Homoeolog expression bias and expression level dominance in allopolyploid cotton
TL;DR: Gene expression patterns in interspecific hybrid F1, and synthetic and natural allopolyploid cotton using RNA-Seq reads from leaf transcriptomes suggest that natural selection reconciles the regulatory mismatches caused by initial genomic merger, while new gene expression conditions are generated for evaluation by selection.
Abstract: Allopolyploidy is an evolutionary and mechanistically intriguing process, in that it entails the reconciliation of two or more sets of diverged genomes and regulatory interactions. In this study, we explored gene expression patterns in interspecific hybrid F(1), and synthetic and natural allopolyploid cotton using RNA-Seq reads from leaf transcriptomes. We determined how the extent and direction of expression level dominance (total level of expression for both homoeologs) and homoeolog expression bias (relative contribution of homoeologs to the transcriptome) changed from hybridization through evolution at the polyploid level and following cotton domestication. Genome-wide expression level dominance was biased toward the A-genome in the diploid hybrid and natural allopolyploids, whereas the direction was reversed in the synthetic allopolyploid. This biased expression level dominance was mainly caused by up- or downregulation of the homoeolog from the 'non-dominant' parent. Extensive alterations in homoeolog expression bias and expression level dominance accompany the initial merger of two diverged diploid genomes, suggesting a combination of regulatory (cis or trans) and epigenetic interactions that may arise and propagate through the transcriptome network. The extent of homoeolog expression bias and expression level dominance increases over time, from genome merger through evolution at the polyploid level. Higher rates of transgressive and novel gene expression patterns as well as homoeolog silencing were observed in natural allopolyploids than in F(1) hybrid and synthetic allopolyploid cottons. These observations suggest that natural selection reconciles the regulatory mismatches caused by initial genomic merger, while new gene expression conditions are generated for evaluation by selection.
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University of Évry Val d'Essonne1, Crops Research Institute2, Agriculture and Agri-Food Canada3, J. Craig Venter Institute4, Fujian Agriculture and Forestry University5, Plant Genome Mapping Laboratory6, University of Giessen7, French Alternative Energies and Atomic Energy Commission8, Institut national de la recherche agronomique9, National Research Council10, Australian Centre for Plant Functional Genomics11, University of Cologne12, Purdue University13, University of California, Berkeley14, University of British Columbia15, Fondation Jean Dausset Centre d'Etude du Polymorphisme Humain16, Huazhong Agricultural University17, Hunan Agricultural University18, Chungnam National University19, University of Arizona20, University of York21, University of Missouri22, Southern Cross University23, University of Western Australia24, Centre national de la recherche scientifique25
TL;DR: The polyploid genome of Brassica napus, which originated from a recent combination of two distinct genomes approximately 7500 years ago and gave rise to the crops of rape oilseed, is sequenced.
Abstract: Oilseed rape (Brassica napus L.) was formed ~7500 years ago by hybridization between B. rapa and B. oleracea, followed by chromosome doubling, a process known as allopolyploidy. Together with more ancient polyploidizations, this conferred an aggregate 72× genome multiplication since the origin of angiosperms and high gene content. We examined the B. napus genome and the consequences of its recent duplication. The constituent An and Cn subgenomes are engaged in subtle structural, functional, and epigenetic cross-talk, with abundant homeologous exchanges. Incipient gene loss and expression divergence have begun. Selection in B. napus oilseed types has accelerated the loss of glucosinolate genes, while preserving expansion of oil biosynthesis genes. These processes provide insights into allopolyploid evolution and its relationship with crop domestication and improvement.
1,743 citations
Academy of Sciences of the Czech Republic1, University of Saskatchewan2, Bayer3, Kansas State University4, University of California, Riverside5, Blaise Pascal University6, Kyoto University7, University of Dundee8, Punjab Agricultural University9, Indian Agricultural Research Institute10, University of Delhi11, University of Tsukuba12, Yokohama City University13, National Research Council14, Norwegian University of Life Sciences15, Sainsbury Laboratory16, Leibniz Association17, United States Department of Energy18, James Hutton Institute19, Institut national de la recherche agronomique20, University of Zurich21, Sabancı University22, Murdoch University23
TL;DR: Insight into the genome biology of a polyploid crop provide a springboard for faster gene isolation, rapid genetic marker development, and precise breeding to meet the needs of increasing food demand worldwide.
Abstract: An ordered draft sequence of the 17-gigabase hexaploid bread wheat (Triticum aestivum) genome has been produced by sequencing isolated chromosome arms. We have annotated 124,201 gene loci distributed nearly evenly across the homeologous chromosomes and subgenomes. Comparative gene analysis of wheat subgenomes and extant diploid and tetraploid wheat relatives showed that high sequence similarity and structural conservation are retained, with limited gene loss, after polyploidization. However, across the genomes there was evidence of dynamic gene gain, loss, and duplication since the divergence of the wheat lineages. A high degree of transcriptional autonomy and no global dominance was found for the subgenomes. These insights into the genome biology of a polyploid crop provide a springboard for faster gene isolation, rapid genetic marker development, and precise breeding to meet the needs of increasing food demand worldwide.
1,421 citations
Norwich Research Park1, Bayer2, University of Toronto3, Agriculture and Agri-Food Canada4, University of Saskatchewan5, Paris Diderot University6, Institut national de la recherche agronomique7, National Research Council8, Technische Universität München9, University of Melbourne10, University of Maryland, College Park11
TL;DR: This study leverages 850 wheat RNA-sequencing samples, alongside the annotated genome, to determine the similarities and differences between homoeolog expression across a range of tissues, developmental stages, and cultivars and suggests that the transposable elements in promoters relate more closely to the variation in the relative expression of homoeologicals across tissues than to a ubiquitous effect across all tissues.
Abstract: The coordinated expression of highly related homoeologous genes in polyploid species underlies the phenotypes of many of the world's major crops. Here we combine extensive gene expression datasets to produce a comprehensive, genome-wide analysis of homoeolog expression patterns in hexaploid bread wheat. Bias in homoeolog expression varies between tissues, with ~30% of wheat homoeologs showing nonbalanced expression. We found expression asymmetries along wheat chromosomes, with homoeologs showing the largest inter-tissue, inter-cultivar, and coding sequence variation, most often located in high-recombination distal ends of chromosomes. These transcriptionally dynamic genes potentially represent the first steps toward neo- or subfunctionalization of wheat homoeologs. Coexpression networks reveal extensive coordination of homoeologs throughout development and, alongside a detailed expression atlas, provide a framework to target candidate genes underpinning agronomic traits in wheat.
609 citations
Cites background from "Homoeolog expression bias and expre..."
...These results suggest that the polyploid context and the polyploidization process itself affect the relative expression of homoeologs comparedwith the baseline expression in the progenitor species (13), which has also been observed during the evolution of polyploid cotton (26) and monkeyflower (27)....
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TL;DR: Perhaps the most important conclusion from recent and ongoing studies of polyploidy is that polyploids may propel a population into a new adaptive sphere given the myriad changes that accompany genome doubling.
Abstract: Polyploidy has long been considered a major force in plant evolution. G. Ledyard Stebbins, Jr., an architect of the Modern Synthesis, elegantly addressed a broad range of topics, from genes to chromosomes to deep phylogeny, but some of his most lasting insights came in the study of polyploidy. Here, we review the immense impact of his work on polyploidy over more than 60 years, from his entrance into this fledgling field in the 1920s until the end of his career. Stebbins and his contemporaries developed a model of polyploid evolution that persisted for nearly half a century. As new perspectives emerged in the 1980s and new genetic tools for addressing key aspects of polyploidy have become available, a new paradigm of polyploidy has replaced much of the Stebbinsian framework. We review that paradigm shift and emphasize those areas in which the ideas of Stebbins continue to propel the field forward, as well as those areas in which the field was held back; we also note new directions that plant geneticists and evolutionists are now exploring in polyploidy research. Perhaps the most important conclusion from recent and ongoing studies of polyploidy is that, following Levin and others, polyploidy may propel a population into a new adaptive sphere given the myriad changes that accompany genome doubling.
400 citations
Cites background from "Homoeolog expression bias and expre..."
...Moreover, the underlying mechanisms responsible for biased gene expression require further investigation (see Yoo et al., 2013 ; M.-J. Yoo et al., Florida Museum of Natural History, unpublished manuscript)....
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...Such expression-level dominance has also been reported in polyploids in Gossypium and Arabidopsis ( Wang et al., 2006b ; Chang et al., 2010 ; Flagel and Wendel, 2010 ; Yoo et al., 2013 ), among others ....
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TL;DR: For advancing the field of polyploid population genetics, most priority should be given to development of new molecular approaches that allow efficient dosage determination, and to further development of analytical approaches to circumvent dosage uncertainty and to accommodate ‘flexible’ modes of inheritance.
Abstract: Despite the importance of polyploidy and the increasing availability of new genomic data, there remain important gaps in our knowledge of polyploid population genetics. These gaps arise from the complex nature of polyploid data (e.g. multiple alleles and loci, mixed inheritance patterns, association between ploidy and mating system variation). Furthermore, many of the standard tools for population genetics that have been developed for diploids are often not feasible for polyploids. This review aims to provide an overview of the state-of-the-art in polyploid population genetics and to identify the main areas where further development of molecular techniques and statistical theory is required. We review commonly used molecular tools (amplified fragment length polymorphism, microsatellites, Sanger sequencing, next-generation sequencing and derived technologies) and their challenges associated with their use in polyploid populations: that is, allele dosage determination, null alleles, difficulty of distinguishing orthologues from paralogues and copy number variation. In addition, we review the approaches that have been used for population genetic analysis in polyploids and their specific problems. These problems are in most cases directly associated with dosage uncertainty and the problem of inferring allele frequencies and assumptions regarding inheritance. This leads us to conclude that for advancing the field of polyploid population genetics, most priority should be given to development of new molecular approaches that allow efficient dosage determination, and to further development of analytical approaches to circumvent dosage uncertainty and to accommodate ‘flexible’ modes of inheritance. In addition, there is a need for more simulation-based studies that test what kinds of biases could result from both existing and novel approaches.
300 citations
Cites methods from "Homoeolog expression bias and expre..."
...For example, following up on microarray-based experiments (Flagel et al. 2008; Flagel & Wendel 2010; Salmon et al. 2010), Yoo et al. (2013) used Illumina technology to sequence the transcriptomes of wild and cultivated cotton to distinguish between expression changes due to biases in which parental…...
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References
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...E-mail: jfw@iastate.edu Received 30 May 2012; revised 3 September 2012; accepted 1 October 2012; published online 21 November 2012 Heredity (2013) 110, 171–180 & 2013 Macmillan Publishers Limited All rights reserved 0018-067X/13 www.nature.com/hdy expression level dominance have not been explored....
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TL;DR: SAMtools as discussed by the authors implements various utilities for post-processing alignments in the SAM format, such as indexing, variant caller and alignment viewer, and thus provides universal tools for processing read alignments.
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45,957 citations
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Availability: http://maq.sourceforge.net
Contact: [email protected]
43,862 citations
"Homoeolog expression bias and expre..." refers background or methods in this paper
...Here, we use the terms ‘homoeolog expression bias’ and ‘expression level dominance’ for expression patterns observed within individual homoeologous genes, and for overall expression of both homoeologs, respectively....
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...After trimming the indexed sequences, fastq formatted reads from each library were mapped to the reference genome using Burrows Wheeler Alignment (Li and Durbin, 2009)....
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...Specifically, the total expression level of a homoeolog pair in an allopolyploid may be similar to that exhibited by only one of the two diploid parents, irrespective of whether that parent displays upor downregulation with respect to the other parent....
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29,413 citations
"Homoeolog expression bias and expre..." refers background or methods in this paper
...E-mail: jfw@iastate.edu Received 30 May 2012; revised 3 September 2012; accepted 1 October 2012; published online 21 November 2012 Heredity (2013) 110, 171–180 & 2013 Macmillan Publishers Limited All rights reserved 0018-067X/13 www.nature.com/hdy expression level dominance have not been explored....
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...…were normalized by the TMM (trimmed mean of M values) method, and then using overall expression level of both homoeologs for a gene, differential expression was assessed in the F1 hybrid and allopolyploids relative to their diploid parents using Fisher’s exact tests (Robinson et al., 2010)....
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TL;DR: From the kinetic data, it becomes evident that the reductive amination reaction is highly adaptive to the ammonium environment.
14,480 citations
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