Alternative splicing dynamics and evolutionary divergence during embryogenesis in wheat species

Gao, Peng; Quilichini, Teagen D.; Zhai, Chun; Qin, Li; Nilsen, Kirby T.; Li, Qiang; Sharpe, Andrew; Kochian, Leon V.; Zou, Jitao; Reddy, Anireddy S. N.; Wei, Yangdou; Pozniak, Curtis; Patterson, N. A.; Gillmor, C. Stewart; Datla, Raju; Xiang, Daoquan

doi:10.1111/pbi.13579

Cited by 25 publications

(24 citation statements)

References 61 publications

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“…AS response to HE. AS was observed to respond to changes of external conditions (such as abiotic/biotic stresses) and internal genomic environment (including WGD and structure variations) in plants ( Staiger and Brown, 2013, Laloum et al, 2018, Gao et al, 2021, which contribute to diversity and complexity of functional genome through enlarging the variety of RNA isoforms (Graveley, 2001, Syed et al, 2012. HE-induced AS response provides an extra dimension to further understand the genetic consequences of allopolyploidy.…”

Section: He-inducedmentioning

confidence: 99%

“…This also raises new questions: besides junction regions, does HE also impact the expression of genes located within HE and on non-HE genomic regions? Moreover, recent studies showed that polyploidization and domestication can generate qualitative (gain and/or loss) changes of AS events in natural wheat species (Yu et al, 2020, Gao et al, 2021. So, is the direct effect of HE on AS in synthetic allopolyploids similar to that seen in established allopolyploid species that experienced natural selection and domestication?…”

Section: Introductionmentioning

confidence: 99%

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Effects of homoeologous exchange on gene expression and alternative splicing in a newly formed allotetraploid wheat

Zhang¹,

Xun²,

Lv³

et al. 2021

Preprint

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Homoeologous exchange (HE) is a major mechanism generating post-polyploidization genetic variation with important evolutionary consequences. However, the direct impacts of HE without entangling with additional evolutionary forces on gene expression remains to be fully understood. Here, we analyzed high-throughput RNA-seq data of young leaves from individuals of a synthetic allotetraploid wheat (AADD), which contain variable numbers of HEs. We aimed to investigate if and to which extent HE directly impacts gene expression and alternative splicing (AS). We found that HE impacts expression of genes located within HE regions primarily via cis-acting dosage effect, which led to significant changes in the total expression of homoeolog pairs, especially for homoeologs whose original expression was biased. In parallel, HE influences expression of a large amount of genes residing in non-HE regions by trans-regulation leading to convergent expression of homoeolog pairs. Intriguingly, when taking into account of the original relative homoeolog expression states, homoeolog pairs under trans-effect are more prone to showing convergent response to HE whereas those under cis-effect trended to show subgenome-specific expression. Moreover, HE induced quantitative, largely individual-specific, changes of alternative splicing (AS) events. Like homoeologs expression, homoeo-AS events which related to trans effect were more responsive to HE. HE therefore exerts multifaceted immediate effects on gene expression and, to a less extent, also transcript diversity in nascent allopolyploidy.

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Section: He-inducedmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Effects of homoeologous exchange on gene expression and alternative splicing in a newly formed allotetraploid wheat

Zhang¹,

Xun²,

Lv³

et al. 2021

Preprint

View full text Add to dashboard Cite

show abstract

Section: Introductionmentioning

confidence: 99%

“…Alternative splicing (AS) is a key post-transcriptional regulatory mechanism for expanding proteomic diversity and functional complexity [ 12 ], even generating trait diversity [ 13 ]. AS mainly results in generation of an alternative 3′ or 5′ splicing site (Alt 3′ ss and Alt 5′ ss, respectively),) intron retention (IR), and exon skipping (ES) [ 13 , 14 ]. AS can produce truncated proteins, disrupting key domains or abolishing interaction with other proteins and thereby preventing the formation of functional protein complexes [ 15 , 16 ].…”

Section: Introductionmentioning

confidence: 99%

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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“…Yet, whether alternative splicing is conserved has conflicting evidence with suggestions of both rapid divergence (Roy and Irimia 2009;Barbosa-Morais, et al 2012;Merkin, et al 2012) and conservation in splicing regulation. Specifically, sex determination genes in insects with sex specific splicing (Burtis and Baker 1989;Telonis-Scott, et al 2009;Salz and Erickson 2010;Graveley, et al 2011;Rogers, et al 2021) and developmental stage specific splicing Gao, et al 2021;Mazin, et al 2021).…”

Section: Introductionmentioning

confidence: 99%

The evolution of splicing: transcriptome complexity and transcript distances implemented inTranD

Nanni

Titus-McQuillan

Moskalenko

et al. 2021

Preprint

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Alternative splicing contributes to organismal complexity. Comparing transcripts between and within species is an important first step toward understanding questions about how evolution of transcript structure changes between species and contributes to sub-functionalization. These questions are confounded with issues of data quality and availability. The recent explosion of affordable long read sequencing of mRNA has considerably widened the ability to study transcriptional variation in non-model species. In this work, we develop a computational framework that uses nucleotide resolution distance metrics to compare transcript models for structural phenotypes: total transcript length, intron retention, donor/acceptor site variation, alternative exon cassettes, alternative 5'/3' UTRs are each scored qualitatively and quantitatively in terms of number of nucleotides. For a single annotation file, all differences among transcripts within a gene are summarized and transcriptome-level complexity metrics: number of variable nucleotides, unique exons per gene, exons per transcript, and transcripts per gene are calculated. To compare two transcriptomes on the same co-ordinates, a weighted total distance between pairs of transcripts for the same gene is calculated. The weight function proposed has larger penalties for intron retention and exon skipping than alternative donor/acceptor sites. Minimum distances can be used to identify both transcript pairs and transcripts missing structural elements in either of the two annotations. This enables a broad range of functionality from comparing sister species to comparing different methods of building and summarizing transcriptomes. Importantly, the philosophy here is to output metrics, enabling others to explore the nucleotide-level distance metrics. Single transcriptome annotation summaries and pairwise comparisons are implemented in a new tool, TranD, distributed as a PyPi package and in the open-source web-based Galaxy (www.galaxyproject.org) platform.

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Alternative splicing dynamics and evolutionary divergence during embryogenesis in wheat species

Cited by 25 publications

References 61 publications

Effects of homoeologous exchange on gene expression and alternative splicing in a newly formed allotetraploid wheat

Effects of homoeologous exchange on gene expression and alternative splicing in a newly formed allotetraploid wheat

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

The evolution of splicing: transcriptome complexity and transcript distances implemented inTranD

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