Genomic dissection of pod shattering in common bean: mutations at non‐orthologous loci at the basis of convergent phenotypic evolution under domestication of leguminous species

Abstract

The complete or partial loss of shattering ability occurred independently during the domestication of several crops. Therefore, the study of this trait can provide an understanding of the link between phenotypic and molecular convergent evolution. The genetic dissection of 'pod shattering' in Phaseolus vulgaris is achieved here using a population of introgression lines and next-generation sequencing techniques. The 'occurrence' of the indehiscent phenotype (indehiscent versus dehiscent) depends on a major locus on chromosome 5. Furthermore, at least two additional genes are associated with the 'level' of shattering (number of shattering pods per plant: low versus high) and the 'mode' of shattering (non-twisting versus twisting pods), with all of these loci contributing to the phenotype by epistatic interactions. Comparative mapping indicates that the major gene identified on common bean chromosome 5 corresponds to one of the four quantitative trait loci for pod shattering in Vigna unguiculata. None of the loci identified comprised genes that are homologs of the known shattering genes in Glycine max. Therefore, although convergent domestication can be determined by mutations at orthologous loci, this was only partially true for P. vulgaris and V. unguiculata, which are two phylogenetically closely related crop species, and this was not the case for the more distant P. vulgaris and G. max. Conversely, comparative mapping suggests that the convergent evolution of the indehiscent phenotype arose through mutations in different genes from the same underlying gene networks that are involved in secondary cell-wall biosynthesis and lignin deposition patterning at the pod level.

Pod indehiscence is a domestication and aridity resilience trait in common bean

“…By contrast, the major QTL on Pv05 discovered in a biparental population by Rau et al . () and confirmed here in a diverse panel of Andean beans is not closely orthologous to PD‐related loci, yet is described in other species. Future investigations may find that this locus has also been subject to parallel molecular evolution among taxa.…”

“…(b) In the Andean Diversity Panel ( ADP ), chromosomes Pv03, Pv05, Pv08, and Pv09 include major regions of interest. SNP s located near Pv MYB 26 (Rau et al ., ) on Pv05 were highly significant. Horizontal red and blue lines indicate the Bonferroni‐corrected significance threshold for an α of 0.01 and 0.05, respectively.…”

“…Wild beans produce a lignified wall fiber layer (LFL) in the pods that is thicker than the vascular bundle sheaths (VS, or suture string) layer, while the LFL is greatly reduced in domesticated varieties. Stringless snap beans have a weakly lignified VS at the suture, with a reduction in the number of lignified cells and the extent of secondary cell wall deposition in each cell, as reported previously (Prakken, ; Rau et al ., ). In stringless beans, the LFL is typically absent.…”

“…Another major QTL for PD in Andean beans maps to Pv05, as described recently (Rau et al ., ), and several genes in this region are candidates for future study. Rau et al .…”

“…Rau et al . () noted that an ortholog of MYB26 exists in the qPD5.1‐Pv region of interest on Pv05, which may be responsible for variation in PD. Significant Pv05 SNPs from our association mapping completely envelope the qPD5.1‐Pv interval, supporting this result.…”