Abstract

The runner bean is a legume species from Mesoamerica closely related to common bean (Phaseolus vulgaris). It is a perennial species, but it is usually cultivated in small-scale agriculture as an annual crop for its dry seeds and edible immature pods. Unlike the common bean, P. coccineus has received little attention from a genetic standpoint. In this work we aim to (1) provide information about the domestication history and domestication events of P. coccineus; (2) examine the distribution and level of genetic diversity in wild and cultivated Mexican populations of this species; and, (3) identify candidate loci to natural and artificial selection. For this, we generated genotyping by sequencing data (42,548 SNPs) from 242 individuals of P. coccineus and the domesticated forms of the closely related species P. vulgaris (20) and P. dumosus (35). Eight genetic clusters were detected, of which half corresponds to wild populations and the rest to domesticated plants. The cultivated populations conform a monophyletic clade, suggesting that only one domestication event occurred in Mexico, and that it took place around populations of the Trans-Mexican Volcanic Belt. No difference between wild and domesticated levels of genetic diversity was detected and effective population sizes are relatively high, supporting a weak genetic bottleneck during domestication. Most populations presented an excess of heterozygotes, probably due to inbreeding depression. One population of P. coccineus subsp. striatus had the greatest excess and seems to be genetically isolated despite being geographically close to other wild populations. Contrasting with previous studies, we did not find evidence of recent gene flow between wild and cultivated populations. Based on outlier detection methods, we identified 24 domestication-related SNPs, 13 related to cultivar diversification and eight under natural selection. Few of these SNPs fell within annotated loci, but the annotated domestication-related SNPs are highly expressed in flowers and pods. Our results contribute to the understanding of the domestication history of P. coccineus, and highlight how the genetic signatures of domestication can be substantially different between closely related species.

Highlights

  • The scarlet runner bean (Phaseolus coccineus L.) is one of the five Phaseolus species that were domesticated in Mesoamerica, and it is the third-most economically important, after P. vulgaris L. and P. lunatus L

  • Half of the genetic groups correspond to the cultivars from the TransMexican Volcanic Belt (Cult-TMVB), Sierra Madre del Sur and Chiapas Highlands (Cult-SUR-CH), Sierra Madre Occidental (Cult-SMOCC) and Oaxaca Valley (Cult-OV)

  • The other half of the genetic clusters belong to wild populations from the Trans-Mexican Volcanic Belt (Wild-TMVB), Sierra Madre del Sur and Chiapas Highlands (Wild-SUR-CH), Sierra Madre

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Summary

Introduction

The scarlet runner bean (Phaseolus coccineus L.) is one of the five Phaseolus species that were domesticated in Mesoamerica, and it is the third-most economically important, after P. vulgaris L. and P. lunatus L. Economic importance, and agronomic potential of P. coccineus, little is known about its domestication history and the genetic variability of its wild and cultivated forms. Wild P. coccineus are perennial climbing plants, occurring mostly at mid-high elevations (1,000–3,000 m.a.s.l.), from northern Mexico (Chihuahua) to Panama (Salinas, 1988). It has 11 pairs of chromosomes and an estimated genome size of 660 Mb (Plant DNA C-values database). No genetic evidence supports these subspecies and varieties, but given the environmental and cultural heterogeneous landscape where P. coccineus occurs, it is expected that the species should be genetically structured

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