS AND ADAPTATION TO STRESS

Induction of Isoforms of Tetrapyrrole Biosynthetic Enzymes, AtHEMA2 and AtFC1, under Stress Conditions and Their Physiological Functions in Arabidopsis^1,2,[W],[OA]

Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, Yokohama 226–8501, Japan (S.N., A.K., Y.S.-S., H.O., K.T.); Graduate School of Arts and Sciences, University of Tokyo, Tokyo 153–8902, Japan (M.K., S.T., T.M.); and Environmental Biology Division, National Institute for Environmental Studies, Tsukuba 305–8506, Japan (M.A.)

In the tetrapyrrole biosynthetic pathway, isoforms of glutamyl-tRNA reductase (HEMA2) and ferrochelatase1 (FC1) are mainly expressed in nonphotosynthetic tissues. Here, using promoter--glucuronidase constructs, we showed that the expressions of Arabidopsis (Arabidopsis thaliana) HEMA2 (AtHEMA2) and FC1 (AtFC1) were induced in photosynthetic tissues by oxidative stresses such as wounding. Transcript levels and -glucronidase activity were rapidly induced within 30 min, specifically in the wound area in a jasmonate-independent manner. Transcriptome analysis of wound-specific early inducible genes showed that AtHEMA2 and AtFC1 were coinduced with hemoproteins outside plastids, which are related to defense responses. Ozone fumigation or reagents generating reactive oxygen species induced the expression of both genes in photosynthetic tissues, suggesting that reactive oxygen species is involved in the induction. Since cycloheximide or puromycin induced the expression of both genes, inhibition of cytosolic protein synthesis is involved in the induction of these genes in photosynthetic tissues. The physiological functions of AtHEMA2 and AtFC1 were investigated using insertional knockout mutants of each gene. Heme contents of the roots of both mutants were about half of that of the respective wild types. In wild-type plants, heme contents were increased by ozone exposure. In both mutants, reduction of the ozone-induced increase in heme content was observed. These results suggest the existence of the tetrapyrrole biosynthetic pathway controlled by AtHEMA2 and AtFC1, which normally functions for heme biosynthesis in nonphotosynthetic tissues, but is induced in photosynthetic tissues under oxidative conditions to supply heme for defensive hemoproteins outside plastids.

² This article is dedicated to the memory of Professor Ken-ichiro Takamiya of the Tokyo Institute of Technology who passed away suddenly after a traffic accident in 2005.

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: Tatsuru Masuda (ctmasuda{at}mail.ecc.u-tokyo.ac.jp).

^[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.107.100065

^* Corresponding author; e-mail ctmasuda{at}mail.ecc.u-tokyo.ac.jp; fax 81–3–5454–4321.

Received March 23, 2007; accepted March 28, 2007; published April 6, 2007.

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