Rapid Evolution of Enormous, Multichromosomal Genomes in Flowering Plant Mitochondria with Exceptionally High Mutation Rates

Sloan, Daniel B.; Alverson, Andrew J.; Chuckalovcak, John P.; Wu, Martin; McCauley, David E.; Palmer, Jeffrey D.; Taylor, Douglas R.

doi:10.1371/journal.pbio.1001241

Cited by 542 publications

(721 citation statements)

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“…Although consistent with our previous findings (22), the low level of nucleotide polymorphism within S. noctiflora mtDNA is surprising given the history of rapid nucleotide substitution in this species. The lack of polymorphism may reflect a very low effective population size and/or a recent reversion to lower mitochondrial mutation rates in S. noctiflora (22). Of the identified SNPs, 498 are transitions (Ti), and 1,846 are transversions (Tv), producing a Ti:Tv ratio of 0.27.…”

Section: S Noctiflora Osr and Brp Mitochondrial Genomes Vary In Thesupporting

confidence: 90%

“…The BRP mitochondrial genome was compared with a previously published mitochondrial genome from S. noctiflora (22). The original genome was derived from a roadside population of S. noctiflora on Old Schoolhouse Road (OSR) in Eggleston, VA.…”

Section: Resultsmentioning

confidence: 99%

“…Instead, like the rest of the genome, these chromosomes consist mostly or entirely of noncoding sequence. Some of this noncoding sequence can be traced to insertions of nuclear or plastid DNA, but the vast majority lacks detectable similarity to any known DNA sequence (22).…”

Section: S Noctiflora Osr and Brp Mitochondrial Genomes Vary In Thementioning

confidence: 99%

“…In contrast, mitochondrial genomes in many other eukaryotes have been radically transformed or even lost entirely. One recurring evolutionary pattern is the fragmentation of mitochondrial DNA (mtDNA) into multichromosomal genomes, which has occurred independently in a wide variety of taxa, including kinetoplastids (8), diplonemids (9), dinoflagellates (10), the green alga Polytomella parva (11), ichthyosporean protists (12), chytrid fungi (13), and multiple lineages of both metazoans (14)(15)(16)(17)(18)(19)(20) and angiosperms (21)(22)(23). The fragmentation of genomes into chromosomes is a very general property of eukaryotic nuclear genomes.…”

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confidence: 99%

“…The most extreme examples of multichromosomal mitochondrial genomes have been found within the genus Silene (Caryophyllaceae). In this genus, species with accelerated rates of mitochondrial substitution harbor exceptionally large mitochondrial genomes that have been fragmented into dozens of circular-mapping chromosomes (22). For example, the sequenced mitochondrial genome of Silene noctiflora (6.7 Mb) is larger than most free-living bacterial genomes and consists of 59 chromosomes ranging in size from 66 to 192 kb.…”

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confidence: 99%

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The massive mitochondrial genome of the angiosperm Silene noctiflora is evolving by gain or loss of entire chromosomes

Cuthbert

Taylor

et al. 2015

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

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Across eukaryotes, mitochondria exhibit staggering diversity in genomic architecture, including the repeated evolution of multichromosomal structures. Unlike in the nucleus, where mitosis and meiosis ensure faithful transmission of chromosomes, the mechanisms of inheritance in fragmented mitochondrial genomes remain mysterious. Multichromosomal mitochondrial genomes have recently been found in multiple species of flowering plants, including Silene noctiflora, which harbors an unusually large and complex mitochondrial genome with more than 50 circular-mapping chromosomes totaling ∼7 Mb in size. To determine the extent to which such genomes are stably maintained, we analyzed intraspecific variation in the mitochondrial genome of S. noctiflora. Complete genomes from two populations revealed a high degree of similarity in the sequence, structure, and relative abundance of mitochondrial chromosomes. For example, there are no inversions between the genomes, and there are only nine SNPs in 25 kb of protein-coding sequence. Remarkably, however, these genomes differ in the presence or absence of 19 entire chromosomes, all of which lack any identifiable genes or contain only duplicate gene copies. Thus, these mitochondrial genomes retain a full gene complement but carry a highly variable set of chromosomes that are filled with presumably dispensable sequence. In S. noctiflora, conventional mechanisms of mitochondrial sequence divergence are being outstripped by an apparently nonadaptive process of whole-chromosome gain/loss, highlighting the inherent challenge in maintaining a fragmented genome. We discuss the implications of these findings in relation to the question of why mitochondria, more so than plastids and bacterial endosymbionts, are prone to the repeated evolution of multichromosomal genomes. meiosis | mitochondrial DNA | mitosis | multichromosomal | multipartite

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Section: S Noctiflora Osr and Brp Mitochondrial Genomes Vary In Thesupporting

confidence: 90%

Section: Resultsmentioning

confidence: 99%

Section: S Noctiflora Osr and Brp Mitochondrial Genomes Vary In Thementioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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The massive mitochondrial genome of the angiosperm Silene noctiflora is evolving by gain or loss of entire chromosomes

Cuthbert

Taylor

et al. 2015

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

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118

106

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Plant Mitochondria

Ghifari¹,

Murcha²

2020

Encyclopedia of Life Sciences

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Plant mitochondria, like the mitochondria of other eukaryotes, originated from an endosymbiotic event and have retained their own genome. Over a billion years of evolution, most mitochondrial genes are laterally transferred to the nucleus. Consequently, most proteins required for mitochondrial biogenesis and activity are synthesised in the cytosol and imported via specific protein import machineries. Mitochondria are energy‐generating organelles that via electron transfer chain (ETC), create a proton gradient and generate adenosine triphosphate (ATP), the energy chemical used by the cell for numerous biochemical reactions. Energy production can come at a cost as reactive oxygen species (ROS) are generated as by‐product. Plant mitochondria have alternative ETC pathways to regulate mitochondrial ROS (mtROS) through modulating the rate of redox reactions, proton gradient and ATP production. Although excessive ROS can damage cellular components and lead to programmed cell death, mtROS also play an important role as signalling molecules. mtROS are involved in nucleus–mitochondria communications (anterograde–retrograde signalling), mitochondrial autophagy (mitophagy) and play a role in the plant response to various environmental stimuli. Considering the pivotal roles of mitochondria in energy generation and cellular signalling, perturbation of mitochondrial biogenesis and activity renders plants to be more susceptible to various stresses and ultimately compromises plant growth, development and reproduction. Key Concepts Plant mitochondria are small (1–2 μm long) rod‐shaped organelle that undergo frequent fusion and fission events. The plant mitochondrial inner membrane houses protein complexes involved in the electron transfer chain (ETC) that creates a proton‐motive gradient across the intermembrane space to drive the production of adenosine triphosphate (ATP) through ATP synthase. The majority of plant mitochondrial proteins (approximately 2000) are encoded in the nuclear genome, whereas the plant mitochondrial genome contains around 50 genes encoding for ETC subunits, mitoribosomal translation machinery and transfer ribonucleic acids (tRNAs). The abundance of mtROS produced by the ETC is proportionally linked with the efficiency and rate of electron transfer and ATP production. Plant mitochondria have alternative ETC pathways to modulate ROS homeostasis, proton gradient and ATP production. mtROS can damage mitochondrial macromolecules and ultimately organelle function but are also important signalling molecules in various pathways, including stress response and anterograde–retrograde signalling. The nucleus controls mitochondrial gene expression through anterograde signalling, yet the mitochondria can also influence nuclear gene expression through retrograde signalling. Disrupted plant mitochondrial function often causes enhanced sensitivity to a number of stresses, disrupted pollen development in cytoplasmic male sterility and affects normal plant growth and development.

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Mitochondrial Dna Repair and Genome Evolution

Christensen¹

2017

Annual Plant Reviews, Volume 50

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Rapid Evolution of Enormous, Multichromosomal Genomes in Flowering Plant Mitochondria with Exceptionally High Mutation Rates

Abstract: A pair of species within the genus Silene have evolved the largest known mitochondrial genomes, coinciding with extreme changes in mutation rate, recombination activity, and genome structure.

Cited by 542 publications

References 106 publications

The massive mitochondrial genome of the angiosperm Silene noctiflora is evolving by gain or loss of entire chromosomes

The massive mitochondrial genome of the angiosperm Silene noctiflora is evolving by gain or loss of entire chromosomes

Plant Mitochondria

Mitochondrial Dna Repair and Genome Evolution

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