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Adaptive gene loss in the common bean pan-genome during range expansion and domestication.

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.

SUBMITTER: Cortinovis G

PROVIDER: S-EPMC11303546 | biostudies-literature | 2024 Aug

REPOSITORIES: biostudies-literature

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Adaptive gene loss in the common bean pan-genome during range expansion and domestication.

Cortinovis Gaia G Vincenzi Leonardo L Anderson Robyn R Marturano Giovanni G Marsh Jacob Ian JI Bayer Philipp Emanuel PE Rocchetti Lorenzo L Frascarelli Giulia G Lanzavecchia Giovanna G Pieri Alice A Benazzo Andrea A Bellucci Elisa E Di Vittori Valerio V Nanni Laura L Ferreira Fernández Juan José JJ Rossato Marzia M Aguilar Orlando Mario OM Morrell Peter Laurent PL Rodriguez Monica M Gioia Tania T Neumann Kerstin K Alvarez Diaz Juan Camilo JC Gratias Ariane A Klopp Christophe C Bitocchi Elena E Geffroy Valérie V Delledonne Massimo M Edwards David D Papa Roberto R

Nature communications 20240807 1

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 ...[more]

PMID: 39107305

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Project description:BackgroundPhysical seed dormancy is an important trait in legume domestication. Although seed dormancy is beneficial in wild ecosystems, it is generally considered to be an undesirable trait in crops due to reduction in yield and / or quality. The physiological mechanism and underlying genetic factor(s) of seed dormancy is largely unknown in several legume species. Here we employed an integrative approach to understand the mechanisms controlling physical seed dormancy in common bean (Phaseolus vulgaris L.).ResultsUsing an innovative CT scan imaging system, we were able to track water movements inside the seed coat. We found that water uptake initiates from the bean seed lens. Using a scanning electron microscopy (SEM) we further identified several micro-cracks on the lens surface of non-dormant bean genotypes. Bulked segregant analysis (BSA) was conducted on a bi-parental RIL (recombinant inbred line) population, segregating for seed dormancy. This analysis revealed that the seed water uptake is associated with a single major QTL on Pv03. The QTL region was fine-mapped to a 118 Kb interval possessing 11 genes. Coding sequence analysis of candidate genes revealed a 5-bp insertion in an ortholog of pectin acetylesterase 8 that causes a frame shift, loss-of-function mutation in non-dormant genotype. Gene expression analysis of the candidate genes in the seed coat of contrasting genotypes indicated 21-fold lower expression of pectin acetylesterase 8 in non-dormant genotype. An analysis of mutational polymorphism was conducted among wild and domesticated beans. Although all the wild beans possessed the functional allele of pectin acetylesterase 8, the majority (77%) of domesticated beans had the non-functional allele suggesting that this variant was under strong selection pressure through domestication.ConclusionsIn this study, we identified the physiological mechanism of physical seed dormancy and have identified a candidate allele causing variation in this trait. Our findings suggest that a 5-bp insertion in an ortholog of pectin acetylesterase 8 is likely a major causative mutation underlying the loss of seed dormancy during domestication. Although the results of current study provide strong evidences for the role of pectin acetylesterase 8 in seed dormancy, further confirmations seem necessary by employing transgenic approaches.

Dataset Information

Adaptive gene loss in the common bean pan-genome during range expansion and domestication.

Publications

Adaptive gene loss in the common bean pan-genome during range expansion and domestication.

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