Genetic analysis of sunflower domestication

Quantitative trait loci (QTL) controlling phenotypic differences between cultivated sunflower and its wild progenitor were investigated in an F(3) mapping population. Composite interval mapping revealed the presence of 78 QTL affecting the 18 quantitative traits of interest, with 2-10 QTL per trait. Each QTL explained 3.0-68.0% of the phenotypic variance, although only 4 (corresponding to 3 of 18 traits) had effects >25%. Overall, 51 of the 78 QTL produced phenotypic effects in the expected direction, and for 13 of 18 traits the majority of QTL had the expected effect. Despite being distributed across 15 of the 17 linkage groups, there was a substantial amount of clustering among QTL controlling different traits. In several cases, regions influencing multiple traits harbored QTL with antagonistic effects, producing a cultivar-like phenotype for some traits and a wild-like phenotype for others. On the basis of the directionality of QTL, strong directional selection for increased achene size appears to have played a central role in sunflower domestication. None of the other traits show similar evidence of selection. The occurrence of numerous wild alleles with cultivar-like effects, combined with the lack of major QTL, suggests that sunflower was readily domesticated.     

Genetic consequences of selection during the evolution of cultivated sunflower

We mapped quantitative trait loci (QTL) controlling differences in seed oil content and composition between cultivated and wild sunflower and used the results, along with those of a previous study of domestication-related QTL, to guide a genome-wide analysis of genetic variation for evidence of past selection. The effects of the seed oil QTL were almost exclusively in the expected direction with respect to the parental phenotypes. A major, oil-related QTL cluster mapped near a cluster of domestication-related QTL on linkage group six (LG06), the majority of which have previously been shown to have effects that are inconsistent with the parental phenotypes. To test the hypothesis that this region was the target of a past selective sweep, perhaps resulting in the fixation of the antagonistic domestication-related QTL, we analyzed simple sequence repeat (SSR) diversity from 102 markers dispersed throughout the sunflower genome. Our results indicate that LG06 was most likely the target of multiple selective sweeps during the postdomestication era. Strong directional selection in concert with genetic hitchhiking therefore offers a possible explanation for the occurrence of numerous domestication-related QTL with apparently maladaptive phenotypic effects.     

Quantitative trait loci analysis of melon (<Emphasis Type="Italic">Cucumis melo</Emphasis> L.) domestication-related traits

Key message

Loci on LGIV, VI, and VIII of melon genome are involved in the control of fruit domestication-related traits and they are candidate to have played a role in the domestication of the crop.

Abstract

The fruit of wild melons is very small (20–50 g) without edible pulp, contrasting with the large size and high pulp content of cultivated melon fruits. An analysis of quantitative trait loci (QTL) controlling fruit morphology domestication-related traits was carried out using an in vitro maintained F₂ population from the cross between the Indian wild melon “Trigonus” and the western elite cultivar ‘Piel de Sapo’. Twenty-seven QTL were identified in at least two out of the three field trials. Six of them were also being detected in BC1 and BC3 populations derived from the same cross. Ten of them were related to fruit morphological traits, 12 to fruit size characters, and 5 to pulp content. The Trigonus alleles decreased the value of the characters, except for the QTL at andromonoecious gene at linkage group (LG) II, and the QTL for pulp content at LGV. QTL genotypes accounted for a considerable degree of the total phenotypic variation, reaching up to 46%. Around 66% of the QTL showed additive gene action, 19% exhibited dominance, and 25% consisted of overdominance. The regions on LGIV, VI, and VIII included the QTL with more consistent and strong effects on domestication-related traits. QTLs on those regions were validated in BC2S1, BC2S2, and BC3 families, with “Trigonus” allele decreasing the fruit morphological traits in all cases. The validated QTL could represent loci involved in melon domestication, although further experiments as genomic variation studies across wild and cultivated genotypes would be necessary to confirm this hypothesis.

     

Conservation of gene function in the solanaceae as revealed by comparative mapping of domestication traits in eggplant

Quantitative trait loci (QTL) for domestication-related traits were identified in an interspecific F(2) population of eggplant (Solanum linnaeanum x S. melongena). Although 62 quantitative trait loci (QTL) were identified in two locations, most of the dramatic phenotypic differences in fruit weight, shape, color, and plant prickliness that distinguish cultivated eggplant from its wild relative could be attributed to six loci with major effects. Comparison of the genomic locations of the eggplant fruit weight, fruit shape, and color QTL with the positions of similar loci in tomato, potato, and pepper revealed that 40% of the different loci have putative orthologous counterparts in at least one of these other crop species. Overall, the results suggest that domestication of the Solanaceae has been driven by mutations in a very limited number of target loci with major phenotypic effects, that selection pressures were exerted on the same loci despite the crops' independent domestications on different continents, and that the morphological diversity of these four crops can be explained by divergent mutations at these loci.     

Contributions of flowering time genes to sunflower domestication and improvement

Determining the identity and distribution of molecular changes leading to the evolution of modern crop species provides major insights into the timing and nature of historical forces involved in rapid phenotypic evolution. In this study, we employed an integrated candidate gene strategy to identify loci involved in the evolution of flowering time during early domestication and modern improvement of the sunflower (Helianthus annuus). Sunflower homologs of many genes with known functions in flowering time were isolated and cataloged. Then, colocalization with previously mapped quantitative trait loci (QTLs), expression, or protein sequence differences between wild and domesticated sunflower, and molecular evolutionary signatures of selective sweeps were applied as step-wise criteria for narrowing down an original pool of 30 candidates. This process led to the discovery that five paralogs in the flowering locus T/terminal flower 1 gene family experienced selective sweeps during the evolution of cultivated sunflower and may be the causal loci underlying flowering time QTLs. Our findings suggest that gene duplication fosters evolutionary innovation and that natural variation in both coding and regulatory sequences of these paralogs responded to a complex history of artificial selection on flowering time during the evolution of cultivated sunflower.     

Genome‐wide analysis of allele frequency change in sunflower crop–wild hybrid populations evolving under natural conditions

Crop‐wild hybridization occurs in numerous plant species and could alter the genetic structure and evolutionary dynamics of wild populations. Studying crop‐derived alleles in wild populations is also relevant to assessing/mitigating the risks associated with transgene escape. To date, crop‐wild hybridization has generally been examined via short‐term studies, typically within a single generation, focusing on few traits or genetic markers. Little is known about patterns of selection on crop‐derived alleles over multiple generations, particularly at a genome‐wide scale. Here, we documented patterns of natural selection in an experimental crop × wild sunflower population that was allowed to evolve under natural conditions for two generations at two locations. Allele frequencies at a genome‐wide collection of SNPs were tracked across generations, and a common garden experiment was conducted to compare trait means between generations. These data allowed us to identify instances of selection on crop‐derived alleles/traits and, in concert with QTL mapping results, test for congruence between our genotypic and phenotypic results. We found that natural selection overwhelmingly favours wild alleles and phenotypes. However, crop alleles in certain genomic regions can be favoured, and these changes often occurred in parallel across locations. We did not, however, consistently observe close agreement between our genotypic and phenotypic results. For example, when a trait evolved towards the wild phenotype, wild QTL alleles associated with that trait did not consistently increase in frequency. We discuss these results in the context of crop allele introgression into wild populations and implications for the management of GM crops.     

Selection on Crop-Derived Traits and QTL in Sunflower (Helianthus annuus) Crop-Wild Hybrids under Water Stress

Locally relevant conditions, such as water stress in irrigated agricultural regions, should be considered when assessing the risk of crop allele introgression into wild populations following hybridization. Although research in cultivars has suggested that domestication traits may reduce fecundity under water stress as compared to wild-like phenotypes, this has not been investigated in crop-wild hybrids. In this study, we examine phenotypic selection acting on, as well as the genetic architecture of vegetative, reproductive, and physiological characteristics in an experimental population of sunflower crop-wild hybrids grown under wild-like low water conditions. Crop-derived petiole length and head diameter were favored in low and control water environments. The direction of selection differed between environments for leaf size and leaf pressure potential. Interestingly, the additive effect of the crop-derived allele was in the direction favored by selection for approximately half the QTL detected in the low water environment. Selection favoring crop-derived traits and alleles in the low water environment suggests that a subset of these alleles would be likely to spread into wild populations under water stress. Furthermore, differences in selection between environments support the view that risk assessments should be conducted under multiple locally relevant conditions.     

Genetic analysis of rice domestication syndrome with the wild annual species, Oryza nivara

With a small and sequenced genome, rice provides an excellent system for studying the genetics of cereal domestication. We conducted a quantitative trait locus (QTL) analysis of key domestication traits using an F2 population derived from a cross between the cultivated rice, Oryza sativa, and the annual wild species, O. nivara. We found that the QTL of large phenotypic effects were targeted by domestication selection for effective harvest and planting, including a reduction in seed shattering and seed dormancy and the synchronization of seed maturation. Selection for higher yield was probably responsible for the fixation of mutations at a cluster of QTL on chromosome 7 and a few other chromosomal locations that could have substantially improved plant architecture and panicle structure, resulting in fewer erect tillers and longer and more highly branched panicles in cultivated rice. In comparison with the wild perennial species, O. rufipogon, rice domestication from O. nivara would have involved QTL with a greater degree of chromosomal co-localization and required little genetic change associated with life history or mating system transitions. The genetic analyses of domestication traits with both wild relatives will open opportunities for the improvement of rice cultivars utilizing natural germplasm.     

A Genomic Scan for Selection Reveals Candidates for Genes Involved in the Evolution of Cultivated Sunflower (Helianthus annuus)

Genomic scans for selection are a useful tool for identifying genes underlying phenotypic transitions. In this article, we describe the results of a genome scan designed to identify candidates for genes targeted by selection during the evolution of cultivated sunflower. This work involved screening 492 loci derived from ESTs on a large panel of wild, primitive (i.e., landrace), and improved sunflower (Helianthus annuus) lines. This sampling strategy allowed us to identify candidates for selectively important genes and investigate the likely timing of selection. Thirty-six genes showed evidence of selection during either domestication or improvement based on multiple criteria, and a sequence-based test of selection on a subset of these loci confirmed this result. In view of what is known about the structure of linkage disequilibrium across the sunflower genome, these genes are themselves likely to have been targeted by selection, rather than being merely linked to the actual targets. While the selection candidates showed a broad range of putative functions, they were enriched for genes involved in amino acid synthesis and protein catabolism. Given that a similar pattern has been detected in maize (Zea mays), this finding suggests that selection on amino acid composition may be a general feature of the evolution of crop plants. In terms of genomic locations, the selection candidates were significantly clustered near quantitative trait loci (QTL) that contribute to phenotypic differences between wild and cultivated sunflower, and specific instances of QTL colocalization provide some clues as to the roles that these genes may have played during sunflower evolution.     

Detection of epistatic interactions between exotic alleles introgressed from wild barley (H. vulgare ssp. spontaneum)

The expression of a quantitative phenotype can be controlled through genotype, environment and genotype by environment interaction effects. Further, genotype effects can be attributed to major genes, quantitative trait loci (QTL) and gene by gene interactions, which are also termed epistatic interactions. The present study demonstrates that two-way epistatic interactions can play an important role for the expression of domestication-related traits like heading date, plant height and yield. In the BC₂DH population S42, carrying wild barley introgressions in the genetic background of the spring barley cultivar Scarlett, 13, 8 and 12 marker by marker interaction effects could be detected for the traits heading date, plant height and yield, respectively. Significant allelic combinations at interacting loci coincided for heading date, plant height and yield suggesting the presence of pleiotropic effects rather than several linked QTL. The mode of epistasis observed was primarily characterised by either (1) compensatory effects, where allelic combinations from the same genotype buffered the phenotype, or (2) augmented effects, where only the combination of the exotic allele at both interacting loci caused an altered phenotype. The present study shows that estimates of main effects of QTL can be confounded by interactions with background loci, suggesting that the identification of epistatic effects is important for gene cloning and marker-assisted selection. Furthermore, interaction effects between loci and putative candidate genes detected in the present study reveal potential functional relationships, which can be used to further elucidate gene networks in barley.     

The genetics of domestication of rice bean, Vigna umbellata

Background and Aims

The Asian genus Vigna, to which four cultivated species (rice bean, azuki bean, mung bean and black gram) belong, is suitable for comparative genomics. The aims were to construct a genetic linkage map of rice bean, to identify the genomic regions associated with domestication in rice bean, and to compare these regions with those in azuki bean.

Methods

A genetic linkage map was constructed by using simple sequence repeat and amplified fragment length polymorphism markers in the BC₁F₁ population derived from a cross between cultivated and wild rice bean. Using this map, 31 domestication-related traits were dissected into quantitative trait loci (QTLs). The genetic linkage map and QTLs of rice bean were compared with those of azuki bean.

Key Results

A total of 326 markers converged into 11 linkage groups (LGs), corresponding to the haploid number of rice bean chromosomes. The domestication-related traits in rice bean associated with a few major QTLs distributed as clusters on LGs 2, 4 and 7. A high level of co-linearity in marker order between the rice bean and azuki bean linkage maps was observed. Major QTLs in rice bean were found on LG4, whereas major QTLs in azuki bean were found on LG9.

Conclusions

This is the first report of a genetic linkage map and QTLs for domestication-related traits in rice bean. The inheritance of domestication-related traits was so simple that a few major QTLs explained the phenotypic variation between cultivated and wild rice bean. The high level of genomic synteny between rice bean and azuki bean facilitates QTL comparison between species. These results provide a genetic foundation for improvement of rice bean; interchange of major QTLs between rice bean and azuki bean might be useful for broadening the genetic variation of both species.     

Selection on domestication traits and quantitative trait loci in crop-wild sunflower hybrids

The strength and extent of gene flow from crops into wild populations depends, in part, on the fitness of the crop alleles, as well as that of alleles at linked loci. Interest in crop-wild gene flow has increased with the advent of transgenic plants, but nontransgenic crop-wild hybrids can provide case studies to understand the factors influencing introgression, provided that the genetic architecture and the fitness effects of loci are known. This study used recombinant inbred lines (RILs) generated from a cross between crop and wild sunflowers to assess selection on domestication traits and quantitative trait loci (QTL) in two contrasting environments, in Indiana and Nebraska, USA. Only a small fraction of plants (9%) produced seed in Nebraska, due to adverse weather conditions, while the majority of plants (79%) in Indiana reproduced. Phenotypic selection analysis found that a mixture of crop and wild traits were favoured in Indiana (i.e. had significant selection gradients), including larger leaves, increased floral longevity, larger disk diameter, reduced ray flower size and smaller achene (seed) mass. Selection favouring early flowering was detected in Nebraska. QTLs for fitness were found at the end of linkage groups six (LG6) and nine (LG9) in both field sites, each explaining 11-12% of the total variation. Crop alleles were favoured on LG9, but wild alleles were favoured on LG6. QTLs for numerous domestication traits overlapped with the fitness QTLs, including flowering date, achene mass, head number, and disk diameter. It remains to be seen if these QTL clusters are the product of multiple linked genes, or individual genes with pleiotropic effects. These results indicate that crop trait values and alleles may sometimes be favoured in a noncrop environment and across broad geographical regions.     

Largely unlinked gene sets targeted by selection for domestication syndrome phenotypes in maize and sorghum

The domestication of diverse grain crops from wild grasses was a result of artificial selection for a suite of overlapping traits producing changes referred to in aggregate as ‘domestication syndrome’. Parallel phenotypic change can be accomplished by either selection on orthologous genes or selection on non‐orthologous genes with parallel phenotypic effects. To determine how often artificial selection for domestication traits in the grasses targeted orthologous genes, we employed resequencing data from wild and domesticated accessions of Zea (maize) and Sorghum (sorghum). Many ‘classic’ domestication genes identified through quantitative trait locus mapping in populations resulting from wild/domesticated crosses indeed show signatures of parallel selection in both maize and sorghum. However, the overall number of genes showing signatures of parallel selection in both species is not significantly different from that expected by chance. This suggests that while a small number of genes will extremely large phenotypic effects have been targeted repeatedly by artificial selection during domestication, the optimization part of domestication targeted small and largely non‐overlapping subsets of all possible genes which could produce equivalent phenotypic alterations.     

Pleiotropy of the branching locus (B) masks linked and unlinked quantitative trait loci affecting seed traits in sunflower

The discovery of unbranched, monocephalic natural variants was pivotal for the domestication of sunflower (Helianthus annuus L.). The branching locus (B), one of several loci apparently targeted by aboriginal selection for monocephaly, pleiotropically affects plant, seed and capitula morphology and, when segregating, confounds the discovery of favorable alleles for seed yield and other traits. The present study was undertaken to gain deeper insights into the genetics of branching and seed traits affected by branching. We produced an unbranched hybrid testcross recombinant inbred line (TC-RIL) population by crossing branched (bb) and unbranched (BB) RILs to an unbranched (BB) tester. The elimination of branching concomitantly eliminated a cluster of B-linked seed trait quantitative trait loci (QTL) identified by RIL per se testing. We identified a seed oil content QTL linked in repulsion and a 100-seed weight QTL linked in coupling to the B locus and additional unlinked QTL, previously masked by B-locus pleiotropy. Genomic segments flanking the B locus harbor multiple loci for domestication and post-domestication traits, the effects of which are masked by B-locus pleiotropy in populations segregating for branching and can only be disentangled by genetic analyses in unbranched populations. QTL analyses of NILs carrying wild B alleles substantiated the pleiotropic effects of the B locus. The effect of the B locus on branching was masked by the effects of wild alleles at independent branching loci in hybrids between monocephalic domesticated lines and polycephalic wild ecotypes; hence, the B locus appears to be necessary, but not sufficient, for monocephaly in domesticated sunflower.     

Classic Selective Sweeps Revealed by Massive Sequencing in Cattle

Human driven selection during domestication and subsequent breed formation has likely left detectable signatures within the genome of modern cattle. The elucidation of these signatures of selection is of interest from the perspective of evolutionary biology, and for identifying domestication-related genes that ultimately may help to further genetically improve this economically important animal. To this end, we employed a panel of more than 15 million autosomal SNPs identified from re-sequencing of 43 Fleckvieh animals. We mainly applied two somewhat complementary statistics, the integrated Haplotype Homozygosity Score (iHS) reflecting primarily ongoing selection, and the Composite of Likelihood Ratio (CLR) having the most power to detect completed selection after fixation of the advantageous allele. We find 106 candidate selection regions, many of which are harboring genes related to phenotypes relevant in domestication, such as coat coloring pattern, neurobehavioral functioning and sensory perception including KIT, MITF, MC1R, NRG4, Erbb4, TMEM132D and TAS2R16, among others. To further investigate the relationship between genes with signatures of selection and genes identified in QTL mapping studies, we use a sample of 3062 animals to perform four genome-wide association analyses using appearance traits, body size and somatic cell count. We show that regions associated with coat coloring significantly (P<0.0001) overlap with the candidate selection regions, suggesting that the selection signals we identify are associated with traits known to be affected by selection during domestication. Results also provide further evidence regarding the complexity of the genetics underlying coat coloring in cattle. This study illustrates the potential of population genetic approaches for identifying genomic regions affecting domestication-related phenotypes and further helps to identify specific regions targeted by selection during speciation, domestication and breed formation of cattle. We also show that Linkage Disequilibrium (LD) decays in cattle at a much faster rate than previously thought.     

Relationship between yield components and partial resistance to Lecanicillium fungicola in the button mushroom, Agaricus bisporus, assessed by quantitative trait locus mapping

Dry bubble, caused by Lecanicillium fungicola, is one of the most detrimental diseases affecting button mushroom cultivation. In a previous study, we demonstrated that breeding for resistance to this pathogen is quite challenging due to its quantitative inheritance. A second-generation hybrid progeny derived from an intervarietal cross between a wild strain and a commercial cultivar was characterized for L. fungicola resistance under artificial inoculation in three independent experiments. Analysis of quantitative trait loci (QTL) was used to determine the locations, numbers, and effects of genomic regions associated with dry-bubble resistance. Four traits related to resistance were analyzed. Two to four QTL were detected per trait, depending on the experiment. Two genomic regions, on linkage group X (LGX) and LGVIII, were consistently detected in the three experiments. The genomic region on LGX was detected for three of the four variables studied. The total phenotypic variance accounted for by all QTL ranged from 19.3% to 42.1% over all traits in all experiments. For most of the QTL, the favorable allele for resistance came from the wild parent, but for some QTL, the allele that contributed to a higher level of resistance was carried by the cultivar. Comparative mapping with QTL for yield-related traits revealed five colocations between resistance and yield component loci, suggesting that the resistance results from both genetic factors and fitness expression. The consequences for mushroom breeding programs are discussed.     

Evidence of selection on fatty acid biosynthetic genes during the evolution of cultivated sunflower

The identification of genes underlying the phenotypic transitions that took place during crop evolution, as well as the genomic extent of resultant selective sweeps, is of great interest to both evolutionary biologists and applied plant scientists. In this study, we report the results of a molecular evolutionary analysis of 11 genes that underlie fatty acid biosynthesis and metabolism in wild and cultivated sunflower (Helianthus annuus). Seven of these 11 genes showed evidence of selection at the nucleotide level, with 1 (FAD7) having experienced selection prior to domestication, 2 (FAD2-3 and FAD3) having experienced selection during domestication, and 4 (FAB1, FAD2-1, FAD6, and FATB) having experienced selection during the subsequent period of improvement. Sequencing of a subset of these genes from an extended panel of sunflower cultivars revealed little additional variation, and an analysis of the genomic region surrounding one of these genes (FAD2-1) revealed the occurrence of an extensive selective sweep affecting a region spanning at least ca. 100 kb. Given that previous population genetic analyses have revealed a relatively rapid decay of linkage disequilibrium in sunflower, this finding indicates the occurrence of strong selection and a rapid sweep.