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Retention of functional genes for S19 ribosomal protein in both the mitochondrion and nucleus for over 60 million years

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Abstract

Ribosomal protein genes occasionally undergo successful migration from the mitochondrion to the nucleus in flowering plants and we previously presented evidence that the S19 ribosomal protein gene (rps19) had been transferred to the nucleus in the common ancestor of Poaceae grasses. In many lineages, the mitochondrial copy was subsequently lost or pseudogenized, although in rice it was retained and the nuclear copy lost. We have now determined that functional rps19 genes are present in both the mitochondrion and nucleus in brome grass (Bromus inermis). The mitochondrion-located rps19 gene, which is immediately downstream of an rpl2 pseudogene, is transcribed and edited. The nuclear-located rps19 gene is also actively expressed and it possesses the same intron-containing hsp70-type presequence as its counterparts in other grasses, as well as shared derived amino acids within the S19 core. We conclude that this brome rps19 gene is derived from the same transfer event that occurred in the common ancestor of grasses at least 60 million years ago. In the oat lineage, a subsequent exon shuffling-type event has resulted in novel amino-terminal sequences replacing part of the hsp70 presequence, and in the barley lineage, there has been an additional DNA-mediated transfer of the mitochondrial rps19 gene and its flanking sequences, followed by relatively recent loss of the mitochondrion-located copy. The prolonged persistence of functional copies in both compartments, as evidenced by present-day brome, raises interesting questions about their respective roles.

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Acknowledgments

We thank members of the Bonen laboratory for helpful discussions and Dr R. Pandeya (Agriculture and Agri-food Canada, Ottawa) for kindly providing seeds. Financial support from the Natural Sciences and Engineering Research Council of Canada is also gratefully acknowledged.

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  1. Sarah N. Rampersad

    Present address: Department of Pathology and Molecular Medicine, Queen’s University, Kingston, ON, K7L 3N6, Canada

Authors and Affiliations

  1. Biology Department, University of Ottawa, 30 Marie Curie, Ottawa, K1N 6N5, Canada

    Sruthi Atluri, Sarah N. Rampersad & Linda Bonen

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  1. Sruthi Atluri
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Correspondence to Linda Bonen.

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Communicated by B. Franz Lang.

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Atluri, S., Rampersad, S.N. & Bonen, L. Retention of functional genes for S19 ribosomal protein in both the mitochondrion and nucleus for over 60 million years. Mol Genet Genomics 290, 2325–2333 (2015). https://doi.org/10.1007/s00438-015-1087-6

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  • DOI: https://doi.org/10.1007/s00438-015-1087-6

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