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MBE Advance Access published online on January 23, 2009
Molecular Biology and Evolution, doi:10.1093/molbev/msp011
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© The Author 2009. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Research article

Comparative analysis of structural diversity and sequence evolution in plant mitochondrial genes transferred to the nucleus

Shao-Lun Liu1,*, Yan Zhuang1,2,*, Peter Zhang1 and Keith L. Adams1

1 UBC Botanical Garden and Centre for Plant Research, and Department of Botany, University of British Columbia, Vancouver, BC, Canada, V6T1Z4
2 Present address: Plant Biology Graduate Group, UC Davis, 1002 Life Sciences Addition, Davis, CA 95616, USA

Corresponding author: Keith Adams, 6270 University Blvd, Department of Botany, Vancouver, Canada, V6T 1Z4, Phone: 604-822-2355, Fax: 604-822-6089, Email: keitha{at}interchange.ubc.ca

Received for publication August 21, 2008. Revision received November 15, 2008. Accepted for publication January 14, 2009.

The transfer of functional mitochondrial genes to the nucleus is an ongoing process during plant evolution that has made a major impact on cyto-nuclear interactions and mitochondrial genome evolution. Analysis of evolutionarily recent transfers in plants provides insights into the evolutionary dynamics of the process and how transferred genes become functional in the nucleus. Here we report 42 new transferred genes in various angiosperms, including 9 separate transfers of the succinate dehydrogenase gene sdh3. We performed comparative analyses of gene structures and sequence evolution of 77 genes transferred to the nucleus in various angiosperms, including multiple transfers of 10 genes in different lineages. Many genes contain mitochondrial targeting presequences, and potentially 5’ cis-regulatory elements, that were acquired from pre-existing nuclear genes for mitochondrial proteins to create chimeric gene structures. In eight separate cases the presequence was acquired from either the hsp70 chaperonin gene or the hsp22 chaperonin gene. The most common location of introns is in the presequence and the least common is in the region transferred from the mitochondrion. Several genes have an intron between the presequence and the core region, or an intron in the 5’UTR or 3’UTR, suggesting presequence and/or regulatory element acquisition by exon shuffling. Both synonymous and non-synonymous substitution rates have increased considerably in the transferred genes compared with their mitochondrial counterparts, and the degree of rate acceleration varies by gene, species, and evolutionary timing of transfer. Pairwise and branchwise Ka/Ks analysis identified four genes with evidence for positive selection, but positive selection is generally uncommon in transferred genes. This study provides a detailed portrayal of structural and sequence evolution in mitochondrial genes transferred to the nucleus, revealing the frequency of different mechanisms for how presequences and introns are acquired and showing how the sequences of transferred genes evolve after movement between cellular genomes.

Key Words: mitochondria • genome evolution • targeting sequence • intron

* equal contributions


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