Allelic Diversity at Abiotic Stress Responsive Genes in Relationship to Ecological Drought Indices for Cultivated Tepary Bean, Phaseolus acutifolius A. Gray, and Its Wild Relatives

Abstract

Some of the major impacts of climate change are expected in regions where drought stress is already an issue. Grain legumes are generally drought susceptible. However, tepary bean and its wild relatives within Phaseolus acutifolius or P. parvifolius are from arid areas between Mexico and the United States. Therefore, we hypothesize that these bean accessions have diversity signals indicative of adaptation to drought at key candidate genes such as: Asr2, Dreb2B, and ERECTA. By sequencing alleles of these genes and comparing to estimates of drought tolerance indices from climate data for the collection site of geo-referenced, tepary bean accessions, we determined the genotype x environmental association (GEA) of each gene. Diversity analysis found that cultivated and wild P. acutifolius were intermingled with var. tenuifolius and P. parvifolius, signifying that allele diversity was ample in the wild and cultivated clade over a broad sense (sensu lato) evaluation. Genes Dreb2B and ERECTA harbored signatures of directional selection, represented by six SNPs correlated with the environmental drought indices. This suggests that wild tepary bean is a reservoir of novel alleles at genes for drought tolerance, as expected for a species that originated in arid environments. Our study corroborated that candidate gene approach was effective for marker validation across a broad genetic base of wild tepary accessions.

Keywords: LRR receptor-like serine/threonine-protein kinase ERECTA-encoding gene; Phaseolus parvifolius Freytag; Thornthwaite’s potential evapotranspiration (PET) model; abscisic acid-, stress-, and ripening-induced (Asr) gene; candidate gene approach; climate adaptation; dehydration responsive element binding (Dreb) gene; drought tolerance; environmental indices.

Figure 1

Geographical representation of collection sites for tepary beans s.l. (P. acutifolius–parvifolius clade) evaluated in this study with (A) altitude in meters above sea level as a background and (B) drought index on a 30 s grid for the region between the Southern United States and Central America, including the collection hotspot of Northwest Mexico. Dots are colored by taxonomic origin (Table S1) as follows: Green and blue for cultivated and wild P. acutifolius, red for wild P. acutifolius var. tenuifolius, and purple for wild P. parvifolius. Altitudes represented in various tones of achromatic gray. Drought severity index based on Thornthwaite’s potential evapotranspiration (PET) model (DI—Thornthwaite’s index) indicated by scales of red (most intense), orange, yellow to green, and blue (least intense). Latitude and longitude represented by grids in both panels. Wild and cultivated accessions marked as filled triangles (▲) and squares (■), respectively.

Figure 2

Dispersal graph boxplots for habitat drought stress index in four taxonomical divisions of broad sense (s.l.) tepary bean (from the P. acutifolius–parvifolius clade) based on the Thornthwaite’s potential evapotranspiration (PET) model. Drought indices computed at (A) three, (B) six, and (C) 12 months. Colors mark taxonomy: Green and blue for cultivated P. acutifolius and wild P. acutifolius, red for wild P. acutifolius var. tenuifolius, and purple for wild P. parvifolius.

Figure 3

Principal component analyses (PCAs) of genetic polymorphism at (A) Asr2, (B) Dreb2B, and (C) ERECTA-encoding candidate genes for drought tolerance in tepary bean s.l. (P. acutifolius–parvifolius clade). Colors follow Figure 1, by taxonomic origin (Table S1): Green and blue for cultivated and wild P. acutifolius, red for P. acutifolius var. tenuifolius, and purple for P. parvifolius, latter two wild entries. First two principal genetic components allow comparisons with previously generated SNP [23] and SSR [10] data.

Figure 4

Boxplots of the pairwise F_ST distributions at (A) Asr2, (B) Dreb2B, and (C) ERECTA-encoding candidate genes for drought tolerance in tepary bean s.l. (P. acutifolius–parvifolius clade). Boxplots colored by taxonomy: Green and blue for cultivated and wild P. acutifolius, red for P. acutifolius var. tenuifolius, and purple for P. parvifolius, the latter two wild.

Figure 5

Haplotype networks of genetic polymorphism at (A) Asr2, (B) Dreb2B, and (C) ERECTA-encoding candidate genes for drought tolerance in tepary bean s.l. (P. acutifolius–parvifolius clade). Nodes represent haplotypes, its size relative to its frequency. Marks above each segment are substitutions. Nodes are colored by taxonomy (Table S1): Green and blue for cultivated and wild P. acutifolius, red for P. acutifolius var. tenuifolius, and purple for P. parvifolius, the latter two wild accessions.