An Interspecific Plant Hybrid Shows Novel Changes in Parental Splice Forms of Genes for Splicing Factors

Scascitelli, Moira; Cognet, Marie; Adams, Keith L.

doi:10.1534/genetics.109.112557

Cited by 18 publications

(17 citation statements)

References 62 publications

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“…Little is known about AS changes at the onset of allopolyploidy and upon interspecific hybridization. New AS events after interspecific hybridization have been shown in the S locus in an interspecific hybrid of Arabidopsis and its derived allopolyploid (16), and for two SR splicing factors in an interspecific Populus hybrid (17).…”

mentioning

confidence: 98%

Extensive changes to alternative splicing patterns following allopolyploidy in natural and resynthesized polyploids

Zhou

Moshgabadi²,

Adams³

2011

Proc. Natl. Acad. Sci. U.S.A.

110

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Polyploidy has been a common process during the evolution of eukaryotes, especially plants, leading to speciation and the evolution of new gene functions. Gene expression levels and patterns can change, and gene silencing can occur in allopolyploids-phenomena sometimes referred to as "transcriptome shock." Alternative splicing (AS) creates multiple mature mRNAs from a single type of precursor mRNA. Here we examined the evolution of AS patterns after polyploidy, with natural and two resynthesized allotetraploid Brassica napus lines, using RT-PCR and sequencing assays of 82 AS events in duplicated gene pairs (homeologs). Comparing the AS patterns between the two homeologs in natural B. napus revealed that many of the gene pairs show different AS patterns, with a few showing variation that was organ specific or induced by abiotic stress treatments. In the resynthesized allotetraploids, 26-30% of the duplicated genes showed changes in AS compared with the parents, including many cases of AS event loss after polyploidy. Parallel losses of many AS events after allopolyploidy were detected in the two independently resynthesized lines. More changes occurred in parallel between the two lines than changes specific to each line. The PASTICCINO gene showed partitioning of two AS events between the two homeologs in the resynthesized allopolyploids. AS changes after allopolyploidy were much more common than homeolog silencing. Our findings indicate that AS patterns can change rapidly after polyploidy, that many genes are affected, and that AS changes are an important component of the transcriptome shock experienced by new allopolyploids.gene duplication | whole genome duplication | molecular evolution P olyploidy is ubiquitous in plants, with many plants being evolutionarily recent polyploids, and all angiosperms having one or more ancient polyploidy events in their lineage (1-3). Polyploids can display novel phenotypes that may contribute to their evolutionary success (4). Gene expression levels and patterns in natural and synthetic polyploids have been widely studied to investigate the immediate and long-term effects of polyploidy. Some of the phenomena revealed include nonadditive patterns of gene expression in polyploids compared with their progenitors, divergence in expression levels and patterns between the homeologs, and gene silencing, with the effects being variable in different organ types, in different developmental stages, and in response to abiotic stresses (reviewed in refs. 5-8).Alternative splicing (AS) is a posttranscriptional mechanism that can regulate gene expression. AS also allows multiple proteins to be produced from the same gene. In addition, AS can cause transcript degradation by including premature stop codons within the coding region that target the transcripts for nonsensemediated decay, and potentially lower levels of gene expression (9, 10). Premature stop codons introduced by AS can sometimes result in truncated proteins that are functional (11). AS can result in phenotypic changes and impact m...

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mentioning

confidence: 98%

Extensive changes to alternative splicing patterns following allopolyploidy in natural and resynthesized polyploids

Zhou

Moshgabadi²,

Adams³

2011

Proc. Natl. Acad. Sci. U.S.A.

110

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“…NRPD1a is a plant-specific nuclear RNA polymerase that functions in various silencing phenomena including the generation of small RNAs (Herr et al 2005), the methylation of DNA (Onodera et al 2005), and the spread and reception of the silencing signal (Palusa et al 2007; Scascitelli et al 2010). Alignments of the predicted amino-acid sequences of NRPD1a and RNA polymerase II from yeast had identified the putative structural domains of NRPD1a (Herr et al 2005).…”

Section: Resultsmentioning

confidence: 99%

Regulation of the S-Locus Receptor Kinase and Self-Incompatibility inArabidopsis thaliana

Strickler

Tantikanjana

Nasrallah

2013

G3 Genes|Genomes|Genetics

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Intraspecific mate selectivity often is enforced by self-incompatibility (SI), a barrier to self-pollination that inhibits productive pollen-pistil interactions. In the Brassicaceae, SI specificity is determined by two highly-polymorphic proteins: the stigmatic S-locus receptor kinase (SRK) and its pollen coat-localized ligand, the S-locus cysteine-rich protein (SCR). Arabidopsis thaliana is self fertile, but several of its accessions can be made to express SI, albeit to various degrees, by transformation with functional SRK-SCR gene pairs isolated from its close self-incompatible relative, Arabidopsis lyrata. Here, we use a newly identified induced mutation that suppresses the SI phenotype in stigmas of SRK-SCR transformants of the Col-0 accession to investigate the regulation of SI and the SRK transgene. This mutation disrupts NRPD1a, a gene that encodes a plant-specific nuclear RNA polymerase required for genomic methylation and production of some types of silencing RNAs. We show that NRPD1a, along with the RNA-dependent RNA polymerase RDR2, is required for SI in some A. thaliana accessions. We also show that Col-0 nrpd1a mutants exhibit decreased accumulation of SRK transcripts in stigmas, which is not, however, responsible for loss of SI in these plants. Together, our analysis of the nrpd1a mutation and of SRK promoter activity in various accessions reveals that the SRK transgene is subject to several levels of regulation, which vary substantially by tissue type and by accession. This study thus helps explain the well-documented differences in expression of SI exhibited by SRK-SCR transformants of different A. thaliana accessions.

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“…Interspecies hybrids are known to harbour many epigenetic modifications, resulting in changes in gene expression (Liu et al., ; Scascitelli, Cognet, & Adams, ) which significantly affect the reproduction capabilities of hybrids, leading to sterility or subfertility (Johnson, ). Therefore, few researchers have attempted to correlate methylation patterns of spermatogenesis‐related genes with fertility status in cattle–yak hybrids.…”

Section: Discussionmentioning

confidence: 99%

“…Unfortunately, the situation is all the more discomforting in case of fertility of cattle bulls that are crosses of Bos indicus and B. taurus (Khatun, Kaur, & Kanchan, 2013). It is been established beyond doubt that epigenetic mechanisms such as DNA methylation, histone modifications and Interspecies hybrids are known to harbour many epigenetic modifications, resulting in changes in gene expression (Liu et al, 2011;Scascitelli, Cognet, & Adams, 2010) which significantly affect the reproduction capabilities of hybrids, leading to sterility or subfertility (Johnson, 2008). Therefore, few researchers have attempted to correlate methylation patterns of spermatogenesis-related genes with fertility status in cattle-yak hybrids.…”

Section: Discussionmentioning

confidence: 99%

Differential promoter methylation of DAZL gene in bulls with varying seminal parameters

Sarova

Ahlawat

Grewal³

et al. 2018

Reprod Domestic Animals

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In India, cross-breeding of indigenous cattle with exotic cattle such as Holstein Friesian and Jersey has been going on since last four decades to improve milk production. Although it has led to increased milk yield, the subfertility in male cross-bred progeny has remained a significant problem. Epigenetic modifications (DNA methylation, histone modifications and chromatin remodelling) are regarded as key players influencing gene expression. DAZL gene plays an important role in germline development and gametogenesis. The methylation and mRNA expression level of this gene have been significantly negatively correlated in the testes of cattle-yak hybrids and their parents. This study analysed the methylation profile of DAZL gene promoter in bull spermatozoa in an attempt to speculate its role in cross-bred cattle subfertility. Semen samples from Sahiwal, Holstein Friesian and Frieswal bulls (Sahiwal X Holstein Friesian) with varying semen motility parameters were collected, and DNA was isolated. Methylation-specific primers were used to amplify part of promoter and exon 1 of DAZL gene using bisulphite-converted DNA. The amplified products were sequenced after cloning in pTZ57R/T vector. Sequence analysis revealed significantly higher DNA methylation of DAZL gene in Frieswal bulls with poor motility (28.26%) as compared to medium (15.21%) and high motility phenotype (6.52%). In pure-bred counterparts, Sahiwal and Holstein Friesian, epigenetic marks were more in the former (15.21%) than the latter (4.34%), but in both cases, the values were lower as compared to the poor motility Frieswal bulls. This suggests that differential hypermethylation of the CpG islands could possibly influence reproductive parameters in bovines.

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An Interspecific Plant Hybrid Shows Novel Changes in Parental Splice Forms of Genes for Splicing Factors

Cited by 18 publications

References 62 publications

Extensive changes to alternative splicing patterns following allopolyploidy in natural and resynthesized polyploids

Extensive changes to alternative splicing patterns following allopolyploidy in natural and resynthesized polyploids

Regulation of the S-Locus Receptor Kinase and Self-Incompatibility inArabidopsis thaliana

Differential promoter methylation of DAZL gene in bulls with varying seminal parameters

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