Extensive Shifts from <i>Cis</i>- to <i>Trans</i>-splicing of Gymnosperm Mitochondrial Introns

Guo, Wenhu; Zhu, Andan; Fan, Weishu; Adams, Robert P.; Mower, Jeffrey P.

doi:10.1093/molbev/msaa029

Cited by 37 publications

(57 citation statements)

References 47 publications

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“…Other NADH-ubiquinone oxidoreductase genes (specifically nad1, nad2, and nad5) typically contain trans-splicing introns (Chapdelaine and Bonen 1991;Knoop, et al 1991;Binder, et al 1992), but this is not the case for nad7 in most angiosperm mitogenomes. Such transitions from cis-to trans-splicing are relatively common in plant mitochondria (Qiu and Palmer 2004), and it was recently shown that the Pinaceae has independently evolved transsplicing of this same nad7 intron (Guo, et al 2020).…”

Section: Agrostemma Githago and Silene Chalcedonicamentioning

confidence: 99%

Rapid shifts in mitochondrial tRNA import in a plant lineage with extensive mitochondrial tRNA gene loss

Warren

Salinas‐Giegé

Triant

et al. 2021

Preprint

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In most eukaryotes, transfer RNAs (tRNAs) are one of the very few classes of genes remaining in the mitochondrial genome, but some mitochondria have lost these vestiges of their prokaryotic ancestry. Sequencing of mitogenomes from the flowering plant genus Silene previously revealed a large range in tRNA gene content, suggesting rapid and ongoing gene loss/replacement. Here, we use this system to test longstanding hypotheses about how mitochondrial tRNA genes are replaced by importing nuclear-encoded tRNAs. We traced the evolutionary history of these gene loss events by sequencing mitochondrial genomes from key outgroups (Agrostemma githago and Silene [=Lychnis] chalcedonica). We then performed the first global sequencing of purified plant mitochondrial tRNA populations to characterize the expression of mitochondrial-encoded tRNAs and the identity of imported nuclear-encoded tRNAs. We also confirmed the utility of high-throughput sequencing methods for the detection of tRNA import by sequencing mitochondrial tRNA populations in a species (Solanum tuberosum) with known tRNA trafficking patterns. Mitochondrial tRNA sequencing in Silene revealed substantial shifts in the abundance of some nuclear-encoded tRNAs in conjunction with their recent history of mt-tRNA gene loss and surprising cases where tRNAs with anticodons still encoded in the mitochondrial genome also appeared to be imported. These data suggest that nuclear-encoded counterparts are likely replacing mitochondrial tRNAs even in systems with recent mitochondrial tRNA gene loss, and the redundant import of a nuclear-encoded tRNA may provide a mechanism for functional replacement between translation systems separated by billions of years of evolutionary divergence.

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Section: Agrostemma Githago and Silene Chalcedonicamentioning

confidence: 99%

Rapid shifts in mitochondrial tRNA import in a plant lineage with extensive mitochondrial tRNA gene loss

Warren

Salinas‐Giegé

Triant

et al. 2021

Preprint

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“…2016 ). This year saw a number of mitochondrial genomes published in short succession ( Guo et al. 2020 ; Kan et al.…”

Section: Introductionmentioning

confidence: 99%

“…Also, trans -spliced genes are common in mitochondrial genomes ( Kamikawa et al. 2016 ; Guo et al. 2020 ), and no purpose-built software tool exists for identifying and annotating trans -spliced genes.…”

Section: Introductionmentioning

confidence: 99%

Complete Mitochondrial Genome of a Gymnosperm, Sitka Spruce (Picea sitchensis), Indicates a Complex Physical Structure

Jackman

Coombe

Warren

et al. 2020

Genome Biology and Evolution

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Plant mitochondrial genomes vary widely in size. Although many plant mitochondrial genomes have been sequenced and assembled, the vast majority are of angiosperms, and few are of gymnosperms. Most plant mitochondrial genomes are smaller than a megabase, with a few notable exceptions. We have sequenced and assembled the complete 5.5 Mbp mitochondrial genome of Sitka spruce (Picea sitchensis), to date, one of the largest mitochondrial genomes of a gymnosperm. We sequenced the whole genome using Oxford Nanopore MinION, and then identified contigs of mitochondrial origin assembled from these long reads based on sequence homology to the white spruce mitochondrial genome. The assembly graph shows a multipartite genome structure, composed of one smaller 168 kbp circular segment of DNA, and a larger 5.4 Mbp single component with a branching structure. The assembly graph gives insight into a putative complex physical genome structure, and its branching points may represent active sites of recombination.

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“…Moreover, studies on intra-specific mitogenome variation demonstrated that a genome rearrangement or a frequency shift between different mitotypes in an individual could occur in a short time [30][31][32]. This extreme genome rearrangement can affect a gene order and shift the splicing mode (from cis to trans) of introns [33]. In angiosperms, it was estimated that the shift in one of the introns of the nad1 gene (nad1i728), which contains the matR gene within it, occurred at least 15 times [34].…”

Section: Introductionmentioning

confidence: 99%

Comparative Mitogenomic Analysis Reveals Gene and Intron Dynamics in Rubiaceae and Intra-Specific Diversification in Damnacanthus indicus

Han

Cho

Tamaki

et al. 2021

IJMS

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The dynamic evolution of mitochondrial gene and intron content has been reported across the angiosperms. However, a reference mitochondrial genome (mitogenome) is not available in Rubiaceae. The phylogenetic utility of mitogenome data at a species level is rarely assessed. Here, we assembled mitogenomes of six Damnacanthus indicus (Rubiaceae, Rubioideae) representing two varieties (var. indicus and var. microphyllus). The gene and intron content of D. indicus was compared with mitogenomes from representative angiosperm species and mitochondrial contigs from the other Rubiaceae species. Mitogenome structural rearrangement and sequence divergence in D. indicus were analyzed in six individuals. The size of the mitogenome in D. indicus varied from 417,661 to 419,435 bp. Comparing the number of intact mitochondrial protein-coding genes in other Gentianales taxa (38), D. indicus included 32 genes representing several losses. The intron analysis revealed a shift from cis to trans splicing of a nad1 intron (nad1i728) in D. indicus and it is a shared character with the other four Rubioideae taxa. Two distinct mitogenome structures (type A and B) were identified. Two-step direct repeat-mediated recombination was proposed to explain structural changes between type A and B mitogenomes. The five individuals from two varieties in D. indicus diverged well in the whole mitogenome-level comparison with one exception. Collectively, our study elucidated the mitogenome evolution in Rubiaceae along with D. indicus and showed the reliable phylogenetic utility of the whole mitogenome data at a species-level evolution.

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Extensive Shifts from Cis- to Trans-splicing of Gymnosperm Mitochondrial Introns

Cited by 37 publications

References 47 publications

Rapid shifts in mitochondrial tRNA import in a plant lineage with extensive mitochondrial tRNA gene loss

Rapid shifts in mitochondrial tRNA import in a plant lineage with extensive mitochondrial tRNA gene loss

Complete Mitochondrial Genome of a Gymnosperm, Sitka Spruce (Picea sitchensis), Indicates a Complex Physical Structure

Comparative Mitogenomic Analysis Reveals Gene and Intron Dynamics in Rubiaceae and Intra-Specific Diversification in Damnacanthus indicus

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