Decreased nucleotide and expression diversity and modified coexpression patterns characterize domestication in the common bean (original) (raw)
Related papers
2013
We have studied the nucleotide diversity of common bean, Phaseolus vulgaris, which is characterized by two independent domestications in two geographically distinct areas: Mesoamerica and the Andes. This provides an important model, as domestication can be studied as a replicate experiment. We used nucleotide data from five gene fragments characterized by large introns to analyse 214 accessions (102 wild and 112 domesticated). The wild accessions represent a crosssection of the entire geographical distribution of P. vulgaris. A reduction in genetic diversity in both of these gene pools was found, which was threefold greater in Mesoamerica compared with the Andes. This appears to be a result of a bottleneck that occurred before domestication in the Andes, which strongly impoverished this wild germplasm, leading to the minor effect of the subsequent domestication bottleneck (i.e. sequential bottleneck). These findings show the importance of considering the evolutionary history of crop species as a major factor that influences their current level and structure of genetic diversity. Furthermore, these data highlight a single domestication event within each gene pool. Although the findings should be interpreted with caution, this evidence indicates the Oaxaca valley in Mesoamerica, and southern Bolivia and northern Argentina in South America, as the origins of common bean domestication.
Evolution Letters
The scarlet runner bean (Phaseolus coccineus) is one of the five domesticated Phaseolus species. It is cultivated in small-scale agriculture in the highlands of Mesoamerica for its dry seeds and immature pods, and unlike the other domesticated beans, P. coccineus is an open-pollinated legume. Contrasting with its close relative, the common bean, few studies focusing on its domestication history have been conducted. Demographic bottlenecks associated with domestication might reduce genetic diversity and facilitate the accumulation of deleterious mutations. Conversely, introgression from wild relatives could be a source of variation. Using Genotyping by Sequencing data (79,286 single-nucleotide variants) from 237 cultivated and wild samples, we evaluated the demographic history of traditional varieties from different regions of Mexico and looked for evidence of introgression between sympatric wild and cultivated populations. Traditional varieties have high levels of diversity, even th...
Genome Biology, 2016
Background: Legumes are the third largest family of angiosperms and the second most important crop class. Legume genomes have been shaped by extensive large-scale gene duplications, including an approximately 58 million year old whole genome duplication shared by most crop legumes. Results: We report the genome and the transcription atlas of coding and non-coding genes of a Mesoamerican genotype of common bean (Phaseolus vulgaris L., BAT93). Using a comprehensive phylogenomics analysis, we assessed the past and recent evolution of common bean, and traced the diversification of patterns of gene expression following duplication. We find that successive rounds of gene duplications in legumes have shaped tissue and developmental expression, leading to increased levels of specialization in larger gene families. We also find that many long non-coding RNAs are preferentially expressed in germ-line-related tissues (pods and seeds), suggesting that they play a significant role in fruit development. Our results also suggest that most bean-specific gene family expansions, including resistance gene clusters, predate the split of the Mesoamerican and Andean gene pools. Conclusions: The genome and transcriptome data herein generated for a Mesoamerican genotype represent a counterpart to the genomic resources already available for the Andean gene pool. Altogether, this information will allow the genetic dissection of the characters involved in the domestication and adaptation of the crop, and their further implementation in breeding strategies for this important crop.
Domestication Genomics of the open-pollinated Scarlet Runner Bean (Phaseolus coccineus L.)
The runner bean is a legume species from Mesoamerica closely related to common bean (Phaseolus vulgaris). It is a perennial species, but it is usually cultivated in small-scale agriculture as an annual crop for its dry seeds and edible immature pods. Unlike the common bean, P. coccineus has received little attention from a genetic standpoint. In this work we aim to (1) provide information about the domestication history and domestication events of P. coccineus; (2) examine the distribution and level of genetic diversity in wild and cultivated Mexican populations of this species; and, (3) identify candidate loci to natural and artificial selection. For this, we generated genotyping by sequencing data (42,548 SNPs) from 242 individuals of P. coccineus and the domesticated forms of the closely related species P. vulgaris (20) and P. dumosus (35). Eight genetic clusters were detected, of which half corresponds to wild populations and the rest to domesticated plants. The cultivated populations conform a monophyletic clade, suggesting that only one domestication event occurred in Mexico, and that it took place around populations of the Trans-Mexican Volcanic Belt. No difference between wild and domesticated levels of genetic diversity was detected and effective population sizes are relatively high, supporting a weak genetic bottleneck during domestication. Most populations presented an excess of heterozygotes, probably due to inbreeding depression. One population of P. coccineus subsp. striatus had the greatest excess and seems to be genetically isolated despite being geographically close to other wild populations. Contrasting with previous studies, we did not find evidence of recent gene flow between wild and cultivated populations. Based on outlier detection methods, we identified 24 domestication-related SNPs, 13 related to cultivar diversification and eight under natural selection. Few of these SNPs fell within annotated loci, but the annotated domestication-related SNPs are highly expressed in flowers and pods. Our results contribute to the understanding of the domestication history of P. coccineus, and highlight how the genetic signatures of domestication can be substantially different between closely related species.
A reference genome for common bean and genome-wide analysis of dual domestications
Nature Genetics, 2014
agriculture owing to its ability to fix atmospheric nitrogen. We assembled 473 Mb of the 587-Mb genome and genetically anchored 98% of this sequence in chromosome-scale pseudomolecules. We compared the genome for the common bean against the soybean genome to find changes in soybean resulting from polyploidy. Using resequencing of 60 wild individuals and 00 landraces from the genetically differentiated Mesoamerican and Andean gene pools, we confirmed 2 independent domestications from genetic pools that diverged before human colonization. Less than 0% of the 74 Mb of sequence putatively involved in domestication was shared by the two domestication events. We identified a set of genes linked with increased leaf and seed size and combined these results with quantitative trait locus data from Mesoamerican cultivars. Genes affected by domestication may be useful for genomics-enabled crop improvement.
Current State and Perspectives in Population Genomics of the Common Bean
Plants
Population genomics integrates advances in sequencing technologies, bioinformatics tools, statistical methods and software into research on evolutionary and population genetics. Its application has provided novel approaches that have significantly advanced our understanding of new and long-standing questions in evolutionary processes. This has allowed the disentangling of locus-specific effects from genome-wide effects and has shed light on the genomic basis of fitness, local adaptation and phenotypes. “-Omics” tools have provided a comprehensive genome-wide view of the action of evolution. The specific features of the Phaseolus genus have made it a unique example for the study of crop evolution. The well-documented history of multiple domestications in Phaseolus vulgaris L. (common bean) and its further adaptation to different environments have provided the opportunity to investigate evolutionary issues, such as convergent evolution in the same species across different domesticatio...
Evolution of genetic diversity during the domestication of common-bean (Phaseolus vulgaris L.)
Theoretical and Applied Genetics, 1994
M13 DNA fingerprinting was used to determine evolutionary changes that occurred in Latin American germ plasm and USA cultivars of commonbean (Phaseolus vulgaris L.) during domestication. Linkage mapping experiments showed that M13-related sequences in the common-bean genome were either located at the distal ends of linkage groups or that they were unlinked to each other or to any previously mapped markers. Levels of polymorphism observed by hybridization with M13 (1 probe-enzyme combination) were comparable to those observed by hybridization with single-copy random PstI genomic probes (36 enzyme-probe combinations) but were higher than those observed for isozymes (10 loci). Results indicated that the wild ancestor had diverged into two taxa, one distributed in Middle America (Mexico, Central America, and Colombia) and the other in the Andes (Peru and Argentina); they also suggested separate domestications in the two areas leading to two cultivated gene pools. Domestication in both areas led to pronounced reductions in diversity in cultivated descendants in Middle America and the Andes. The marked lack of polymorphism within commercial classes of USA cultivars suggests that the dispersal of cultivars from the centers of origin and subsequent breeding of improved cultivars led to high levels of genetic uniformity. To our knowledge, this is the first crop for which this reduction in diversity has been documented with a single type of
Genomics of Phaseolus Beans, a Major Source of Dietary Protein and Micronutrients in the Tropics
Common bean is grown and consumed principally in developing countries in Latin America, Africa, and Asia. It is largely a subsistence crop eaten by its producers and, hence, is underestimated in production and commerce statistics. Common bean is a major source of dietary protein, which complements carbohydrate-rich sources such as rice, maize, and cassava. It is also a rich source of minerals, such as iron and zinc, and certain vitamins. Several large germplasm collections have been established, which contain large amounts of genetic diversity, including the five domesticated Phaseolus species and wild species, as well as an incipient stock collection. The genealogy and genetic diversity of P. vulgaris are among the best known in crop species through the systematic use of molecular markers, from seed proteins and isozymes to simple sequence repeats, and DNA sequences. Common bean exhibits a high level of genetic diversity, compared with other selfing species. A hierarchical organization into gene pools and ecogeographic races has been established. There are over 15 mapping populations that have been established to study the inheritance of agronomic traits in different locations. Most linkage maps have been correlated with the core map established in the BAT93 x Jalo EEP558 cross, which includes several hundreds of markers, including Restriction Fragment Length Polymorphisms, Random Amplified Polymorphic DNA, Amplified Fragment Length Polymorphisms, Short Sequence Repeats, Sequence Tagged Sites, and Target Region Amplification Polymorphisms. Over 30 individual genes for disease resistance and some 30 Quantitative Trait Loci for a broad range of agronomic traits have been tagged. Eleven BAC libraries have been developed in genotypes that represent key steps in the evolution before and after domestication of common bean, a unique resource among crops. Fluorescence in situ hybridization provides the first links between chromosomal and genetic maps. A gene index based on some P. vulgaris 21,000 expressed sequence tags (ESTs) has been developed. ESTs were developed from different genotypes, organs, and physiological conditions. They resolve currently in some 6,500–6,800 singletons and 2,900 contigs. An additional 20,000 embryonic P. coccineus ESTs provides an additional resource. Some 1,500 M2 Targeting Local Lesions In Genomes populations exist currently. Finally, transformation methods by biolistics and Agrobacterium have been developed, which can be applied for genetic engineering. Root transformation via A. rhizogenes is also possible. Thus, the Phaseomics community has laid a solid foundation towards its ultimate goal, namely the sequencing of the Phaseolus genome. These genomic resources are a much-needed source of additional markers of known map location for marker-assisted selection and the accelerated improvement of common bean cultivars.
The plant genome, 2018
Common bean ( L.) is the most important grain legume for human consumption and is a major nutrition source in the tropics. Because bean production is reduced by both abiotic and biotic constraints, current breeding efforts are focused on the development of improved varieties with tolerance to these stresses. We characterized materials from different breeding programs spanning three continents to understand their sequence diversity and advance the development of molecular breeding tools. For this, 37 varieties belonging to , (A. Gray), and L. were sequenced by whole-genome sequencing, identifying more than 40 million genomic variants. Evaluation of nuclear DNA content and analysis of copy number variation revealed important differences in genomic content not only between and the two other domesticated species, but also within , affecting hundreds of protein-coding genomic regions. A large number of inter-gene pool introgressions were identified. Furthermore, interspecific introgressi...
Genomic history of the origin and domestication of common bean unveils its closest sister species
Genome Biology, 2017
Background: Modern civilization depends on only a few plant species for its nourishment. These crops were derived via several thousands of years of human selection that transformed wild ancestors into high-yielding domesticated descendants. Among cultivated plants, common bean (Phaseolus vulgaris L.) is the most important grain legume. Yet, our understanding of the origins and concurrent shaping of the genome of this crop plant is limited. Results: We sequenced the genomes of 29 accessions representing 12 Phaseolus species. Single nucleotide polymorphism-based phylogenomic analyses, using both the nuclear and chloroplast genomes, allowed us to detect a speciation event, a finding further supported by metabolite profiling. In addition, we identified 1200 protein coding genes (PCGs) and~100 long non-coding RNAs with domestication-associated haplotypes. Finally, we describe asymmetric introgression events occurring among common bean subpopulations in Mesoamerica and across hemispheres. Conclusions: We uncover an unpredicted speciation event in the tropical Andes that gave rise to a sibling species, formerly considered the "wild ancestor" of P. vulgaris, which diverged before the split of the Mesoamerican and Andean P. vulgaris gene pools. Further, we identify haplotypes strongly associated with genes underlying the emergence of domestication traits. Our findings also reveal the capacity of a predominantly autogamous plant to outcross and fix loci from different populations, even from distant species, which led to the acquisition by domesticated beans of adaptive traits from wild relatives. The occurrence of such adaptive introgressions should be exploited to accelerate breeding programs in the near future.