Evolutionary transfers of mitochondrial genes to the nucleus in the <i>Populus</i> lineage and coexpression of nuclear and mitochondrial <i>Sdh4</i> genes

Choi, Catherine; Liu, Zhenlan; Adams, Keith L.

doi:10.1111/j.1469-8137.2006.01821.x

Cited by 25 publications

(20 citation statements)

References 47 publications

(63 reference statements)

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“…Altogether our data revealed a short divergence in terms of evolution and proximity of eukaryotic cells with the mitochondria ancestor. In good agreement with the view concerning the evolutionary history of SDH from mitochondria to nuclear genome, it has been demonstrated that at least some SDH genes were lost during horizontal gene transfer (Adams et al 2002; Choi et al 2006). Taken as a whole this feature might, at least partially, explain cross kingdom differences in the structural architecture of SDH (e.g., A. thaliana has 12 subunits; supplementary table S1, Supplementary Material online).…”

Section: Resultssupporting

confidence: 77%

Evolution and Functional Implications of the Tricarboxylic Acid Cycle as Revealed by Phylogenetic Analysis

Cavalcanti

Esteves‐Ferreira

Quinhones

et al. 2014

Genome Biology and Evolution

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The tricarboxylic acid (TCA) cycle, a crucial component of respiratory metabolism, is composed of a set of eight enzymes present in the mitochondrial matrix. However, most of the TCA cycle enzymes are encoded in the nucleus in higher eukaryotes. In addition, evidence has accumulated demonstrating that nuclear genes were acquired from the mitochondrial genome during the course of evolution. For this reason, we here analyzed the evolutionary history of all TCA cycle enzymes in attempt to better understand the origin of these nuclear-encoded proteins. Our results indicate that prior to endosymbiotic events the TCA cycle seemed to operate only as isolated steps in both the host (eubacterial cell) and mitochondria (alphaproteobacteria). The origin of isoforms present in different cell compartments might be associated either with gene-transfer events which did not result in proper targeting of the protein to mitochondrion or with duplication events. Further in silico analyses allow us to suggest new insights into the possible roles of TCA cycle enzymes in different tissues. Finally, we performed coexpression analysis using mitochondrial TCA cycle genes revealing close connections among these genes most likely related to the higher efficiency of oxidative phosphorylation in this specialized organelle. Moreover, these analyses allowed us to identify further candidate genes which might be used for metabolic engineering purposes given the importance of the TCA cycle during development and/or stress situations.

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Section: Resultssupporting

confidence: 77%

Evolution and Functional Implications of the Tricarboxylic Acid Cycle as Revealed by Phylogenetic Analysis

Cavalcanti

Esteves‐Ferreira

Quinhones

et al. 2014

Genome Biology and Evolution

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“…Coexpression of an organellar gene in two different cellular genetic compartments has only been reported for a few mitochondrial genes (cox2, rpl5, sdh4) in land plants (Adams et al, 1999;Sandoval et al, 2004;Choi et al, 2006). In our study, none of the 18 species tested showed coexpression of n-accD and pt-accD.…”

Section: Discussioncontrasting

confidence: 59%

Potential Functional Replacement of the Plastidic Acetyl-CoA Carboxylase Subunit (accD) Gene by Recent Transfers to the Nucleus in Some Angiosperm Lineages

et al. 2013

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(M.A.) Eukaryotic cells originated when an ancestor of the nucleated cell engulfed bacterial endosymbionts that gradually evolved into the mitochondrion and the chloroplast. Soon after these endosymbiotic events, thousands of ancestral prokaryotic genes were functionally transferred from the endosymbionts to the nucleus. This process of functional gene relocation, now rare in eukaryotes, continues in angiosperms. In this article, we show that the chloroplastic acetyl-CoA carboxylase subunit (accD) gene that is present in the plastome of most angiosperms has been functionally relocated to the nucleus in the Campanulaceae. Surprisingly, the nucleus-encoded accD transcript is considerably smaller than the plastidic version, consisting of little more than the carboxylase domain of the plastidic accD gene fused to a coding region encoding a plastid targeting peptide. We verified experimentally the presence of a chloroplastic transit peptide by showing that the product of the nuclear accD fused to green fluorescent protein was imported in the chloroplasts. The nuclear gene regulatory elements that enabled the erstwhile plastidic gene to become functional in the nuclear genome were identified, and the evolution of the intronic and exonic sequences in the nucleus is described. Relocation and truncation of the accD gene is a remarkable example of the processes underpinning endosymbiotic evolution.

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“…Moreover, the mitochondrial copy lacks nonsense mutations and transcriptome data showed that the mitochondrial rps14 is co-transcribed with rpl5 (Figure 3A) as a reported for tobacco [19]. Following transfers to the nucleus, the co-existence of putative functional nuclear and mitochondrial gene copies has been suggested for only three genes among angiosperms, including cox2 in some Fabaceae [55], rpl5 in Triticum [56], and sdh4 in Populus [57]. …”

Section: Discussionmentioning

confidence: 93%

Complete sequences of organelle genomes from the medicinal plant Rhazya stricta(Apocynaceae) and contrasting patterns of mitochondrial genome evolution across asterids

et al. 2014

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BackgroundRhazya stricta is native to arid regions in South Asia and the Middle East and is used extensively in folk medicine to treat a wide range of diseases. In addition to generating genomic resources for this medicinally important plant, analyses of the complete plastid and mitochondrial genomes and a nuclear transcriptome from Rhazya provide insights into inter-compartmental transfers between genomes and the patterns of evolution among eight asterid mitochondrial genomes.ResultsThe 154,841 bp plastid genome is highly conserved with gene content and order identical to the ancestral organization of angiosperms. The 548,608 bp mitochondrial genome exhibits a number of phenomena including the presence of recombinogenic repeats that generate a multipartite organization, transferred DNA from the plastid and nuclear genomes, and bidirectional DNA transfers between the mitochondrion and the nucleus. The mitochondrial genes sdh3 and rps14 have been transferred to the nucleus and have acquired targeting presequences. In the case of rps14, two copies are present in the nucleus; only one has a mitochondrial targeting presequence and may be functional. Phylogenetic analyses of both nuclear and mitochondrial copies of rps14 across angiosperms suggests Rhazya has experienced a single transfer of this gene to the nucleus, followed by a duplication event. Furthermore, the phylogenetic distribution of gene losses and the high level of sequence divergence in targeting presequences suggest multiple, independent transfers of both sdh3 and rps14 across asterids. Comparative analyses of mitochondrial genomes of eight sequenced asterids indicates a complicated evolutionary history in this large angiosperm clade with considerable diversity in genome organization and size, repeat, gene and intron content, and amount of foreign DNA from the plastid and nuclear genomes.ConclusionsOrganelle genomes of Rhazya stricta provide valuable information for improving the understanding of mitochondrial genome evolution among angiosperms. The genomic data have enabled a rigorous examination of the gene transfer events. Rhazya is unique among the eight sequenced asterids in the types of events that have shaped the evolution of its mitochondrial genome. Furthermore, the organelle genomes of R. stricta provide valuable genomic resources for utilizing this important medicinal plant in biotechnology applications.Electronic supplementary materialThe online version of this article (doi: 10.1186/1471-2164-15-405) contains supplementary material, which is available to authorized users.

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Evolutionary transfers of mitochondrial genes to the nucleus in the Populus lineage and coexpression of nuclear and mitochondrial Sdh4 genes

Cited by 25 publications

References 47 publications

Evolution and Functional Implications of the Tricarboxylic Acid Cycle as Revealed by Phylogenetic Analysis

Evolution and Functional Implications of the Tricarboxylic Acid Cycle as Revealed by Phylogenetic Analysis

Potential Functional Replacement of the Plastidic Acetyl-CoA Carboxylase Subunit (accD) Gene by Recent Transfers to the Nucleus in Some Angiosperm Lineages

Complete sequences of organelle genomes from the medicinal plant Rhazya stricta(Apocynaceae) and contrasting patterns of mitochondrial genome evolution across asterids

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