Domestication Genes Research Articles

AFLP analysis of genetic diversity in five accessions of Polish runner bean (Phaseolus coccineus L.)

Runner bean (Phaseolus coccineus L.) is traditionally cultivated in Poland for dry seeds. The national collection of runner bean maintained in the National Center for Plant Genetic Resources gathers 152 accessions, which are mainly landraces originated in Poland (68%), Ukraine (17%) and Slovakia (10%). The collection contains valuable genetic resources for bean breeders and research. The aim of this study was to describe the level and structure of genetic diversity of three landraces and two commercial cultivars of runner bean from the national collection in order to assess their genetic potential for breeding. Amplified Fragment Length Polymorphism analysis included five combinations of selective primers. Analysis of seven genetic diversity parameters reveled fair amount of genetic variation both in landraces and cultivars. High genetic diversity of commercial cultivars relative those of landraces suggests that the breeding process leading to their release was rather moderate and most likely included domestic gene pool of runner bean. Low gene diversity and low Nei’s genetic distance values as well as intergradations among accessions in the PCoA may indicate reduced variability P. coccineus grown in Poland as a result of its migration pathways.

Heritable genome-wide variation of gene expression and promoter methylation between wild and domesticated chickens

BackgroundVariations in gene expression, mediated by epigenetic mechanisms, may cause broad phenotypic effects in animals. However, it has been debated to what extent expression variation and epigenetic modifications, such as patterns of DNA methylation, are transferred across generations, and therefore it is uncertain what role epigenetic variation may play in adaptation.ResultsIn Red Junglefowl, ancestor of domestic chickens, gene expression and methylation profiles in thalamus/hypothalamus differed substantially from that of a domesticated egg laying breed. Expression as well as methylation differences were largely maintained in the offspring, demonstrating reliable inheritance of epigenetic variation. Some of the inherited methylation differences were tissue-specific, and the differential methylation at specific loci were little changed after eight generations of intercrossing between Red Junglefowl and domesticated laying hens. There was an over-representation of differentially expressed and methylated genes in selective sweep regions associated with chicken domestication.ConclusionsOur results show that epigenetic variation is inherited in chickens, and we suggest that selection of favourable epigenomes, either by selection of genotypes affecting epigenetic states, or by selection of methylation states which are inherited independently of sequence differences, may have been an important aspect of chicken domestication.

The role of genes domesticated from LTR retrotransposons and retroviruses in mammals

The acquisition of multiple genes from long terminal repeat (LTR) retrotransposons occurred in mammals. Genes belonging to a sushi-ichi-related retrotransposon homologs (SIRH) family emerged around the time of the establishment of two viviparous mammalian groups, marsupials and eutherians. These genes encode proteins that are homologous to a retrotransposon Gag capsid protein and sometimes also have a Pol-like region. We previously demonstrated that PEG10 (SIRH1) and PEG11/RTL1 (SIRH2) play essential but different roles in placental development. PEG10 is conserved in both the marsupials and the eutherians, while PEG11/RTL1 is a eutherian-specific gene, suggesting that these two domesticated genes were deeply involved in the evolution of mammals via the establishment of the viviparous reproduction system. In this review, we introduce the roles of PEG10 and PEG11/RTL1 in mammalian development and evolution, and summarize the other genes domesticated from LTR retrotransposons and endogenous retroviruses (ERVs) in mammals. We also point out the importance of DNA methylation in inactivating and neutralizing the integrated retrotransposons and ERVs in the process of domestication.

Discrimination of alleles and copy numbers at the Q locus in hexaploid wheat using quantitative pyrosequencing

Speltoid spikes are characterized by pyramidal spike morphology featuring an elongated rachis and tenacious glumes. Speltoids are considered undesirable spike aberrants in wheat breeding leading to increased heterogeneity within a cultivar candidate. As a consequence, the presence of speltoids may result in rejection of a cultivar candidate during official field trials or denial of cultivar certification during seed multiplication. A reliable method is, thus, required to assess the occurrence of speltoids, early on in a wheat breeding program. The domestication gene Q located on the long arm of wheat chromosome 5A is known to suppress the speltoid phenotype in wheat. Here, a quantitative pyrosequencing assay was developed to distinguish between normal wheat plants, which possess two copies of the Q allele, and aberrants, which are either aneuploids lacking the correct number of chromosome 5A copies or plants which carry the primitive q allele. An accurate and reproducible determination of the Q gene copy number was achieved for different wheat genotypes based on homoeologous sequence quantification with two primer combinations at the Q locus. Single plants with one to four copies of the Q allele could be detected by quantitative pyrosequencing which corresponded to the occurrence of speltoid (1 Q allele), normal (2 Q alleles), and compact (more than 2 Q alleles) spikes. Q and q specific alleles could be differentiated at SNP position 2299 of the Q gene. This SNP is assumed to be related to the emergence of free-threshing wheat forms. To our knowledge this is the first report for detection of aneuploids and differentiation of Q alleles in bread wheat using pyrosequencing technology. In future, quantitative pyrosequencing assay can be applied in wheat breeding programs to carry out marker-assisted selection against the presence of speltoid spike aberrants.

Next-generation sequencing for understanding and accelerating crop domestication

Next generation Sequencing (NGS) provides a powerful tool for discovery of domestication genes in crop plants and their wild relatives. The accelerated domestication of new plant species as crops may be facilitated by this knowledge. Re-sequencing of domesticated genotypes can identify regions of low diversity associated with domestication. Species-specific data can be obtained from related wild species by whole-genome shot-gun sequencing. This sequence data can be used to design species specific polymerase chain reaction (PCR) primers. Sequencing of the products of PCR amplification of target genes can be used to explore genetic variation in large numbers of genes and gene families. Novel allelic variation in close or distant relatives can be characterized by NGS. Examples of recent applications of NGS to capture of genetic diversity for crop improvement include rice, sugarcane and Eucalypts. Populations of large numbers of individuals can be screened rapidly. NGS supports the rapid domestication of new plant species and the efficient identification and capture of novel genetic variation from related species.

Identification of a functional transposon insertion in the maize domestication gene tb1

Genetic diversity created by transposable elements is an important source of functional variation upon which selection acts during evolution. Transposable elements are associated with adaptation to temperate climates in Drosophila, a SINE element is associated with the domestication of small dog breeds from the gray wolf and there is evidence that transposable elements were targets of selection during human evolution. Although the list of examples of transposable elements associated with host gene function continues to grow, proof that transposable elements are causative and not just correlated with functional variation is limited. Here we show that a transposable element (Hopscotch) inserted in a regulatory region of the maize domestication gene, teosinte branched1 (tb1), acts as an enhancer of gene expression and partially explains the increased apical dominance in maize compared to its progenitor, teosinte. Molecular dating indicates that the Hopscotch insertion predates maize domestication by at least 10,000 years, indicating that selection acted on standing variation rather than new mutation.

Sunflower domestication alleles support single domestication center in eastern North America

Phylogenetic analyses of genes with demonstrated involvement in evolutionary transitions can be an important means of resolving conflicting hypotheses about evolutionary history or process. In sunflower, two genes have previously been shown to have experienced selective sweeps during its early domestication. In the present study, we identified a third candidate early domestication gene and conducted haplotype analyses of all three genes to address a recent, controversial hypothesis about the origin of cultivated sunflower. Although the scientific consensus had long been that sunflower was domesticated once in eastern North America, the discovery of pre-Columbian sunflower remains at archaeological sites in Mexico led to the proposal of a second domestication center in southern Mexico. Previous molecular studies with neutral markers were consistent with the former hypothesis. However, only two indigenous Mexican cultivars were included in these studies, and their provenance and genetic purity have been questioned. Therefore, we sequenced regions of the three candidate domestication genes containing SNPs diagnostic for domestication from large, newly collected samples of Mexican sunflower landraces and Mexican wild populations from a broad geographic range. The new germplasm also was genotyped for 12 microsatellite loci. Our evidence from multiple evolutionarily important loci and from neutral markers supports a single domestication event for extant cultivated sunflower in eastern North America.

Population genetics of Toxoplasma gondii: New perspectives from parasite genotypes in wildlife

Toxoplasma gondii, a zoonotic protozoal parasite, is well-known for its global distribution and its ability to infect virtually all warm-blooded vertebrates. Nonetheless, attempts to describe the population structure of T. gondii have been primarily limited to samples isolated from humans and domesticated animals. More recent studies, however, have made efforts to characterize T. gondii isolates from a wider range of host species and geographic locales. These findings have dramatically changed our perception of the extent of genetic diversity in T. gondii and the relative roles of sexual recombination and clonal propagation in the parasite's lifecycle. In particular, identification of novel, disease-causing T. gondii strains in wildlife has raised concerns from both a conservation and public health perspective as to whether distinct domestic and sylvatic parasite gene pools exist. If so, overlap of these cycles may represent regions of high probability of disease emergence. Here, we attempt to answer these key questions by reviewing recent studies of T. gondii infections in wildlife, highlighting those which have advanced our understanding of the genetic diversity and population biology of this important zoonotic pathogen.

Characterizing homologues of crop domestication genes in poorly described wild relatives by high‐throughput sequencing of whole genomes

Wild crop relatives represent a source of novel alleles for crop genetic improvement. Screening biodiversity for useful or diverse gene homologues has often been based upon the amplification of targeted genes using available sequence information to design primers that amplify the target gene region across species. The crucial requirement of this approach is the presence of sequences with sufficient conservation across species to allow for the design of universal primers. This approach is often not successful with diverse organisms or highly variable genes. Massively parallel sequencing (MPS) can quickly produce large amounts of sequence data and provides a viable option for characterizing homologues of known genes in poorly described genomes. MPS of genomic DNA was used to obtain species-specific sequence information for 18 rice genes related to domestication characteristics in a wild relative of rice, Microlaena stipoides. Species-specific primers were available for 16 genes compared with 12 genes using the universal primer method. The use of species-specific primers had the potential to cover 92% of the sequence of these genes, while traditional universal primers could only be designed to cover 80%. A total of 24 species-specific primer pairs were used to amplify gene homologues, and 11 primer pairs were successful in capturing six gene homologues. The 23 million, 36-base pair (bp) paired end reads, equated to an average of 2X genome coverage, facilitated the successful amplification and sequencing of six target gene homologues, illustrating an important approach to the discovery of useful genes in wild crop relatives.

Do Large Effect QTL Fractionate? A Case Study at the Maize Domestication QTLteosinte branched1

Quantitative trait loci (QTL) mapping is a valuable tool for studying the genetic architecture of trait variation. Despite the large number of QTL studies reported in the literature, the identified QTL are rarely mapped to the underlying genes and it is usually unclear whether a QTL corresponds to one or multiple linked genes. Similarly, when QTL for several traits colocalize, it is usually unclear whether this is due to the pleiotropic action of a single gene or multiple linked genes, each affecting one trait. The domestication gene teosinte branched1 (tb1) was previously identified as a major domestication QTL with large effects on the differences in plant and ear architecture between maize and teosinte. Here we present the results of two experiments that were performed to determine whether the single gene tb1 explains all trait variation for its genomic region or whether the domestication QTL at tb1 fractionates into multiple linked QTL. For traits measuring plant architecture, we detected only one QTL per trait and these QTL all mapped to tb1. These results indicate that tb1 is the sole gene for plant architecture traits that segregates in our QTL mapping populations. For most traits related to ear morphology, we detected multiple QTL per trait in the tb1 genomic region, including a large effect QTL at tb1 itself plus one or two additional linked QTL. tb1 is epistatic to two of these additional QTL for ear traits. Overall, these results provide examples for both a major QTL that maps to a single gene, as well as a case in which a QTL fractionates into multiple linked QTL.

The Same Regulatory Point Mutation Changed Seed-Dispersal Structures in Evolution and Domestication

It is unclear whether gene regulatory changes that drive evolution at the population and species levels [1-3] can be extrapolated to higher taxonomic levels. Here, we investigated the role of cis-regulatory changes in fruit evolution within the Brassicaceae family. REPLUMLESS (RPL, At5g02030) controls development of the replum, a structure with an important role in fruit opening and seed dispersal [6]. We show that reduced repla resembling the Arabidopsis rpl mutant correlated across the Brassicaceae with a point mutation in a conserved cis-element of RPL. When introduced in Arabidopsis, this nucleotide change specifically reduced RPL expression and function in the fruit. Conversely, Brassica RPL containing the Arabidopsis version of the cis-element was sufficient to convert the Brassica replum to an Arabidopsis-like morphology. A mutation in the same nucleotide position of the same cis-element in a RPL ortholog has been independently selected to reduce seed dispersal during domestication of rice, in spite of its very different fruit anatomy. Thus, single-nucleotide regulatory mutations at the same position explain developmental variation in seed-dispersal structures at the population and family levels and suggest that the same genetic toolkit is relevant to domestication and natural evolution in widely diverged species.

Two transposable element insertions are causative mutations for the major domestication gene teosinte branched 1 in modern maize

Two transposable element insertions are causative mutations for the major domestication gene teosinte branched 1 in modern maize

Two Evolutionary Histories in the Genome of Rice: the Roles of Domestication Genes

Genealogical patterns in different genomic regions may be different due to the joint influence of gene flow and selection. The existence of two subspecies of cultivated rice provides a unique opportunity for analyzing these effects during domestication. We chose 66 accessions from the three rice taxa (about 22 each from Oryza sativa indica, O. sativa japonica, and O. rufipogon) for whole-genome sequencing. In the search for the signature of selection, we focus on low diversity regions (LDRs) shared by both cultivars. We found that the genealogical histories of these overlapping LDRs are distinct from the genomic background. While indica and japonica genomes generally appear to be of independent origin, many overlapping LDRs may have originated only once, as a result of selection and subsequent introgression. Interestingly, many such LDRs contain only one candidate gene of rice domestication, and several known domestication genes have indeed been “rediscovered” by this approach. In summary, we identified 13 additional candidate genes of domestication.

On the Trail of Brain Domestication Genes

Researchers have found that the activity of a group of genes in the prefrontal cortex of bonobos was clearly "domesticated" compared with that of chimps, they reported at the Biology of Genomes meeting.

Rapid evolutionary divergence and ecotypic diversification of germination behavior in weedy rice populations

Feral plants have evolved from well-studied crops, providing good systems for elucidation of how weediness evolves. As yet, they have been largely neglected for this purpose. The evolution of weediness can occur by simple back mutations in domestication genes (domestication in reverse). Whether the evolutionary steps to weediness always occur in reverse remains largely unknown. We examined seed germination behavior in recently evolved weedy rice (Oryza sativa f. spontanea) populations and their coexisting cultivars in eastern and north-eastern China to address whether 'dedomestication' is the simple reverse of domestication. We found that these weedy populations did not diverge from their progenitors by reverting to the pre-domestication trait of seed dormancy. Instead, they have evolved a novel mechanism to avoid growing in inappropriate environments via changes in critical temperature cues for seed germination. Furthermore, we found evidence for subsequent ecotypic divergence of these populations such that the critical temperature for germination correlates with the local habitat temperature at latitudinal gradients. The origins of problematic plant species, weeds and invasives, have already been studied in detail. These plants can thus be used as systems for studying rapid evolution. To determine whether and how that evolution is adaptive, experiments such as those described here can be performed.

A model to predict the frequency of integration of fitness-related QTLs from cultivated to wild soybean

With the proliferation of genetically modified (GM) products and the almost exponential growth of land use for GM crops, there is a growing need to develop quantitative approaches to estimating the risk of escape of transgenes into wild populations of crop relatives by natural hybridization. We assessed the risk of transgene escape by constructing a population genetic model based on information on fitness-related QTLs obtained from an F (2) population of wild soybean G. soja × cultivated soybean Glycine max. Simulation started with ten F (1) and 990 wild soybeans reproducing by selfing or outcrossing. Seed production was determined from the genetic effects of two QTLs for number of seeds (SN). Each seed survived winter according to the maternal genotype at three QTLs for winter survival (WS). We assumed that one neutral transgene was inserted at various sites and calculated its extinction rate. The presence of G. max alleles at SN and WS QTLs significantly decreased the probability of introgression of the neutral transgene at all insertion sites equally. The presence of G. max alleles at WS QTLs lowered the risk more than their presence at SN QTLs. Although most model studies have concentrated only on genotypic effects of transgenes, we show that the presence of fitness-related domestication genes has a large effect on the risk of transgene escape. Our model offers the advantage of considering the effects of both domestication genes and a transgene, and they can be widely applied to other wild × crop relative complexes.

Analysis of >1000 single nucleotide polymorphisms in geographically matched samples of landrace and wild barley indicates secondary contact and chromosome‐level differences in diversity around domestication genes

Barley is a model species for the investigation of the evolution, adaptation and spread of the world's important crops. In this article, we describe the first application of an oligonucleotide pool assay single nucleotide polymorphism (SNP) platform to assess the evolution of barley in a portion of the Fertile Crescent, a key region in the development of farming. A large collection of >1000 genetically mapped, genome-wide SNPs was assayed in geographically matched landrace and wild barley accessions (N=448) from Jordan and Syria. Landrace and wild barley categories were clearly genetically differentiated, but a limited degree of secondary contact was evident. Significant chromosome-level differences in diversity between barley types were observed around genes known to be involved in the evolution of cultivars. The region of Jordan and southern Syria, compared with the north of Syria, was supported by SNP data as a more likely domestication origin. Our data provide evidence for hybridization as a possible mechanism for the continued adaptation of landrace barley under cultivation, indicate regions of the genome that may be subject to selection processes and suggest limited origins for the development of the cultivated crop.

A molecular marker linked to the mollis gene conferring soft-seediness for marker-assisted selection applicable to a wide range of crosses in lupin (Lupinus angustifolius L.) breeding

To broaden the gene pool of domesticated commercial cultivars of narrow-leafed lupin (Lupinus angustifolius L.), wild accessions are used as parents in crossing in lupin breeding. Among the progenies from wild × domesticated (W × D) crosses, the soft-seediness gene mollis is the most difficult domestication gene to be selected by conventional breeding methods, where molecular marker-assisted selection (MAS) is highly desirable. MAS in plant breeding requires markers to be cost-effective and high-throughput, and be applicable to a wide range of crosses in a breeding program. In this study, representative plants from an F8 recombinant inbred line (RIL) population derived from a W × D cross, together with four cultivars and four wild types, were used in DNA fingerprinting by microsatellite-anchored fragment length polymorphisms (MFLP). Two co-dominant MFLP polymorphisms were identified as candidate markers linked to the mollis gene, and one of the candidate markers was selected and converted into a co-dominant, sequence-specific PCR marker. This marker, designated MoLi, showed a perfect match with phenotypes of seed coat permeability on a segregating population consisting of 115 F8 RILs, confirming the close genetic linkage to the mollis gene. Validation tests showed that the banding pattern of marker MoLi is consistent with all the 25 historical and current commercial cultivars released in Australia, and is consistent with mollis genotypes in 119 of the 125 accessions in the Australian L. angustifolius core collection. Marker MoLi provides a cost-effective way to select the mollis gene in a wide range of W × D crosses in lupin breeding.

Gene flow among different teosinte taxa and into the domesticated maize gene pool

Maize (Zea mays L. ssp. mays) was domesticated from one wild species ancestor, the Balsas teosinte (Zea mays ssp. parviglumis) about 9000 years ago. Higher levels of gene diversity are found in teosinte taxa compared to maize, following domestication and selection bottlenecks. Diversity in maize can be increased via gene flow from teosinte, which has certainly occurred from various taxa, but the rate of flow from different teosinte taxa and the final impact on maize evolution has been difficult to measure. One hundred populations from six Zea taxa, both domesticated (maize) and wild (teosinte), including domesticated landraces from Asia, Africa, and the Americas, were genotyped with 17 SSR markers using 15 individuals per population. Overall levels of diversity were high, and populations could be distinguished based on markers. Relationships between populations followed most published reports, or can now help resolve previously conflicting reports. Gene flow into maize from different teosinte groups, and gene flow between different teosintes, was estimated. Evidence for contributions from the Balsas teosintes and from Chalco teosintes (Z. mays ssp. mexicana) to the maize gene pool was found, as well as from Chalco into ssp. mexicana race “Durango” and Z. mays ssp. huehuetenengensis. These contributions are almost certainly the result of post-domestication (and ongoing) exchanges. This information must give more impetus to in situ conservation of teosinte species, and use of these teosintes to continue to direct the evolution of maize, especially in response to new diseases, insect pests, and other biotic and abiotic stresses.

INTERMEDIUM-C, a modifier of lateral spikelet fertility in barley, is an ortholog of the maize domestication gene TEOSINTE BRANCHED 1

The domestication of cereals has involved common changes in morphological features, such as seed size, seed retention and modification of vegetative and inflorescence architecture that ultimately contributed to an increase in harvested yield. In barley, this process has resulted in two different cultivated types, two-rowed and six-rowed forms, both derived from the wild two-rowed ancestor, with archaeo-botanical evidence indicating the origin of six-rowed barley early in the domestication of the species, some 8,600-8,000 years ago. Variation at SIX-ROWED SPIKE 1 (VRS1) is sufficient to control this phenotype. However, phenotypes imposed by VRS1 alleles are modified by alleles at the INTERMEDIUM-C (INT-C) locus. Here we show that INT-C is an ortholog of the maize domestication gene TEOSINTE BRANCHED 1 (TB1) and identify 17 coding mutations in barley TB1 correlated with lateral spikelet fertility phenotypes.