Artificial selection of mutations in two nearby genes gave rise to shattering resistance in soybean.

Resistance to pod shattering is a key domestication-related trait selected for seed production in many crops. Here, we show that the transition from shattering in wild soybeans to shattering resistance in cultivated soybeans resulted from selection of mutations within the coding sequences of two nearby genes - Sh1 and Pdh1. Sh1 encodes a C2H2-like zinc finger transcription factor that promotes shattering by repressing SHAT1-5 expression, thereby reducing the secondary wall thickness of fiber cap cells in the abscission layers of pod sutures, while Pdh1 encodes a dirigent protein that orchestrates asymmetric lignin distribution in inner sclerenchyma, creating torsion in pod walls that facilitates shattering. Integration analyses of quantitative trait locus mapping, genome-wide association studies, and allele distribution in representative soybean germplasm suggest that these two genes are primary modulators underlying this domestication trait. Our study thus provides comprehensive understanding regarding the genetic, molecular, and cellular bases of shattering resistance in soybeans.

Long noncoding RNAs underlie multiple domestication traits and leafhopper resistance in soybean.

The origin and functionality of long noncoding RNA (lncRNA) remain poorly understood. Here, we show that multiple quantitative trait loci modulating distinct domestication traits in soybeans are pleiotropic effects of a locus composed of two tandem lncRNA genes. These lncRNA genes, each containing two inverted repeats, originating from coding sequences of the MYB genes, function in wild soybeans by generating clusters of small RNA (sRNA) species that inhibit the expression of their MYB gene relatives through post-transcriptional regulation. By contrast, the expression of lncRNA genes in cultivated soybeans is severely repressed, and, consequently, the corresponding MYB genes are highly expressed, shaping multiple distinct domestication traits as well as leafhopper resistance. The inverted repeats were formed before the divergence of the Glycine genus from the Phaseolus-Vigna lineage and exhibit strong structure-function constraints. This study exemplifies a type of target for selection during plant domestication and identifies mechanisms of lncRNA formation and action.

Genetic dissection of domestication-related traits in soybean through genotyping-by-sequencing of two interspecific mapping populations.

KEY MESSAGE: A total of 132 domestication-related QTLs, of which 41 were novel, were identified through genotyping-by-sequencing of two Glycine max × Glycine soja populations. Soybean [Glycine max (L.) Merr.] was domesticated in East Asia from the wild progenitor Glycine soja. The domestication process led to many distinct morphological changes that adapt it to cultivation. These include larger seeds, erect growth, larger stem diameter, reduced pod shattering, and altered growth habit. The objective of this study was to identify QTLs controlling key domestication-related traits (DRTs) using interspecific mapping populations. A total of 151 RILs from Williams 82 × PI 468916 and 510 RILs from Williams 82 × PI 479752 were utilized for QTL mapping. These lines were genotyped using a genotyping-by-sequencing protocol which resulted in approximately 5000 polymorphic SNP markers. The number of QTLs detected for each of the eleven DRTs ranged between 0-4 QTLs in the smaller Williams 82 × PI 468916 population and 3-16 QTLs in the larger Williams 82 × PI 479752 population. A total of 132 QTLs were detected, of which 51 are associated with selective sweeps previously related to soybean domestication. These QTLs were detected across all 20 chromosomes within 42 genomic regions. This study identifies 41 novel QTLs not detected in previous studies using smaller populations while also confirming the quantitative nature for several of the important DRTs in soybeans. These results would enable more effective use of the wild germplasm for soybean improvement.

Elevation of soybean seed oil content through selection for seed coat shininess.

Many leguminous species have adapted their seed coat with a layer of powdery bloom that contains hazardous allergens and makes the seeds less visible, offering duel protection against potential predators 1 . Nevertheless, a shiny seed surface without bloom is desirable for human consumption and health, and is targeted for selection under domestication. Here we show that seed coat bloom in wild soybeans is mainly controlled by Bloom1 (B1), which encodes a transmembrane transporter-like protein for biosynthesis of the bloom in pod endocarp. The transition from the 'bloom' to 'no-bloom' phenotypes is associated with artificial selection of a nucleotide mutation that naturally occurred in the coding region of B1 during soybean domestication. Interestingly, this mutation not only 'shined' the seed surface, but also elevated seed oil content in domesticated soybeans. Such an elevation of oil content in seeds appears to be achieved through b1-modulated upregulation of oil biosynthesis in pods. This study shows pleiotropy as a mechanism underlying the domestication syndrome 2 , and may pave new strategies for development of soybean varieties with increased seed oil content and reduced seed dust.

GmHs1-1, encoding a calcineurin-like protein, controls hard-seededness in soybean.

Loss of seed-coat impermeability was essential in the domestication of many leguminous crops to promote the production of their highly nutritious seeds. Here we show that seed-coat impermeability in wild soybean is controlled by a single gene, GmHs1-1, which encodes a calcineurin-like metallophosphoesterase transmembrane protein. GmHs1-1 is primarily expressed in the Malpighian layer of the seed coat and is associated with calcium content. The transition from impermeability to permeability in domesticated soybean was caused by artificial selection of a point mutation in GmHs1-1. Interestingly, a number of soybean landraces evaded selection for permeability because of an alternative selection for seed-coat cracking that also enables seed imbibition. Despite the single origin of the mutant allele Gmhs1-1, the distribution pattern of allelic variants in the context of soybean population structure and the detected signature of genomic introgression between wild and cultivated soybeans suggest that Gmhs1-1 may have experienced reselection for seed-coat permeability.