The genetics and physiology of seed dormancy, a crucial trait in common bean domestication

BMC Plant Biol. 2021 Jan 22;21(1):58. doi: 10.1186/s12870-021-02837-6.

Abstract

Background: Physical 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.).

Results: Using 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.

Conclusions: In 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.

Keywords: Common bean; Domestication; Dormancy; Germination; Imbibition; Pectin.

MeSH terms

  • Chromosome Mapping
  • Chromosomes, Plant / genetics*
  • Crops, Agricultural
  • Domestication
  • Ecosystem
  • Esterases / genetics
  • Esterases / metabolism*
  • Genotype
  • Microscopy, Electron, Scanning
  • Mutagenesis, Insertional
  • Phaseolus / enzymology
  • Phaseolus / genetics*
  • Phaseolus / physiology
  • Phaseolus / ultrastructure
  • Phenotype
  • Plant Dormancy / genetics*
  • Plant Proteins / genetics
  • Plant Proteins / metabolism
  • Quantitative Trait Loci / genetics*
  • Seeds / enzymology
  • Seeds / genetics
  • Seeds / physiology
  • Seeds / ultrastructure
  • Water / metabolism

Substances

  • Plant Proteins
  • Water
  • Esterases
  • pectinacetylesterase