Adaptive gene loss in the common bean pan-genome during range expansion and domestication
Gaia Cortinovis, Leonardo Vincenzi, Robyn Anderson, Giovanni Marturano, Jacob I. Marsh, Philipp E. Bayer, Lorenzo Rocchetti, Giulia Frascarelli, Giovanna Lanzavecchia, Alice Pieri, Andrea Benazzo, Elisa Bellucci, Valerio Di Vittori, Laura Nanni, Juan José Ferreira Fernández, Marzia Rossato, O. Mario Aguilar, Peter L. Morrell, Monica Rodriguez, Tania Gioia, Kerstin Neumann, Juan Camilo Álvarez Díaz, Ariane Gratias, Christophe Klopp, Elena Bitocchi, Valérie Geffroy, Massimo Delledonne, David Edwards, Roberto Papa
Abstract
The common bean (Phaseolus vulgaris L.) is a crucial legume crop and an ideal evolutionary model to study adaptive diversity in wild and domesticated populations. Here, we present a common bean pan-genome based on five high-quality genomes and whole-genome reads representing 339 genotypes. It reveals ~234 Mb of additional sequences containing 6,905 protein-coding genes missing from the reference, constituting 49% of all presence/absence variants (PAVs). More non-synonymous mutations are found in PAVs than core genes, probably reflecting the lower effective population size of PAVs and fitness advantages due to the purging effect of gene loss. Our results suggest pan-genome shrinkage occurred during wild range expansion. Selection signatures provide evidence that partial or complete gene loss was a key adaptive genetic change in common bean populations with major implications for plant adaptation. The pan-genome is a valuable resource for food legume research and breeding for climate change mitigation and sustainable agriculture.