Histone Modifications Define Expression Bias of Homoeologous Genomes in Allotetraploid Cotton

Zheng, Dewei; Ye, Wenxue; Song, Qingxin; Han, Fangpu; Zhang, Tianzhen; Chen, Z Jeffrey

doi:10.1104/pp.16.01210

Cited by 35 publications

(36 citation statements)

References 48 publications

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“…4b), indicating that more CG methylation occurred in the A homoeologs of allotetraploid cotton. This is consistent with higher H3K4me3 levels in the D than in the A homoeologs in allotetraploid cotton [47], as intragenic DNA methylation antagonizes H3K4 trimethylation in plants [48, 49] and mammalian cells [50]. Using an absolute value of at least 0.6 in CG methylation changes between wild G. hirsutum and diploid species, we identified 501 hypermethylated and 137 hypomethylated genes in wild G. hirsutum compared with diploid species (Additional file 5: Table S4).…”

Section: Resultssupporting

confidence: 77%

Epigenomic and functional analyses reveal roles of epialleles in the loss of photoperiod sensitivity during domestication of allotetraploid cottons

et al. 2017

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BackgroundPolyploidy is a pervasive evolutionary feature of all flowering plants and some animals, leading to genetic and epigenetic changes that affect gene expression and morphology. DNA methylation changes can produce meiotically stable epialleles, which are transmissible through selection and breeding. However, the relationship between DNA methylation and polyploid plant domestication remains elusive.ResultsWe report comprehensive epigenomic and functional analyses, including ~12 million differentially methylated cytosines in domesticated allotetraploid cottons and their tetraploid and diploid relatives. Methylated genes evolve faster than unmethylated genes; DNA methylation changes between homoeologous loci are associated with homoeolog-expression bias in the allotetraploids. Significantly, methylation changes induced in the interspecific hybrids are largely maintained in the allotetraploids. Among 519 differentially methylated genes identified between wild and cultivated cottons, some contribute to domestication traits, including flowering time and seed dormancy. CONSTANS (CO) and CO-LIKE (COL) genes regulate photoperiodicity in Arabidopsis. COL2 is an epiallele in allotetraploid cottons. COL2A is hypermethylated and silenced, while COL2D is repressed in wild cottons but highly expressed due to methylation loss in all domesticated cottons tested. Inhibiting DNA methylation activates COL2 expression, and repressing COL2 in cultivated cotton delays flowering.ConclusionsWe uncover epigenomic signatures of domestication traits during cotton evolution. Demethylation of COL2 increases its expression, inducing photoperiodic flowering, which could have contributed to the suitability of cotton for cultivation worldwide. These resources should facilitate epigenetic engineering, breeding, and improvement of polyploid crops.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-017-1229-8) contains supplementary material, which is available to authorized users.

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Section: Resultssupporting

confidence: 77%

Epigenomic and functional analyses reveal roles of epialleles in the loss of photoperiod sensitivity during domestication of allotetraploid cottons

et al. 2017

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“…In Arabidopsis, histone modifications and DNA methylation are coordinated to regulate gene expression changes in allopolyploids and between progenitors (Wang et al, 2004;Ha et al, 2011), associated with cis-and trans-acting genes in F 1 allotetraploids (Shi et al, 2012), and related to dosage-dependent and -independent gene expression in allopolyploids (Shi et al, 2015). In allotetraploid cotton, histone H3K4me3 levels per chromosome unit are generally higher in the D subgenome than in the A subgenome, which correlates with more D homoeologs with higher expression levels than A homoeologs (Zheng et al, 2016). In the two wheat allotetraploids, putative homologs of histone H3K9 methyltransferase genes are generally repressed in both endosperm and root of AADD but not in the endosperm of S l S l AA.…”

Section: Discussionmentioning

confidence: 99%

Asymmetrical changes of gene expression, small RNAs and chromatin in two resynthesized wheat allotetraploids

Yuan

Jiang

et al. 2018

The Plant Journal

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Polyploidy occurs in some animals and all flowering plants, including important crops such as wheat. The consequences of polyploidy in crops remain elusive, partly because their progenitors are unknown. Using two resynthesized wheat allotetraploids S S AA and AADD with known diploid progenitors, we analyzed mRNA and small RNA transcriptomes in the endosperm, compared transcriptomes between endosperm and root in AADD, and examined chromatin changes in the allotetraploids. In the endosperm, there were more non-additively expressed genes in S S AA than in AADD. In AADD, non-additively expressed genes were developmentally regulated, and the majority (62-70%) were repressed. The repressed genes in AADD included a group of histone methyltransferase gene homologs, which correlated with reduced histone H3K9me2 levels and activation of various transposable elements in AADD. In S S AA, there was a tendency for expression dominance of S over A homoeologs, but the histone methyltransferase gene homologs were additively expressed, correlating with insignificant changes in histone H3K9me2 levels. Moreover, more 24-nucleotide small inferring RNAs (siRNAs) in the A subgenome were disrupted in AADD than in S S AA, which were associated with expression changes of siRNA-associated genes. Our results indicate that asymmetrical changes in siRNAs, chromatin modifications, transposons and gene expression coincide with unstable AADD genomes and stable S S AA genomes, which could help explain the evolutionary trajectories of wheat allotetraploids formed by different progenitors.

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“…In another report, hypermethylated DNA governs the fiber differentiation by the H3K9me2-dependent pathway in Gossypium barbadense . The histone methylation mark H3K4me3 has also been implicated in the expression bias of homoeologous genes in root-tip cells in Gossypium hirsutum (Zheng et al, 2016). Recently, extensive studies have generated a plethora of information about small RNAs that are expressed during the cotton fiber development (Guan et al, 2014b;Sun et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Role of GhHDA5 in H3K9 deacetylation and fiber initiation in Gossypium hirsutum

Kumar

Singh

et al. 2018

The Plant Journal

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Cotton fibers are single-celled trichomes that initiate from the epidermal cells of the ovules at or before anthesis. Here, we identified that the histone deacetylase (HDAC) activity is essential for proper cotton fiber initiation. We further identified 15 HDACs homoeologs in each of the A- and D-subgenomes of Gossypium hirsutum. Few of these HDAC homoeologs expressed preferentially during the early stages of fiber development [-1, 0 and 6 days post-anthesis (DPA)]. Among them, GhHDA5 expressed significantly at the time of fiber initiation (-1 and 0 DPA). The in vitro assay for HDAC activity indicated that GhHDA5 primarily deacetylates H3K9 acetylation marks. Moreover, the reduced expression of GhHDA5 also suppresses fiber initiation and lint yield in the RNA interference (RNAi) lines. The 0 DPA ovules of GhHDA5RNAi lines also showed alterations in reactive oxygen species homeostasis and elevated autophagic cell death in the developing fibers. The differentially expressed genes (DEGs) identified through RNA-seq of RNAi line (DEP12) and their pathway analysis showed that GhHDA5 modulates expression of many stress and development-related genes involved in fiber development. The reduced expression of GhHDA5 in the RNAi lines also resulted in H3K9 hyper-acetylation on the promoter region of few DEGs assessed by chromatin immunoprecipitation assay. The positively co-expressed genes with GhHDA5 showed cumulative higher expression during fiber initiation, and gene ontology annotation suggests their involvement in fiber development. Furthermore, the predicted protein interaction network in the positively co-expressed genes indicates HDA5 modulates fiber initiation-specific gene expression through a complex involving reported repressors.

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Histone Modifications Define Expression Bias of Homoeologous Genomes in Allotetraploid Cotton

Cited by 35 publications

References 48 publications

Epigenomic and functional analyses reveal roles of epialleles in the loss of photoperiod sensitivity during domestication of allotetraploid cottons

Epigenomic and functional analyses reveal roles of epialleles in the loss of photoperiod sensitivity during domestication of allotetraploid cottons

Asymmetrical changes of gene expression, small RNAs and chromatin in two resynthesized wheat allotetraploids

Role of GhHDA5 in H3K9 deacetylation and fiber initiation in Gossypium hirsutum

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