The Cross‐Talk between Genomes: How Co‐Evolution Shaped Plant Mitochondrial Gene Expression

Budar, Françoise; Mireau, Hakim

doi:10.1002/9781119312994.apr0545

Cited by 4 publications

(7 citation statements)

References 198 publications

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“…Intergenomic coevolution between the nucleus and organelle(s) is a common feature among eukaryotes. Gene loss and transfers to the nucleus have greatly reduced the coding regions of modern mitochondrial and plastid genomes to a limited number of essential genes ( Greiner and Bock 2013 ; Budar and Mireau 2018 ; Giannakis et al 2021 ). Consequently, these organelles must coordinate transcripts and protein products from 2 or more different genomic compartments to carry out essential cellular functions.…”

Section: Introductionmentioning

confidence: 99%

“…biparental for the nucleus and cytoplasmic for the organelles) can lead to incompatibilities between nuclear and organellar alleles, particularly in hybrid lineages ( Camus et al 2022 ). These cytonuclear incompatibilities are widespread among species and can have dramatic consequences for fitness ( Fishman and Willis 2006 ; Hill 2017 ; Fishman and Sweigart 2018 ; Postel and Touzet 2020 ), even leading to hybrid breakdown in some cases ( Burke and Arnold 2001 ; Greiner et al 2011 ; Burton and Barreto 2012 ; Burton et al 2013 ; Budar and Mireau 2018 ).…”

Section: Introductionmentioning

confidence: 99%

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Variation in cytonuclear expression accommodation among allopolyploid plants

et al. 2022

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Cytonuclear coevolution is a common feature among plants, which coordinates gene expression and protein products between the nucleus and organelles. Consequently, lineage-specific differences may result in incompatibilities between the nucleus and cytoplasm in hybrid taxa. Allopolyploidy is also a common phenomenon in plant evolution. The hybrid nature of allopolyploids may result in cytonuclear incompatibilities, but the massive nuclear redundancy created during polyploidy affords additional avenues for resolving cytonuclear conflict (i.e., cytonuclear accommodation). Here we evaluate expression changes in organelle-targeted nuclear genes for six allopolyploid lineages that represent four genera (i.e., Arabidopsis, Arachis, Chenopodium, and Gossypium) and encompass a range in polyploid ages. Because incompatibilities between the nucleus and cytoplasm could potentially result in biases toward the maternal homoeolog and/or maternal expression level, we evaluate patterns of homoeolog usage, expression bias, and expression-level dominance in cytonuclear genes relative to the background of non-cytonuclear expression changes and to the diploid parents. Although we find subsets of cytonuclear genes in most lineages that match our expectations of maternal preference, these observations are not consistent among either allopolyploids or categories of organelle-targeted genes. Our results indicate that cytonuclear expression evolution may be subtle and variable among genera and genes, likely reflecting a diversity of mechanisms to resolve nuclear-cytoplasmic incompatibilities in allopolyploid species.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Variation in cytonuclear expression accommodation among allopolyploid plants

et al. 2022

View full text Add to dashboard Cite

show abstract

Section: Introductionmentioning

confidence: 99%

“…Intergenomic coevolution between the nucleus and organelle(s) is a common feature among eukaryotes. Gene loss and transfers to the nucleus have greatly reduced the coding regions of modern mitochondrial and plastid genomes to a limited number of essential genes (Greiner and Bock 2013;Budar and Mireau 2018;Giannakis et al 2021). Consequently, these organelles must coordinate transcripts and protein products from two or more different genomic compartments to carry out essential cellular functions.…”

Section: Introductionmentioning

confidence: 99%

“…Over time, this functional interdependence results in coadaptation between the nucleus and each organelle; however, differences in mode of inheritance (i.e., biparental for the nucleus and cytoplasmic for the organelles) can lead to incompatibilities between nuclear and organellar alleles, particularly in hybrid lineages. These cytonuclear incompatibilities are widespread among species and can have dramatic consequences for fitness (Fishman and Willis 2006;Hill 2017;Fishman and Sweigart 2018;Postel and Touzet 2020), even leading to hybrid breakdown in some cases (Burke and Arnold 2001;Greiner et al 2011;Burton and Barreto 2012;Burton et al 2013;Budar and Mireau 2018).…”

Section: Introductionmentioning

confidence: 99%

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Variation in cytonuclear expression accommodation among allopolyploid plants

Grover

Forsythe

Sharbrough

et al. 2022

Preprint

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Cytonuclear coevolution is a common feature among plants, which coordinates gene expression and protein products between the nucleus and organelles. Consequently, lineage-specific differences may result in incompatibilities between the nucleus and cytoplasm in hybrid taxa. Allopolyploidy is also a common phenomenon in plant evolution. The hybrid nature of allopolyploids may result in cytonuclear incompatibilities, but the massive nuclear redundancy created during polyploidy affords additional avenues for resolving cytonuclear conflict (i.e., cytonuclear accommodation). Here we evaluate expression changes in organelle-targeted nuclear genes for six allopolyploid lineages that represent four genera (i.e., Arabidopsis, Arachis, Chenopodium, and Gossypium) and encompass a range in polyploid ages. Because incompatibilities between the nucleus and cytoplasm could potentially result in biases toward the maternal homoeolog and/or maternal expression level, we evaluate patterns of homoeolog usage, expression bias, and expression level dominance in cytonuclear genes relative to the background of non-cytonuclear expression changes and to the diploid parents. Although we find subsets of cytonuclear genes in most lineages that match our expectations of maternal preference, these observations are not consistent among either allopolyploids or categories of organelle-targeted genes. Our results indicate that cytonuclear expression accommodation may be a subtle and/or variable phenomenon that does not capture the full range of mechanisms by which allopolyploid plants resolve nuclear-cytoplasmic incompatibilities.

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Deficiency of mitoribosomal S10 protein affects translation and splicing in Arabidopsis mitochondria

Kwasniak-Owczarek

Kaźmierczak

Tomal

et al. 2019

Nucleic Acids Research

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The ribosome is not only a protein-making machine, but also a regulatory element in protein synthesis. This view is supported by our earlier data showing that Arabidopsis mitoribosomes altered due to the silencing of the nuclear RPS10 gene encoding mitochondrial ribosomal protein S10 differentially translate mitochondrial transcripts compared with the wild-type. Here, we used ribosome profiling to determine the contribution of transcriptional and translational control in the regulation of protein synthesis in rps10 mitochondria compared with the wild-type ones. Oxidative phosphorylation system proteins are preferentially synthesized in wild-type mitochondria but this feature is lost in the mutant. The rps10 mitoribosomes show slightly reduced translation efficiency of most respiration-related proteins and at the same time markedly more efficiently synthesize ribosomal proteins and MatR and TatC proteins. The mitoribosomes deficient in S10 protein protect shorter transcript fragments which exhibit a weaker 3-nt periodicity compared with the wild-type. The decrease in the triplet periodicity is particularly drastic for genes containing introns. Notably, splicing is considerably less effective in the mutant, indicating an unexpected link between the deficiency of S10 and mitochondrial splicing. Thus, a shortage of the mitoribosomal S10 protein has wide-ranging consequences on mitochondrial gene expression.

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The Cross‐Talk between Genomes: How Co‐Evolution Shaped Plant Mitochondrial Gene Expression

Cited by 4 publications

References 198 publications

Variation in cytonuclear expression accommodation among allopolyploid plants

Variation in cytonuclear expression accommodation among allopolyploid plants

Variation in cytonuclear expression accommodation among allopolyploid plants

Deficiency of mitoribosomal S10 protein affects translation and splicing in Arabidopsis mitochondria

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