The contributions from the progenitor genomes of the mesopolyploid Brassiceae are evolutionarily distinct but functionally compatible

Hao, Yue; Mabry, Makenzie E.; Edger, Patrick P.; Freeling, Michael; Zheng, Chunfang; Jin, Lingling; VanBuren, Robert; Colle, Marivi; An, Hong; Abrahams, R. Shawn; Washburn, Jacob D.; Qi, Xuchen; Barry, Kerrie; Daum, Christopher; Shu, Shengqiang; Schmutz, Jeremy; Sankoff, David; Barker, Michael S.; Lyons, Eric; Pires, J. Chris; Conant, Gavin C.

doi:10.1101/gr.270033.120

Cited by 28 publications

(24 citation statements)

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“…This study provides new insight into the role of dosage constraint on gene balance in affecting gene expression changes from genomic rearrangements. These findings may help fuel more integrative genetic and evolution investigations of homoeologous exchange, subgenome expression dominance, and duplicate gene evolution that can leverage the vast new output of genomes with ancestral and recent polyploidy and explicit evolutionary models of ancestral subenomes (Emery et al 2018;Hao et al 2021Hao et al , 2022Parey et al 2022). This new avenue of investigation may help further examine evolution and epistasis as well as selection and divergence among paralogs (Qi et al 2021;Conover and Wendel, 2022;Kwon et al 2022), and spur further integration of methods and data across phylogenomics, comparative and population genomics, and network biology (Renny-Byfield et al 2017;Blischak et al 2018).…”

Section: Discussionmentioning

confidence: 88%

Dosage-sensitivity shapes how genes transcriptionally respond to allopolyploidy and homoeologous exchange in resynthesized Brassica napus

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Allopolyploidy involves the hybridization of two evolutionary diverged species and the doubling of genomic material. Frequently, allopolyploids exhibit genomic rearrangements that recombine, duplicate, or delete homoeologous regions of the newly formed genome. While decades of investigation have focused on how genome duplication leads to systematic differences in the retention and expression of duplicate genes, the impact of genomic rearrangements on genome evolution has received less attention. We used genomic and transcriptomic data for six independently resynthesized, isogenic Brassica napus lines in the first, fifth, and tenth generation to identify genomic rearrangements and assess their impact on gene expression dynamics related to subgenome dominance and gene dosage constraint. We find that dosage constraints on the gene expression response to polyploidy begin to loosen within the first ten generations of evolution and systematically differ between dominant and non-dominant subgenomes. We also show that genomic rearrangements can bias estimation of homoeolog expression bias, but fail to fully obscure which subgenome is dominantly expressed. Finally, we demonstrate that dosage-sensitive genes exhibit the same kind of coordinated response to homoeologous exchange as they do for genome duplication, suggesting constraint on dosage balance also acts on these changes to gene dosage.

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Section: Discussionmentioning

confidence: 88%

Dosage-sensitivity shapes how genes transcriptionally respond to allopolyploidy and homoeologous exchange in resynthesized Brassica napus

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“…Hexaploid genomes also show biases in their gene losses. Our analysis of the Brassiceae hexaploidy confirmed that one of the three subgenomes retained many more homoeologous genes than did the other two, and we determined that this ‘least fractionated’ (LF) subgenome was the last arriving of the three present [30]. The ‘order of arrival’ effect, therefore, is a potential source of the biased fractionation in hexaploids and makes them a useful system for testing hypotheses about its origins.…”

Section: Introductionmentioning

confidence: 90%

“…We then sequentially fit models that further differentiated among the subgenomes, first allowing one to have more surviving homoeologues than the other two (WGT 1D ), then allowing all three subgenomes to differ in their loss propensities (WGT 3G ) and finally, allowing the loss rates from each of the three duplicated states to differ (WGT Arb ). For comparison, we also fit each of these models to the Brassiceae hexaploidy we had previously analysed [30].…”

Section: (C) Testing Models Of Post-polyploidy Homoeologue Losses Wit...mentioning

confidence: 99%

“…The models employed so far do not directly address the question of the order of arrival of the subgenomes. To explore that question, we used our prior approach [30] of comparing three 'arrival' models, each proposing a different last-arriving subgenome. The model proposing that IF arrived last collapses back into the WGT Arb model and can be dismissed ( p > 0.5).…”

Section: (C) Order Of Subgenome Arrivalmentioning

confidence: 99%

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Hybridization order is not the driving factor behind biases in duplicate gene losses among the hexaploid Solanaceae

2022

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We model the post-hexaploidy evolution of four genomes from the Solanaceae, a group of flowering plants comprising tomatoes, potatoes and their relatives. The hexaploidy that these genomes descend from occurred through two sequential allopolyploidy events and was marked by the unequal losses of duplicated genes from the different progenitor subgenomes. In contrast with the hexaploid Brassiceae (broccoli and its relatives), where the subgenome with the most surviving genes arrived last in the hexaploidy, among the Solanaceae the most preserved subgenome descends from one of the original two tetraploid progenitors. In fact, the last-arriving subgenome in these plants actually has the fewest surviving genes in the modern genomes. We explore whether the distribution of repetitive elements (REs) in these genomes can explain the biases in gene losses, but while the signals we find are broadly consistent with a role for high RE density in driving gene losses, the REs turn over so quickly that little signal of the RE condition at the time of paleopolyploidy is extant in the modern genomes.

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“…Brassicas, which are closely related to Arabidopsis (tribe Arabideae), are a member of the tribe Brassiceae within the family Brassicaceae, constituting nearly 50% of the entire 3740 species in the family [3], and are represented by large morphological diversity [4]. After the split of the Arabideae and Brassiceae tribes 5-9 million years ago, whole-genome triplication (WGT) of the hexaploid Brassica ancestor occurred, leading to massive chromosomal rearrangements, with re-construction to a more stabilised diploid Brassica species belonging to the Brassiceae tribe through many rounds of polyploidisation [5][6][7].…”

Section: Introductionmentioning

confidence: 99%

Understanding R Gene Evolution in Brassica

et al. 2022

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Brassica crop diseases caused by various pathogens, including viruses, bacteria, fungi and oomycetes, have devastating effects on the plants, leading to significant yield loss. This effect is worsened by the impact of climate change and the pressure to increase cultivation worldwide to feed the burgeoning population. As such, managing Brassica diseases has become a challenge demanding a rapid solution. In this review, we provide a detailed introduction of the plant immune system, discuss the evolutionary pattern of both dominant and recessive disease resistance (R) genes in Brassica and discuss the role of epigenetics in R gene evolution. Reviewing the current findings of how R genes evolve in Brassica spp. provides further insight for the development of creative ideas for crop improvement in relation to breeding sustainable, high quality, disease-resistant Brassica crops.

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The contributions from the progenitor genomes of the mesopolyploid Brassiceae are evolutionarily distinct but functionally compatible

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Cited by 28 publications

References 116 publications

Dosage-sensitivity shapes how genes transcriptionally respond to allopolyploidy and homoeologous exchange in resynthesized Brassica napus

Dosage-sensitivity shapes how genes transcriptionally respond to allopolyploidy and homoeologous exchange in resynthesized Brassica napus

Hybridization order is not the driving factor behind biases in duplicate gene losses among the hexaploid Solanaceae

Understanding R Gene Evolution in Brassica

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