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1

Forsythe, Evan S., Joel Sharbrough, Justin C. Havird, Jessica M. Warren e Daniel B. Sloan. "CyMIRA: The Cytonuclear Molecular Interactions Reference for Arabidopsis". Genome Biology and Evolution 11, n.º 8 (8 de julho de 2019): 2194–202. http://dx.doi.org/10.1093/gbe/evz144.

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AbstractThe function and evolution of eukaryotic cells depend upon direct molecular interactions between gene products encoded in nuclear and cytoplasmic genomes. Understanding how these cytonuclear interactions drive molecular evolution and generate genetic incompatibilities between isolated populations and species is of central importance to eukaryotic biology. Plants are an outstanding system to investigate such effects because of their two different genomic compartments present in the cytoplasm (mitochondria and plastids) and the extensive resources detailing subcellular targeting of nuclear-encoded proteins. However, the field lacks a consistent classification scheme for mitochondrial- and plastid-targeted proteins based on their molecular interactions with cytoplasmic genomes and gene products, which hinders efforts to standardize and compare results across studies. Here, we take advantage of detailed knowledge about the model angiosperm Arabidopsis thaliana to provide a curated database of plant cytonuclear interactions at the molecular level. CyMIRA (Cytonuclear Molecular Interactions Reference for Arabidopsis) is available at http://cymira.colostate.edu/ and https://github.com/dbsloan/cymira and will serve as a resource to aid researchers in partitioning evolutionary genomic data into functional gene classes based on organelle targeting and direct molecular interaction with cytoplasmic genomes and gene products. It includes 11 categories (and 27 subcategories) of different cytonuclear complexes and types of molecular interactions, and it reports residue-level information for cytonuclear contact sites. We hope that this framework will make it easier to standardize, interpret, and compare studies testing the functional and evolutionary consequences of cytonuclear interactions.
2

Roux, Fabrice, Tristan Mary-Huard, Elise Barillot, Estelle Wenes, Lucy Botran, Stéphanie Durand, Romain Villoutreix, Marie-Laure Martin-Magniette, Christine Camilleri e Françoise Budar. "Cytonuclear interactions affect adaptive traits of the annual plant Arabidopsis thaliana in the field". Proceedings of the National Academy of Sciences 113, n.º 13 (15 de março de 2016): 3687–92. http://dx.doi.org/10.1073/pnas.1520687113.

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Although the contribution of cytonuclear interactions to plant fitness variation is relatively well documented at the interspecific level, the prevalence of cytonuclear interactions at the intraspecific level remains poorly investigated. In this study, we set up a field experiment to explore the range of effects that cytonuclear interactions have on fitness-related traits in Arabidopsis thaliana. To do so, we created a unique series of 56 cytolines resulting from cytoplasmic substitutions among eight natural accessions reflecting within-species genetic diversity. An assessment of these cytolines and their parental lines scored for 28 adaptive whole-organism phenotypes showed that a large proportion of phenotypic traits (23 of 28) were affected by cytonuclear interactions. The effects of these interactions varied from slight but frequent across cytolines to strong in some specific parental pairs. Two parental pairs accounted for half of the significant pairwise interactions. In one parental pair, Ct-1/Sha, we observed symmetrical phenotypic responses between the two nuclear backgrounds when combined with specific cytoplasms, suggesting nuclear differentiation at loci involved in cytonuclear epistasis. In contrast, asymmetrical phenotypic responses were observed in another parental pair, Cvi-0/Sha. In the Cvi-0 nuclear background, fecundity and phenology-related traits were strongly affected by the Sha cytoplasm, leading to a modified reproductive strategy without penalizing total seed production. These results indicate that natural variation in cytoplasmic and nuclear genomes interact to shape integrative traits that contribute to adaptation, thereby suggesting that cytonuclear interactions can play a major role in the evolutionary dynamics of A. thaliana.
3

Babcock, Christina S., e Marjorie A. Asmussen. "Effects of Differential Selection in the Sexes on Cytonuclear Dynamics: Life Stages With Sex Differences". Genetics 149, n.º 4 (1 de agosto de 1998): 2063–77. http://dx.doi.org/10.1093/genetics/149.4.2063.

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Abstract We extend our investigation of cytonuclear selection by determining when differential selection between the sexes will generate allele frequency changes or cytonuclear disequilibria in populations with constant viability selection and an adult census. We demonstrate analytically that there can be a cytonuclear hitchhiking effect upon a selectively neutral marker in either sex provided the other marker is selected in that sex and there is allelic disequilibrium between the loci in females. Cytonuclear disequilibria are generated de novo in both sexes when both loci affect fitness in females and there is a nonmultiplicative fitness interaction between them. Similar fitness interactions in males generate male disequilibria only. Through numerical analyses, we investigate the potential magnitude of such disequilibria, their qualitative dynamics, the expected frequency of detectable disequilibria under particular patterns or strengths of selection, and the possible disequilibrium sign patterns resulting from selection. These adult/viability results subsume those for populations with a gamete census and either constant fertility or viability selection. Although previous work suggests that the disequilibria generated by cytonuclear selection may be difficult to detect experimentally, this study shows that cytonuclear disequilibria at life stages with sex differences can be useful markers of the presence and strength of selection.
4

Burton, Ronald S., Ricardo J. Pereira e Felipe S. Barreto. "Cytonuclear Genomic Interactions and Hybrid Breakdown". Annual Review of Ecology, Evolution, and Systematics 44, n.º 1 (23 de novembro de 2013): 281–302. http://dx.doi.org/10.1146/annurev-ecolsys-110512-135758.

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5

Rand, David M., Andrew G. Clark e Lisa M. Kann. "Sexually Antagonistic Cytonuclear Fitness Interactions inDrosophila melanogaster". Genetics 159, n.º 1 (1 de setembro de 2001): 173–87. http://dx.doi.org/10.1093/genetics/159.1.173.

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AbstractTheoretical and empirical studies have shown that selection cannot maintain a joint nuclear-cytoplasmic polymorphism within a population except under restrictive conditions of frequency-dependent or sex-specific selection. These conclusions are based on fitness interactions between a diploid autosomal locus and a haploid cytoplasmic locus. We develop a model of joint transmission of X chromosomes and cytoplasms and through simulation show that nuclear-cytoplasmic polymorphisms can be maintained by selection on X-cytoplasm interactions. We test aspects of the model with a “diallel” experiment analyzing fitness interactions between pairwise combinations of X chromosomes and cytoplasms from wild strains of Drosophila melanogaster. Contrary to earlier autosomal studies, significant fitness interactions between X chromosomes and cytoplasms are detected among strains from within populations. The experiment further demonstrates significant sex-by-genotype interactions for mtDNA haplotype, cytoplasms, and X chromosomes. These interactions are sexually antagonistic—i.e., the “good” cytoplasms in females are “bad” in males—analogous to crossing reaction norms. The presence or absence of Wolbachia did not alter the significance of the fitness effects involving X chromosomes and cytoplasms but tended to reduce the significance of mtDNA fitness effects. The negative fitness correlations between the sexes demonstrated in our empirical study are consistent with the conditions that maintain cytoplasmic polymorphism in simulations. Our results suggest that fitness interactions with the sex chromosomes may account for some proportion of cytoplasmic variation in natural populations. Sexually antagonistic selection or reciprocally matched fitness effects of nuclear-cytoplasmic genotypes may be important components of cytonuclear fitness variation and have implications for mitochondrial disease phenotypes that differ between the sexes.
6

Ramsey, Adam J., David E. McCauley e Jennifer R. Mandel. "Heteroplasmy and Patterns of Cytonuclear Linkage Disequilibrium in Wild Carrot". Integrative and Comparative Biology 59, n.º 4 (11 de junho de 2019): 1005–15. http://dx.doi.org/10.1093/icb/icz102.

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Abstract Organellar genomes are considered to be strictly uniparentally-inherited. Uniparental inheritance allows for cytonuclear coevolution and the development of highly coordinated cytonuclear interactions. Yet, instances of biparental inheritance have been documented across eukaryotes. Biparental inheritance in otherwise uniparentally-inherited organelles is termed leakage (maternal or paternal) and allows for the presence of multiple variants of the same organellar genome within an individual, called heteroplasmy. It is unclear what, if any, evolutionary consequences are placed on nuclear and/or organellar genomes due to heteroplasmy. One way of accessing cytonuclear interactions and potential coevolution is through calculating cytonuclear linkage disequilibrium (cnLD), or the non-random association of alleles between nuclear and organellar genomes. Patterns of cnLD can indicate positive or negative cytonuclear selection, coevolution between the nuclear and organellar genomes, non-traditional organellar inheritance, or instances of ancestral heteroplasmy. In plants, cytonuclear interactions have been shown to play a role in cytoplasmic male sterility which occurs in gynodioecious species and is associated with leakage. We used the gynodioecious species, Daucus carota L. spp. carota, or wild carrot, to investigate cnLD. We genotyped a total of 265 individuals from two regions of the USA at 15 nuclear microsatellites, the mitochondrial genes cox1 and atp9, and an intergenic region between trnS and trnG (StoG) in the plastid genome to calculate nuclear–nuclear LD (nucLD), cnLD, and organellar LD (i.e., within the mtDNA and between mtDNA and ptDNA) within the two regions. We were further able to identify cox1 and StoG heteroplasmy and calculate some of the same LD measures within heteroplasmic and homoplasmic (non-heteroplasmic) datasets. We used a Z-transformation test to demonstrate that heteroplasmic individuals display significantly higher levels of cnLD within both regions. In spite of this, within and between organellar LD is low to moderate. Given these patterns of LD in two regions of the USA in which gene flow has been shown to occur between crop and wild carrot, we suggest that heteroplasmy is an evolutionary mechanism which permits the maintenance of cnLD while also acting to disrupt organellar LD.
7

Caruso, Christina M., Andrea L. Case e Maia F. Bailey. "The evolutionary ecology of cytonuclear interactions in angiosperms". Trends in Plant Science 17, n.º 11 (novembro de 2012): 638–43. http://dx.doi.org/10.1016/j.tplants.2012.06.006.

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8

Wolf, Jason B. "CYTONUCLEAR INTERACTIONS CAN FAVOR THE EVOLUTION OF GENOMIC IMPRINTING". Evolution 63, n.º 5 (maio de 2009): 1364–71. http://dx.doi.org/10.1111/j.1558-5646.2009.00632.x.

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9

Forsythe, Evan S., Andrew D. L. Nelson e Mark A. Beilstein. "Biased Gene Retention in the Face of Introgression Obscures Species Relationships". Genome Biology and Evolution 12, n.º 9 (16 de julho de 2020): 1646–63. http://dx.doi.org/10.1093/gbe/evaa149.

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Abstract Phylogenomic analyses are recovering previously hidden histories of hybridization, revealing the genomic consequences of these events on the architecture of extant genomes. We applied phylogenomic techniques and several complementary statistical tests to show that introgressive hybridization appears to have occurred between close relatives of Arabidopsis, resulting in cytonuclear discordance and impacting our understanding of species relationships in the group. The composition of introgressed and retained genes indicates that selection against incompatible cytonuclear and nuclear–nuclear interactions likely acted during introgression, whereas linkage also contributed to genome composition through the retention of ancient haplotype blocks. We also applied divergence-based tests to determine the species branching order and distinguish donor from recipient lineages. Surprisingly, these analyses suggest that cytonuclear discordance arose via extensive nuclear, rather than cytoplasmic, introgression. If true, this would mean that most of the nuclear genome was displaced during introgression whereas only a small proportion of native alleles were retained.
10

Pett, Walker, e Dennis V. Lavrov. "Cytonuclear Interactions in the Evolution of Animal Mitochondrial tRNA Metabolism". Genome Biology and Evolution 7, n.º 8 (27 de junho de 2015): 2089–101. http://dx.doi.org/10.1093/gbe/evv124.

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11

Dowling, Damian K., Tejashwari Meerupati e Göran Arnqvist. "Cytonuclear Interactions and the Economics of Mating in Seed Beetles". American Naturalist 176, n.º 2 (agosto de 2010): 131–40. http://dx.doi.org/10.1086/653671.

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12

Sloan, Daniel B., Deborah A. Triant, Martin Wu e Douglas R. Taylor. "Cytonuclear Interactions and Relaxed Selection Accelerate Sequence Evolution in Organelle Ribosomes". Molecular Biology and Evolution 31, n.º 3 (13 de dezembro de 2013): 673–82. http://dx.doi.org/10.1093/molbev/mst259.

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13

Jelic, Mihailo, Bojan Kenig, Marija Tanaskovic, Marina Stamenkovic-Radak e Marko Andjelkovic. "Relationship between chromosomal and mitochondrial DNA variability of Drosophila subobscura population from the Lazar’s river canyon". Genetika 44, n.º 2 (2012): 409–17. http://dx.doi.org/10.2298/gensr1202409j.

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The genetic structure of Drosophila subobscura population from the Lazar?s River Canyon (Serbia) was studied with respect to restriction site polymorphism of mitochondrial DNA and chromosomal inversion polymorphism. The aim was to shed more light on the role of cytonuclear interactions in shaping mitochondrial DNA variability in this species. Similar to other populations of D. subobscura two main haplotypes (I and II) were found, as well as less common ones that appeared at very low frequencies. The frequency distribution of haplotypes did not depart from neutrality. We did not find statistically significant linkage disequilibrium between the haplotypes belonging to haplogroups I and II and any of the chromosomal arrangements. However, when we compared the data in hereby analyzed population and two previously analyzed populations we observed that haplotype I is more frequent in populations where standard inversion arrangements are less frequent. Pattern of the observed mitochondrial variability could be influenced either directly by environmental variability or through environmentally specific cytonuclear coadaptation.
14

Etterson, Julie R., Stephen R. Keller e Laura F. Galloway. "EPISTATIC AND CYTONUCLEAR INTERACTIONS GOVERN OUTBREEDING DEPRESSION IN THE AUTOTETRAPLOID CAMPANULASTRUM AMERICANUM". Evolution 61, n.º 11 (novembro de 2007): 2671–83. http://dx.doi.org/10.1111/j.1558-5646.2007.00234.x.

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15

Martin, Noland H., e John H. Willis. "Geographical variation in postzygotic isolation and its genetic basis within and between two Mimulus species". Philosophical Transactions of the Royal Society B: Biological Sciences 365, n.º 1552 (27 de agosto de 2010): 2469–78. http://dx.doi.org/10.1098/rstb.2010.0030.

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The aim of this study is to investigate the evolution of intrinsic postzygotic isolation within and between populations of Mimulus guttatus and Mimulus nasutus . We made 17 intraspecific and interspecific crosses, across a wide geographical scale. We examined the seed germination success and pollen fertility of reciprocal F 1 and F 2 hybrids and their pure-species parents, and used biometrical genetic tests to distinguish among alternative models of inheritance. Hybrid seed inviability was sporadic in both interspecific and intraspecific crosses. For several crosses, Dobzhansky–Muller incompatibilities involving nuclear genes were implicated, while two interspecific crosses revealed evidence of cytonuclear interactions. Reduced hybrid pollen fertility was found to be greatly influenced by Dobzhansky–Muller incompatibilities in five out of six intraspecific crosses and nine out of 11 interspecific crosses. Cytonuclear incompatibilities reduced hybrid fitness in only one intraspecific and one interspecific cross. This study suggests that intrinsic postzygotic isolation is common in hybrids between these Mimulus species, yet the particular hybrid incompatibilities responsible for effecting this isolation differ among the populations tested. Hence, we conclude that they evolve and spread only at the local scale.
16

Colombo, N. "TAKING ADVANTAGE OF ORGANELLE GENOMES IN PLANT BREEDING: AN INTEGRATED APPROACH". Journal of Basic and Applied Genetics 30, n.º 1 (julho de 2019): 35–51. http://dx.doi.org/10.35407/bag.2019.xxx.01.05.

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Plant cells carry their genetic information in three compartments: the nucleus, the plastids and the mitochondria. In last years, next-generation sequencing has allowed the development of genomic databases, which are increasingly improving our knowledge about the role of nuclear and cytoplasmic genes as well as their interactions in plant development. However, most plant breeding efforts consider the utilization of the nuclear genome, while less attention is given to plastid and mitochondrial genomes. The objective of this review is to present current knowledge about cytoplasmic and cytonuclear effects on agronomic traits bearing in mind the prospective utilization of all the genomes in plant breeding. Key words: Cytoplasmic genes, cytoplasmic-nuclear interactions, plant breeding methods.
17

Ferreira de Carvalho, Julie, Jérémy Lucas, Gwenaëlle Deniot, Cyril Falentin, Olivier Filangi, Marie Gilet, Fabrice Legeai et al. "Cytonuclear interactions remain stable during allopolyploid evolution despite repeated whole‐genome duplications in Brassica". Plant Journal 98, n.º 3 (25 de fevereiro de 2019): 434–47. http://dx.doi.org/10.1111/tpj.14228.

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18

Abe, T. A., J. R. Spence e F. A. H. Sperling. "Mitochondrial introgression is restricted relative to nuclear markers in a water strider (Hemiptera: Gerridae) hybrid zone". Canadian Journal of Zoology 83, n.º 3 (1 de março de 2005): 432–44. http://dx.doi.org/10.1139/z05-030.

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Although cytonuclear incompatibilities between species have been implicated in a variety of theoretical and experimental studies, the influence of such fitness interactions on gene introgression has been demonstrated in very few hybrid zones. We examined patterns of introgression between two species of Limnoporus Stål, 1868 water striders from 10 populations transecting a hybrid zone in Alberta and British Columbia. DNA-sequence variation in mitochondrial locus COI was compared with two nuclear loci, EF1-α and ITS 1. The spatial distribution of haplotype lineages showed strong barriers to gene exchange for mtDNA. Constraints on introgression were weaker for the nuclear markers, particularly ITS 1. The mtDNA from Limnoporus dissortis Drake and Harris, 1930 was associated with nuclear genes from Limnoporus notabilis Drake and Hottes, 1925 less often than expected by random mating, indicating that some cytoplasmic and nuclear combinations are favored over others and that cytonuclear incompatibilities play a role in structuring this hybrid zone. Mitochondrial mobility across the hybrid zone is likely to be restrained by the unusual hybrid inviability of these species. In a reversal of the pattern expected on the basis of Haldane's rule, females are the XX sex and yet hybrid females are much more inviable than males. Differential removal of hybrid females, which carry mtDNA, can explain disproportionately low mitochondrial introgression across the hybrid zone.
19

Forsythe, Evan S., Alissa M. Williams e Daniel B. Sloan. "Genome-wide signatures of plastid-nuclear coevolution point to repeated perturbations of plastid proteostasis systems across angiosperms". Plant Cell 33, n.º 4 (28 de janeiro de 2021): 980–97. http://dx.doi.org/10.1093/plcell/koab021.

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Abstract Nuclear and plastid (chloroplast) genomes experience different mutation rates, levels of selection, and transmission modes, yet key cellular functions depend on their coordinated interactions. Functionally related proteins often show correlated changes in rates of sequence evolution across a phylogeny [evolutionary rate covariation (ERC)], offering a means to detect previously unidentified suites of coevolving and cofunctional genes. We performed phylogenomic analyses across angiosperm diversity, scanning the nuclear genome for genes that exhibit ERC with plastid genes. As expected, the strongest hits were highly enriched for genes encoding plastid-targeted proteins, providing evidence that cytonuclear interactions affect rates of molecular evolution at genome-wide scales. Many identified nuclear genes functioned in post-transcriptional regulation and the maintenance of protein homeostasis (proteostasis), including protein translation (in both the plastid and cytosol), import, quality control, and turnover. We also identified nuclear genes that exhibit strong signatures of coevolution with the plastid genome, but their encoded proteins lack organellar-targeting annotations, making them candidates for having previously undescribed roles in plastids. In sum, our genome-wide analyses reveal that plastid–nuclear coevolution extends beyond the intimate molecular interactions within chloroplast enzyme complexes and may be driven by frequent rewiring of the machinery responsible for maintenance of plastid proteostasis in angiosperms.
20

Hamzeh, Mona, Christina Sawchyn, Pierre Périnet e Selvadurai Dayanandan. "Asymmetrical natural hybridization between Populus deltoides and P. balsamifera (Salicaceae)This note is one of a selection of papers published in the Special Issue on Poplar Research in Canada." Canadian Journal of Botany 85, n.º 12 (dezembro de 2007): 1227–32. http://dx.doi.org/10.1139/b07-105.

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Natural hybridization has long been recognized as a means for gene flow between species and has important evolutionary consequences. Although hybridization is generally considered to be symmetrical, with both hybridizing species being equally likely to be the male or female parent, several studies have demonstrated the presence of asymmetrical hybridization and introgression from one species to the other. We investigated the direction of natural hybridization between two sympatric forest tree species in North America ( Populus deltoides Bartr. ex Marsh. and Populus balsamifera L.) using species-specific single nucleotide polymorphism (SNP) markers in both the nuclear and chloroplast genomes. All natural hybrid individuals, identified from morphological traits, had nuclear alleles corresponding to both parental species, while the chloroplast genotypes showed similarity to P. deltoides, indicating asymmetrical hybridization with P. deltoides as the maternal and P. balsamifera as the paternal donor species. This observed asymmetrical hybridization may be attributable to cytonuclear interactions.
21

Maroof, M. A., Q. Zhang, D. B. Neale e R. W. Allard. "Associations between nuclear loci and chloroplast DNA genotypes in wild barley." Genetics 131, n.º 1 (1 de maio de 1992): 225–31. http://dx.doi.org/10.1093/genetics/131.1.225.

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Abstract Associations among alleles at nine nuclear loci and three chloroplast DNA (cpDNA) genotypes were assessed in a sample of 247 accessions of the wild barley, Hordeum vulgare ssp. spontaneum. Alleles at two of the nine nuclear loci are marked by length variations in the intergenic spacer region of ribosomal DNA (rDNA), and those of the other seven loci are well characterized allozymes. The three chloroplast DNA (cpDNA) genotypes are marked by restriction fragment length polymorphisms resulting from three polymorphic restriction sites detected by Southern blot hybridization. The analyses were performed by dividing the nine nuclear loci into a series of two-locus subsets and constructing log-linear models to characterize associations between the subsets of two nuclear loci and the cpDNA genotypes. Statistically significant associations were detected between six of the nine nuclear loci and the cpDNA genotypes, either individually as pairwise correlations, or through interaction with another nuclear locus to form three-variate complexes. Although the sample size of the present study was inadequate for statistical evaluation of higher order interactions, the results suggest the existence of interactions in which more than two nuclear loci are involved in associations with cpDNA genotypes. The observed cytonuclear associations appear to result from interplay among a number of evolutionary forces including a mating system of predominant selfing, differentiation among gene pools of local populations, and adaptation of barley genotypes to specific environmental conditions.
22

Powell, W., M. Morgante, J. J. Doyle, J. W. McNicol, S. V. Tingey e A. J. Rafalski. "Genepool Variation in Genus Glycine Subgenus Soja Revealed by Polymorphic Nuclear and Chloroplast Microsatellites". Genetics 144, n.º 2 (1 de outubro de 1996): 793–803. http://dx.doi.org/10.1093/genetics/144.2.793.

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Abstract A combination of nuclear and chloroplast simple sequence repeats (SSRs) have been used to investigate the levels and pattern of variability detected in Glycine max and G. soja genotypes. Based on the analysis of 700 soybean genotypes with 115 restriction fragment length polymorphism (RFLP) probes, 12 accessions were identified that represent 92% of the allelic variability detected in this genepool. These 12 core genotypes together with a sample of G. max and G. soja accessions were evaluated with 11 nuclear SSRs that detected 129 alleles. Compared with the other G. max and G. soja genotypes sampled, the core genotypes represent 40% of the allelic variability detected with SSRs. Despite the multi-allelic nature of soybean SSRs, dendrograms representing phenetic relationships between accessions clustered according to their subspecies origin. In addition to biparentally inherited nuclear SSRs, two uniparentally (maternally) transmitted chloroplast SSRs were also studied. A total of seven haplotypes were identified, and diversity indices of 0.405 ± 0.088 and 0.159 ± 0.071 were obtained for the two chloroplast SSRs. The availability of polymorphic SSR loci in the chloroplast genome provides new opportunities to investigate cytonuclear interactions in plants.
23

Oliver, Pedro, Joan Balanyà, Maria Misericòrdia Ramon, Antònia Picornell, Lluis Serra, Andrés Moya e José A. Castro. "Population dynamics of the 2 major mitochondrial DNA haplotypes in experimental populations of Drosophila subobscura". Genome 48, n.º 6 (1 de dezembro de 2005): 1010–18. http://dx.doi.org/10.1139/g05-077.

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The evolution of Drosophila subobscura mitochondrial DNA has been studied in experimental populations, founded with flies from a natural population from Calvià (Majorca, Balearic Islands, Spain). This population, like others founded in Europe, is characterized by the presence of 2 very common (>95%) mitochondrial haplotypes (named I and II) and rare and endemic haplotypes that appear at very low frequencies. Four experimental populations were established with flies having a heterogeneous nuclear genetic background, which was representative of the composition of the natural population. The populations were started with haplotypes I and II at an initial frequency of 50% each. After 33 generations, the 2 haplotypes coexisted. Random drift could be rejected as the only force responsible for the observed changes in haplotype frequencies. A slight but significant linear trend favouring a mtDNA (haploid) fitness effect has been detected, with a nonlinear deviation that could be due to a nuclear component. An analysis of chromosomal arrangements was made before the foundations of the cages and at generation 23. Our results indicated that the hypothesis that the maintenance of the frequencies of haplotypes I and II in natural populations could be due to their association with chromosomal arrangements remains controversial.Key words: natural selection, random drift, cytonuclear interactions, chromosomal arrangements, mtDNA haplotypes, Drosophila subobscura.
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Jelić, Mihailo, José A. Castro, Zorana Kurbalija Novičić, Bojan Kenig, Danica Dimitrijević, Marija Savić Veselinović, Miloš Jovanović, Dragomir Milovanović, Marina Stamenković-Radak e Marko Andjelković. "Absence of linkage disequilibria between chromosomal arrangements and mtDNA haplotypes in natural populations of Drosophila subobscura from the Balkan Peninsula". Genome 55, n.º 3 (março de 2012): 214–21. http://dx.doi.org/10.1139/g2012-004.

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The genetic structure of Drosophila subobscura from the Balkan Peninsula was studied with respect to restriction site polymorphism of mitochondrial DNA in populations from the Derventa River Gorge and Sicevo Gorge (Serbia). To investigate the role of cytonuclear interactions in shaping mitochondrial DNA variability in natural populations of this species, the study was complemented with the analysis of linkage disequilibria between mitochondrial haplotypes and chromosomal inversion arrangements. Similar to other populations of D. subobscura, two main haplotypes (I and II) were found, as well as a series of less common ones. The frequencies of haplotypes I and II accounted for 25.8% and 71.0%, respectively, in the population from the Derventa River Gorge, and for 32.4% and 58.1%, respectively, in the population from Sicevo Gorge. One of the haplotypes harbored a large insertion (2.7 kb) in the A+T rich region. The frequency distribution of both haplotypes did not depart from neutrality. Contrary to prior studies, we did not detect any significant linkage disequilibrium between the two most frequent mtDNA haplotypes and any of the chromosomal arrangements in either of the populations. We conclude that linkage disequilibrium is not a general occurrence in natural populations of D. subobscura, and we discuss how transient coadaptations, ecologically specific selective pressures, and demographics could contribute to population-specific patterns of linkage disequilibrium.
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Fotouhi, Omid, Sheikh Nizamuddin, Stephanie Falk, Oliver Schilling, Ruth Knüchel-Clarke, Martin L. Biniossek e H. T. Marc Timmers. "Alternative mRNA Splicing Controls the Functions of the Histone H3K27 Demethylase UTX/KDM6A". Cancers 15, n.º 12 (8 de junho de 2023): 3117. http://dx.doi.org/10.3390/cancers15123117.

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The UTX/KDM6A histone H3K27 demethylase plays an important role in development and is frequently mutated in cancers such as urothelial cancer. Despite many studies on UTX proteins, variations in mRNA splicing have been overlooked. Using Nanopore sequencing, we present a comprehensive analysis of UTX/KDM6A splicing events in human cell lines and in tissue samples from bladder cancer cases and normal epithelia. We found that the central region of UTX mRNAs encoded by exons 12 to 17 undergoes extensive alternative splicing. Up to half of all stable mRNAs (8–48% in bladder tissues and 18–58% in cell lines) are represented by the UTX canonical isoform lacking exon 14 encoding a nuclear localization sequence, and hence exon 14-containing UTX isoforms exclusively localize to the nucleus, unlike the cytonuclear localization of the canonical isoform. Chromatin association was also higher for exon-14-containing isoforms compared to the canonical UTX. Using quantitative mass spectrometry, we found that all UTX isoforms integrated into the MLL3 and MLL4, PR-DUB and MiDAC complexes. Interestingly, one of the novel UTX isoforms, which lacks exons 14 and 16, fails to interact with PR-DUB and MiDAC complex members. In conclusion, UTX mRNAs undergo extensive alternative splicing, which controls the subcellular localization of UTX and its interactions with other chromatin regulatory complexes.
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Babcock, Christina S., e Marjorie A. Asmussen. "Effects of Differential Selection in the Sexes on Cytonuclear Polymorphism and Disequilibria". Genetics 144, n.º 2 (1 de outubro de 1996): 839–53. http://dx.doi.org/10.1093/genetics/144.2.839.

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Abstract We develop a series of models that examine the effects of differential selection between the sexes on cytonuclear polymorphism and disequilibria. A detailed analysis is provided for populations under constant fertility or viability selection censused at life stages without frequency differences in the sexes. We show analytically that cytonuclear disequilibria can be generated de novo if the cytoplasmic and nuclear loci each affect female fitness and there is a nonmultiplicative fitness interaction between them. While computer simulations demonstrate that the majority of disequilibria produced by random selection are transient and small in magnitude, measurable permanent disequilibria can result from selective differences both within and between the two sexes. We derive analytic conditions for a protected cytonuclear polymorphism and use numerical simulations to quantitate the likelihood of obtaining permanent nuclear, cytoplasmic, and cytonuclear variation under various patterns of selection. The numerical analysis identifies special selection regimes more likely to generate disequilibria and maintain cytonuclear polymorphism and reveals a direct correlation to the strength of selection. As a byproduct, our models also provide the first decomposition of the different parental contributions to cytonuclear dynamics and the analytic conditions under which selection can cause cytoplasmic frequency changes or a cytonuclear hitchhiking effect.
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Postel, Zoé, e Pascal Touzet. "Cytonuclear Genetic Incompatibilities in Plant Speciation". Plants 9, n.º 4 (10 de abril de 2020): 487. http://dx.doi.org/10.3390/plants9040487.

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Due to the endosymbiotic origin of organelles, a pattern of coevolution and coadaptation between organellar and nuclear genomes is required for proper cell function. In this review, we focus on the impact of cytonuclear interaction on the reproductive isolation of plant species. We give examples of cases where species exhibit barriers to reproduction which involve plastid-nuclear or mito-nuclear genetic incompatibilities, and describe the evolutionary processes at play. We also discuss potential mechanisms of hybrid fitness recovery such as paternal leakage. Finally, we point out the possible interplay between plant mating systems and cytonuclear coevolution, and its consequence on plant speciation.
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Zhai, Yufei, Xiaqing Yu, Zaobing Zhu, Panqiao Wang, Ya Meng, Qinzheng Zhao, Ji Li e Jinfeng Chen. "Nuclear–Cytoplasmic Coevolution Analysis of RuBisCO in Synthesized Cucumis Allopolyploid". Genes 10, n.º 11 (30 de outubro de 2019): 869. http://dx.doi.org/10.3390/genes10110869.

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Allopolyploids are often faced with the challenge of maintaining well-coordination between nuclear and cytoplasmic genes inherited from different species. The synthetic allotetraploid Cucumis × hytivus is a useful model to explore cytonuclear coevolution. In this study, the sequences and expression of cytonuclear enzyme complex RuBisCO as well as its content and activity in C. × hytivus were compared to its parents to explore plastid–nuclear coevolution. The plastome-coded rbcL gene sequence was confirmed to be stable maternal inheritance, and parental copy of nuclear rbcS genes were both preserved in C. × hytivus. Thus, the maternal plastid may interact with the biparentally inherited rbcS alleles. The expression of the rbcS gene of C-homoeologs (paternal) was significantly higher than that of H-homoeologs (maternal) in C. × hytivus (HHCC). Protein interaction prediction analysis showed that the rbcL protein has stronger binding affinity to the paternal copy of rbcS protein than that of maternal copy in C. × hytivus, which might explain the transcriptional bias of the rbcS homoeologs. Moreover, both the activity and content of RuBisCO in C. × hytivus showed mid-parent heterosis. In summary, our results indicate a paternal transcriptional bias of the rbcS genes in C. × hytivus, and we found new nuclear–cytoplasmic combination may be one of the reasons for allopolyploids heterosis.
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Li, Changping, Xiaofei Wang, Yaxian Xiao, Xuhan Sun, Jinbin Wang, Xuan Yang, Yuchen Sun et al. "Coevolution in Hybrid Genomes: Nuclear-Encoded Rubisco Small Subunits and Their Plastid-Targeting Translocons Accompanying Sequential Allopolyploidy Events in Triticum". Molecular Biology and Evolution 37, n.º 12 (30 de junho de 2020): 3409–22. http://dx.doi.org/10.1093/molbev/msaa158.

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Abstract The Triticum/Aegilops complex includes hybrid species resulting from homoploid hybrid speciation and allopolyploid speciation. Sequential allotetra- and allohexaploidy events presumably result in two challenges for the hybrids, which involve 1) cytonuclear stoichiometric disruptions caused by combining two diverged nuclear genomes with the maternal inheritance of the cytoplasmic organellar donor; and 2) incompatibility of chimeric protein complexes with diverged subunits from nuclear and cytoplasmic genomes. Here, we describe coevolution of nuclear rbcS genes encoding the small subunits of Rubisco (ribulose 1,5-bisphosphate carboxylase/oxygenase) and nuclear genes encoding plastid translocons, which mediate recognition and translocation of nuclear-encoded proteins into plastids, in allopolyploid wheat species. We demonstrate that intergenomic paternal-to-maternal gene conversion specifically occurred in the genic region of the homoeologous rbcS3 gene from the D-genome progenitor of wheat (abbreviated as rbcS3D) such that it encodes a maternal-like or B-subgenome-like SSU3D transit peptide in allohexaploid wheat but not in allotetraploid wheat. Divergent and limited interaction between SSU3D and the D-subgenomic TOC90D translocon subunit is implicated to underpin SSU3D targeting into the chloroplast of hexaploid wheat. This implicates early selection favoring individuals harboring optimal maternal-like organellar SSU3D targeting in hexaploid wheat. These data represent a novel dimension of cytonuclear evolution mediated by organellar targeting and transportation of nuclear proteins.
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Normark, Benjamin B., e Laura Ross. "Genetic conflict, kin and the origins of novel genetic systems". Philosophical Transactions of the Royal Society B: Biological Sciences 369, n.º 1642 (19 de maio de 2014): 20130364. http://dx.doi.org/10.1098/rstb.2013.0364.

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Genetic conflict may have played an important role in the evolution of novel genetic systems. The ancestral system of eumendelian genetics is highly symmetrical. Those derived from it (e.g. thelytokous parthenogenesis, haplodiploidy and parent-specific allele expression) are more asymmetrical in the genetic role played by maternal versus paternal alleles. These asymmetries may have arisen from maternal–paternal genetic conflict, or cytonuclear conflict, or from an interaction between them. Asymmetric genetic systems are much more common in terrestrial and freshwater taxa than in marine taxa. We suggest three reasons for this, based on the relative inhospitability of terrestrial environments to three types of organism: (i) pathogens—departure from the marine realm meant escape from many pathogens and parasites, reducing the need for sexual reproduction; (ii) symbionts—symbionts are no more important in the terrestrial realm than the marine realm but are more likely to be obligately intracellular and vertically transmitted, making them more likely to disrupt their host's genetic systems; (iii) Gametes and embryos—because neither gametes nor embryos can be shed into air as easily as into seawater, the mother's body is a more important environment for both types of organisms in the terrestrial realm than in the marine realm. This environment of asymmetric kinship (with neighbours more closely related by maternal alleles than by paternal alleles) may have helped to drive asymmetries in expression and transmission.
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Lian, Qun, Shuai Li, Shenglong Kan, Xuezhu Liao, Sanwen Huang, Daniel B. Sloan e Zhiqiang Wu. "Association analysis provides insights into plant mitonuclear interactions". Molecular Biology and Evolution, 7 de fevereiro de 2024. http://dx.doi.org/10.1093/molbev/msae028.

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Abstract Cytonuclear interaction refers to the complex and ongoing process of coevolution between nuclear and organelle genomes, which are responsible for cellular respiration, photosynthesis, lipid metabolism, etc. and play a significant role in adaptation and speciation. There have been a large number of studies to detect signatures of cytonuclear interactions. However, identification of the specific nuclear and organelle genetic polymorphisms that are involved in these interactions within a species remains relatively rare. The recent surge in whole genome sequencing has provided us an opportunity to explore cytonuclear interaction from a population perspective. In this study, we analyzed a total of 3,439 genomes from seven species to identify signals of cytonuclear interactions by association (linkage disequilibrium) analysis of variants in both the mitochondrial and nuclear genomes across flowering plants. We also investigated examples of nuclear loci identified based on these association signals using subcellular localization assays, gene editing and transcriptome sequencing. Our study provides a novel perspective on the investigation of cytonuclear coevolution, thereby enriching our understanding of plant fitness and offspring sterility.
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Shahbazi, Mehrdad, Joanna Majka, Denisa Kubíková, Zbigniew Zwierzykowski, Marek Glombik, Jonathan F. Wendel, Joel Sharbrough et al. "Cytonuclear interplay in auto‐ and allopolyploids: a multifaceted perspective from the Festuca‐Lolium complex". Plant Journal, 7 de fevereiro de 2024. http://dx.doi.org/10.1111/tpj.16659.

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SUMMARYRestoring cytonuclear stoichiometry is necessary after whole‐genome duplication (WGD) and interspecific/intergeneric hybridization in plants. We investigated this phenomenon in auto‐ and allopolyploids of the Festuca‐Lolium complex providing insights into the mechanisms governing cytonuclear interactions in early polyploid and hybrid generations. Our study examined the main processes potentially involved in restoring the cytonuclear balance after WGD comparing diploids and new and well‐established autopolyploids. We uncovered that both the number of chloroplasts and the number of chloroplast genome copies were significantly higher in the newly established autopolyploids and grew further in more established autopolyploids. The increase in the copy number of the chloroplast genome exceeded the rise in the number of chloroplasts and fully compensated for the doubling of the nuclear genome. In addition, changes in nuclear and organelle gene expression were insignificant. Allopolyploid Festuca × Lolium hybrids displayed potential structural conflicts in parental protein variants within the cytonuclear complexes. While biased maternal allele expression has been observed in numerous hybrids, our results suggest that its role in cytonuclear stabilization in the Festuca × Lolium hybrids is limited. This study provides insights into the restoration of the cytonuclear stoichiometry, yet it emphasizes the need for future research to explore post‐transcriptional regulation and its impact on cytonuclear gene expression stoichiometry. Our findings may enhance the understanding of polyploid plant evolution, with broader implications for the study of cytonuclear interactions in diverse biological contexts.
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Sloan, Daniel B., Justin L. Conover, Corrine E. Grover, Jonathan F. Wendel e Joel Sharbrough. "Polyploid plants take cytonuclear perturbations in stride". Plant Cell, 24 de janeiro de 2024. http://dx.doi.org/10.1093/plcell/koae021.

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Abstract Hybridization in plants is often accompanied by nuclear genome doubling (allopolyploidy), which has been hypothesized to perturb interactions between nuclear and organellar (mitochondrial and plastid) genomes by creating imbalances in the relative copy number of these genomes and producing genetic incompatibilities between maternally derived organellar genomes and the half of the allopolyploid nuclear genome from the paternal progenitor. Several evolutionary responses have been predicted to ameliorate these effects, including selection for changes in protein sequences that restore cytonuclear interactions; biased gene retention/expression/conversion favoring maternal nuclear gene copies; and fine-tuning of relative cytonuclear genome copy numbers and expression levels. Numerous recent studies, however, have found that evolutionary responses are inconsistent and rarely scale to genome-wide generalities. The apparent robustness of plant cytonuclear interactions to allopolyploidy may reflect features that are general to allopolyploids such as the lack of F2 hybrid breakdown under disomic inheritance, and others that are more plant-specific, including slow sequence divergence in organellar genomes and pre-existing regulatory responses to changes in cell size and endopolyploidy during development. Thus, cytonuclear interactions may only rarely act as the main barrier to establishment of allopolyploid lineages, perhaps helping to explain why allopolyploidy is so pervasive in plant evolution.
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Forsythe, Evan S., Corrinne E. Grover, Emma R. Miller, Justin L. Conover, Mark A. Arick, M. Carolina F. Chavarro, Soraya C. M. Leal-Bertioli et al. "Organellar transcripts dominate the cellular mRNA pool across plants of varying ploidy levels". Proceedings of the National Academy of Sciences 119, n.º 30 (19 de julho de 2022). http://dx.doi.org/10.1073/pnas.2204187119.

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Mitochondrial and plastid functions depend on coordinated expression of proteins encoded by genomic compartments that have radical differences in copy number of organellar and nuclear genomes. In polyploids, doubling of the nuclear genome may add challenges to maintaining balanced expression of proteins involved in cytonuclear interactions. Here, we use ribo-depleted RNA sequencing (RNA-seq) to analyze transcript abundance for nuclear and organellar genomes in leaf tissue from four different polyploid angiosperms and their close diploid relatives. We find that even though plastid genomes contain <1% of the number of genes in the nuclear genome, they generate the majority (69.9 to 82.3%) of messenger RNA (mRNA) transcripts in the cell. Mitochondrial genes are responsible for a much smaller percentage (1.3 to 3.7%) of the leaf mRNA pool but still produce much higher transcript abundances per gene compared to nuclear genome. Nuclear genes encoding proteins that functionally interact with mitochondrial or plastid gene products exhibit mRNA expression levels that are consistently more than 10-fold lower than their organellar counterparts, indicating an extreme cytonuclear imbalance at the RNA level despite the predominance of equimolar interactions at the protein level. Nevertheless, interacting nuclear and organellar genes show strongly correlated transcript abundances across functional categories, suggesting that the observed mRNA stoichiometric imbalance does not preclude coordination of cytonuclear expression. Finally, we show that nuclear genome doubling does not alter the cytonuclear expression ratios observed in diploid relatives in consistent or systematic ways, indicating that successful polyploid plants are able to compensate for cytonuclear perturbations associated with nuclear genome doubling.
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Tiwari, Lalit Dev, Eyal Bdolach, Manas Ranjan Prusty, Schewach Bodenheimer, Avital Be'ery, Adi Faigenboim‐Doron, Eiji Yamamoto et al. "Cytonuclear interactions modulate the plasticity of photosynthetic rhythmicity and growth in wild barley". Physiologia Plantarum 176, n.º 1 (janeiro de 2024). http://dx.doi.org/10.1111/ppl.14192.

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AbstractIn plants, the contribution of the plasmotype (mitochondria and chloroplast) in controlling the circadian clock plasticity and possible consequences on cytonuclear genetic makeup have yet to be fully elucidated. A genome‐wide association study in the wild barley (Hordeum vulgare ssp. spontaneum) B1K collection identified overlap with our previously mapped DRIVERS OF CLOCKS (DOCs) loci in wild‐cultivated interspecific population. Moreover, we identified non‐random segregation and epistatic interactions between nuclear DOCs loci and the chloroplastic RpoC1 gene, indicating an adaptive value for specific cytonuclear gene combinations. Furthermore, we show that DOC1.1, which harbours the candidate SIGMA FACTOR‐B (SIG‐B) gene, is linked with the differential expression of SIG‐B and CCA1 genes and contributes to the circadian gating response to heat. High‐resolution temporal growth and photosynthesis measurements of B1K also link the DOCs loci to differential growth, Chl content and quantum yield. To validate the involvement of the Plastid encoded polymerase (PEP) complex, we over‐expressed the two barley chloroplastic RpoC1 alleles in Arabidopsis and identified significant differential plasticity under elevated temperatures. Finally, enhanced clock plasticity of de novo ENU (N‐Ethyl‐N‐nitrosourea) ‐induced barley rpoB1 mutant further implicates the PEP complex as a key player in regulating the circadian clock output. Overall, this study highlights the contribution of specific cytonuclear interaction between rpoC1 (PEP gene) and SIG‐B with distinct circadian timing regulation under heat, and their pleiotropic effects on growth implicate an adaptive value.
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Kan, Shenglong, Xuezhu Liao, Lan Lan, Jiali Kong, Jie Wang, Liyun Nie, Jun Zou, Hong An e Zhiqiang Wu. "Cytonuclear interactions and subgenome dominance shape the evolution of organelle-targeted genes in the Brassica triangle of U". Molecular Biology and Evolution, 23 de fevereiro de 2024. http://dx.doi.org/10.1093/molbev/msae043.

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Abstract The interaction and co-evolution between nuclear and cytoplasmic genomes are one of the fundamental hallmarks of eukaryotic genome evolution and, two billion years later, are still major contributors to the formation of new species. Although many studies have investigated the role of cytonuclear interactions following allopolyploidization, the relative magnitude of the effect of subgenome dominance vs. cytonuclear interaction on genome evolution remains unclear. The Brassica triangle of U features three diploid species that together have formed three separate allotetraploid species on similar evolutionary timescales, providing an ideal system for understanding the contribution of the cytoplasmic donor to hybrid polyploid. Here, we investigated the evolutionary pattern of organelle-targeted genes in B. carinata (BBCC) and two varieties of B. juncea (AABB) at the whole-genome level, with particular focus on cytonuclear enzyme complexes. We found partial evidence that plastid-targeted genes experience selection to match plastid genomes, but no obvious corresponding signal in mitochondria-targeted genes from these two separately formed allopolyploids. Interestingly, selection acting on plastid genomes always reduced the retention rate of plastid-targeted genes encoded by the B subgenome, regardless of whether the B. nigra (BB) subgenome was contributed by the paternal or maternal progenitor. More broadly, this study illustrates the distinct selective pressures experienced by plastid- and mitochondria-targeted genes, despite a shared pattern of inheritance and natural history. Our study also highlights an important role for subgenome dominance in allopolyploid genome evolution, even in genes whose function depends on separately inherited molecules.
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Singh, Saurabh, Reeta Bhatia, Raj Kumar, Tusar K. Behera, Khushboo Kumari, Achintya Pramanik, Hemant Ghemeray, Kanika Sharma, R. C. Bhattacharya e Shyam S. Dey. "Elucidating Mitochondrial DNA Markers of Ogura-Based CMS Lines in Indian Cauliflowers (Brassica oleracea var. botrytis L.) and Their Floral Abnormalities Due to Diversity in Cytonuclear Interactions". Frontiers in Plant Science 12 (30 de abril de 2021). http://dx.doi.org/10.3389/fpls.2021.631489.

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Mitochondrial markers can be used to differentiate diverse mitotypes as well as cytoplasms in angiosperms. In cauliflower, cultivation of hybrids is pivotal in remunerative agriculture and cytoplasmic male sterile lines constitute an important component of the hybrid breeding. In diversifying the source of male sterility, it is essential to appropriately differentiate among the available male sterile cytoplasms in cauliflower. PCR polymorphism at the key mitochondrial genes associated with male sterility will be instrumental in analyzing, molecular characterization, and development of mitotype-specific markers for differentiation of different cytoplasmic sources. Presence of auto- and alloplasmic cytonuclear combinations result in complex floral abnormalities. In this context, the present investigation highlighted the utility of organelle genome-based markers in distinguishing cytoplasm types in Indian cauliflowers and unveils the epistatic effects of the cytonuclear interactions influencing floral phenotypes. In PCR-based analysis using a set of primers targeted to orf-138, 76 Indian cauliflower lines depicted the presence of Ogura cytoplasm albeit the amplicons generated exhibited polymorphism within the ofr-138 sequence. The polymorphic fragments were found to be spanning over 200–280 bp and 410–470 bp genomic regions of BnTR4 and orf125, respectively. Sequence analysis revealed that such cytoplasmic genetic variations could be attributed to single nucleotide polymorphisms and insertion or deletions of 31/51 nucleotides. The cytoplasmic effects on varying nuclear-genetic backgrounds rendered an array of floral abnormalities like reduction in flower size, fused flowers, splitted style with the exposed ovule, absence of nonfunctional stamens, and petaloid stamens. These floral malformations caused dysplasia of flower structure affecting female fertility with inefficient nectar production. The finding provides an important reference to ameliorate understanding of mechanism of cytonuclear interactions in floral organ development in Brassicas. The study paves the way for unraveling developmental biology of CMS phenotypes in eukaryotic organisms and intergenomic conflict in plant speciation.
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Sharbrough, Joel, Justin L. Conover, Matheus Fernandes Gyorfy, Corrinne E. Grover, Emma R. Miller, Jonathan F. Wendel e Daniel B. Sloan. "Global Patterns of subgenome evolution in organelle-targeted genes of six allotetraploid angiosperms". Molecular Biology and Evolution, 6 de abril de 2022. http://dx.doi.org/10.1093/molbev/msac074.

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Abstract Whole-genome duplications (WGDs) are a prominent process of diversification in eukaryotes. The genetic and evolutionary forces that WGD imposes upon cytoplasmic genomes are not well understood, despite the central role that cytonuclear interactions play in eukaryotic function and fitness. Cellular respiration and photosynthesis depend upon successful interaction between the 3000+ nuclear-encoded proteins destined for the mitochondria or plastids and the gene products of cytoplasmic genomes in multi-subunit complexes such as OXPHOS, organellar ribosomes, Photosystems I and II, and Rubisco. Allopolyploids are thus faced with the critical task of coordinating interactions between nuclear and cytoplasmic genes that were inherited from different species. Because cytoplasmic genomes share a more recent history of common descent with the maternal nuclear subgenome than the paternal subgenome, evolutionary “mismatches” between the paternal subgenome and the cytoplasmic genomes in allopolyploids might lead to accelerated rates of evolution in the paternal homoeologs of allopolyploids, either through relaxed purifying selection or strong directional selection to rectify these mismatches. We report evidence from six independently formed allotetraploids that subgenomes exhibit unequal rates of protein-sequence evolution, but we found no evidence that cytonuclear incompatibilities result in altered evolutionary trajectories of paternal homoeologs of organelle-targeted genes. Analyses of gene content revealed mixed evidence for whether organelle-targeted genes are lost more rapidly than non-organelle-targeted genes. Together, these global analyses provide insights into the complex evolutionary dynamics of allopolyploids, showing that allopolyploid subgenomes have separate evolutionary trajectories despite sharing the same nucleus, generation time, and ecological context.
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June, Viviana, Xiaoya Song e Z. Jeffrey Chen. "Imprinting but not cytonuclear interactions determines seed size heterosis in Arabidopsis hybrids". Plant Physiology, 6 de fevereiro de 2024. http://dx.doi.org/10.1093/plphys/kiae061.

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Abstract The parent-of-origin effect on seeds can result from imprinting (unequal expression of paternal and maternal alleles) or combinational effects between cytoplasmic and nuclear genomes, but their relative contributions remain unknown. To discern these confounding factors, we produced cytoplasmic-nuclear substitution (CNS) lines using recurrent backcrossing in Arabidopsis (Arabidopsis thaliana) ecotypes Col-0 and C24. These CNS lines differed only in the nuclear genome (imprinting) or cytoplasm. The CNS reciprocal hybrids with the same cytoplasm displayed ∼20% seed size difference, whereas the seed size was similar between the reciprocal cybrids with fixed imprinting. Transcriptome analyses in the endosperm of CNS hybrids using laser-capture microdissection identified 104 maternally expressed genes (MEGs) and 90 paternally-expressed genes (PEGs). These imprinted genes were involved in pectin catabolism and cell wall modification in the endosperm. Homeodomain Glabrous9 (HDG9), an epiallele and one of 11 cross-specific imprinted genes, affected seed size. In the embryo, there were a handful of imprinted genes in the CNS hybrids but only one was expressed at higher levels than in the endosperm. AT4G13495 was found to encode a long-noncoding RNA (lncRNA), but no obvious seed phenotype was observed in lncRNA knockout lines. Nuclear RNA Polymerase D1 (NRPD1), encoding the largest subunit of RNA Pol IV, was involved in the biogenesis of small interfering RNAs. Seed size and embryos were larger in the cross using nrpd1 as the maternal parent than in the reciprocal cross, supporting a role of the maternal NRPD1 allele in seed development. Although limited ecotypes were tested, these results suggest that imprinting and the maternal NRPD1-mediated small RNA pathway play roles in seed size heterosis in plant hybrids.
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Wang, Nan, Chaochao Li, Lihua Kuang, Xiaomeng Wu, Kaidong Xie, Andan Zhu, Qiang Xu et al. "Pan-mitogenomics reveals the genetic basis of cytonuclear conflicts in citrus hybridization, domestication, and diversification". Proceedings of the National Academy of Sciences 119, n.º 43 (19 de outubro de 2022). http://dx.doi.org/10.1073/pnas.2206076119.

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Although interactions between the cytoplasmic and nuclear genomes occurred during diversification of many plants, the evolutionary conflicts due to cytonuclear interactions are poorly understood in crop breeding. Here, we constructed a pan-mitogenome and identified chimeric open reading frames (ORFs) generated by extensive structural variations (SVs). Meanwhile, short reads from 184 accessions of citrus species were combined to construct three variation maps for the nuclear, mitochondrial, and chloroplast genomes. The population genomic data showed discordant topologies between the cytoplasmic and nuclear genomes because of differences in mutation rates and levels of heteroplasmy from paternal leakage. An analysis of species-specific SVs indicated that mitochondrial heteroplasmy was common and that chloroplast heteroplasmy was undetectable. Interestingly, we found a prominent divergence in the mitogenomes and the highest genetic load in the, which may provide the basis for cytoplasmic male sterility (CMS) and thus influence the reshuffling of the cytoplasmic and nuclear genomes during hybridization. Using cytoplasmic replacement experiments, we identified a type of species-specific CMS in mandarin related to two chimeric mitochondrial genes. Our analyses indicate that cytoplasmic genomes from mandarin have rarely been maintained in hybrids and that paternal leakage produced very low levels of mitochondrial heteroplasmy in mandarin. A genome-wide association study (GWAS) provided evidence for three nuclear genes that encode pentatricopeptide repeat (PPR) proteins contributing to the cytonuclear interactions in the Citrus genus. Our study demonstrates the occurrence of evolutionary conflicts between cytoplasmic and nuclear genomes in citrus and has important implications for genetics and breeding.
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Joseph, Bindu, Jason A. Corwin, Baohua Li, Suzi Atwell e Daniel J. Kliebenstein. "Cytoplasmic genetic variation and extensive cytonuclear interactions influence natural variation in the metabolome". eLife 2 (8 de outubro de 2013). http://dx.doi.org/10.7554/elife.00776.

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Understanding genome to phenotype linkages has been greatly enabled by genomic sequencing. However, most genome analysis is typically confined to the nuclear genome. We conducted a metabolomic QTL analysis on a reciprocal RIL population structured to examine how variation in the organelle genomes affects phenotypic variation. This showed that the cytoplasmic variation had effects similar to, if not larger than, the largest individual nuclear locus. Inclusion of cytoplasmic variation into the genetic model greatly increased the explained phenotypic variation. Cytoplasmic genetic variation was a central hub in the epistatic network controlling the plant metabolome. This epistatic influence manifested such that the cytoplasmic background could alter or hide pairwise epistasis between nuclear loci. Thus, cytoplasmic genetic variation plays a central role in controlling natural variation in metabolomic networks. This suggests that cytoplasmic genomes must be included in any future analysis of natural variation.
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Skejo, Josip, Sriram G. Garg, Sven B. Gould, Michael Hendriksen, Fernando D. K. Tria, Nico Bremer, Damjan Franjević, Neil W. Blackstone e William F. Martin. "Evidence for a Syncytial Origin of Eukaryotes from Ancestral State Reconstruction". Genome Biology and Evolution 13, n.º 7 (8 de maio de 2021). http://dx.doi.org/10.1093/gbe/evab096.

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Abstract Modern accounts of eukaryogenesis entail an endosymbiotic encounter between an archaeal host and a proteobacterial endosymbiont, with subsequent evolution giving rise to a unicell possessing a single nucleus and mitochondria. The mononucleate state of the last eukaryotic common ancestor (LECA) is seldom, if ever, questioned, even though cells harboring multiple (syncytia, coenocytes, and polykaryons) are surprisingly common across eukaryotic supergroups. Here, we present a survey of multinucleated forms. Ancestral character state reconstruction for representatives of 106 eukaryotic taxa using 16 different possible roots and supergroup sister relationships, indicate that LECA, in addition to being mitochondriate, sexual, and meiotic, was multinucleate. LECA exhibited closed mitosis, which is the rule for modern syncytial forms, shedding light on the mechanics of its chromosome segregation. A simple mathematical model shows that within LECA’s multinucleate cytosol, relationships among mitochondria and nuclei were neither one-to-one, nor one-to-many, but many-to-many, placing mitonuclear interactions and cytonuclear compatibility at the evolutionary base of eukaryotic cell origin. Within a syncytium, individual nuclei and individual mitochondria function as the initial lower-level evolutionary units of selection, as opposed to individual cells, during eukaryogenesis. Nuclei within a syncytium rescue each other’s lethal mutations, thereby postponing selection for viable nuclei and cytonuclear compatibility to the generation of spores, buffering transitional bottlenecks at eukaryogenesis. The prokaryote-to-eukaryote transition is traditionally thought to have left no intermediates, yet if eukaryogenesis proceeded via a syncytial common ancestor, intermediate forms have persisted to the present throughout the eukaryotic tree as syncytia but have so far gone unrecognized.
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Wu, Ying, Fan Lin, Yao Zhou, Jie Wang, Shuai Sun, Bin Wang, Zhibin Zhang et al. "Genomic mosaicism due to homoeologous exchange generates extensive phenotypic diversity in nascent allopolyploids". National Science Review, 7 de novembro de 2020. http://dx.doi.org/10.1093/nsr/nwaa277.

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Abstract Allopolyploidy is an important process in plant speciation, yet newly formed allopolyploid species typically suffer from extreme genetic bottlenecks. One escape from this impasse might be homoeologous meiotic pairing, during which homoeologous exchanges (HEs) generate phenotypically variable progeny. However, the immediate genome-wide patterns and resulting phenotypic diversity generated by HEs remain largely unknown. Here, we analyzed the genome composition of 202 phenotyped euploid segmental allopolyploid individuals from the 4th selfed generation following chromosomal doubling of reciprocal F1 hybrids of crosses between rice subspecies, using whole genome sequencing. We describe rampant occurrence of HEs that, by overcoming incompatibility or conferring superiority of hetero-cytonuclear interactions, generate extensive and individualized genomic mosaicism across the analyzed tetraploids. We show that the resulting homoeolog copy number alteration in tetraploids affects known-function genes and their complex genetic interactions, in the process creating extraordinary phenotypic diversity at the population level following a single initial hybridization. Our results illuminate the immediate genomic landscapes possible in a tetraploid genomic environment, and underscore HE as an important mechanism that fuels rapid phenotypic diversification accompanying the initial stages of allopolyploid evolution.
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Williams, Alissa M., Michael W. Itgen, Amanda K. Broz, Olivia G. Carter e Daniel B. Sloan. "Long-read transcriptome and other genomic resources for the angiosperm Silene noctiflora". G3 Genes|Genomes|Genetics, 3 de junho de 2021. http://dx.doi.org/10.1093/g3journal/jkab189.

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Abstract The angiosperm genus Silene is a model system for several traits of ecological and evolutionary significance in plants, including breeding system and sex chromosome evolution, host-pathogen interactions, invasive species biology, heavy metal tolerance, and cytonuclear interactions. Despite its importance, genomic resources for this large genus of approximately 850 species are scarce, with only one published whole-genome sequence (from the dioecious species Silene latifolia). Here, we provide genomic and transcriptomic resources for a hermaphroditic representative of this genus (S. noctiflora), including a PacBio Iso-Seq transcriptome, which uses long-read, single-molecule sequencing technology to analyze full-length mRNA transcripts. Using these data, we have assembled and annotated high-quality full-length cDNA sequences for approximately 14,126 S. noctiflora genes and 25,317 isoforms. We demonstrated the utility of these data to distinguish between recent and highly similar gene duplicates by identifying novel paralogous genes in an essential protease complex. Furthermore, we provide a draft assembly for the approximately 2.7-Gb genome of this species, which is near the upper range of genome-size values reported for diploids in this genus and threefold larger than the 0.9-Gb genome of Silene conica, another species in the same subgenus. Karyotyping confirmed that S. noctiflora is a diploid, indicating that its large genome size is not due to polyploidization. These resources should facilitate further study and development of this genus as a model in plant ecology and evolution.
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Tiwari, Lalit Dev, Ayelet Kurtz-Sohn, Eyal Bdolach e Eyal Fridman. "Crops under past diversification and ongoing climate change: More than selection on nuclear genes for flowering". Journal of Experimental Botany, 22 de julho de 2023. http://dx.doi.org/10.1093/jxb/erad283.

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Abstract Diversification and breeding following domestication and current climate change across the globe are the two most significant events experienced by major crops. Diversification of crops from their wild ancestors has favored dramatic changes in the plant’s sensitivity to environment, significantly in transducing light inputs to the circadian clock, which allowed the growth of major crops in the shorter growing season in the Northern hemisphere. Historically, mutants and quantitative trait loci (QTL) mapping have facilitated the identification and cloning of genes underlying major changes of the clock and flowering regulation. Recent studies suggest that thermal plasticity of circadian clock output, not just the core genes that follow temperature compensation, was also under selection during diversification and breeding. Wild alleles that accelerate output rhythmicity could be beneficial for crop resilience. Furthermore, wild alleles with beneficial and flowering-independent effects under stress indicate their possible role in maintaining a balanced source-sink relationship, allowing productivity under climatic change. Because the chloroplast genome also regulates the plasticity of the clock output, mapping populations including cytonuclear interactions should be utilized in an integrated field and clock phenomics framework. We highlight the need to integrate physiological and developmental approaches (Physio-Devo) to gain a better understanding while re-domesticating wild gene alleles into modern cultivars to increase their robustness under abiotic heat and drought stresses.
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Li, Changping, Baoxu Ding, Xintong Ma, Xuan Yang, Hongyan Wang, Yuefan Dong, Zhibin Zhang et al. "A temporal gradient of cytonuclear coordination of chaperonins and chaperones during RuBisCo biogenesis in allopolyploid plants". Proceedings of the National Academy of Sciences 119, n.º 34 (15 de agosto de 2022). http://dx.doi.org/10.1073/pnas.2200106119.

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Ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCo) has long been studied from many perspectives. As a multisubunit (large subunits [LSUs] and small subunits[SSUs]) protein encoded by genes residing in the chloroplast ( rbcL ) and nuclear ( rbcS ) genomes, RuBisCo also is a model for cytonuclear coevolution following allopolyploid speciation in plants. Here, we studied the genomic and transcriptional cytonuclear coordination of auxiliary chaperonin and chaperones that facilitate RuBisCo biogenesis across multiple natural and artificially synthesized plant allopolyploids. We found similar genomic and transcriptional cytonuclear responses, including respective paternal-to-maternal conversions and maternal homeologous biased expression, in chaperonin/chaperon-assisted folding and assembly of RuBisCo in different allopolyploids. One observation is about the temporally attenuated genomic and transcriptional cytonuclear evolutionary responses during early folding and later assembly process of RuBisCo biogenesis, which were established by long-term evolution and immediate onset of allopolyploidy, respectively. Our study not only points to the potential widespread and hitherto unrecognized features of cytonuclear evolution but also bears implications for the structural interaction interface between LSU and Cpn60 chaperonin and the functioning stage of the Raf2 chaperone.
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Sato, Yukie, Satoshi Fujiwara, Martijn Egas, Tomoko Matsuda e Tetsuo Gotoh. "Patterns of reproductive isolation in a haplodiploid mite, Amphitetranychus viennensis: prezygotic isolation, hybrid inviability and hybrid sterility". BMC Ecology and Evolution 21, n.º 1 (23 de setembro de 2021). http://dx.doi.org/10.1186/s12862-021-01896-5.

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Abstract Background Evolution of reproductive isolation is an important process, generating biodiversity and driving speciation. To better understand this process, it is necessary to investigate factors underlying reproductive isolation through various approaches but also in various taxa. Previous studies, mainly focusing on diploid animals, supported the prevalent view that reproductive barriers evolve gradually as a by-product of genetic changes accumulated by natural selection by showing a positive relationship between the degree of reproductive isolation and genetic distance. Haplodiploid animals are expected to generate additional insight into speciation, but few studies investigated the prevalent view in haplodiploid animals. In this study, we investigate whether the relationship also holds in a haplodiploid spider mite, Amphitetranychus viennensis (Zacher). Results We sampled seven populations of the mite in the Palaearctic region, measured their genetic distance (mtDNA) and carried out cross experiments with all combinations. We analyzed how lack of fertilization rate (as measure of prezygotic isolation) as well as hybrid inviability and hybrid sterility (as measures of postzygotic isolation) varies with genetic distance. We found that the degree of reproductive isolation varies among cross combinations, and that all three measures of reproductive isolation have a positive relationship with genetic distance. Based on the mtDNA marker, lack of fertilization rate, hybrid female inviability and hybrid female sterility were estimated to be nearly complete (99.0–99.9% barrier) at genetic distances of 0.475–0.657, 0.150–0.209 and 0.145–0.210, respectively. Besides, we found asymmetries in reproductive isolation. Conclusions The prevalent view on the evolution of reproductive barriers is supported in the haplodiploid spider mite we studied here. According to the estimated minimum genetic distance for total reproductive isolation in parent population crosses in this study and previous work, a genetic distance of 0.15–0.21 in mtDNA (COI) appears required for speciation in spider mites. Variations and asymmetries in the degree of reproductive isolation highlight the importance of reinforcement of prezygotic reproductive isolation through incompatibility and the importance of cytonuclear interactions for reproductive isolation in haplodiploid spider mites.
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Leigh, Brittany A., Sarah R. Bordenstein, Andrew W. Brooks, Aram Mikaelyan e Seth R. Bordenstein. "Finer-Scale Phylosymbiosis: Insights from Insect Viromes". mSystems 3, n.º 6 (18 de dezembro de 2018). http://dx.doi.org/10.1128/msystems.00131-18.

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ABSTRACTPhylosymbiosis was recently proposed to describe the eco-evolutionary pattern whereby the ecological relatedness (e.g., beta diversity relationships) of host-associated microbial communities parallels the phylogeny of the host species. Representing the most abundant biological entities on the planet and common members of the animal-associated microbiome, viruses can be influential members of host-associated microbial communities that may recapitulate, reinforce, or ablate phylosymbiosis. Here we sequence the metagenomes of purified viral communities from three different parasitic waspNasoniaspecies, one cytonuclear introgression line ofNasonia, and the flour moth outgroupEphestia kuehniella. Results demonstrate complete phylosymbiosis between the viral metagenome and insect phylogeny. Across allNasoniacontigs, 69% of the genes in the viral metagenomes are either new to the databases or uncharacterized, yet over 99% of the contigs have at least one gene with similarity to a known sequence. The coreNasoniavirome spans 21% of the total contigs, and the majority of that core is likely derived from induced prophages residing in the genomes of commonNasonia-associated bacterial genera:Proteus,Providencia, andMorganella. We also assemble the first complete viral particle genomes fromNasonia-associated gut bacteria. Taken together, results reveal the first complete evidence for phylosymbiosis in viral metagenomes, new genome sequences of viral particles fromNasonia-associated gut bacteria, and a large set of novel or uncharacterized genes in theNasoniavirome. This work suggests that phylosymbiosis at the host-microbiome level will likely extend to the host-virome level in other systems as well.IMPORTANCEViruses are the most abundant biological entity on the planet and interact with microbial communities with which they associate. The virome of animals is often dominated by bacterial viruses, known as bacteriophages or phages, which can (re)structure bacterial communities potentially vital to the animal host. Beta diversity relationships of animal-associated bacterial communities in laboratory and wild populations frequently parallel animal phylogenetic relationships, a pattern termed phylosymbiosis. However, little is known about whether viral communities also exhibit this eco-evolutionary pattern. Metagenomics of purified viruses from recently diverged species ofNasoniaparasitoid wasps reared in the lab indicates for the first time that the community relationships of the virome can also exhibit complete phylosymbiosis. Therefore, viruses, particularly bacteriophages here, may also be influenced by animal evolutionary changes either directly or indirectly through the tripartite interactions among hosts, bacteria, and phage communities. Moreover, we report several new bacteriophage genomes from the common gut bacteria inNasonia.
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Doyle, Jeff J. "The recipe for cytonuclear interaction begins with a superabundance of plastid and mitochondrial mRNAs". Proceedings of the National Academy of Sciences 119, n.º 34 (9 de agosto de 2022). http://dx.doi.org/10.1073/pnas.2211133119.

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Yao, Xin, Yun-hong Tan, Jun-bo Yang, Yan Wang, Richard T. Corlett e Jean-François Manen. "Exceptionally high rates of positive selection on the rbcL gene in the genus Ilex (Aquifoliaceae)". BMC Evolutionary Biology 19, n.º 1 (21 de outubro de 2019). http://dx.doi.org/10.1186/s12862-019-1521-1.

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Abstract Background The genus Ilex (Aquifoliaceae) has a near-cosmopolitan distribution in mesic habitats from tropical to temperate lowlands and in alpine forests. It has a high rate of hybridization and plastid capture, and comprises four geographically structured plastid groups. A previous study showed that the plastid rbcL gene, coding for the large subunit of Rubisco, has a particularly high rate of non-synonymous substitutions in Ilex, when compared with other plant lineages. This suggests a strong positive selection on rbcL, involved in yet unknown adaptations. We therefore investigated positive selection on rbcL in 240 Ilex sequences from across the global range. Results The rbcL gene shows a much higher rate of positive selection in Ilex than in any other plant lineage studied so far (> 3000 species) by tests in both PAML and SLR. Most positively selected residues are on the surface of the folded large subunit, suggesting interaction with other subunits and associated chaperones, and coevolution between positively selected residues is prevalent, indicating compensatory mutations to recover molecular stability. Coevolution between positively selected sites to restore global stability is common. Conclusions This study has confirmed the predicted high incidence of positively selected residues in rbcL in Ilex, and shown that this is higher than in any other plant lineage studied so far. The causes and consequences of this high incidence are unclear, but it is probably associated with the similarly high incidence of hybridization and introgression in Ilex, even between distantly related lineages, resulting in large cytonuclear discordance in the phylogenies.

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