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Arabidopsis mutants reveal multiple singlet oxygen signaling pathways involved in stress response and development

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Abstract

Shortly after the release of singlet oxygen (1O2) in chloroplasts drastic changes in nuclear gene expression occur in the conditional flu mutant of Arabidopsis that reveal a rapid transfer of signals from the plastid to the nucleus. Factors involved in this retrograde signaling were identified by mutagenizing a transgenic flu line expressing a 1O2-responsive reporter gene. The reporter gene consisted of the luciferase open reading frame and the promoter of an AAA-ATPase gene (At3g28580) that was selectively activated by 1O2 but not by superoxide or hydrogen peroxide. A total of eight second-site mutants were identified that either constitutively activate the reporter gene and the endogenous AAA-ATPase irrespectively of whether 1O2 was generated or not (constitutive activators of AAA-ATPase, caa) or abrogated the 1O2-dependent up-regulation of these genes as seen in the transgenic parental flu line (non-activators of AAA-ATPase, naa). The characterization of the mutants strongly suggests that 1O2-signaling does not operate as an isolated linear pathway but rather forms an integral part of a signaling network that is modified by other signaling routes and impacts not only stress responses of plants but also their development.

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Acknowledgments

We are indebted to Dr. Laszlo Kozma-Bognár (Biological Research Center, Szeged, Hungary) for the gift of LUC+ -NOS pPCV binary vector, Prof. Wilhelm Gruissem for the use of the Hamamatsu imaging system, Piotr Pawlak for artwork, André Imboden for taking care of plants, Dr. Rasa Meskauskiene for valuable discussions and Prof. Teresa Fitzpatrick for critical reading of the manuscript. This work was supported by grants from the Swiss National Science Foundation (SNSF), the ETH-Zurich and the Boyce Thompson Institute.

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Correspondence to Klaus Apel.

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Aiswarya Baruah and Klára Šimková contributed equally to the article.

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Baruah, A., Šimková, K., Apel, K. et al. Arabidopsis mutants reveal multiple singlet oxygen signaling pathways involved in stress response and development. Plant Mol Biol 70, 547–563 (2009). https://doi.org/10.1007/s11103-009-9491-0

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