Interspecific common bean population derived from Phaseolus acutifolius using a bridging genotype demonstrate useful adaptation to heat tolerance

Abstract

Common bean (Phaseolus vulgaris L.) is an important legume crop worldwide and is a major nutrient source in the tropics. Common bean reproductive development is strongly affected by heat stress, particularly overnight temperatures above 20°C. The desert Tepary bean (Phaseolus acutifolius A. Gray) offers a promising source of adaptative genes due to its natural acclimation to arid conditions. Hybridization between both species is challenging, requiring in vitro embryo rescue and multiple backcrossing cycles to restore fertility. This labor-intensive process constrains developing mapping populations necessary for studying heat tolerance. Here we show the development of an interspecific mapping population using a novel technique based on a bridging genotype derived from P. vulgaris, P. Acutifolius and P. parvifolius named VAP1 and is compatible with both common and tepary bean. The population was based on two wild P. acutifolius accessions, repeatedly crossed with Mesoamerican elite common bush bean breeding lines. The population was genotyped through genotyping-by-sequencing and evaluated for heat tolerance by genome-wide association studies. We found that the population harbored 59.8% introgressions from wild tepary, but also genetic regions from Phaseolus parvifolius, a relative represented in some early bridging crosses. We found 27 significative quantitative trait loci, nine located inside tepary introgressed segments exhibiting allelic effects that reduced seed weight, and increased the number of empty pods, seeds per pod, stem production and yield under high temperature conditions. Our results demonstrate that the bridging genotype VAP1 can intercross common bean with tepary bean and positively influence the physiology of derived interspecific lines, which displayed useful variance for heat tolerance.

Keywords: genome wide association study (GWAS); heat tolerance; interspecific; introgression analysis; phaseolus acutifolius (tepary bean); yield.

Figure 1

Crossing scheme used for IMAWT population development. First the bridging genotype (VAP 1) and a wild tepary accession was intercrossed using the first as a female. The F₁ was then crossed twice with a common bean parental line to produce the secondary F_1:2 generation.

Figure 2

Distribution of the phenotypic values by environment in three locations; NS (Field, non-stress) and heat greenhouses GH1 and GH2. Horizontal lines represent comparisons of means using a paired t-test. The average value for environment is annotated. Markers indicate phenotypic values for the IMAWT population parents. (A) Empty pods per plant (EPP). (B) Number of seeds per pod (NSP). (C) Pod harvest index (PHI). (D) Pods per plant (PP). (E) Seeds per plant (SP). (F) Seed weight (SW). (G) Dry stem weight per plant (StWP). (H) Yield per plant (YdPl). (I) Harvest index (HI). Plots D and E are in log scale for better representation. Asterisks between violins represents the significance of comparison of means through independent t-test method, ns P > 0.05; * P ≤ 0.05; ** P ≤ 0.01; *** P ≤ 0.001; **** P ≤ 0.0001.

Figure 3

Phenotypic correlations between traits by environment. (A) Field. (B) GH1. (C) GH2. EPP, Empty pods per plant; NSP, Number of seeds per pod; PHI, Pod harvest index; PP, Pods per plant; SP, Seeds per plant; SW, Seed weight; StWP, Dry stem weight per plant; YdPl, Yield per plant. Asterisks indicate the significance of Pearson correlation coefficients ns P > 0.05; * P ≤ 0.05; ** P ≤ 0.01; *** P ≤ 0.001.

Figure 4

Principal component analysis of 263 samples using 24.205 biallelic SNPs. Markers were colored according to the introgression percentage obtained from introgression analysis. Parental lines were highlighted with different colors.

Figure 5

Genome-wide distribution of Acutifolii interspecific introgressions in VAP 1 and IMAWT population. The rings of the circle show (A) variant density of full genotype matrix, (B) Absolute frequency of samples carrying Acutifolii alleles of selected subset, (C) Absolute frequency of samples carrying wild P. acutifolius alleles of selected subset, (D) detected introgressions for VAP 1 sequenced in this study and (E) of sample provided by Barrera et al. (2022). (F) Acutifolii introgressions detected in IMAWT Population. Green tiles represent homozygous Acutifolii introgressions and grey tiles undefined regions.

Figure 6

Pearson correlation heatmap of introgression percentage by sample (IP) carried at least one introgression event with traits for the subset of 185 samples. EPP: Empty pods per plant. NSP: Number of seeds per pod. PHI: Pod harvest index. PP: Pods per plant. SP: Seeds per plant. SW: Seed weight. StWP: Dry stem weight per plant. YdPl: Yield per plant. Asterisks indicate the significance of Pearson correlation coefficients ns P > 0.05; ^*P ≤ 0.05; ^**P ≤ 0.01; ^***P ≤ 0.001; ^****P ≤ 0.0001.