Comparative analysis of structural diversity and sequence evolution in plant mitochondrial genes transferred to the nucleus.
The transfer of functional mitochondrial genes to the nucleus is an ongoing process during plant evolution that has made a major impact on cytonuclear 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 (untranslated region) or 3'UTR, suggesting presequence and/or regulatory element acquisition by exon shuffling. Both synonymous and nonsynonymous 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 K(a)/K(s) 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.
Liu
Shao-Lun
SL
UBC Botanical Garden and Centre for Plant Research, and Department of Botany, University of British Columbia, Vancouver, BC, Canada.
Zhuang
Yan
Y
Zhang
Peter
P
Adams
Keith L
KL
D002467:Cell Nucleus / Q000235:genetics; D019143:Evolution, Molecular; D050259:Genes, Mitochondrial; D017343:Genes, Plant; D007438:Introns; D019684:Magnoliopsida / Q000235:genetics*; D024101:Mitochondrial Proteins / Q000235:genetics*; D008969:Molecular Sequence Data; D012269:Ribosomal Proteins / Q000235:genetics; D013385:Succinate Dehydrogenase / Q000235:genetics*
D024101:Mitochondrial Proteins; D012269:Ribosomal Proteins; D013385:Succinate Dehydrogenase