Artificial Selection of Seed-Coat Permeability during Domestication: The Desirable Accompanied by the Undesirable

Loss or reduction of hard seededness or impermeability to water was a key step that led to domestication of many leguminous crops for agricultural production. However, the molecular basis underlying this trait remains unknown. Here we report map-based cloning and characterization of a major quantitative trait locus (QTL), designated as Hs1, which controls the seed hardedness in Glycine soja, the wild progenitor species of the cultivated soybean (Glycine max). We demonstrate that Hs1 encodes a calcineurin-like metallo-phosphoesterase-like transmembrane protein localized in cellular membranes, and the transition from hard seededness in the wild accessions to soft seededness in the cultivated soybeans was caused by a single nucleotide mutation within Hs1, which changed an amino acid of the gene and resulted in a recessive mutation allele (hs1). Hs1 and hs1 are both expressed in the seed coats during seed development, but the former is expressed at a level significantly higher than the latter, particularly, in the late stage of seed development prior to seed maturity. In-situ hybridization demonstrates that Hs1 is primarily expressed in malphighian layer that is responsible for the impermeability of seed coats. Although hs1 was artificially selected and fixed in most cultivated soybeans, a number of landraces was escaped from the selection for hs1, possibly due to introgression of Hs1 from seed-coat cracking landraces and subsequent selection for permeable but non-cracking varieties. These findings will facilitate the exploitation of genetic diversity from wild soybeans for cultivar enhancement, and the improvement of seed qualities for production, storage, and special uses.