Mitochondrial Retroprocessing Promoted Functional Transfers of rpl5 to the Nucleus in Grasses

• Published in: Molecular biology and evolution Vol. 34; no. 9; pp. 2340 - 2354
• Main Authors: Wu, Zhiqiang, Sloan, Daniel B., Brown, Colin W., Rosenblueth, Mónica, Palmer, Jeffrey D., Ong, Han Chuan
• Format: Journal Article
• Language: English
• Published: United States Oxford University Press 01.09.2017
• Subjects: Amino Acid Sequence - genetics; Angiosperms; Cell Nucleus - genetics; Deoxyribonucleic acid; Discoveries; DNA; DNA, Mitochondrial - genetics; Evolution, Molecular; Gene conversion; Gene Conversion - genetics; Gene transfer; Genes; Genes, Mitochondrial - genetics; Genes, Plant; Genome, Mitochondrial; Grasses; Introns; Magnoliopsida - genetics; Mitochondria - genetics; Mitochondrial DNA; Nuclei (cytology); Nucleotide sequence; Phylogeny; Plant Proteins - genetics; Poaceae - genetics; Pseudogenes - genetics; Ribonucleic acid; Ribosomal Proteins - genetics; RNA; RNA Editing; Sequence Homology, Amino Acid; Yeast; endosymbiotic gene transfer; pseudogene; intracellular gene transfer; mtDNA; reverse transcription
• DOI: 10.1093/molbev/msx170
• ISSN: 0737-4038; 1537-1719

Functional gene transfers from the mitochondrion to the nucleus are ongoing in angiosperms and have occurred repeatedly for all 15 ribosomal protein genes, but it is not clear why some of these genes are transferred more often than others nor what the balance is between DNA- and RNA-mediated transfers. Although direct insertion of mitochondrial DNA into the nucleus occurs frequently in angiosperms, case studies of functional mitochondrial gene transfer have implicated an RNA-mediated mechanism that eliminates introns and RNA editing sites, which would otherwise impede proper expression of mitochondrial genes in the nucleus. To elucidate the mechanisms that facilitate functional gene transfers and the evolutionary dynamics of the coexisting nuclear and mitochondrial gene copies that are established during these transfers, we have analyzed rpl5 genes from 90 grasses (Poaceae) and related monocots. Multiple lines of evidence indicate that rpl5 has been functionally transferred to the nucleus at least three separate times in the grass family and that at least seven species have intact and transcribed (but not necessarily functional) copies in both the mitochondrion and nucleus. In two grasses, likely functional nuclear copies of rpl5 have been subject to recent gene conversion events via secondarily transferred mitochondrial copies in what we believe are the first described cases of mitochondrial-to-nuclear gene conversion. We show that rpl5 underwent a retroprocessing event within the mitochondrial genome early in the evolution of the grass family, which we argue predisposed the gene towards successful, DNA-mediated functional transfer by generating a “pre-edited” sequence.