scholarly journals Pooled Single-Molecule transcriptomics identifies a giant gene under balancing selection in sunflower

2021 ◽  
Author(s):  
Hélène Badouin ◽  
Marie-Claude Boniface ◽  
Nicolas Pouilly ◽  
Anne-Laure Fuchs ◽  
Felicity Vear ◽  
...  
Keyword(s):  
Single Molecule ◽  
Genome Duplication ◽  
Balancing Selection ◽  
Self Incompatibility ◽  
Balanced Polymorphism ◽  
Negative Frequency Dependent Selection ◽  
Suppressed Recombination ◽  
Trait Locus ◽  
Special Case ◽  
Tandem Duplications

SummaryGenes under balancing selection control phenotypes such as immunity, color or sex, but are difficult to identify. Self-incompatibility genes are under negative frequency-dependent selection, a special case of balancing selection, with up to 30 to 50 alleles segregating per population. We developed a method based on pooled Single-Molecule transcriptomics to identify balanced polymorphisms expressed in tissues of interest. We searched for multi-allelic, non-recombining genes causing self-incompatibility in wild sunflower (Helianthus annuus). A diversity scan in pistil identified a gene,Ha7650b,that displayed balanced polymorphism and colocalized with a quantitative trait locus for self-incompatibility. Unexpectedly,Ha7650bdisplayed gigantism (400 kb), which was caused by increase in intron size as a consequence of suppressed recombination.Ha7650bemerged after a whole-genome duplication (29 millions years ago) followed by tandem duplications and neofunctionalisation.Ha7650bshows expression, genetic location, genomic neighbourhood and predicted function that provide strong evidence that it is involved in self-incompatibility. Pooled Single-Molecule transcriptomics is an affordable and powerful new method that makes it possible to identify diversity and structural outliers simultaneously. It will allow a breakthrough in the discovery of self-incompatibility genes and other expressed genes under balancing selection.

Recombination, Balancing Selection and Phylogenies in MHC and Self-Incompatibility Genes

Genetics ◽  
2001 ◽  
Vol 159 (4) ◽  
pp. 1833-1844 ◽  
Author(s):  
Mikkel H Schierup ◽  
Anders M Mikkelsen ◽  
Jotun Hein
Keyword(s):  
Major Histocompatibility Complex ◽  
Phylogenetic Tree ◽  
Balancing Selection ◽  
Nucleotide Sequences ◽  
Recombination Process ◽  
Self Incompatibility ◽  
Selection Coefficient ◽  
Histocompatibility Complex ◽  
A Site ◽  
Possible Cause

AbstractUsing a coalescent model of multiallelic balancing selection with recombination, the genealogical process as a function of recombinational distance from a site under selection is investigated. We find that the shape of the phylogenetic tree is independent of the distance to the site under selection. Only the timescale changes from the value predicted by Takahata's allelic genealogy at the site under selection, converging with increasing recombination to the timescale of the neutral coalescent. However, if nucleotide sequences are simulated over a recombining region containing a site under balancing selection, a phylogenetic tree constructed while ignoring such recombination is strongly affected. This is true even for small rates of recombination. Published studies of multiallelic balancing selection, i.e., the major histocompatibility complex (MHC) of vertebrates, gametophytic and sporophytic self-incompatibility of plants, and incompatibility of fungi, all observe allelic genealogies with unexpected shapes. We conclude that small absolute levels of recombination are compatible with these observed distortions of the shape of the allelic genealogy, suggesting a possible cause of these observations. Furthermore, we illustrate that the variance in the coalescent with recombination process makes it difficult to locate sites under selection and to estimate the selection coefficient from levels of variability.

scholarly journals Recombination and Selection at Brassica Self-Incompatibility Loci

Genetics ◽  
1999 ◽  
Vol 152 (1) ◽  
pp. 413-425 ◽  
Author(s):  
Philip Awadalla ◽  
Deborah Charlesworth
Keyword(s):  
Linkage Disequilibrium ◽  
Balancing Selection ◽  
Brassica Species ◽  
Selective Constraint ◽  
Intragenic Recombination ◽  
Self Incompatibility ◽  
History Of ◽  
Unknown Gene ◽  
Slg Gene ◽  
High Diversity

Abstract In Brassica species, self-incompatibility is controlled genetically by haplotypes involving two known genes, SLG and SRK, and possibly an as yet unknown gene controlling pollen incompatibility types. Alleles at the incompatibility loci are maintained by frequency-dependent selection, and diversity at SLG and SRK appears to be very ancient, with high diversity at silent and replacement sites, particularly in certain “hypervariable portions of the genes. It is important to test whether recombination occurs in these genes before inferences about function of different parts of the genes can be made from patterns of diversity within their sequences. In addition, it has been suggested that, to maintain the relationship between alleles within a given S-haplotype, recombination is suppressed in the S-locus region. The high diversity makes many population genetic measures of recombination inapplicable. We have analyzed linkage disequilibrium within the SLG gene of two Brassica species, using published coding sequences. The results suggest that intragenic recombination has occurred in the evolutionary history of these alleles. This is supported by patterns of synonymous nucleotide diversity within both the SLG and SRK genes, and between domains of the SRK gene. Finally, clusters of linkage disequilibrium within the SLG gene suggest that hypervariable regions are under balancing selection, and are not merely regions of relaxed selective constraint.

scholarly journals Evolutionary strata on young mating-type chromosomes despite the lack of sexual antagonism

2017 ◽  
Vol 114 (27) ◽  
pp. 7067-7072 ◽  
Author(s):  
Sara Branco ◽  
Hélène Badouin ◽  
Ricardo C. Rodríguez de la Vega ◽  
Jérôme Gouzy ◽  
Fantin Carpentier ◽  
...  
Keyword(s):  
Mating Type ◽  
Balancing Selection ◽  
Smut Fungi ◽  
Mating Types ◽  
Sexual Antagonism ◽  
Recombination Suppression ◽  
Ancestral Gene ◽  
Anther Smut ◽  
Mating Type Genes ◽  
Suppressed Recombination

Sex chromosomes can display successive steps of recombination suppression known as “evolutionary strata,” which are thought to result from the successive linkage of sexually antagonistic genes to sex-determining genes. However, there is little evidence to support this explanation. Here we investigate whether evolutionary strata can evolve without sexual antagonism using fungi that display suppressed recombination extending beyond loci determining mating compatibility despite lack of male/female roles associated with their mating types. By comparing full-length chromosome assemblies from five anther-smut fungi with or without recombination suppression in their mating-type chromosomes, we inferred the ancestral gene order and derived chromosomal arrangements in this group. This approach shed light on the chromosomal fusion underlying the linkage of mating-type loci in fungi and provided evidence for multiple clearly resolved evolutionary strata over a range of ages (0.9–2.1 million years) in mating-type chromosomes. Several evolutionary strata did not include genes involved in mating-type determination. The existence of strata devoid of mating-type genes, despite the lack of sexual antagonism, calls for a unified theory of sex-related chromosome evolution, incorporating, for example, the influence of partially linked deleterious mutations and the maintenance of neutral rearrangement polymorphism due to balancing selection on sexes and mating types.

scholarly journals Interaction Between Ploidy, Breeding System, and Lineage Diversification

2019 ◽  
Author(s):  
Rosana Zenil-Ferguson ◽  
J. Gordon Burleigh ◽  
William A. Freyman ◽  
Boris Igić ◽  
Itay Mayrose ◽  
...  
Keyword(s):  
Breeding System ◽  
Whole Genome Duplication ◽  
Genome Duplication ◽  
Whole Genome ◽  
Self Incompatibility ◽  
Evolutionary Pathway ◽  
Diversification Rates ◽  
Extinction Rates ◽  
Biological Hierarchy ◽  
Lineage Diversification

AbstractIf particular traits consistently affect rates of speciation and extinction, broad macroevolutionary patterns can be understood as consequences of selection at high levels of the biological hierarchy. Identifying traits associated with diversification rate differences is complicated by the wide variety of characters under consideration and the statistical challenges of testing for associations from comparative phylogenetic data. Ploidy (diploid vs. polyploid states) and breeding system (self-incompatible vs. self-compatible states) have been repeatedly suggested as possible drivers of differential diversification. We investigate the connections of these traits, including their interaction, to speciation and extinction rates in Solanaceae. We show that the effect of ploidy on diversification can be largely explained by its correlation with breeding system and that additional unknown factors, alongside breeding system, influence diversification rates. These results are largely robust to allowing for diploidization. Finally, we find that the most common evolutionary pathway to polyploidy in Solanaceae occurs via direct breakdown of self-incompatibility by whole genome duplication, rather than indirectly via breakdown followed by polyploidization.

scholarly journals Negative frequency dependent selection contributes to the maintenance of a global polymorphism in mitochondrial DNA

2020 ◽  
Vol 20 (1) ◽  
Author(s):  
Zorana Kurbalija Novičić ◽  
Ahmed Sayadi ◽  
Mihailo Jelić ◽  
Göran Arnqvist
Keyword(s):  
Mitochondrial Dna ◽  
Genetic Variation ◽  
Life History ◽  
Balancing Selection ◽  
Food Resource ◽  
Ecological Processes ◽  
Central Process ◽  
Frequency Dependent ◽  
Frequency Dependent Selection ◽  
Negative Frequency Dependent Selection

Abstract Background Understanding the forces that maintain diversity across a range of scales is at the very heart of biology. Frequency-dependent processes are generally recognized as the most central process for the maintenance of ecological diversity. The same is, however, not generally true for genetic diversity. Negative frequency dependent selection, where rare genotypes have an advantage, is often regarded as a relatively weak force in maintaining genetic variation in life history traits because recombination disassociates alleles across many genes. Yet, many regions of the genome show low rates of recombination and genetic variation in such regions (i.e., supergenes) may in theory be upheld by frequency dependent selection. Results We studied what is essentially a ubiquitous life history supergene (i.e., mitochondrial DNA) in the fruit fly Drosophila subobscura, showing sympatric polymorphism with two main mtDNA genotypes co-occurring in populations world-wide. Using an experimental evolution approach involving manipulations of genotype starting frequencies, we show that negative frequency dependent selection indeed acts to maintain genetic variation in this region. Moreover, the strength of selection was affected by food resource conditions. Conclusions Our work provides novel experimental support for the view that balancing selection through negative frequency dependency acts to maintain genetic variation in life history genes. We suggest that the emergence of negative frequency dependent selection on mtDNA is symptomatic of the fundamental link between ecological processes related to resource use and the maintenance of genetic variation.

scholarly journals Long-read bitter gourd (Momordica charantia) genome and the genomic architecture of nonclassic domestication

2020 ◽  
Vol 117 (25) ◽  
pp. 14543-14551 ◽  
Author(s):  
Hideo Matsumura ◽  
Min-Chien Hsiao ◽  
Ya-Ping Lin ◽  
Atsushi Toyoda ◽  
Naoki Taniai ◽  
...  
Keyword(s):  
Selective Sweep ◽  
Consumer Preferences ◽  
Balancing Selection ◽  
Female Flower ◽  
Momordica Charantia ◽  
Bitter Gourd ◽  
Plant Domestication ◽  
Trait Divergence ◽  
Balanced Polymorphism ◽  
Cultivar Groups

The genetic architecture of quantitative traits is determined by both Mendelian and polygenic factors, yet classic examples of plant domestication focused on selective sweep of newly mutated Mendelian genes. Here we report the chromosome-level genome assembly and the genomic investigation of a nonclassic domestication example, bitter gourd (Momordica charantia), an important Asian vegetable and medicinal plant of the family Cucurbitaceae. Population resequencing revealed the divergence between wild and South Asian cultivars about 6,000 y ago, followed by the separation of the Southeast Asian cultivars about 800 y ago, with the latter exhibiting more extreme trait divergence from wild progenitors and stronger signs of selection on fruit traits. Unlike some crops where the largest phenotypic changes and traces of selection happened between wild and cultivar groups, in bitter gourd large differences exist between two regional cultivar groups, likely reflecting the distinct consumer preferences in different countries. Despite breeding efforts toward increasing female flower proportion, a gynoecy locus exhibits complex patterns of balanced polymorphism among haplogroups, with potential signs of selective sweep within haplogroups likely reflecting artificial selection and introgression from cultivars back to wild accessions. Our study highlights the importance to investigate such nonclassic example of domestication showing signs of balancing selection and polygenic trait architecture in addition to classic selective sweep in Mendelian factors.

scholarly journals Genotyping and De Novo Discovery of Allelic Variants at the Brassicaceae Self-Incompatibility Locus from Short-Read Sequencing Data

2019 ◽  
Vol 37 (4) ◽  
pp. 1193-1201 ◽  
Author(s):  
Mathieu Genete ◽  
Vincent Castric ◽  
Xavier Vekemans
Keyword(s):  
De Novo ◽  
Balancing Selection ◽  
Methodological Approach ◽  
Natural Populations ◽  
Sequence Divergence ◽  
Reference Database ◽  
Self Incompatibility ◽  
Sequencing Data ◽  
Allelic Series ◽  
S Alleles

Abstract Plant self-incompatibility (SI) is a genetic system that prevents selfing and enforces outcrossing. Because of strong balancing selection, the genes encoding SI are predicted to maintain extraordinarily high levels of polymorphism, both in terms of the number of functionally distinct S-alleles that segregate in SI species and in terms of their nucleotide sequence divergence. However, because of these two combined features, documenting polymorphism of these genes also presents important methodological challenges that have so far largely prevented the comprehensive analysis of complete allelic series in natural populations, and also precluded the obtention of complete genic sequences for many S-alleles. Here, we develop a powerful methodological approach based on a computationally optimized comparison of short Illumina sequencing reads from genomic DNA to a database of known nucleotide sequences of the extracellular domain of SRK (eSRK). By examining mapping patterns along the reference sequences, we obtain highly reliable predictions of S-genotypes from individuals collected from natural populations of Arabidopsis halleri. Furthermore, using a de novo assembly approach of the filtered short reads, we obtain full-length sequences of eSRK even when the initial sequence in the database was only partial, and we discover putative new SRK alleles that were not initially present in the database. When including those new alleles in the reference database, we were able to resolve the complete diploid SI genotypes of all individuals. Beyond the specific case of Brassicaceae S-alleles, our approach can be readily applied to other polymorphic loci, given reference allelic sequences are available.

scholarly journals Explaining the heritability of an ecologically significant trait in terms of individual quantitative trait loci

2011 ◽  
Vol 7 (6) ◽  
pp. 896-898 ◽  
Author(s):  
Alison G. Scoville ◽  
Young Wha Lee ◽  
John H. Willis ◽  
John K. Kelly
Keyword(s):  
Qtl Mapping ◽  
Quantitative Trait ◽  
Complex Traits ◽  
Genetic Variance ◽  
Balancing Selection ◽  
Natural Populations ◽  
Population Based ◽  
Population Variation ◽  
Trait Locus ◽  
Genomic Regions

Most natural populations display substantial genetic variation in behaviour, morphology, physiology, life history and the susceptibility to disease. A major challenge is to determine the contributions of individual loci to variation in complex traits. Quantitative trait locus (QTL) mapping has identified genomic regions affecting ecologically significant traits of many species. In nearly all cases, however, the importance of these QTLs to population variation remains unclear. In this paper, we apply a novel experimental method to parse the genetic variance of floral traits of the annual plant Mimulus guttatus into contributions of individual QTLs. We first use QTL-mapping to identify nine loci and then conduct a population-based breeding experiment to estimate V Q , the genetic variance attributable to each QTL. We find that three QTLs with moderate effects explain up to one-third of the genetic variance in the natural population. Variation at these loci is probably maintained by some form of balancing selection. Notably, the largest effect QTLs were relatively minor in their contribution to heritability.

scholarly journals Nonself-recognition-based self-incompatibility can alternatively promote or prevent introgression

2020 ◽  
Author(s):  
Alexander Harkness ◽  
Yaniv Brandvain
Keyword(s):  
Pollen Limitation ◽  
List Type ◽  
Self Incompatibility ◽  
Core Eudicots ◽  
S Alleles ◽  
Self Fertilization ◽  
Nonself Recognition ◽  
Negative Frequency Dependent Selection ◽  
Incompatibility Alleles ◽  
S Allele

1SummaryTraditionally, we expect that self-incompatibility alleles (S-alleles), which prevent self-fertilization, should benefit from negative-frequency dependent selection and rise to high frequency when introduced to a new population through gene flow. However, the most taxonomically widespread form of self-incompatibility, the ribonuclease-based system ancestral to the core eudicots, functions through nonself-recognition, which drastically alters the process of S-allele diversification.We analyze a model of S-allele evolution in two populations connected by migration, focusing on comparisons among the fates of S-alleles originally unique to each population and those shared among populations.We find that both shared and unique S-alleles originating from the population with more unique S-alleles were usually fitter than S-alleles from the population with fewer. Resident S-alleles were often driven extinct and replaced by migrant S-alleles, though this outcome could be averted by pollen limitation or biased migration.Nonself-recognition-based self-incompatibility will usually either disfavor introgression of S-alleles or result in the whole-sale replacement of S-alleles from one population with those from another.

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