Punctuated evolution of mitochondrial gene content: High and variable rates of mitochondrial gene loss and transfer to the nucleus during angiosperm evolution

Adams, Keith L.; Qiu, Yin Long; Stoutemyer, Mark; Palmer, Jeffrey D.

doi:10.1073/pnas.042694899

Cited by 389 publications

(413 citation statements)

References 56 publications

(70 reference statements)

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“…Angiosperm mitogenomes virtually always share the same set of 24 core protein genes, mostly coding for respiratory proteins, but often differ substantially in their inventories of a further 17 protein genes mostly encoding ribosomal proteins (17,18). Three species of Silene possess the most protein-gene-poor angiosperm mitogenomes described to date (9).…”

Section: Resultsmentioning

confidence: 99%

Miniaturized mitogenome of the parasitic plant Viscum scurruloideum is extremely divergent and dynamic and has lost all nad genes

Skippington

Barkman

Rice

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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285

325

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Despite the enormous diversity among parasitic angiosperms in form and structure, life-history strategies, and plastid genomes, little is known about the diversity of their mitogenomes. We report the sequence of the wonderfully bizarre mitogenome of the hemiparasitic aerial mistletoe Viscum scurruloideum. This genome is only 66 kb in size, making it the smallest known angiosperm mitogenome by a factor of more than three and the smallest land plant mitogenome. Accompanying this size reduction is exceptional reduction of gene content. Much of this reduction arises from the unexpected loss of respiratory complex I (NADH dehydrogenase), universally present in all 300+ other angiosperms examined, where it is encoded by nine mitochondrial and many nuclear nad genes. Loss of complex I in a multicellular organism is unprecedented. We explore the potential relationship between this loss in Viscum and its parasitic lifestyle. Despite its small size, the Viscum mitogenome is unusually rich in recombinationally active repeats, possessing unparalleled levels of predicted sublimons resulting from recombination across short repeats. Many mitochondrial gene products exhibit extraordinary levels of divergence in Viscum, indicative of highly relaxed if not positive selection. In addition, all Viscum mitochondrial protein genes have experienced a dramatic acceleration in synonymous substitution rates, consistent with the hypothesis of genomic streamlining in response to a high mutation rate but completely opposite to the pattern seen for the high-rate but enormous mitogenomes of Silene. In sum, the Viscum mitogenome possesses a unique constellation of extremely unusual features, a subset of which may be related to its parasitic lifestyle.

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Section: Resultsmentioning

confidence: 99%

Miniaturized mitogenome of the parasitic plant Viscum scurruloideum is extremely divergent and dynamic and has lost all nad genes

Skippington

Barkman

Rice

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

285

325

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“…Nonetheless, the reshuffling of genetic sequences in large chunks is a critical mechanism in eukaryotic evolution as large changes occur very quickly during adaptation to changing environments. Such a mechanism helps to explain the evolution of novel genetic sequences for which no intermediate forms are evident (Adams et al 2002).…”

Section: The Gene Silencing Conceptmentioning

confidence: 99%

RNA interference: The molecular immune system

Bagasra

Prilliman²

2004

Histochem J

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SummaryIntroduction of double-stranded RNA (dsRNA) into cells expressing a homologous gene triggers RNA interference (RNAi), or RNA-based gene silencing (RBGS). The dsRNA degrades corresponding host mRNA into small interfering RNAs (siRNAs) by a protein complex containing Dicer. siRNAs in turn are incorporated into the RNA-induced silencing complex (RISC) that includes helicase, RecA, and exo-and endo-nucleases as well as other proteins. Following its assembly, the RISC guides the RNA degradation machinery to the target RNAs and cleaves the cognate target RNA in a sequence-specific, siRNA-dependent manner. RNAi has now been documented in a wide variety of organisms, including plants, fungi, flies, worms, and more recently, higher mammals. In eukaryotes, dsRNA directed against a range of viruses (i.e., HIV-1, RSV, HPV, poliovirus and others) and endogenous genes can induce sequence-specific inhibition of gene expression. In invertebrates, RNAi can be efficiently triggered by either long dsRNAs or 21-to 23-nt-long siRNAs. However, in jawed vertebrates, dsRNA longer than 30 bp can induce interferon and thus trigger undesirable side effects instead of initiating RNAi. siRNAs have been shown to act as potent inducers of RNAi in cultured mammalian cells. Many investigators have suggested that siRNAs may have evolved as a normal defense against endogenous and exogenous transposons and retroelements. Through a combination of genetic and biochemical approaches, some of the mechanisms underlying RNAi have been described. Recent data in C. elegans shows that two homologs of siRNAs, microRNAs (miRNAs) and tiny noncoding RNAs (tncRNAs) are endogenously expressed. However, many aspects of RNAi-induced gene silencing, including its origins and the selective pressures which maintain it, remain undefined. Its evolutionary history may pass through the more primitive immune functions of prokaryotes involving restriction enzymes that degrade plasmid DNA molecules that enter bacterial cells. RNAi has evolved further among eukaryotes, in which its wide distribution suggests early origins. RNAi seems to be involved in a variety of regulatory and immune functions that may differ among various kingdoms and phyla. We present here proposed mechanisms by which RBGS protects the host against endogenous and exogenous transposons and retroelements. The potential for therapeutic application of RBGS technology in treating viral infections such as HIV is also discussed.

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“…A reduction in the accumulation of deleterious mutations is a prime benefit for cymt genes that are subsequently located in the nuclear genome (where DNA repair is more efficient). However, functional gene transfers have been documented almost exclusively in plants (e.g., Adams et al, 2002) and green algae (e.g., Perez-Martinez et al, 2000;Funes et al, 2002), suggesting that in animals, where the mitochondrial genetic code differs from the standard code (Wolstenholme, 1992), most numts are non functional upon arrival.…”

Section: Numt As a Pseudogene: Evolution And Functional Implicationsmentioning

confidence: 99%

Evolutionary analysis of a large mtDNA translocation (numt) into the nuclear genome of the Panthera genus species

Kim

Antunes

Luo

et al. 2006

Gene

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Translocation of cymtDNA into the nuclear genome, also referred to as numt, has been reported in many species, including several closely related to the domestic cat (Felis catus). We describe the recent transposition of 12,536 bp of the 17 kb mitochondrial genome into the nucleus of the common ancestor of the five Panthera genus species: tiger, P. tigris; snow leopard, P. uncia; jaguar, P. onca; leopard, P. pardus; and lion, P. leo. This nuclear integration, representing 74% of the mitochondrial genome, is one of the largest to be reported in eukaryotes. The Panthera genus numt differs from the numt previously described in the Felis genus in: (1) chromosomal location (F2 -telomeric region vs. D2 -centromeric region), (2) gene make up (from the ND5 to the ATP8 vs. from the CR to the COII), (3) size (12.5 kb vs. 7.9 kb), and (4) structure (single monomer vs. tandemly repeated in Felis). These distinctions indicate that the origin of this large numt fragment in the nuclear genome of the Panthera species is an independent insertion from that of the domestic cat lineage, which has been further supported by phylogenetic analyses. The tiger cymtDNA shared around 90% sequence identity with the homologous numt sequence, suggesting an origin for the Panthera numt at around 3.5 million years ago, prior to the radiation of the five extant Panthera species. Keywords big cats; mitochondrial DNA; nuclear insertion; numt; Panthera genus; pseudogene; tiger Abbreviations ATP8, ATP synthase subunit 8; bp, base pairs; Cyt b, cytochrome b; COI, cytochrome c oxidase subunit I; COII, cytochrome c oxidase subunit II; cymtDNA, cytoplasmic mitochondrial DNA; CR, control region; kb, kilobase(s); FISH, fluorescence in situ hybridization; MYA, million years ago; mtDNA, mitochondrial DNA; ND1, NADH dehydrogenase subunit 1; ND2, NADH dehydrogenase subunit 2; ND5, NADH dehydrogenase subunit 5; ND6, NADH dehydrogenase subunit 6; PCR, polymerase chain reaction; RFLP, restriction fragment length polymorphism; 16S, 16S ribosomal RNA; 12S, 12S ribosomal RNA

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Punctuated evolution of mitochondrial gene content: High and variable rates of mitochondrial gene loss and transfer to the nucleus during angiosperm evolution

Cited by 389 publications

References 56 publications

Miniaturized mitogenome of the parasitic plant Viscum scurruloideum is extremely divergent and dynamic and has lost all nad genes

Miniaturized mitogenome of the parasitic plant Viscum scurruloideum is extremely divergent and dynamic and has lost all nad genes

RNA interference: The molecular immune system

Evolutionary analysis of a large mtDNA translocation (numt) into the nuclear genome of the Panthera genus species

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