Mesoamerican origin of the common bean (Phaseolus vulgaris L.) is revealed by sequence data Elena Bitocchia, Laura Nannia, Elisa Belluccia, Monica Rossia, Alessandro Giardinia, Pierluigi Spagnoletti Zeulib, Giuseppina Logozzob, Jens Stougaardc, Phillip McCleand, Giovanna Attenee, and Roberto Papaa,f,1 aDipartimento di Scienze Agrarie, Alimentari ed Ambientali, Università Politecnica delle Marche, 60131 Ancona, Italy; bDipartimento di Biologia Difesa e Biotecnologie Agro-Forestali, Università degli Studi della Basilicata, 85100 Potenza, Italy; cCentre for Carbohydrate Recognition and Signalling, Department of Molecular Biology, Aarhus University, DK-8000 Aarhus C, Denmark; dDepartment of Plant Sciences, North Dakota State University, Fargo, ND 58105; eDipartimento di Scienze Agronomiche e Genetica Vegetale Agraria, Università degli Studi di Sassari, 07100 Sassari, Italy; and fCereal Research Centre, Agricultural Research Council (CRA-CER), S.S. 16, Km 675, 71122 Foggia, Italy Edited* by Jeffrey L. Bennetzen, University of Georgia, Athens, GA, and approved December 16, 2011 (received for review June 3, 2011) Knowledge about the origins and evolution of crop species rep- scenario of P. vulgaris (20, 21), although a recent study has sug- resents an important prerequisite for efficient conservation and use gested a single domestication event at the origin of the indica and of existing plant materials. This study was designed to solve the japonica subgroups (22). While only these two major gene pools ongoing debate on the origins of the common bean by investigating are recognized in the domesticated population, the geographical the nucleotide diversity at five gene loci of a large sample that structure of the wild form of the common bean is more complex, represents the entire geographical distribution of the wild forms of with an additional third gene pool that is localized between Peru this species. Our data clearly indicate a Mesoamerican origin of the and Ecuador (23) and characterized by a specific storage seed common bean. They also strongly support the occurrence of a protein, phaseolin type I (24). Moreover, wild populations from bottleneck during the formation of the Andean gene pool that Colombia are often seen as intermediates, and a marked geo- predates the domestication, which was suggested by recent studies graphical structure is observed in wild beans from Mesoamerica based on multilocus molecular markers. Furthermore, a remarkable (12). The population from northern Peru and Ecuador is usually result was the genetic structure that was seen for the Mesoamerican considered the ancestral population from which P. vulgaris origi- accessions, with the identification of four different genetic groups nated (the northern Peru–Ecuador hypothesis) (11, 24, 25). In- that have different relationships with the sets of wild accessions deed, the work by Kami et al. (24) analyzed a portion of the gene from the Andes and northern Peru–Ecuador. This finding implies that codes for the storage seed protein phaseolin, including pha- that both of the gene pools from South America originated through seolin type (type I) from northern Peru–Ecuador accessions that different migration events from the Mesoamerican populations that was not present in the other gene pools, which indicates that type I were characteristic of central Mexico. phaseolin is ancestral to the other phaseolin sequences of P. vul- garis (24). Thus, the work by Kami et al. (24) suggested that, crop evolution | Phaseoleae | population structure | mutation rate starting from the core area of the western slopes of the Andes in northern Peru and Ecuador, the wild bean was dispersed north he common bean (Phaseolus vulgaris L.) is the main grain (Colombia, Central America, and Mexico) and south (southern Tlegume for direct human consumption, and it represents Peru, Bolivia, and Argentina), which resulted in the Mesoamer- a rich source of protein, vitamins, minerals, and fiber, especially ican and Andean gene pools, respectively. for the poorer populations of Africa and Latin America (1). The Mesoamerican origin of the common bean is an alterna- Investigations into the origins and evolution of this species would tive and older hypothesis. This hypothesis is supported by the be expected to highlight the structure and organization of its observations that the closest relatives of wild P. vulgaris in the genetic diversity and the role of the evolutionary forces that have Phaseolus genus are distributed throughout Mesoamerica (26– been shaping this diversity. Such knowledge is a crucial pre- 29). Additionally, the higher diversity found in the Mesoamer- requisite for efficient conservation and use of the existing ican compared with the Andean gene pool (phaseolin types, germplasm for the development of new improved plant varieties. allozyme alleles, and molecular markers) (8–10, 30, 31) supports The current distribution of the wild common bean encompasses a Mesoamerican origin. a large geographical area: from northern Mexico to northwestern Recently, the work by Rossi et al. (13) compared amplified Argentina (2). In general, two major ecogeographical gene pools fragment length polymorphism (AFLP) data based on an anal- are recognized: Mesoamerica and the Andes. These two gene ysis of wild and domesticated P. vulgaris accessions with the data pools are characterized by partial reproductive isolation (3, 4), from the work by Kwak and Gepts (14) based on simple se- and they are seen in both wild and domesticated materials. They quence repeats (SSRs) obtained on a similar sample. This have been recognized in several studies based on morphology (5– analysis suggested that, before domestication, there was a severe 7), agronomic traits (7), seed proteins (8), allozymes (9), and bottleneck in the Andean populations, and they reproposed the different types of molecular markers (10–15), which have given Mesoamerican origin of the common bean. the overall indication of the occurrence of at least two in- dependent domestication events in the two different hemispheres. The existence of these two geographically distinct and isolated Author contributions: E. Bitocchi and R.P. designed research; E. Bitocchi, L.N., E. Bellucci, evolutionary lineages that predate the domestication of the M.R., A.G., P.S.Z., G.L., and J.S., P.M., G.A., and R.P. performed research; E. Bitocchi, L.N., common bean represents a unique scenario among crops. This E. Bellucci, G.A., and R.P. analyzed data; and E. Bitocchi and R.P. wrote the paper. scenario differs from the occurrence over a smaller geographical The authors declare no conflict of interest. range of multiple domestications that have been proposed for *This Direct Submission article had a prearranged editor. other species, such as barley (16) and wheat (17), and indeed, Data deposition: The sequences reported in this paper have been deposited in the Gen- within the Mesoamerican gene pool of the common bean itself Bank database (accession nos. JN796475-JN796922). (18, but see 13, 19). In these cases, the lack of isolation between 1To whom correspondence should be addressed. E-mail: [email protected]. the populations prevented independent evolution of different See Author Summary on page 5148 (volume 109, number 14). lineages in both the wild and domesticated forms. Rice is the only This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. crop that may show a scenario that is to some extent similar to the 1073/pnas.1108973109/-/DCSupplemental. E788–E796 | PNAS | Published online March 5, 2012 www.pnas.org/cgi/doi/10.1073/pnas.1108973109 Downloaded by guest on September 28, 2021 The main aim of the present study was to investigate the evolu- 34-aa sequence has 85% identity with histidinol dehydrogenase of PNAS PLUS tionary history of P. vulgaris to solve the issue regarding the origin Arabidopsis thaliana. This enzyme catalyses the last two steps in of this species. We have investigated the nucleotide diversity for the L-histidine biosynthesis pathway, which is conserved in bac- five different genes from a wide sample of wild P. vulgaris that teria, archaea, fungi, and plants. For Leg100, a coding region of is representative of its geographical distribution. Our findings 45 bp was identified at the 3′ extremity of the sequence, and its identify the origin of P. vulgaris as Mesoamerican, and they also deduced 15-aa sequence showed 100% identity with biotin syn- reveal the level and structure of the genetic diversity that char- thase of A. thaliana, an enzyme that is involved in the biotin acterizes the wild accessions of this species. Our data are relevant biosynthetic process. Three exons were found in Leg133 of 75, 72, for crop improvement and in particular, maximization of the and 90 bp. The corresponding 79-aa sequence showed 84% efficient use of wild genetic diversity for breeding programs. identity with dolichyl-diphosphooligosaccharide-protein glyco- transferase of A. thaliana, an enzyme that is involved in aspara- Results gine-linked protein glycosylation. Two exons (88 and 56 bp) were Nucleotide Variation in the Wild Common Bean. We sequenced five identified in Leg223, with an identity of 71% of the translated loci of a large collection that included wild common bean acces- protein fragment with the eukaryotic translation initiation factor sions from Mesoamerican (n = 49) and Andean (n = 47) gene SUI1 family protein of A. thaliana. This protein seems to have an pools and genotypes from northern Peru–Ecuador (n = 6) that are important role in accurate initiator codon recognition during characterized by the ancestral type I phaseolin (Table S1). These translation initiation. The structure of PvSHP1 was characterized gene pools represent a cross-section of the entire geographical in the work by Nanni et al. (19) (Fig. S1 and Table S2), and the distribution of the wild form of P. vulgaris. The sequenced region fragment sequenced in this study included three coding regions of for each gene is located within the transcriptional unit and 12, 42, and 42 bp. This sequence was identified as homologous to encompasses between 500 and 900 bp, which includes both introns Arabidopsis SHP1 (SHATTERPROOF 1), a gene that is involved and exons.