Landscape genomics integrates population genetics with landscape ecology, allowing the identification of putative molecular determinants involved in environmental adaptation across the natural geographic and ecological range of populations. Wild Phaseolus vulgaris , the progenitor of common bean ( P. vulgaris ), has a remarkably extended distribution over 10,000 km from northern Mexico to northwestern Argentina. Earlier research has shown that this distribution represents a range expansion from Mesoamerica to the southern Andes through several discrete migration events and that the species colonized areas with different temperature and rainfall compared to its core area of origin. Thus, this species provides an opportunity to examine to what extent adaptation of a species can be broadened or, conversely, ecological or geographical distribution can be limited by inherent adaptedness. In the current study, we applied a landscape genomics approach to a collection of 246 wild common bean accessions representative of its broad geographical and climatic distribution and genotyped for ∼20K SNPs. We applied two different but complementary approaches for identifying loci putatively involved in environmental adaptation: i) an outlier-detection method that identifies loci showing strong differentiation between sub-populations; ii) an association method based on the identification of loci associated with bio-climatic variables. This integrated approach allowed the identification of several genes showing signature of selection across the different natural sub-populations of this species, as well as genes associated with specific bio-climatic variables related to temperature and precipitation. The current study demonstrates the feasibility of landscape genomics approach for a preliminary identification of specific populations and novel candidate genes involved in environmental adaptation in P. vulgaris . As a resource for broadening the genetic diversity of the domesticated gene pool of this species, the genes identified constitute potential molecular markers and introgression targets for the breeding improvement of domesticated common bean.

Author Summary

The ancestral form of common bean has an unusually large distribution in the Americas, extending over 10,000 km from ∼35° N. Lat. to ∼35° S. Lat. This wide distribution results from discrete long-range dissemination events to the Andes region from the original environments in Mesoamerica. It also suggests adaptation to new environments that are distinct from those encountered in Mesoamerica. In this research, we identified genes that may be involved in adaptation to climate variables in these new environments using two methods. A first method – outlier detection – was used to identify genome regions that differentiated the wild bean groups in the Andes resulting from discrete dissemination events among themselves and the different groups in Mesoamerica. The second method – genome-wide association – was used to identify candidate genome regions correlated with these same variables across the entire distribution from Mesoamerica to the southern Andes. The two methods identified two sets of candidate genes, several of which were related to the water status of plants, and illustrate how the genetic architecture of adaptation following long-range dissemination. This study provides sets of candidate genes as well as candidate wild bean populations that need to be corroborated for their use in increasing the water use efficiency of domesticated beans.

Plant aquaporins are a large and diverse family of water channel proteins that are essential for several physiological processes in living organisms. Numerous studies have linked plant aquaporins with a plethora of processes, such as nutrient acquisition, CO2 transport, plant growth and development, and response to abiotic stresses. However, little is known about this protein family in common bean. Here, we present a genome-wide identification of the aquaporin gene family in common bean (Phaseolus vulgaris L.), a legume crop essential for human nutrition. We identified 41 full-length coding aquaporin sequences in the common bean genome, divided by phylogenetic analysis into five sub-families (PIPs, TIPs, NIPs, SIPs and XIPs). Residues determining substrate specificity of aquaporins (i.e., NPA motifs and ar/R selectivity filter) seem conserved between common bean and other plant species, allowing inference of substrate specificity for these proteins. Thanks to the availability of RNA-sequencing datasets, expression levels in different organs and in leaves of wild and domesticated bean accessions were evaluated. Three aquaporins (PvTIP1;1, PvPIP2;4 and PvPIP1;2) have the overall highest mean expressions, with PvTIP1;1 having the highest expression among all aquaporins. We performed an EST database mining to identify drought-responsive aquaporins in common bean. This analysis showed a significant increase in expression for PvTIP1;1 in drought stress conditions compared to well-watered environments. The pivotal role suggested for PvTIP1;1 in regulating water homeostasis and drought stress response in the common bean should be verified by further field experimentation under drought stress.

The wild progenitor of common-bean has an exceptionally large distribution from northern Mexico to northwestern Argentina, unusual among crop wild progenitors. This research sought to document major events of range expansion that led to this distribution and associated environmental changes. Through the use of genotyping-by-sequencing (∼20,000 SNPs) and geographic information systems applied to a sample of 246 accessions of wild Phaseolus vulgaris, including 157 genotypes of the Mesoamerican, 77 of the southern Andean, and 12 of the Northern Peru-Ecuador gene pools, we identified five geographically distinct subpopulations. Three of these subpopulations belong to the Mesoamerican gene pool (Northern and Central Mexico, Oaxaca, and Southern Mexico, Central America and northern South America) and one each to the Northern Peru-Ecuador (PhI) and the southern Andean gene pools. The five subpopulations were distributed in different floristic provinces of the Neotropical seasonally dry forest and showed distinct distributions for temperature and rainfall resulting in decreased local potential evapotranspiration (PhI and southern Andes groups) compared with the two Mexican groups. Three of these subpopulations represent long-distance dispersal events from Mesoamerica into Northern Peru-Ecuador, southern Andes, and Central America and Colombia, in chronological order. Of particular note is that the dispersal to Northern Peru-Ecuador markedly predates the dispersal to the southern Andes (∼400 vs. ∼100 ky), consistent with the ancestral nature of the phaseolin seed protein and chloroplast sequences observed in the PhI group. Seed dispersal in common bean can be, therefore, described at different spatial and temporal scales, from localized, annual seed shattering to long-distance, evolutionarily rare migration.

Next-generation sequencing technologies have increased markedly the throughput of genetic studies, allowing the identification of several thousands of SNPs within a single experiment. Even though sequencing cost is rapidly decreasing, the price for whole-genome re-sequencing of a large number of individuals is still costly, especially in plants with a large and highly redundant genome. In recent years, several reduced representation library approaches have been developed for reducing the sequencing cost per individual. Among them, genotyping-by-sequencing (GBS) represents a simple, cost-effective, and highly multiplexed alternative for species with or without an available reference genome. However, this technology requires specific optimization for each species, especially for the restriction enzyme (RE) used. Here we report on the application of GBS in a test experiment with 18 genotypes of wild and domesticated Phaseolus vulgaris. After an in silico digestion with different RE of the P. vulgaris genome reference sequence, we selected CviAII as the most suitable RE for GBS in common bean based on the high frequency and even distribution of restriction sites. A total of 44,875 SNPs, 1940 deletions, and 1693 insertions were identified, with 50 % of the variants located in genic sequences and tagging 11,027 genes. SNP and InDel distributions were positively correlated with gene density across the genome. In addition, we were able to also identify putative copy number variations of genomic segments between different genotypes. In conclusion, GBS with the CviAII enzyme results in thousands of evenly spaced markers and provides a reliable, high-throughput, and cost-effective approach for genotyping both wild and domesticated common beans.

The common-bean (Phaseolus vulgaris), a widely consumed legume, originated in Mesoamerica and expanded to South America, resulting in the development of two geographically distinct gene pools. Poor soil condition, including metal toxicity, are often constraints to common-bean crop production. Several P. vulgaris miRNAs, including miR1511, respond to metal toxicity. The MIR1511 gene sequence from the two P. vulgaris model sequenced genotypes revealed that, as opposed to BAT93 (Mesoamerican), the G19833 (Andean) accession displays a 58-bp deletion, comprising the mature and star miR1511 sequences. Genotyping-By-Sequencing data analysis from 87 non-admixed Phaseolus genotypes, comprising different Phaseolus species and P. vulgaris populations, revealed that all the P. vulgaris Andean genotypes and part of the Mesoamerican (MW1) genotypes analyzed displayed a truncated MIR1511 gene. The geographic origin of genotypes with a complete versus truncated MIR1511 showed a distinct distribution. The P. vulgaris ALS3 (Aluminum Sensitive Protein 3) gene, known to be important for aluminum detoxification in several plants, was experimentally validated as the miR1511 target. Roots from BAT93 plants showed decreased miR1511 and increased ALS3 transcript levels at early stages under aluminum toxicity (AlT), while G19833 plants, lacking mature miR1511, showed higher and earlier ALS3 response. Root architecture analyses evidenced higher tolerance of G19833 plants to AlT. However, G19833 plants engineered for miR1511 overexpression showed lower ALS3 transcript level and increased sensitivity to AlT. Absence of miR1511 in Andean genotypes, resulting in a diminished ALS3 transcript degradation, appears to be an evolutionary advantage to high Al levels in soils with increased drought conditions.

Background

Wild crop relatives have been potentially subjected to stresses on an evolutionary time scale prior to domestication. Among these stresses, drought is one of the main factors limiting crop productivity and its impact is likely to increase under current scenarios of global climate change. We sought to determine to what extent wild common bean (Phaseolus vulgaris) exhibited adaptation to drought stress, whether this potential adaptation is dependent on the climatic conditions of the location of origin of individual populations, and to what extent domesticated common bean reflects potential drought adaptation.

Methods

An extensive and diverse set of wild beans from across Mesoamerica, along with a set of reference Mesoamerican domesticated cultivars, were evaluated for root and shoot traits related to drought adaptation. A water deficit experiment was conducted by growing each genotype in a long transparent tube in greenhouse conditions so that root growth, in addition to shoot growth, could be monitored.

Results

Phenotypic and landscape genomic analyses, based on single-nucleotide polymorphisms, suggested that beans originating from central and north-west Mexico and Oaxaca, in the driest parts of their distribution, produced more biomass and were deeper-rooted. Nevertheless, deeper rooting was correlated with less root biomass production relative to total biomass. Compared with wild types, domesticated types showed a stronger reduction and delay in growth and development in response to drought stress. Specific genomic regions were associated with root depth, biomass productivity and drought response, some of which showed signals of selection and were previously related to productivity and drought tolerance.

Conclusions

The drought tolerance of wild beans consists in its stronger ability, compared with domesticated types, to continue growth in spite of water-limited conditions. This study is the first to relate bean response to drought to environment of origin for a diverse selection of wild beans. It provides information that needs to be corroborated in crosses between wild and domesticated beans to make it applicable to breeding programmes.

Abiotic stress is a limiting factor for common bean (Phaseolus vulgaris L.) production globally. The study of the genotypic, phenotypic, and bio-climatic variables in a broad set of accessions may assist the identification of genomic regions involved in the climatic adaptation of the common bean. We conducted a genotyping-by-sequencing analysis using 28,823 SNPs on 110 georeferenced common bean accessions from Brazil to discover associations between SNPs and bio-climatic indexes. The population structure analysis clustered the accessions into two groups corresponding to the Andean and Mesoamerican gene pools. Of the 19 bioclimatic variables, 17 exhibited a significant association with SNPs on chromosomes Pv01, Pv02, Pv03, Pv04, Pv06, Pv09, Pv10, and Pv11 of common bean. Ten candidate genes were associated with specific bio-climatic variables related to temperature and precipitation. The candidate genes associated with this significant Pv09 region encode a Platz transcription factor family protein previously reported to be an essential regulator of drought stress. The SNP markers and candidate genes associated with the bio-climatic variables should be validated in segregating populations for water stress, which could further be used for marker-assisted selection. As a result, bean breeding programs may be able to provide advances in obtaining drought-tolerant cultivars.

Lima bean (Phaseolus lunatus L.), one of the five domesticated Phaseolus bean crops, shows a wide range of ecological adaptations along its distribution range from Mexico to Argentina. These adaptations make it a promising crop for improving food security under predicted scenarios of climate change in Latin America and elsewhere. In this work, we combine long and short read sequencing technologies with a dense genetic map from a biparental population to obtain the chromosome-level genome assembly for Lima bean. Annotation of 28,326 gene models show high diversity among 1917 genes with conserved domains related to disease resistance. Structural comparison across 22,180 orthologs with common bean reveals high genome synteny and five large intrachromosomal rearrangements. Population genomic analyses show that wild Lima bean is organized into six clusters with mostly non-overlapping distributions and that Mesomerican landraces can be further subdivided into three subclusters. RNA-seq data reveal 4275 differentially expressed genes, which can be related to pod dehiscence and seed development. We expect the resources presented here to serve as a solid basis to achieve a comprehensive view of the degree of convergent evolution of Phaseolus species under domestication and provide tools and information for breeding for climate change resiliency.

Domesticated crops have been disseminated by humans over vast geographic areas. Common bean (Phaseolus vulgaris L.) was introduced in Europe after 1492. Here, by combining whole-genome profiling, metabolic fingerprinting and phenotypic characterisation, we show that the first common bean cultigens successfully introduced into Europe were of Andean origin, after Francisco Pizarro's expedition to northern Peru in 1529. We reveal that hybridisation, selection and recombination have shaped the genomic diversity of the European common bean in parallel with political constraints. There is clear evidence of adaptive introgression into the Mesoamerican-derived European genotypes, with 44 Andean introgressed genomic segments shared by more than 90% of European accessions and distributed across all chromosomes except PvChr11. Genomic scans for signatures of selection highlight the role of genes relevant to flowering and environmental adaptation, suggesting that introgression has been crucial for the dissemination of this tropical crop to the temperate regions of Europe.