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J. Biol. Chem., Vol. 282, Issue 25, 18532-18541, June 22, 2007

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Top-down Phenomics of Arabidopsis thaliana

METABOLIC PROFILING BY ONE- AND TWO-DIMENSIONAL NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY AND TRANSCRIPTOME ANALYSIS OF ALBINO MUTANTS^*

Chunjie Tian, Eisuke Chikayama^¶, Yuuri Tsuboi, Takashi Kuromori^||, Kazuo Shinozaki^||, Jun Kikuchi^¶**1, and Takashi Hirayama^**2

From the Laboratory of Environmental Molecular Biology, RIKEN Wako Institute, 2-1 Hirosawa, Wako, Saitama 351-0198, Japan,Graduate School of Integrated Science, Yokohama City University, 1-7-29 Suehiro, Tsurumi, Yokohama 230-0045, Japan,^¶Metabolomics Research Group, RIKEN Plant Science Center, 1-7-22 Tsurumi, Yokohama 230-0045, Japan, ^||Gene Discovery Research Group, RIKEN Plant Science Center, 1-7-22 Tsurumi, Yokohama 230-0045, Japan, ^**CREST, Japan Science and Technology Agency, 4-1-8 Hon-cho, Kawaguchi 332-0012, Japan, and the Graduate School of Bioagriculture Science, Nagoya University, 1 Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan

Elucidating the function of each gene in a genome is important for understanding the whole organism. We previously constructed 4000 disruptant mutants of Arabidopsis by insertion of Ds transposons. Here, we describe a top-down phenomics approach based on metabolic profiling that uses one-dimensional ¹H and two-dimensional ¹H,¹³C NMR analyses and transcriptome analysis of albino mutant lines of Arabidopsis. One-dimensional ¹H NMR metabolic fingerprinting revealed global metabolic changes in the albino mutants, notably a decrease in aromatic metabolites and changes in aliphatic metabolites. NMR measurements of plants fed with ¹³C₆-glucose showed that the albino lines had dramatically different ¹³C-labeling patterns and increased levels of several amino acids, especially Asn and Gln. Microarray analysis of one of the albino lines revealed a unique expression profile and showed that changes in the expression of genes encoding metabolic enzymes did not correspond with changes in the levels of metabolites. Collectively, these results suggest that albino mutants lose the normal carbon/nitrogen balance, presumably mainly through lack of photosynthesis. Our study offers an idea of how much the metabolite network is affected by chloroplast function in plants and shows the effectiveness of NMR-based metabolic analysis for metabolite profiling. On the basis of these findings, we propose that future investigations of plant systems biology combine transcriptomic, metabolomic, and phenomic analyses of gene disruptant lines.

Received for publication, January 19, 2007 , and in revised form, April 26, 2007.

^* This work was supported by the RIKEN President's Special Research Grant (to T. H. and J. K.) and by CREST, Japan Science and Technology Agency, Grant A88-54366 (to J. K. and T. H.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Tables S1-S4 and Figs. S1-S3.

¹ To whom correspondence may be addressed: RIKEN Yokohama Institute, 1-7-22 Suehiro, Tsurumi, Yokohama 230-0045, Japan. Tel.: 81-45-503-9439; Fax: 81-45-503-9490; E-mail: kikuchi{at}psc.riken.jp.

² To whom correspondence may be addressed: RIKEN Yokohama Institute, 1-7-22 Suehiro, Tsurumi, Yokohama 230-0045, Japan. Tel.: 81-45-508-7220; Fax: 81-45-508-7363; E-mail: hirayama{at}gsc.riken.jp.

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