Multichromosomal structure and foreign tracts in the Ombrophytum subterraneum (Balanophoraceae) mitochondrial genome

Roulet, M. Emilia; García, Laura E.; Gandini, Carolina L.; Sato, Héctor Arnaldo; Ponce, Gabriela; Sanchez‐Puerta, M. Virginia

doi:10.1007/s11103-020-01014-x

Cited by 32 publications

(35 citation statements)

References 74 publications

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“…Homologous recombination between native and horizontally acquired genes has been described in many angiosperm mtDNAs (Cho et al ., 1998; Bergthorsson et al ., 2003; Barkman et al ., 2007; Sanchez‐Puerta et al ., 2008; Hao et al ., 2010; Hepburn et al ., 2012; Park et al ., 2015; Roulet et al ., 2020). However, this is the first evidence in plants that this process can lead to the replacement of an entire native gene, much less do so as part of an HGT event itself.…”

Section: Discussionmentioning

confidence: 99%

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Horizontal gene transfers dominate the functional mitochondrial gene space of a holoparasitic plant

et al. 2020

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Summary Although horizontal gene transfer (HGT) is common in angiosperm mitochondrial DNAs (mtDNAs), few cases of functional foreign genes have been identified. The one outstanding candidate for large‐scale functional HGT is the holoparasite Lophophytum mirabile, whose mtDNA has lost most native genes but contains intact foreign homologs acquired from legume host plants. To investigate the extent to which this situation results from functional replacement of native by foreign genes, functional mitochondrial gene transfer to the nucleus, and/or loss of mitochondrial biochemical function in the context of extreme parasitism, we examined the Lophophytum mitochondrial and nuclear transcriptomes by deep paired‐end RNA sequencing. Most foreign mitochondrial genes in Lophophytum are highly transcribed, accurately spliced, and efficiently RNA edited. By contrast, we found no evidence for functional gene transfer to the nucleus or loss of mitochondrial functions in Lophophytum. Many functional replacements occurred via the physical replacement of native genes by foreign genes. Some of these events probably occurred as the final act of HGT itself. Lophophytum mtDNA has experienced an unprecedented level of functional replacement of native genes by foreign copies. This raises important questions concerning population‐genetic and molecular regimes that underlie such a high level of foreign gene takeover.

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Section: Discussionmentioning

confidence: 99%

“…a Based onSanchez-Puerta et al (2017) andRoulet et al (2020).b P ≤ 0.05 are in bold. c Number of first and second codon position editing sites at which ≥ 70% of RNA reads show C-to-U editing.…”

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confidence: 99%

Horizontal gene transfers dominate the functional mitochondrial gene space of a holoparasitic plant

et al. 2020

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“…In contrast, angiosperm mitogenomes are remarkably divergent in size, structure, and mutation rate. Most angiosperm mt genomes contain 24 to 41 protein coding genes, three rRNA genes, and two or three rRNA genes [ 2 , 3 , 4 , 5 , 6 , 7 ]. Recent mitochondrial genome studies have demonstrated horizontal gene transfer (HGT) and intracellular gene transfer (IGT) [ 5 , 8 , 9 , 10 , 11 ].…”

Section: Introductionmentioning

confidence: 99%

Complete Plastid and Mitochondrial Genomes of Aeginetia indica Reveal Intracellular Gene Transfer (IGT), Horizontal Gene Transfer (HGT), and Cytoplasmic Male Sterility (CMS)

Choi

Park

2021

IJMS

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Orobanchaceae have become a model group for studies on the evolution of parasitic flowering plants, and Aeginetia indica, a holoparasitic plant, is a member of this family. In this study, we assembled the complete chloroplast and mitochondrial genomes of A. indica. The chloroplast and mitochondrial genomes were 56,381 bp and 401,628 bp long, respectively. The chloroplast genome of A. indica shows massive plastid genes and the loss of one IR (inverted repeat). A comparison of the A. indica chloroplast genome sequence with that of a previous study demonstrated that the two chloroplast genomes encode a similar number of proteins (except atpH) but differ greatly in length. The A. indica mitochondrial genome has 53 genes, including 35 protein-coding genes (34 native mitochondrial genes and one chloroplast gene), 15 tRNA (11 native mitochondrial genes and four chloroplast genes) genes, and three rRNA genes. Evidence for intracellular gene transfer (IGT) and horizontal gene transfer (HGT) was obtained for plastid and mitochondrial genomes. ψndhB and ψcemA in the A. indica mitogenome were transferred from the plastid genome of A. indica. The atpH gene in the plastid of A. indica was transferred from another plastid angiosperm plastid and the atpI gene in mitogenome A. indica was transferred from a host plant like Miscanthus siensis. Cox2 (orf43) encodes proteins containing a membrane domain, making ORF (Open Reading Frame) the most likely candidate gene for CMS development in A. indica.

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“…Relative to other species in Santalales with available sequenced mitogenome, the mitogenome size of T. maclurei is the second smallest, higher than that of Viscum scurruloideum (Skippington et al, 2015), but much smaller than those of Ombrophytum subterraneum (Roulet et al, 2020) and Lophophytum mirabile (Sanchez-Puerta et al, 2019). The overall GC content is 44.4%, which is similar to other species of Santalales (44.2-47.4%) (Skippington et al, 2015;Sanchez-Puerta et al, 2019;Roulet et al, 2020). Depth of coverage across the whole mitogenome except the MTPTs are relatively even, indicating the continuity of our assembly (Fig.…”

Section: Mitogenome Structure and Gene Contentmentioning

confidence: 84%

Shifts from cis-to trans-splicing of five mitochondrial introns in Tolypanthus maclurei

Yu¹,

Sun²,

Liu³

et al. 2021

PeerJ

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Shifts from cis-to trans-splicing of mitochondrial introns tend to correlate with relative genome rearrangement rates during vascular plant evolution, as is particularly apparent in some lineages of gymnosperms. However, although many angiosperms have also relatively high mitogenomic rearrangement rates, very few cis-to trans-splicing shifts except for five trans-spliced introns shared in seed plants have been reported. In this study, we sequenced and characterized the mitogenome of Tolypanthus maclurei, a hemiparasitic plant from the family Loranthaceae (Santalales). The mitogenome was assembled into a circular chromosome of 256,961 bp long, relatively small compared with its relatives from Santalales. It possessed a gene content of typical angiosperm mitogenomes, including 33 protein-coding genes, three rRNA genes and ten tRNA genes. Plastid-derived DNA fragments took up 9.1% of the mitogenome. The mitogenome contained one group I intron (cox1i729) and 23 group II introns. We found shifts from cis-to trans-splicing of five additional introns in its mitogenome, of which two are specific in T. maclurei. Moreover, atp1 is a chimeric gene and phylogenetic analysis indicated that a 356 bp region near the 3′ end of atp1 of T. maclurei was acquired from Lamiales via horizontal gene transfer. Our results suggest that shifts to trans-splicing of mitochondrial introns may not be uncommon among angiosperms.

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Multichromosomal structure and foreign tracts in the Ombrophytum subterraneum (Balanophoraceae) mitochondrial genome

Cited by 32 publications

References 74 publications

Horizontal gene transfers dominate the functional mitochondrial gene space of a holoparasitic plant

Horizontal gene transfers dominate the functional mitochondrial gene space of a holoparasitic plant

Complete Plastid and Mitochondrial Genomes of Aeginetia indica Reveal Intracellular Gene Transfer (IGT), Horizontal Gene Transfer (HGT), and Cytoplasmic Male Sterility (CMS)

Shifts from cis-to trans-splicing of five mitochondrial introns in Tolypanthus maclurei

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