Allopolyploidisation merges evolutionarily distinct parental genomes (subgenomes) into a single nucleus. A frequent observation is that one subgenome is ‘dominant’ over the other subgenome, often being more highly expressed. Here, we ‘replayed the evolutionary tape’ with six isogenic resynthesised We found that the same subgenome was consistently more dominantly expressed in all lines and generations and that >70% of biased gene pairs showed the same dominance patterns across all lines and an These findings demonstrate that ‘replaying the evolutionary tape’ in an allopolyploid results in largely repeatable and predictable subgenome expression dominance patterns.
This content will become publicly available on March 7, 2025
Polyploidy is an important evolutionary force, yet epigenetic mechanisms, such as DNA methylation, that regulate genome‐wide expression of duplicated genes remain largely unknown. Here, we use The naturally occurring allotetraploid Genome‐wide methylation levels in This study provides the first assessment of both overall and locus‐specific patterns of DNA methylation in a recent natural allopolyploid and shows that novel methylation variants can be generated rapidly after polyploid formation. Together, these results demonstrate that mechanisms to regulate duplicate gene expression may arise soon after allopolyploid formation and that these mechanisms vary among genes.
- Award ID(s):
- 2242696
- NSF-PAR ID:
- 10494506
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- New Phytologist
- ISSN:
- 0028-646X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Summary Brassica napus allopolyploid lines and investigated subgenome dominance patterns over the first 10 generations postpolyploidisation.in silico hybrid of the parents. Gene network analyses indicated an enrichment for network interactions and several biological functions for theBrassica oleracea subgenome biased pairs, but no enrichment was identified forBrassica rapa subgenome biased pairs. Furthermore, DNA methylation differences between subgenomes mirrored the observed gene expression bias towards the dominant subgenome in all lines and generations. Many of these differences in gene expression and methylation were also found when comparing the progenitor genomes, suggesting that subgenome dominance is partly related to parental genome differences rather than just a byproduct of allopolyploidisation. -
more » « less
SUMMARY Medicago truncatula is a model legume for fundamental research on legume biology and symbiotic nitrogen fixation.Tnt1 , a retrotransposon from tobacco, was used to generate insertion mutants inM. truncatula R108. Approximately 21 000 insertion lines have been generated and publicly available.Tnt1 retro‐transposition event occurs during somatic embryogenesis (SE), a pivotal process that triggers massive methylation changes. We studied the SE ofM. truncatula R108 using leaf explants and explored the dynamic shifts in the methylation landscape from leaf explants to callus formation and finally embryogenesis. Higher cytosine methylation in all three contexts of CG, CHG, and CHH patterns was observed during SE compared to the controls. Higher methylation patterns were observed in assumed promoter regions (~2‐kb upstream regions of transcription start site) of the genes, while lowest was recorded in the untranslated regions. Differentially methylated promoter region analysis showed a higher CHH methylation in embryogenesis tissue samples when compared to CG and CHG methylation. Strong correlation (89.71%) was identified between the differentially methylated regions (DMRs) and the site ofTnt1 insertions inM. truncatula R108 and stronger hypermethylation of genes correlated with higher number ofTnt1 insertions in all contexts of CG, CHG, and CHH methylation. Gene ontology enrichment and KEGG pathway enrichment analysis identified genes and pathways enriched in the signal peptide processing, ATP hydrolysis, RNA polymerase activity, transport, secondary metabolites, and nitrogen metabolism pathways. Combined gene expression analysis and methylation profiling showed an inverse relationship between methylation in the DMRs (regions spanning genes) and the expression of genes. Our results show that a dynamic shift in methylation happens during the SE process in the context of CG, CHH and CHG methylation, and theTnt1 retrotransposition correlates with the hyperactive methylation regions. -
more » « less
Abstract It has been hypothesized that environmentally induced changes to gene body methylation could facilitate adaptive transgenerational responses to changing environments.
We compared patterns of global gene expression (Tag‐seq) and gene body methylation (reduced representation bisulfite sequencing) in 80 eastern oysters
Crassostrea virginica from six full‐sib families, common gardened for 14 months at two sites in the northern Gulf of Mexico that differed in mean salinity.At the time of sampling, oysters from the two sites differed in mass by 60% and in parasite loads by nearly two orders of magnitude. They also differentially expressed 35% of measured transcripts. However, we observed differential methylation at only 1.4% of potentially methylated loci in comparisons between individuals from these different environments, and little correspondence between differential methylation and differential gene expression.
Instead, methylation patterns were largely driven by genetic differences among families, with a PERMANOVA analysis indicating nearly a two orders of magnitude greater number of genes differentially methylated between families than between environments.
An analysis of CpG observed/expected values (CpG O/E) across the
C .virginica genome showed a distinct bimodal distribution, with genes from the first cluster showing the lower CpG O/E values, greater methylation and higher and more stable gene expression, while genes from the second cluster showed lower methylation, and lower and more variable gene expression.Taken together, the differential methylation results suggest that only a small portion of the
C .virginica genome is affected by environmentally induced changes in methylation. At this point, there is little evidence to suggest that environmentally induced methylation states would play a leading role in regulating gene expression responses to new environments. -
more » « less
Abstract Background Environmental fluctuation during embryonic and fetal development can permanently alter an organism’s morphology, physiology, and behaviour. This phenomenon, known as developmental plasticity, is particularly relevant to reptiles that develop in subterranean nests with variable oxygen tensions. Previous work has shown hypoxia permanently alters the cardiovascular system of snapping turtles and may improve cardiac anoxia tolerance later in life. The mechanisms driving this process are unknown but may involve epigenetic regulation of gene expression via DNA methylation. To test this hypothesis, we assessed in situ cardiac performance during 2 h of acute anoxia in juvenile turtles previously exposed to normoxia (21% oxygen) or hypoxia (10% oxygen) during embryogenesis. Next, we analysed DNA methylation and gene expression patterns in turtles from the same cohorts using whole genome bisulfite sequencing, which represents the first high-resolution investigation of DNA methylation patterns in any reptilian species.
Results Genome-wide correlations between CpG and CpG island methylation and gene expression patterns in the snapping turtle were consistent with patterns observed in mammals. As hypothesized, developmental hypoxia increased juvenile turtle cardiac anoxia tolerance and programmed DNA methylation and gene expression patterns. Programmed differences in expression of genes such as
SCN5A may account for differences in heart rate, while genes such asTNNT2 andTPM3 may underlie differences in calcium sensitivity and contractility of cardiomyocytes and cardiac inotropy. Finally, we identified putative transcription factor-binding sites in promoters and in differentially methylated CpG islands that suggest a model linking programming of DNA methylation during embryogenesis to differential gene expression and cardiovascular physiology later in life. Binding sites for hypoxia inducible factors (HIF1A, ARNT, and EPAS1) and key transcription factors activated by MAPK and BMP signaling (RREB1 and SMAD4) are implicated.Conclusions Our data strongly suggests that DNA methylation plays a conserved role in the regulation of gene expression in reptiles. We also show that embryonic hypoxia programs DNA methylation and gene expression patterns and that these changes are associated with enhanced cardiac anoxia tolerance later in life. Programming of cardiac anoxia tolerance has major ecological implications for snapping turtles, because these animals regularly exploit anoxic environments throughout their lifespan.
-
Abstract Background Mutations in LMNA , encoding lamin A/C, lead to a variety of diseases known as laminopathies including dilated cardiomyopathy (DCM) and skeletal abnormalities. Though previous studies have investigated the dysregulation of gene expression in cells from patients with DCM, the role of epigenetic (gene regulatory) mechanisms, such as DNA methylation, has not been thoroughly investigated. Furthermore, the impact of family-specific LMNA mutations on DNA methylation is unknown. Here, we performed reduced representation bisulfite sequencing on ten pairs of fibroblasts and their induced pluripotent stem cell (iPSC) derivatives from two families with DCM due to distinct LMNA mutations, one of which also induces brachydactyly. Results Family-specific differentially methylated regions (DMRs) were identified by comparing the DNA methylation landscape of patient and control samples. Fibroblast DMRs were found to enrich for distal regulatory features and transcriptionally repressed chromatin and to associate with genes related to phenotypes found in tissues affected by laminopathies. These DMRs, in combination with transcriptome-wide expression data and lamina-associated domain (LAD) organization, revealed the presence of inter-family epimutation hotspots near differentially expressed genes, most of which were located outside LADs redistributed in LMNA -related DCM. Comparison of DMRs found in fibroblasts and iPSCs identified regions where epimutations were persistent across both cell types. Finally, a network of aberrantly methylated disease-associated genes revealed a potential molecular link between pathways involved in bone and heart development. Conclusions Our results identified both shared and mutation-specific laminopathy epimutation landscapes that were consistent with lamin A/C mutation-mediated epigenetic aberrancies that arose in somatic and early developmental cell stages.more » « less
