Here, we aim to provide a comprehensive and up-to-date overview of the most significant outcomes in the literature regarding the origin of Phaseolus genus, the geographical distribution of the wild species, the domestication process, and the wide spread out of the centers of origin. Phaseolus can be considered as a unique model for the study of crop evolution, and in particular, for an understanding of the convergent phenotypic evolution that occurred under domestication. The almost unique situation that characterizes the Phaseolus genus is that five of its ∼70 species have been domesticated (i.e., Phaseolus vulgaris, P. coccineus, P. dumosus, P. acutifolius, and P. lunatus), and in addition, for P. vulgaris and P. lunatus, the wild forms are distributed in both Mesoamerica and South America, where at least two independent and isolated episodes of domestication occurred. Thus, at least seven independent domestication events occurred, which provides the possibility to unravel the genetic basis of the domestication process not only among species of the same genus, but also between gene pools within the same species. Along with this, other interesting features makes Phaseolus crops very useful in the study of evolution, including: (i) their recent divergence, and the high level of collinearity and synteny among their genomes; (ii) their different breeding systems and life history traits, from annual and autogamous, to perennial and allogamous; and (iii) their adaptation to different environments, not only in their centers of origin, but also out of the Americas, following their introduction and wide spread through different countries. In particular for P. vulgaris this resulted in the breaking of the spatial isolation of the Mesoamerican and Andean gene pools, which allowed spontaneous hybridization, thus increasing of the possibility of novel genotypes and phenotypes. This knowledge that is associated to the genetic resources that have been conserved ex situ and in situ represents a crucial tool in the hands of researchers, to preserve and evaluate this diversity, and at the same time, to identify the genetic basis of adaptation and to develop new improved varieties to tackle the challenges of climate change, and food security and sustainability.

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.

Seed shattering in crops is a key domestication trait due to its relevance for seed dispersal, yield, and fundamental questions in evolution (e.g., convergent evolution). Here, we focused on pod shattering in common bean (Phaseolus vulgaris L.), the most important legume crop for human consuption in the world. With this main aim, we developed a methodological pipeline that comprises a thorough characterization under field conditions, including also the chemical composition and histological analysis of the pod valves. The pipeline was developed based on the assumption that the shattering trait itself can be treated in principle as a “syndrome” (i.e., a set of correlated different traits) at the pod level. We characterized a population of 267 introgression lines that were developed ad-hoc to study shattering in common bean. Three main objectives were sought: (1) to dissect the shattering trait into its “components,” of level (percentage of shattering pods per plant) and mode (percentage of pods with twisting or non-twisting valves); (2) to test whether shattering is associated to the chemical composition and/or the histological characteristics of the pod valves; and (3) to test the associations between shattering and other plant traits. We can conclude the following: Very high shattering levels can be achieved in different modes; shattering resistance is mainly a qualitative trait; and high shattering levels is correlated with high carbon and lignin contents of the pod valves and with specific histological charaterstics of the ventral sheath and the inner fibrous layer of the pod wall. Our data also suggest that shattering comes with a “cost,” as it is associated with low pod size, low seed weight per pod, high pod weight, and low seed to pod-valves ratio; indeed, it can be more exaustively described as a syndrome at the pod level. Our work suggests that the valve chemical composition (i.e., carbon and lignin content) can be used for a high troughput phenotyping procedures for shattering phenotyping. Finally, we believe that the application of our pipeline will greatly facilitate comparative studies among legume crops, and gene tagging.

In legumes, pod shattering occurs when mature pods dehisce along the sutures, and detachment of the valves promotes seed dispersal. In Phaseolus vulgaris (L)., the major locus qPD5.1-Pv for pod indehiscence was identified recently. We developed a BC4/F4 introgression line population and narrowed the major locus down to a 22.5-kb region. Here, gene expression and a parallel histological analysis of dehiscent and indehiscent pods identified an AtMYB26 orthologue as the best candidate for loss of pod shattering, on a genomic region ~11 kb downstream of the highest associated peak. Based on mapping and expression data, we propose early and fine up-regulation of PvMYB26 in dehiscent pods. Detailed histological analysis establishes that pod indehiscence is associated to the lack of a functional abscission layer in the ventral sheath, and that the key anatomical modifications associated with pod shattering in common bean occur early during pod development. We finally propose that loss of pod shattering in legumes resulted from histological convergent evolution and that it is the result of selection at orthologous loci.

Short title:The pod-shattering syndrome in common bean 32 33 One-sentence summary: A non-functional abscission layer determines the loss of pod 34 shattering; mapping data, and parallel gene expression and histological analysis support 35 PvMYB26 as the candidate gene for pod indehiscence.36 37The author responsible for distribution of materials integral to the findings presented in this 38 article in accordance with the policy described in the Instructions for Authors 39 (www.plantcell.org) is: Roberto Papa (r.papa@univpm.it). 40 41 42 2 43 ABSTRACT 44In legumes, pod shattering occurs when mature pods dehisce along the sutures, and detachment 45 of the valves promotes seed dispersal. In Phaseolus vulgaris, the major locus qPD5.1-Pv for pod 46 indehiscence was identified recently. We developed a BC4/F4 introgression line population and 47 narrowed the major locus down to a 22.5-kb region. Here, gene expression and a parallel 48 histological analysis of dehiscent and indehiscent pods identified an AtMYB26 orthologue as the 49 best candidate for loss of pod shattering, on a genomic region ~11 kb downstream of the highest 50 associated peak. Based on mapping and expression data, we propose early and fine up-regulation 51 of PvMYB26 in dehiscent pods. Detailed histological analysis establishes that pod indehiscence is 52 associated to the lack of a functional abscission layer in the ventral sheath, and that the key 53 anatomical modifications associated with pod shattering in common bean occur early during pod 54 development. We finally propose that loss of pod shattering in legumes resulted from histological 55 convergent evolution and that this is the result of selection at orthologous loci. 56 57 58 Keywords: pod shattering, common bean, MYB26, genome-wide association study, gene 59 expression, pod anatomy, convergent evolution, introgression lines.60 61 62 63 Loss of seed shattering is a paradigmatic example of the changes that have occurred to crop plant 64 traits compared to their wild progenitors, which collectively constitute the 'domestication 65 syndrome' (Hammer 1984). In wild species, specialised seed-dispersal strategies are of 66 fundamental importance for plant survival and fitness. Conversely, in domesticated forms, loss or 67 reduction of seed shattering is desired to reduce yield losses. 68 Due to its complex evolutionary history, common bean (Phaseolus vulgaris L.) is an 69 excellent model to study the domestication process (Bitocchi et al., 2017), which included its 70 parallel domestication in the Andes and Mesoamerica (Bitocchi et al., 2013). In P. vulgaris, the 71 dry beans are characterised by different degrees of pod shattering. These represent the majority of 72 the domesticated pool (Gepts and Debouck 1991), where a limited level of pod shattering has 73 been conserved to favour the threshing of the dry pods. Variations in the pod shattering intensity 74 are also associated with the environmental conditions during maturation (e.g., humidity and 75 temperature) (Parker et al., 2020). 76 ...