Illegitimate Recombination Between Homeologous Genes in Wheat Genome

Liu, Chao; Wang, Jinpeng; Sun, Pengchuan; Yu, Jigao; Meng, Fanbo; Zhang, Zhikang; Guo, He; Wei, Chendan; Li, Xinyu; Shen, Shaoqi; Wang, Xiyin

doi:10.3389/fpls.2020.01076

Cited by 12 publications

(16 citation statements)

References 47 publications

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“…This is a strict criterion used for the detection of whole gene conversion (called WCV-II), as paralogues were produced at least 100 mya, whereas orthologues have diverged more recently. The similarity between sequences representing different rice subspecies is often very high due to the relatively close genetic relationship between these three rice genomes, as in our previous study of the conversion between hexaploid wheat subgenomes [ 32 ].…”

Section: Methodsmentioning

confidence: 99%

“…One result of this recombination is gene conversion, where one gene (or DNA segment) replaces another gene (or DNA segment) on a homeologous chromosome or chromosomal region. Gene conversion between duplicated genes produced by WGD has been identified in the genomes of Poaceae, Arachis hypogaea, Gossypium, Brassica campestris, and Brassica oleracea [18,[28][29][30][31][32]. In addition, gene conversion is frequent and ongoing between homologous chromosomes, such as homeologous chromosomes 11 and 12 produced from the duplication common to grasses (ρ event) in the modern rice genome [26,28,33,34].…”

Section: Introductionmentioning

confidence: 99%

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Conversion between 100-million-year-old duplicated genes contributes to rice subspecies divergence

Wei

Wang

et al. 2021

BMC Genomics

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Background Duplicated gene pairs produced by ancient polyploidy maintain high sequence similarity over a long period of time and may result from illegitimate recombination between homeologous chromosomes. The genomes of Asian cultivated rice Oryza sativa ssp. indica (XI) and Oryza sativa ssp. japonica (GJ) have recently been updated, providing new opportunities for investigating ongoing gene conversion events and their impact on genome evolution. Results Using comparative genomics and phylogenetic analyses, we evaluated gene conversion rates between duplicated genes produced by polyploidization 100 million years ago (mya) in GJ and XI. At least 5.19–5.77% of genes duplicated across the three rice genomes were affected by whole-gene conversion after the divergence of GJ and XI at ~ 0.4 mya, with more (7.77–9.53%) showing conversion of only portions of genes. Independently converted duplicates surviving in the genomes of different subspecies often use the same donor genes. The ongoing gene conversion frequency was higher near chromosome termini, with a single pair of homoeologous chromosomes, 11 and 12, in each rice genome being most affected. Notably, ongoing gene conversion has maintained similarity between very ancient duplicates, provided opportunities for further gene conversion, and accelerated rice divergence. Chromosome rearrangements after polyploidization are associated with ongoing gene conversion events, and they directly restrict recombination and inhibit duplicated gene conversion between homeologous regions. Furthermore, we found that the converted genes tended to have more similar expression patterns than nonconverted duplicates. Gene conversion affects biological functions associated with multiple genes, such as catalytic activity, implying opportunities for interaction among members of large gene families, such as NBS-LRR disease-resistance genes, contributing to the occurrence of the gene conversion. Conclusion Duplicated genes in rice subspecies generated by grass polyploidization ~ 100 mya remain affected by gene conversion at high frequency, with important implications for the divergence of rice subspecies.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Conversion between 100-million-year-old duplicated genes contributes to rice subspecies divergence

Wei

Wang

et al. 2021

BMC Genomics

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“…Instead of using Ks values as a metric here, identical sites between homoeologous sequences were calculated directly. The similarity between sequences representing different rice subspecies is often very high, as in a previous study of hexaploid wheat (Liu et al, 2020).…”

Section: Inference Of Gene Conversionmentioning

confidence: 74%

“…One result of this recombination is gene conversion, where one gene (or DNA fragment) replaces another gene (or DNA fragment) on a homologous chromosome or chromosomal region. Gene conversion between duplicated genes produced by polyploidization has been identified in the genomes of Poaceae, Arachis hypogaea, Gossypium, Brassica campestris, and Brassica oleracea (Wang et al, 2009, Paterson et al, 2012, Zhuang et al, 2019, Yu et al, 2013, Liu et al, 2020. Gene conversion is frequent and on-going between homologous chromosomes, such as homologous chromosomes 11 and 12 produced from the duplication common to grasses (ρ event) in the modern rice genome (Wang et al, 2009, Kurosawa and Ohta, 2011, Wang et al, 2019.…”

Section: Introductionmentioning

confidence: 99%

Conversion between 100-million-year-old duplicated genes contributes to rice subspecies divergence

Wang

Wei

et al. 2020

Preprint

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Extensive sequence similarity between duplicated gene pairs produced by paleo-polyploidization may result from illegitimate recombination between homologous chromosomes. The genomes of Asian cultivated rice Xian/indica (XI) and Geng/japonica (GJ) have recently been updated, providing new opportunities for investigating on-going gene conversion events. Using comparative genomics and phylogenetic analyses, we evaluated gene conversion rates between duplicated genes produced by polyploidization 100 million years ago (mya) in GJ and XI. At least 5.19%–5.77% of genes duplicated across three genomes were affected by whole-gene conversion after the divergence of GJ and XI at ~0.4 mya, with more (7.77%–9.53%) showing conversion of only gene portions. Independently converted duplicates surviving in genomes of different subspecies often used the same donor genes. On-going gene conversion frequency was higher near chromosome termini, with a single pair of homoeologous chromosomes 11 and 12 in each genome most affected. Notably, on-going gene conversion has maintained similarity between very ancient duplicates, provided opportunities for further gene conversion, and accelerated rice divergence. Chromosome rearrangement after polyploidization may result in gene loss, providing a basis for on-going gene conversion, and may have contributed directly to restricted recombination/conversion between homoeologous regions. Gene conversion affected biological functions associated with multiple genes, such as catalytic activity, implying opportunities for interaction among members of large gene families, such as NBS-LRR disease-resistance genes, resulting in gene conversion. Duplicated genes in rice subspecies generated by grass polyploidization ~100 mya remain affected by gene conversion at high frequency, with important implications for the divergence of rice subspecies.One-sentence summaryOn-going gene conversion between duplicated genes produced by 100 mya polyploidization contributes to rice subspecies divergence, often involving the same donor genes at chromosome termini.

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“…In particular, genes that are more highly expressed [134,135], have higher local recombination rates [136][137][138][139], or lower local TE densities [140][141][142] (but see [143]), are expected to experience increased efficacies of natural selection and thus exhibit reduced rates of protein-sequence evolution [144]. That is, genome-wide differences between the progenitors at the time of allopolyploid formation (e.g., transcriptome size, recombination rate, TE load) would not only be expected to give rise to subgenomic differences in the immediate aftermath of polyploidization [101,[145][146][147][148], but also contribute to evolved differences across subgenomes [10,11,[149][150][151][152][153].…”

Section: Differential Rates Of Protein-sequence Evolution Across Allopolyploid Subgenomesmentioning

confidence: 99%

Global patterns of subgenome evolution in organelle-targeted genes of six allotetraploid angiosperms

Sharbrough

Conover

Gyorfy

et al. 2021

Preprint

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Whole-genome duplications (WGDs), in which the number of nuclear genome copies is elevated as a result of autopolyploidy or allopolyploidy, 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 tested this hypothesis in maternal vs. paternal copies of organelle-targeted genes in six allotetraploids: Brachypodium hybridum, Chenopodium quinoa, Coffea arabica, Gossypium hirsutum, Nicotiana tabacum, and Triticum dicoccoides. We report evidence that allopolyploid subgenomes exhibit unequal rates of protein-sequence evolution, but we did not observe global effects of cytonuclear incompatibilities on paternal homoeologs of organelle-targeted genes. Analyses of gene content revealed mixed evidence for whether organelle-targeted genes re-diploidize 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.AUTHOR SUMMARYWhole genome duplication, in which the size and content of the nuclear genome is instantly doubled, represents one of the most profound forms of mutational change. The consequences of duplication events are equally monumental, especially considering that almost all eukaryotes have undergone whole genome duplications during their evolutionary history. While myriad genetic, cellular, organismal, and ecological effects of whole genome duplications have been extensively documented, relatively little attention has been paid to the diminutive but essential “other” genomes present inside the cell, those of chloroplasts and mitochondria. In this study, we compared the evolutionary patterns of >340,000 genes from 23 species to test whether whole genome duplications are associated with genetic mismatches between the nuclear, mitochondrial, and chloroplast genomes. We discovered tremendous differences between duplicated copies of nuclear genomes; however, mitochondria-nuclear and chloroplast-nuclear mismatches do not appear to be common following whole genome duplications. Together these genomic data represent the most extensive analysis yet performed on how polyploids maintain the delicate and finely tuned balance between the nuclear, mitochondrial, and chloroplast genomes.

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Illegitimate Recombination Between Homeologous Genes in Wheat Genome

Abstract: Homeologous genes in common wheat, likely converted by one another, show long-lasting genome instability after polyploidization. The handling editor declared a past co-authorship with one of the authors XW.

Cited by 12 publications

References 47 publications

Conversion between 100-million-year-old duplicated genes contributes to rice subspecies divergence

Conversion between 100-million-year-old duplicated genes contributes to rice subspecies divergence

Conversion between 100-million-year-old duplicated genes contributes to rice subspecies divergence

Global patterns of subgenome evolution in organelle-targeted genes of six allotetraploid angiosperms

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