Identification and mapping of a recessive allele, dt3, specifying semideterminate stem growth habit in soybean.

KEY MESSAGE: A locus, dt3, modulating semideterminancy in soybean, was discovered by a combination of genome-wide association studies and linkage mapping with multiple distinct biparental populations. Stem growth habit is a key architectural trait in many plants that contributes to plant productivity and environmental adaptation. In soybean, stem growth habit is classified as indeterminate, semideterminate, or determinate, of which semideterminacy is often considered as a counterpart of the "Green Revolution" trait in cereals that significantly increased grain yields. It has been demonstrated that semideterminacy in soybean is modulated by epistatic interaction between two loci, Dt1 on chromosome 19 and Dt2 on chromosome 18, with the latter as a negative regulator of the former. Here, we report the discovery of a third locus, Dt3, modulating soybean stem growth habit, which was delineated to a ~ 196-kb region on chromosome 10 by a combination of allelic and haplotypic analysis of the Dt1 and Dt2 loci in the USDA soybean Germplasm Collection, genome-wide association studies with three subsets of the collection, and linkage mapping with four biparental populations derived from crosses between one of two elite indeterminate cultivars and each of four semideterminate varieties possessing neither Dt2 nor dt1. These four semideterminate varieties are recessive mutants (i.e., dt3/dt3) in the Dt1/Dt1;dt2/dt2 background. As the semideterminacy modulated by the Dt2 allele has unfavorable pleotropic effects such as sensitivity to drought stress, dt3 may be an ideal alternative for use to develop semideterminate cultivars that are more resilient to such an environmental stress. This study enhances our understanding of the genetic factors underlying semideterminacy and enables more accurate marker-assisted selection for stem growth habit in soybean breeding.

The genetic basis of shoot architecture in soybean.

Shoot architecture refers to the three-dimensional body plan of the above ground organs of the plant. The patterning of this body plan results from the tight genetic control of the size and maintenance of meristems, the initiation of axillary growth, and the timing of developmental phase transition. Variation in shoot architecture can result in dramatic differences in plant productivity and/or grain yield due to their effects on light interception, photosynthetic efficiency, response to agronomic inputs, and environmental adaptation. The fine-tuning of shoot architecture has consequently been of great interest to plant breeders, driving the need for deeper understanding of the genes and molecular mechanisms governing these traits. In soybean, the world's most important oil and protein crop, major components of shoot architecture include stem growth habit, plant height, branch angle, branch number, leaf petiole angle, and the size and shape of leaves. Key genes underlying some of these traits have been identified to integrate hormonal, developmental, and environmental signals modulating the growth and orientation of shoot organs. Here we summarize the current knowledge and recent advances in the understanding of the genetic control of these important architectural traits in soybean.

Identification and molecular mapping of a major quantitative trait locus underlying branch angle in soybean.

KEY MESSAGE: A major quantitative trait locus (QTL) modulating soybean (Glycine max) branch angle was identified by linkage analysis using two bi-parental mapping populations with and without pedigree from wild soybean (Glycine soja). Soybean branch angle is a critical architectural trait that affects many other traits of agronomic importance associated with the plant's productivity and grain yield and is thus a vital consideration in soybean breeding. However, the genetic basis for modulating this important trait in soybean and many other crops remain unknown. Previously, we developed a recombinant inbred line (RIL) population derived from a cross between a domesticated soybean (Glycine max) variety, Williams 82, and a wild soybean (Glycine soja) accession, PI 479,752, and observed drastic variation in plant architecture including branch angle among individual RILs. In this study, one of the RILs possessing extremely wide branch angle (WBA) was crossed with an elite soybean cultivar (LD00-3309) possessing narrow branch angle (NBA) to produce an F2 population composed of 147 plants and F2-derived F3 families for inheritance analysis and QTL mapping. We found that branch angle is controlled by a major QTL located on chromosome 19, designated qGmBa1 and that WBA-derived from the wild soybean accession-is dominant over NBA. This locus was also detected as a major one underlying branch angle by QTL mapping using a subset of the soybean nested association mapping (SoyNAM) population composed of 140 RILs, which were derived from a cross between a landrace, PI 437169B, possessing WBA and an elite variety, IA3023, possessing NBA. Molecular markers located in the QTL region defined by both mapping populations can be used for marker-assisted selection of branch angle in soybean breeding.

A transposon-mediated reciprocal translocation promotes environmental adaptation but compromises domesticability of wild soybeans.

Large structural variations frequently occur in higher plants; however, the impact of such variations on plant diversification, adaptation and domestication remains elusive. Here, we mapped and characterised a reciprocal chromosomal translocation in soybeans and assessed its effects on diversification and adaptation of wild (Glycine soja) and semiwild (Glycine gracilis) soybeans, and domestication of cultivated soybean (Glycine max), by tracing the distribution of the translocation in the USDA Soybean Germplasm Collection and population genetics analysis. We demonstrate that the translocation occurred through CACTA transposon-mediated chromosomal breakage in wild soybean c. 0.34 Ma and is responsible for semisterility in translocation heterozygotes and reduces their reproductive fitness. The translocation has differentiated Continental (i.e. China and Russia) populations from Maritime (i.e. Korea and Japan) populations of G. soja and predominately adapted to cold and dry climates. Further analysis revealed that the divergence of G. max from G. soja predates the translocation event and that G. gracilis is an evolutionary intermediate between G. soja and G. max. Our results highlight the effects of a chromosome rearrangement on the processes leading to plant divergence and adaptation, and provides evidence that suggests G. gracilis, rather than G. soja, as the ancestor of cultivated soybean.

Identification and molecular mapping of Rps14, a gene conferring broad-spectrum resistance to Phytophthora sojae in soybean.

KEY MESSAGE: A soybean landrace carries broad-spectrum resistance to Phytophthora sojae, which is conferred by a single gene, designated Rps14, on the short arm of chromosome 3. Phytophthora sojae is the causative agent for Phytophthora root and stem rot in soybean [Glycine max (L.) Merr.] and can be managed by deployment of resistance to P. sojae (Rps) genes. PI 340,029 is a soybean landrace carrying broad-spectrum resistance to the pathogen. Analysis of an F2 population derived from a cross between PI 340,029 and a susceptible cultivar 'Williams' reveals that the resistance to P. sojae race 1 is conferred by a single gene, designated Rps14, which was initially mapped to a 4.5-cM region on the short arm of chromosome 3 by bulked segregant analysis (BSA), and subsequently narrowed to a 1.48 cM region corresponding to 229-kb in the Williams 82 reference genome (Wm82 v2.a1), using F3:4 families derived from the F2 population. Further analysis indicates that the broad-spectrum resistance carried by PI 340,029 is fully attributable to Rps14. The genomic sequences corresponding to the defined Rps14 region from a set of diverse soybean varieties exhibit drastic NBS-LRR gene copy number variation, ranging from 3 to 17 copies. Ultimate isolation of Rps14 would be critical for precise selection and deployment of the gene for soybean protection.

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.

Unidirectional movement of small RNAs from shoots to roots in interspecific heterografts.

Long-distance RNA movement is important for plant growth and environmental responses; however, the extent to which RNAs move between distant tissues, their relative magnitude and functional importance remain to be elucidated on a genomic scale. Using a soybean (Glycine max)-common bean (Phaseolus vulgaris) grafting system, we identified 100 shoot-root mobile microRNAs and 32 shoot-root mobile phased secondary small interfering RNAs (phasiRNAs), which were predominantly produced in shoots and transported to roots, and, in most cases, accumulated to a level similar to that observed in shoots. Many of these microRNAs or phasiRNAs enabled cleavage of their messenger RNA targets or phasiRNA precursors in roots. In contrast, most mobile-capable mRNAs were transcribed in both shoots and roots, with only small proportions transported to recipient tissues. These findings suggest that the regulatory mechanisms for small RNA movement are different from those for mRNA movement, and that the former is more strictly regulated and, probably, more functionally important than the latter.

A giant NLR gene confers broad-spectrum resistance to Phytophthora sojae in soybean.

Phytophthora root and stem rot caused by P. sojae is a destructive soybean soil-borne disease found worldwide. Discovery of genes conferring broad-spectrum resistance to the pathogen is a need to prevent the outbreak of the disease. Here, we show that soybean Rps11 is a 27.7-kb nucleotide-binding site-leucine-rich repeat (NBS-LRR or NLR) gene conferring broad-spectrum resistance to the pathogen. Rps11 is located in a genomic region harboring a cluster of large NLR genes of a single origin in soybean, and is derived from rounds of unequal recombination. Such events result in promoter fusion and LRR expansion that may contribute to the broad resistance spectrum. The NLR gene cluster exhibits drastic structural diversification among phylogenetically representative varieties, including gene copy number variation ranging from five to 23 copies, and absence of allelic copies of Rps11 in any of the non-Rps11-donor varieties examined, exemplifying innovative evolution of NLR genes and NLR gene clusters.