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Mutation of the pentatricopeptide repeat-SMR protein SVR7 impairs accumulation and translation of chloroplast ATP synthase subunits in Arabidopsis thaliana

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Abstract

RNA processing, RNA editing, RNA splicing and translational activation of RNAs are essential post-transcriptional steps in chloroplast gene expression. Typically, the factors mediating those processes are nuclear encoded and post-translationally imported into the chloroplasts. In land plants, members of the large pentatricopeptide repeat (PPR) protein family are required for individual steps in chloroplast RNA processing. Interestingly, a subgroup of PPR proteins carries a C-terminal small MutS related (SMR) domain. Here we analyzed the consequences of mutations in the SVR7 gene, which encodes a PPR-SMR protein, in Arabidopsis thaliana. We demonstrate that SVR7 mutations lead to a specific reduction in chloroplast ATP synthase levels. Furthermore, we found aberrant transcript patterns for ATP synthase coding mRNAs in svr7 mutants. Finally, a reduced ribosome association of atpB/E and rbcL mRNAs in svr7 mutants suggests the involvement of the PPR-SMR protein SVR7 in translational activation of these mRNAs. We describe that the function of SVR7 in translation has expanded relative to its maize ortholog ATP4. The results provide evidence for a relaxed functional conservation of this PPR-SMR protein in eudicotyledonous and monocotyledonous plants, thus adding to the knowledge about the function and evolution of PPR-SMR proteins.

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Abbreviations

Col:

Columbia (Arabidopsis accession)

Cyt b 6 f :

Cytochrome b 6 f complex

GUN:

Genomes uncoupled

Ler:

Landsberg erecta (Arabidopsis accession)

LHC:

Light harvesting complex

NF:

Norflurazon

PPR:

Pentatricopeptide repeat (protein domain)

PSI/II:

Photosystem I/II

RT-PCR:

Reverse transcription PCR

SMR:

Small MutS related (protein domain)

WT:

Wild-type

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Acknowledgments

The authors thank Reik Modrozynski and Simone Hardel for excellent technical support. We acknowledge Alice Barkan for providing the antibodies used in this study. We thank Michael Tillich for the introduction of Norflurazon assays. We acknowledge the Nottingham Arabidopsis Stock Centre and Rob Martienssen from the Cold Spring Harbor Laboratory for providing Arabidopsis seeds for insertion lines. We thank Alice Barkan, Ian Small, Kate Howell, Michael Tillich, and Karsten Liere for helpful discussions. This work was supported by the German Academic Exchange Service, and the German Research Foundation [Grant Numbers SCHM 1698/2-1, ZO 302/1].

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  1. Reimo Zoschke

    Present address: Institute of Molecular Biology, University of Oregon, Klamath Hall, Eugene, OR, 97403, USA

  2. Yan O. Zubo

    Present address: Department of Biological Sciences, Dartmouth College, Hanover, NH, 03755, USA

Authors and Affiliations

  1. Molekulare Genetik, Institut für Biologie, Humboldt-Universität zu Berlin, 10115, Berlin, Germany

    Reimo Zoschke, Yujiao Qu & Christian Schmitz-Linneweber

  2. Genetik, Institut für Biologie, Humboldt-Universität zu Berlin, 10115, Berlin, Germany

    Yan O. Zubo & Thomas Börner

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  1. Reimo Zoschke
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Correspondence to Reimo Zoschke.

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Zoschke, R., Qu, Y., Zubo, Y.O. et al. Mutation of the pentatricopeptide repeat-SMR protein SVR7 impairs accumulation and translation of chloroplast ATP synthase subunits in Arabidopsis thaliana . J Plant Res 126, 403–414 (2013). https://doi.org/10.1007/s10265-012-0527-1

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