Dispersed emergence and protracted domestication of polyploid wheat uncovered by mosaic ancestral haploblock inference.
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ABSTRACT:
SUBMITTER: Wang Z
PROVIDER: S-EPMC9259585 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Wheat was domesticated about 10,000 years ago and has since spread worldwide to become one of the major crops. Its adaptability to diverse environments and end uses is surprising given the diversity bottlenecks expected from recent domestication and polyploid speciation events. Wheat compensates for these bottlenecks by capturing part of the genetic diversity of its progenitors and by generating new diversity at a relatively fast pace. Frequent gene deletions and disruptions generated by a fast replacement rate of repetitive sequences are buffered by the polyploid nature of wheat, resulting in subtle dosage effects on which selection can operate.
| S-EPMC4737438 | biostudies-literature
Project description:The Q gene encodes an AP2-like transcription factor that played an important role in domestication of polyploid wheat. The chromosome 5A Q alleles (5AQ and 5Aq) have been well studied, but much less is known about the q alleles on wheat homoeologous chromosomes 5B (5Bq) and 5D (5Dq). We investigated the organization, evolution, and function of the Q/q homoeoalleles in hexaploid wheat (Triticum aestivum L.). Q/q gene sequences are highly conserved within and among the A, B, and D genomes of hexaploid wheat, the A and B genomes of tetraploid wheat, and the A, S, and D genomes of the diploid progenitors, but the intergenic regions of the Q/q locus are highly divergent among homoeologous genomes. Duplication of the q gene 5.8 Mya was likely followed by selective loss of one of the copies from the A genome progenitor and the other copy from the B, D, and S genomes. A recent V(329)-to-I mutation in the A lineage is correlated with the Q phenotype. The 5Bq homoeoalleles became a pseudogene after allotetraploidization. Expression analysis indicated that the homoeoalleles are coregulated in a complex manner. Combined phenotypic and expression analysis indicated that, whereas 5AQ plays a major role in conferring domestication-related traits, 5Dq contributes directly and 5Bq indirectly to suppression of the speltoid phenotype. The evolution of the Q/q loci in polyploid wheat resulted in the hyperfunctionalization of 5AQ, pseudogenization of 5Bq, and subfunctionalization of 5Dq, all contributing to the domestication traits.
| S-EPMC3219148 | biostudies-literature
Project description:BackgroundPolyploidy has played a prominent role in the evolution of plants and many other eukaryotic lineages. However, how polyploid genomes adapt to the abrupt presence of two or more sets of chromosomes via genome regulation remains poorly understood. Here, we analyzed genome-wide histone modification and gene expression profiles in relation to domestication and ploidy transition in the A and B subgenomes of polyploid wheat.ResultsWe found that epigenetic modification patterns by two typical euchromatin histone markers, H3K4me3 and H3K27me3, for the great majority of homoeologous triad genes in A and B subgenomes were highly conserved between wild and domesticated tetraploid wheats and remained stable in the process of ploidy transitions from hexaploid to extracted tetraploid and then back to resynthesized hexaploid. However, a subset of genes was differentially modified during tetraploid and hexaploid wheat domestication and in response to ploidy transitions, and these genes were enriched for particular gene ontology (GO) terms. The extracted tetraploid wheat manifested higher overall histone modification levels than its hexaploid donor, and which were reversible and restored to normal levels in the resynthesized hexaploid. Further, while H3K4me3 marks were distally distributed along each chromosome and significantly correlated with subgenome expression as expected, H3K27me3 marks showed only a weak distal bias and did not show a significant correlation with gene expression.ConclusionsOur results reveal overall high stability of histone modification patterns in the A and B subgenomes of polyploid wheat during domestication and in the process of ploidy transitions. However, modification levels of a subset of functionally relevant genes in the A and B genomes were trans-regulated by the D genome in hexaploid wheat.
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Project description:Comprehensive reverse genetic resources, which have been key to understanding gene function in diploid model organisms, are missing in many polyploid crops. Young polyploid species such as wheat, which was domesticated less than 10,000 y ago, have high levels of sequence identity among subgenomes that mask the effects of recessive alleles. Such redundancy reduces the probability of selection of favorable mutations during natural or human selection, but also allows wheat to tolerate high densities of induced mutations. Here we exploited this property to sequence and catalog more than 10 million mutations in the protein-coding regions of 2,735 mutant lines of tetraploid and hexaploid wheat. We detected, on average, 2,705 and 5,351 mutations per tetraploid and hexaploid line, respectively, which resulted in 35-40 mutations per kb in each population. With these mutation densities, we identified an average of 23-24 missense and truncation alleles per gene, with at least one truncation or deleterious missense mutation in more than 90% of the captured wheat genes per population. This public collection of mutant seed stocks and sequence data enables rapid identification of mutations in the different copies of the wheat genes, which can be combined to uncover previously hidden variation. Polyploidy is a central phenomenon in plant evolution, and many crop species have undergone recent genome duplication events. Therefore, the general strategy and methods developed herein can benefit other polyploid crops.
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Project description:We present a novel algorithm, implemented in the software ARGinfer, for probabilistic inference of the Ancestral Recombination Graph under the Coalescent with Recombination. Our Markov Chain Monte Carlo algorithm takes advantage of the Succinct Tree Sequence data structure that has allowed great advances in simulation and point estimation, but not yet probabilistic inference. Unlike previous methods, which employ the Sequentially Markov Coalescent approximation, ARGinfer uses the Coalescent with Recombination, allowing more accurate inference of key evolutionary parameters. We show using simulations that ARGinfer can accurately estimate many properties of the evolutionary history of the sample, including the topology and branch lengths of the genealogical tree at each sequence site, and the times and locations of mutation and recombination events. ARGinfer approximates posterior probability distributions for these and other quantities, providing interpretable assessments of uncertainty that we show to be well calibrated. ARGinfer is currently limited to tens of DNA sequences of several hundreds of kilobases, but has scope for further computational improvements to increase its applicability.
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Project description:One of the most important crops worldwide is wheat. Wheat domestication took place about 10,000 years ago. Not only that its wild progenitors have been discovered and phenotypically characterized, but their genomes were also sequenced and compared to modern wheat. While comparative genomics is essential to track genes that contribute to improvement in crop yield, comparative analyses of functional biological end-products, such as metabolites, are still lacking. With the advent of rigorous mass-spectrometry technologies, it is now possible to address that problem on a big-data scale. In attempt to reveal classes of metabolites, which are associated with wheat domestication, we analyzed the metabolomes of wheat kernel samples from various wheat lines. These wheat lines represented subspecies of tetraploid wheat along primary and secondary domestications, including wild emmer, domesticated emmer, landraces durum, and modern durum. We detected that the groups of plant metabolites such as plant-defense metabolites, antioxidants and plant hormones underwent significant changes during wheat domestication. Our data suggest that these metabolites may have contributed to the improvement in the agricultural fitness of wheat. Closer evaluation of specific metabolic pathways may result in the future in genetically-engineered high-yield crops.
| S-EPMC9122938 | biostudies-literature
Project description:Gene regulatory networks are powerful tools which facilitate hypothesis generation and candidate gene discovery. However, the extent to which the network predictions are biologically relevant is often unclear. Recently a GENIE3 network which predicted targets of wheat transcription factors was produced. Here we used an independent RNA-Seq dataset to test the predictions of the wheat GENIE3 network for the senescence-regulating transcription factor NAM-A1 (TraesCS6A02G108300). We re-analyzed the RNA-Seq data against the RefSeqv1.0 genome and identified a set of differentially expressed genes (DEGs) between the wild-type and nam-a1 mutant which recapitulated the known role of NAM-A1 in senescence and nutrient remobilisation. We found that the GENIE3-predicted target genes of NAM-A1 overlap significantly with the DEGs, more than would be expected by chance. Based on high levels of overlap between GENIE3-predicted target genes and the DEGs, we identified candidate senescence regulators. We then explored genome-wide trends in the network related to polyploidy and found that only homeologous transcription factors are likely to share predicted targets in common. However, homeologs which vary in expression levels across tissues are less likely to share predicted targets than those that do not, suggesting that they may be more likely to act in distinct pathways. This work demonstrates that the wheat GENIE3 network can provide biologically-relevant predictions of transcription factor targets, which can be used for candidate gene prediction and for global analyses of transcription factor function. The GENIE3 network has now been integrated into the KnetMiner web application, facilitating its use in future studies.
| S-EPMC7534433 | biostudies-literature
Project description:The complex correlation structure of a collection of orthologous DNA sequences is uniquely captured by the "ancestral recombination graph" (ARG), a complete record of coalescence and recombination events in the history of the sample. However, existing methods for ARG inference are computationally intensive, highly approximate, or limited to small numbers of sequences, and, as a consequence, explicit ARG inference is rarely used in applied population genomics. Here, we introduce a new algorithm for ARG inference that is efficient enough to apply to dozens of complete mammalian genomes. The key idea of our approach is to sample an ARG of [Formula: see text] chromosomes conditional on an ARG of [Formula: see text] chromosomes, an operation we call "threading." Using techniques based on hidden Markov models, we can perform this threading operation exactly, up to the assumptions of the sequentially Markov coalescent and a discretization of time. An extension allows for threading of subtrees instead of individual sequences. Repeated application of these threading operations results in highly efficient Markov chain Monte Carlo samplers for ARGs. We have implemented these methods in a computer program called ARGweaver. Experiments with simulated data indicate that ARGweaver converges rapidly to the posterior distribution over ARGs and is effective in recovering various features of the ARG for dozens of sequences generated under realistic parameters for human populations. In applications of ARGweaver to 54 human genome sequences from Complete Genomics, we find clear signatures of natural selection, including regions of unusually ancient ancestry associated with balancing selection and reductions in allele age in sites under directional selection. The patterns we observe near protein-coding genes are consistent with a primary influence from background selection rather than hitchhiking, although we cannot rule out a contribution from recurrent selective sweeps.
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Project description:Wheat has been domesticated into a large number of agricultural environments and has the ability to adapt to diverse environments. To understand this process, we survey genotype, repeat content, and DNA methylation across a bread wheat landrace collection representing global genetic diversity. We identify independent variation in methylation, genotype, and transposon copy number. We show that these, so far unexploited, sources of variation have had a significant impact on the wheat genome and that ancestral methylation states become preferentially "hard coded" as single nucleotide polymorphisms (SNPs) via 5-methylcytosine deamination. These mechanisms also drive local adaption, impacting important traits such as heading date and salt tolerance. Methylation and transposon diversity could therefore be used alongside SNP-based markers for breeding.
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Project description:The emergence of new sequencing technologies has provided fast and cost-efficient strategies for high-resolution mapping of complex genomes. Although these approaches hold great promise to accelerate genome analysis, their application in studying genetic variation in wheat has been hindered by the complexity of its polyploid genome. Here, we applied the next-generation sequencing of a wheat doubled-haploid mapping population for high-resolution gene mapping and tested its utility for ordering shotgun sequence contigs of a flow-sorted wheat chromosome. A bioinformatical pipeline was developed for reliable variant analysis of sequence data generated for polyploid wheat mapping populations. The results of variant mapping were consistent with the results obtained using the wheat 9000 SNP iSelect assay. A reference map of the wheat genome integrating 2740 gene-associated single-nucleotide polymorphisms from the wheat iSelect assay, 1351 diversity array technology, 118 simple sequence repeat/sequence-tagged sites, and 416,856 genotyping-by-sequencing markers was developed. By analyzing the sequenced megabase-size regions of the wheat genome we showed that mapped markers are located within 40-100 kb from genes providing a possibility for high-resolution mapping at the level of a single gene. In our population, gene loci controlling a seed color phenotype cosegregated with 2459 markers including one that was located within the red seed color gene. We demonstrate that the high-density reference map presented here is a useful resource for gene mapping and linking physical and genetic maps of the wheat genome.
| S-EPMC3704239 | biostudies-literature