STOP1 Regulates Multiple Genes That Protect Arabidopsis from Proton and Aluminum Toxicities

Yoshiharu Sawaki,Nozomu Sakurai,Kazuo Shinozaki,Hiroyuki Koyama,Takashi Ikka,Yuriko Kobayashi,Daisuke Shibata,Masatomo Kobayashi,Satoshi Iuchi,Yasufumi Kobayashi,Miki Fujita

doi:10.1104/pp.108.134700

Abstract

The Arabidopsis (Arabidopsis thaliana) mutant stop1 (for sensitive to proton rhizotoxicity1) carries a missense mutation at an essential domain of the histidine-2-cysteine-2 zinc finger protein STOP1. Transcriptome analyses revealed that various genes were down-regulated in the mutant, indicating that STOP1 is involved in signal transduction pathways regulating aluminum (Al)- and H(+)-responsive gene expression. The Al hypersensitivity of the mutant could be caused by down-regulation of AtALMT1 (for Arabidopsis ALUMINUM-ACTIVATED MALATE TRANSPORTER1) and ALS3 (ALUMINUM-SENSITIVE3). This hypothesis was supported by comparison of Al tolerance among T-DNA insertion lines and a transgenic stop mutant carrying cauliflower mosaic virus 35SAtALMT1. All T-DNA insertion lines of STOP1, AtALMT1, and ALS3 were sensitive to Al, but introduction of cauliflower mosaic virus 35SAtALMT1 did not completely restore the Al tolerance of the stop1 mutant. Down-regulation of various genes involved in ion homeostasis and pH-regulating metabolism in the mutant was also identified by microarray analyses. CBL-INTERACTING PROTEIN KINASE23, regulating a major K(+) transporter, and a sulfate transporter, SULT3;5, were down-regulated in the mutant. In addition, integral profiling of the metabolites and transcripts revealed that pH-regulating metabolic pathways, such as the gamma-aminobutyric acid shunt and biochemical pH stat pathways, are down-regulated in the mutant. These changes could explain the H(+) hypersensitivity of the mutant and would make the mutant more susceptible in acid soil stress than other Al-hypersensitive T-DNA insertion lines. Finally, we showed that STOP1 is localized to the nucleus, suggesting that the protein regulates the expression of multiple genes that protect Arabidopsis from Al and H(+) toxicities, possibly as a transcription factor.

Highlights

IntroductionThe Arabidopsis (Arabidopsis thaliana) mutant stop (for sensitive to proton rhizotoxicity1) carries a missense mutation at an essential domain of the histidine-2-cysteine-2 zinc finger protein STOP1
The Arabidopsis (Arabidopsis thaliana) mutant stop1 carries a missense mutation at an essential domain of the histidine-2-cysteine-2 zinc finger protein STOP1
Zinc finger proteins have various functions (Englbrecht et al, 2004), these results suggest that STOP1 is one of the key factors involved in the signal transduction pathways regulating tolerance mechanisms to Al and H1 rhizotoxicities, which would consist of various genes other than AtALMT1 (Iuchi et al, 2007) and AtMATE for Al tolerance (Liu et al, 2009)

Summary

Introduction

The Arabidopsis (Arabidopsis thaliana) mutant stop (for sensitive to proton rhizotoxicity1) carries a missense mutation at an essential domain of the histidine-2-cysteine-2 zinc finger protein STOP1. The Al hypersensitivity of the mutant could be caused by down-regulation of AtALMT1 (for Arabidopsis ALUMINUM-ACTIVATED MALATE TRANSPORTER1) and ALS3 (ALUMINUM-SENSITIVE3) This hypothesis was supported by comparison of Al tolerance among T-DNA insertion lines and a transgenic stop mutant carrying cauliflower mosaic virus 35STAtALMT1. Plants modulate tolerant mechanisms to adapt to various environmental stresses, such as drought, salinity, and soil acidity (Seki et al, 2003; Kochian et al, 2004) Molecular characterization of such systems is critical to develop efficient breeding programs to make crop plants with high productivity under stress environments. Studies on rhizotoxicity indicate that patterns of damage caused by H1 are distinct from those induced by Al (Koyama et al, 1995) These stress factors were distinguished by a modeling of root elongation in acidic forest soil (Kinraide, 2003). The mutant might be a useful model to dissect the mechanism(s) of H1 tolerance at the molecular level and the interaction of tolerance mechanisms to Al31 and H1

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Conclusion