Chromatin modification contributes to the expression divergence of three TaGS2 homoeologs in hexaploid wheat

Wei, Zhang; Fan, Xiangtao; Gao, Yingjie; Liu, Lei; Sun, Lijing; Su, Qiannan; Han, Jie; Zhang, Na; Cui, Fa; Ji, Jun; Tong, Yiping; Li, Junming

doi:10.1038/srep44677

Cited by 13 publications

(5 citation statements)

References 39 publications

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“…Previous studies have revealed that rRNA expression in allopolyploids is regulated by DNA methylation and histone acetylation [ 62 , 63 ]. Besides rRNA, several studies have shown that epigenetic modifications in allopolyploids contribute to expression divergence of homoeologous genes [ 64 , 65 ]. In the present study, we found that genes involved in epigenetic regulation, including histone modifying genes express with a homoeolog expression bias towards Fso_h (Additional file 9 : Figure S8).…”

Section: Discussionmentioning

confidence: 99%

Homoeolog expression bias in allopolyploid oleaginous marine diatom Fistulifera solaris

et al. 2018

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BackgroundAllopolyploidy is a genomic structure wherein two or more sets of chromosomes derived from divergent parental species coexist within an organism. It is a prevalent genomic configuration in plants, as an important source of genetic variation, and also frequently confers environmental adaptability and increased crop productivity. We previously reported the oleaginous marine diatom Fistulifera solaris JPCC DA0580 to be a promising host for biofuel production and that its genome is allopolyploid, which had never previously been reported in eukaryotic microalgae. However, the study of allopolyploidy in F. solaris was hindered by the difficulty in classifying the homoeologous genes based on their progenitor origins, owing to the shortage of diatom genomic references.ResultsIn this study, the allopolyploid genome of F. solaris was tentatively classified into two pseudo-parental subgenomes using sequence analysis based on GC content and codon frequency in each homoeologous gene pair. This approach clearly separated the genome into two distinct fractions, subgenome Fso_h and Fso_l, which also showed the potency of codon usage analysis to differentiate the allopolyploid subgenome. Subsequent homoeolog expression bias analysis revealed that, although both subgenomes appear to contribute to global transcription, there were subgenomic preferences in approximately 61% of homoeologous gene pairs, and the majority of these genes showed continuous bias towards a specific subgenome during lipid accumulation. Additional promoter analysis indicated the possibility of promoter motifs involved in biased transcription of homoeologous genes. Among these subgenomic preferences, genes involved in lipid metabolic pathways showed interesting patterns in that biosynthetic and degradative pathways showed opposite subgenomic preferences, suggesting the possibility that the oleaginous characteristics of F. solaris derived from one of its progenitors.ConclusionsWe report the detailed genomic structure and expression patterns in the allopolyploid eukaryotic microalga F. solaris. The allele-specific patterns reported may contribute to the oleaginous characteristics of F. solaris and also suggest the robust oleaginous characteristics of one of its progenitors. Our data reveal novel aspects of allopolyploidy in a diatom that is not only important for evolutionary studies but may also be advantageous for biofuel production in microalgae.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-4691-0) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

Homoeolog expression bias in allopolyploid oleaginous marine diatom Fistulifera solaris

et al. 2018

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“…() is, to some extent, congruent with the prevailing explanation for biased homoeolog expression and biased genome fractionation, which is framed in terms of the ‘genomic legacy’ of transposable element (TE) differences contributed by the two diploid parents (Steige & Slotte, ; Wendel et al ., ). This explanation, hereafter referred to as the TE model, has emerged in recent years from the accumulating literature on chromatin modification, TE content and small RNA biology (Diez et al ., ; Springer et al ., ; Yang et al ., ; Renny‐Byfield et al ., ; Zhang et al ., ). Phrased simply, the different parental TE loads and their relative distribution between sub‐genomes lead to differentiated epigenetic controls (e.g.…”

Section: The Extended Cis–trans Framework and Expression Patterns In mentioning

confidence: 97%

Cis–trans controls and regulatory novelty accompanying allopolyploidization

Wendel

2018

New Phytologist

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Summary Allopolyploidy is a prevalent process in plants, having important physiological, ecological and evolutionary consequences. Transcriptomic responses to genomic merger and doubling have been demonstrated in many allopolyploid systems, encompassing a diversity of phenomena including homoeolog expression bias, genome dominance, expression‐level dominance and revamping of co‐expression networks. Notwithstanding the foregoing, there remains a need to develop a conceptual framework that will stimulate a deeper understanding of these diverse phenomena and their mechanistic interrelationships. Here we introduce considerations relevant to this framework with a focus on cis–trans interactions among duplicated genes and alleles in hybrids and allopolyploids. By extending classic allele‐specific expression analysis to the allopolyploid level, we distinguish the distinct effects of progenitor regulatory interactions from the novel intergenomic interactions that arise from genome merger and allopolyploidization. This perspective informs experiments designed to reveal the molecular genetic basis of gene regulatory control, and will facilitate the disentangling of genetic from epigenetic and higher‐order effects that impact gene expression. Finally, we suggest that the extended cis–trans model may help conceptually unify several presently disparate hallmarks of allopolyploid evolution, including genome‐wide expression dominance and biased fractionation, and lead to a new level of understanding of phenotypic novelty accompanying polyploidy.

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“…Whether the presence of TaGS3.2 contributes to increased TaGS3 expression levels needs further investigation. Our findings here indicate that genomic-structure-triggered AS could contribute to functional diversity among homeologs in bread wheat, which is different from those caused by epigenetic modifications [ 41 , 42 , 43 ]. Grain size is a complex trait, and different levels of gene function regulation may dominate grain development.…”

Section: Discussionmentioning

confidence: 76%

Alternative Splicing of TaGS3 Differentially Regulates Grain Weight and Size in Bread Wheat

Ren

Zhi

Liu

et al. 2021

IJMS

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The heterotrimeric G-protein mediates growth and development by perceiving and transmitting signals in multiple organisms. Alternative splicing (AS), a vital process for regulating gene expression at the post-transcriptional level, plays a significant role in plant adaptation and evolution. Here, we identified five splicing variants of Gγ subunit gene TaGS3 (TaGS3.1 to TaGS3.5), which showed expression divergence during wheat polyploidization, and differential function in grain weight and size determination. TaGS3.1 overexpression significantly reduced grain weight by 5.89% and grain length by 5.04%, while TaGS3.2–3.4 overexpression did not significantly alter grain size compared to wild type. Overexpressing TaGS3.5 significantly increased the grain weight by 5.70% and grain length by 4.30%. Biochemical assays revealed that TaGS3 isoforms (TaGS3.1–3.4) with an intact OSR domain interact with WGB1 to form active Gβγ heterodimers that further interact with WGA1 to form inactive Gαβγ heterotrimers. Truncated isoforms TaGS3.2–3.4 , which lack the C-terminal Cys-rich region but have enhanced binding affinity to WGB1, antagonistically compete with TaGS3.1 to bind WGB1, while TaGS3.5 with an incomplete OSR domain does not interact with WGB1. Taking these observations together, we proposed that TaGS3 differentially regulates grain size via AS, providing a strategy by which the grain size is fine-tuned and regulated at the post-transcriptional level.

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Chromatin modification contributes to the expression divergence of three TaGS2 homoeologs in hexaploid wheat

Cited by 13 publications

References 39 publications

Homoeolog expression bias in allopolyploid oleaginous marine diatom Fistulifera solaris

Homoeolog expression bias in allopolyploid oleaginous marine diatom Fistulifera solaris

Cis–trans controls and regulatory novelty accompanying allopolyploidization

Alternative Splicing of TaGS3 Differentially Regulates Grain Weight and Size in Bread Wheat

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