Sequencing of the genus Arabidopsis identifies a complex history of nonbifurcating speciation and abundant trans-specific polymorphism

Novikova, Polina Yu.; Hohmann, Nora; Nizhynska, Viktoria; Tsuchimatsu, Takashi; Ali, Jamshaid; Muir, G. W.; Guggisberg, Alessia; Paape, Tim; Schmid, Karl; Федоренко, О. М.; Holm, Svante; Säll, Torbjörn; Schlötterer, Christian; Marhold, Karol; Widmer, Alex; Sese, Jun; Shimizu, Kentaro; Weigel, Detlef; Krämer, Ute; Koch, Marcus A.; Nordborg, Magnus

doi:10.1038/ng.3617

Cited by 193 publications

(251 citation statements)

References 72 publications

(45 reference statements)

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“…We sampled individuals from 3-5 populations of each "type": A2x refers to diploid A. arenosa, A4x to tetraploid A. arenosa, L2x to diploid A. lyrata and L4x to tetraploid A. lyrata. Tetraploid populations occurring in a hybrid zone between the two species (Schmickl, 2009;Schmickl and Koch, 2011;Hohmann et al, 2014;Muir et al, 2015;Novikova et al, 2016) were included to test for patterns of introgression. Diploids have not been found to hybridize (Jørgensen et al, 2011) and so were considered "pure" populations.…”

Section: Sampling and Overview Of Methodsmentioning

confidence: 99%

“…We used a combination of approaches to address the main research questions: (1) 454 pyrosequencing using degenerate primers (Supplementary Table 1) targeting the SRK gene family (Jørgensen et al, 2012) to characterize diversity and patterns of allele sharing in diploids and polyploids; (2) direct Sanger sequencing to investigate signatures of introgression in shared haplotypes and for segregation analyses to test linkage to the SI phenotype; (3) cloning and Sanger sequencing using degenerate primers (Supplementary Table 1) to obtain longer products than possible with 454 pyrosequencing to further characterize potentially new alleles; and (4) using data from a recent genomic resequencing study (Novikova et al, 2016) to search for the SRK gene family using novel assembly approaches, to test whether copy number variation and patterns of introgression can be mined using existing genomic data. We focused on variation in exon 1 (the S-domain) because it contains the sites used for recognition of self vs. non-self (Schierup et al, 2001;Charlesworth et al, 2003a).…”

Section: Sampling and Overview Of Methodsmentioning

confidence: 99%

“…Several known paralogs (Aly8, Aly9, Aly13-2/13-7) were expected to amplify with the primer set used. Polymorphic regions like the S-locus are known to be difficult to assemble in genome resequencing studies due to divergence from the reference genome (Mable et al, 2017) but we tested whether de novo assemblies from a genome resequencing study (Novikova et al, 2016) could be used to assess copy number of the SRK-related kinase gene family. We also attempted to pull out full-length sequences that spanned the S-domain (exon 1), transmembrane (exon 2) and kinase domains (exons 3-7) (Charlesworth et al, 2003a).…”

Section: Mining Srk Alleles From Genome Resequencing Datamentioning

confidence: 99%

“…The purpose of this paper is to discuss these issues in the context of understanding the evolutionary dynamics of the SRK gene family in a species complex (A. lyrata and A. arenosa) that includes both diploids and tetraploids, with tetraploids showing extensive introgression in a hybrid zone in central Europe (Schmickl et al, 2010;Jørgensen et al, 2011;Schmickl and Koch, 2011;Hohmann et al, 2014;Muir et al, 2015;Novikova et al, 2016;Hohmann and Koch, 2017). In A. arenosa, tetraploids have been predicted to have arisen through autopolyploidisation (Arnold et al, 2015); secondary contact with A. lyrata during interglacial and postglacial range contractions and expansions has subsequently led to introgression between tetraploids in the two species.…”

Section: Introduction Background and Aimsmentioning

confidence: 99%

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Adding Complexity to Complexity: Gene Family Evolution in Polyploids

et al. 2018

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Comparative genomics of non-model organisms has resurrected whole genome duplication (WGD) from being viewed as a somewhat obscure process that happens in plants to a primary driver of eukaryotic diversification. The shadow of past ploidy increases has left a strong signature of duplicated genes organized into gene families, even in small genomes that have undergone effectively complete rediploidization. Nevertheless, despite continually advancing technologies and bioinformatics pipelines, resolving the fate of duplicate genes remains a substantial challenge. For example, many important recognition processes are driven not only by allelic expansion through retention of duplicates but also by diversification and copy number variation. This creates technical difficulties with assembly to reference genomes and accurate interpretation of homology. Thus, relatively little is known about the impacts of recent polyploidization and hybridization on the evolution of gene families under selective forces that maintain diversity, such as balancing selection. Here we use a complex of species and ploidy levels in the genus Arabidopsis (A. lyrata and A. arenosa) as a model to investigate the evolutionary dynamics of a large and complicated gene family known to be under strong balancing selection: the receptor-like kinases, which include the female component of genetically controlled self-incompatibility. Specifically, we question: (1) How does diversity of S-receptor kinase (SRK) alleles in tetraploids compare to that in their close diploid relatives? (2) Is there increased trans-specific polymorphism (i.e., sharing of alleles that transcend speciation, characteristic of balancing selection) in tetraploids compared to diploids due to the higher number of copies they carry? (3) Do these highly variable loci show evidence of introgression among extant species/ploidy levels within or outside known zones of hybridization? (4) Is there evidence for copy number variation among paralogs? We use this example to highlight specific issues to consider when interpreting gene family evolution, particularly in relation to polyploids but also more generally in diploids. We conclude with recommendations for strategies to address the challenges of resolving such complex loci in the future, using advances in deep sequencing approaches.

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Section: Sampling and Overview Of Methodsmentioning

confidence: 99%

Section: Sampling and Overview Of Methodsmentioning

confidence: 99%

Section: Mining Srk Alleles From Genome Resequencing Datamentioning

confidence: 99%

Section: Introduction Background and Aimsmentioning

confidence: 99%

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Adding Complexity to Complexity: Gene Family Evolution in Polyploids

et al. 2018

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“…On the other hand, microevolutionary approaches based on the analytical tools of population genetics have proven to be highly useful for understanding the actual mechanisms acting during population divergence and speciation 'in real time', as exemplified by rapid recent progress in the field of speciation genomics (Smadja & Butlin 2011;The Marie Curie SPECIATION network 2012;Feder et al 2012;Nosil 2012;Seehausen et al 2014). Only recently, connecting these two conceptual worlds within one single convincing study or research programme has come truly within reach for many groups of taxa, thanks mainly to the availability of high-throughput genomic technologies and analytical tools for analysing these novel types of data across the relevant taxonomic, spatial, temporal and hierarchical/organismal scales (The Heliconius Genome Consortium 2012; Brawand et al 2014;Cornetti et al 2015;Lamichhaney et al 2015;Nicholls et al 2015;Charlesworth & Charlesworth 2016;Novikova et al 2016).…”

Section: Introductionmentioning

confidence: 99%

Molecular ecology studies of species radiations: current research gaps, opportunities and challenges

et al. 2017

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Understanding the drivers and limits of species radiations is a crucial goal of evolutionary genetics and molecular ecology, yet research on this topic has been hampered by the notorious difficulty of connecting micro-and macroevolutionary approaches to studying the drivers of diversification. To chart the current research gaps, opportunities and challenges of molecular ecology approaches to studying radiations, we examine the literature in the journal MOLECULAR ECOLOGY and revisit recent high-profile examples of evolutionary genomic research on radiations. We find that available studies of radiations are highly unevenly distributed among taxa, with many ecologically important and species-rich organismal groups remaining severely understudied, including arthropods, plants and fungi. Most studies employed molecular methods suitable over either short or long evolutionary time scales, such as microsatellites or restriction site-associated DNA sequencing (RAD-seq) in the former case and conventional amplicon sequencing of organellar DNA in the latter. The potential of molecular ecology studies to address and resolve patterns and processes around the species level in radiating groups of taxa is currently limited primarily by sample size and a dearth of information on radiating nuclear genomes as opposed to organellar ones. Based on our literature survey and personal experience, we suggest possible ways forward in the coming years. We touch on the potential and current limitations of whole-genome sequencing (WGS) in studies of radiations. We suggest that WGS and targeted ('capture') resequencing emerge as the methods of choice for scaling up the sampling of populations, species and genomes, including currently understudied organismal groups and the genes or regulatory elements expected to matter most to species radiations.

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Patterns of polymorphism, recombination, and selection in Medicago truncatula

Paape

2019

The Model Legume Medicago Truncatula

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Sequencing of the genus Arabidopsis identifies a complex history of nonbifurcating speciation and abundant trans-specific polymorphism

Cited by 193 publications

References 72 publications

Adding Complexity to Complexity: Gene Family Evolution in Polyploids

Adding Complexity to Complexity: Gene Family Evolution in Polyploids

Molecular ecology studies of species radiations: current research gaps, opportunities and challenges

Patterns of polymorphism, recombination, and selection in Medicago truncatula

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