Duplicate gene expression in allopolyploid Gossypiumreveals two temporally distinct phases of expression evolution

Flagel, Lex; Udall, Joshua A.; Nettleton, Dan; Wendel, Jonathan F.

doi:10.1186/1741-7007-6-16

Cited by 246 publications

(267 citation statements)

References 44 publications

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“…The short read lengths of next-generation sequencing hinder assembly through complex regions, and fragmented draft and reference genomes usually lack skewed (G+C)-content sequences and repetitive intergenic sequences. Furthermore, in allopolyploid species, homoeolog expression dominance or bias, and specifically differential homoelog gene expression, has often been detected, for instance in Gossypium [15][16][17] Triticum 18,19 and Arabidopsis 20,21 , but the role of this phenomenon in selection for phenotypic traits remains mechanistically mysterious 22 .…”

Section: 5mentioning

confidence: 99%

The genome sequence of allopolyploid Brassica juncea and analysis of differential homoeolog gene expression influencing selection

et al. 2016

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2 2 5The Brassica genus contains a diverse range of oilseed and vegetable crops important for human nutrition 1 . Crops of particular agricultural importance include three diploid species, Brassica rapa (AA), Brassica nigra (BB) and Brassica oleracea (CC), and three allopolyploid species, B. napus (AACC), B. juncea (AABB) and Brassica carinata (BBCC). The evolutionary relationships among these Brassica species are described by what is called the 'triangle of U' model 2 , which proposes how the genomes of the three ancestral Brassica species, B. rapa, B. nigra and Brassica oleracae, combined to give rise to the allopolyploid species of this genus. B. juncea formed by hybridization between the diploid ancestors of B. rapa and B. nigra, followed by spontaneous chromosome doubling. Subsequent diversifying selection then gave rise to the vegetable-and oil-use subvarieties of B. juncea. These subvarieties include vegetable and oilseed mustard in China, oilseed crops in India, canola crops in Canada and Australia, and condiment crops in Europe and other regions 3 . Cultivation of B. juncea began in China about 6,000 to 7,000 years ago 4 , and flourished in India from 2,300 BC onward 5 .The genomes of B. rapa, B. oleracea and their allopolyploid offspring B. napus have been published recently [6][7][8] , and are often used to explain genome evolution in angiosperms [6][7][8] . The genomes of all Brassica species underwent a lineage-specific whole-genome triplication 6,7,9 , followed by diploidization that involved substantial genome reshuffling and gene losses 6,10-13 . In general, plant genomes are typically repetitive, polyploid and heterozygous, which complicates genome assembly 14 . The short read lengths of next-generation sequencing hinder assembly through complex regions, and fragmented draft and reference genomes usually lack skewed (G+C)-content sequences and repetitive intergenic sequences. Furthermore, in allopolyploid species, homoeolog expression dominance or bias, and specifically differential homoelog gene expression, has often been detected, for instance in Gossypium [15][16][17] Triticum 18,19 and Arabidopsis 20,21 , but the role of this phenomenon in selection for phenotypic traits remains mechanistically mysterious 22 .We reported here the draft genomes of an allopolyploid, B. juncea var. tumida, constructed by de novo assembly using shotgun reads, single-molecule long reads (PacBio sequencing), genomic (optical) mapping (BioNano sequencing) and genetic mapping, serving to resolve complicated allopolyploid genomes. The multiuse allopolyploid B. juncea genome offers a distinctive model to study the underlying genomic basis for selection in breeding improvement. These findings place this work into the broader context of plant breeding, highlighting The Brassica genus encompasses three diploid and three allopolyploid genomes, but a clear understanding of the evolution of agriculturally important traits via polyploidy is lacking. We assembled an allopolyploid Brassica juncea genome by shotgun and single-m...

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Section: 5mentioning

confidence: 99%

The genome sequence of allopolyploid Brassica juncea and analysis of differential homoeolog gene expression influencing selection

et al. 2016

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“…Moreover, interactions between Aa trans factors and cis elements of At alleles or vice versa result in up-or down-regulation of At and Aa alleles. This may explain at least in part why different dominant expression patterns were identified in the same 8,40 or different allopolyploids 7 .…”

Section: Discussionmentioning

confidence: 99%

“…Barbara McClintock 6 coined the term 'genome shock' to describe unprepared changes to cope with an existing programmed response in interspecific hybrids, leading to transposon activation and genomic instability. Recent studies have shown that genome hybridization between species also induces novel changes in geneexpression 'shock' , as observed in many allopolyploids including Arabidopsis 7 , cotton 8 , and Senecio 9 . The induced variation in the interspecific hybrids can be transmitted to the progeny if chromosomes are doubled to form stable allopolyploids 5,10 .…”

mentioning

confidence: 99%

Cis- and trans-regulatory divergence between progenitor species determines gene-expression novelty in Arabidopsis allopolyploids

et al. 2012

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Gene-expression divergence between species shapes morphological evolution, but the molecular basis is largely unknown. Here we show cis-and trans-regulatory elements and chromatin modifications on gene-expression diversity in genetically tractable Arabidopsis allotetraploids. In Arabidopsis thaliana and Arabidopsis arenosa, both cis and trans with predominant cis-regulatory effects mediate gene-expression divergence. The majority of genes with both cis-and trans-effects are subjected to compensating interactions and stabilizing selection. Interestingly, cis-and trans-regulation is associated with chromatin modifications. In F1 allotetraploids, Arabidopsis arenosa trans factors predominately affect allelic expression divergence. Arabidopsis arenosa trans factors tend to upregulate Arabidopsis thaliana alleles, whereas Arabidopsis thaliana trans factors up-or down-regulate Arabidopsis arenosa alleles. In resynthesized and natural allotetraploids, trans effects drive expression of both homoeologous loci into the same direction. We provide evidence for natural selection and chromatin regulation in shaping gene-expression diversity during plant evolution and speciation.

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“…Upland cotton was formed by ancient interspecific hybridization between AA and DD genome species. In a large microarray study of ovular tissue, Yang et al (2006) demonstrated that AA subgenome genes of all functional classifications were selectively enriched in G. hirsutum L., whereas in a recent study of petal tissues, Flagel et al (2008) encountered the opposite generalized bias and concluded that neither Gossypium genome is globally dominant with respect to expression, but rather, each genome may have local dominance in certain tissue types or developmental stages. Therefore, transcriptome dominance is probably a general consequence of hybridization effects on gene expression in interspecific hybrids and allopolyploids, and seems to be potentially oriented differently in different organs as a probable result of subfunctionalization of duplicated genes (Lynch and Force, 2000).…”

Section: Discussionmentioning

confidence: 99%

Non-additive gene regulation in a citrus allotetraploid somatic hybrid between C. reticulata Blanco and C. limon (L.) Burm

et al. 2009

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Polyploid plants often produce new phenotypes, exceeding the range of variability existing in the diploid gene pool. Several hundred citrus allotetraploid hybrids have been created by somatic hybridization. These genotypes are interesting models to study the immediate effects of allopolyploidization on the regulation of gene expression. Here, we report genome-wide gene expression analysis in fruit pulp of a Citrus interspecific somatic allotetraploid between C. reticulata cv 'Willowleaf mandarin' þ C. limon cv 'Eureka lemon', using a Citrus 20K cDNA microarray. Around 4% transcriptome divergence was observed between the two parental species, and 212 and 160 genes were more highly expressed in C. reticulata and C. limon, respectively. Differential expression of certain genes was confirmed by quantitative real-time RT-PCR. A global downregulation of the allotetraploid hybrid transcriptome was observed, as compared with a theoretical mid parent, for the genes displaying interspecific expression divergence between C. reticulata and C. limon. The genes underexpressed in mandarin, as compared with lemon, were also systematically repressed in the allotetraploid. When genes were overexpressed in C. reticulata compared with C. limon, the distribution of allotetraploid gene expression was far more balanced. Cluster analysis on the basis of gene expression clearly indicated the hybrid was much closer to C. reticulata than to C. limon. These results suggest there is a global dominance of the mandarin transcriptome, in consistence with our previous studies on aromatic compounds and proteomics. Interspecific differentiation of gene expression and non-additive gene regulation involved various biological pathways and different cellular components.

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Duplicate gene expression in allopolyploid Gossypiumreveals two temporally distinct phases of expression evolution

Cited by 246 publications

References 44 publications

The genome sequence of allopolyploid Brassica juncea and analysis of differential homoeolog gene expression influencing selection

The genome sequence of allopolyploid Brassica juncea and analysis of differential homoeolog gene expression influencing selection

Cis- and trans-regulatory divergence between progenitor species determines gene-expression novelty in Arabidopsis allopolyploids

Non-additive gene regulation in a citrus allotetraploid somatic hybrid between C. reticulata Blanco and C. limon (L.) Burm

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