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Adaptive changes in plant phenology are often considered to be a feature of the so-called ‘domestication syndrome’ that distinguishes modern crops from their wild progenitors, but little detailed evidence supports this idea. In soybean, a major legume crop, flowering time variation is well characterized within domesticated germplasm and is critical for modern production, but its importance during domestication is unclear. Here, we identify sequential contributions of two homeologous pseudo-response-regulator genes, Tof12 and Tof11 , to ancient flowering time adaptation, and demonstrate that they act via LHY homologs to promote expression of the legume-specific E1 gene and delay flowering under long photoperiods. We show that Tof12 -dependent acceleration of maturity accompanied a reduction in dormancy and seed dispersal during soybean domestication, possibly predisposing the incipient crop to latitudinal expansion. Better understanding of this early phase of crop evolution will help to identify functional variation lost during domestication and exploit its potential for future crop improvement. Whole-genome resequencing and association analyses in 424 soybean accessions identify two homeologous genes that contributed to flowering time adaptation during soybean domestication.

Background Soybean ( Glycine max ) is an economically important oil and protein crop. Plant height is a key trait that significantly impacts the yield of soybean; however, research on the molecular mechanisms associated with soybean plant height is lacking. The CRISPR (clustered regularly interspaced short palindromic repeat)/Cas9 (CRISPR-associated system 9) system is a recently developed technology for gene editing that has been utilized to edit the genomes of crop plants. Results Here, we designed four gRNAs to mutate four LATE ELONGATED HYPOCOTYL ( LHY ) genes in soybean. In order to test whether the gRNAs could perform properly in transgenic soybean plants, we first tested the CRISPR construct in transgenic soybean hairy roots using Agrobacterium rhizogenes strain K599. Once confirmed, we performed stable soybean transformation and obtained 19 independent transgenic soybean plants. Subsequently, we obtained one T 1 transgene-free homozygous quadruple mutant of GmLHY by self-crossing. The phenotypes of the T 2 -generation transgene-free quadruple mutant plants were observed, and the results showed that the quadruple mutant of GmLHY displayed reduced plant height and shortened internodes. The levels of endogenous gibberellic acid (GA3) in Gmlhy1a1b2a2b was lower than in the wild type (WT), and the shortened internode phenotype could be rescued by treatment with exogenous GA3. In addition, the relative expression levels of GA metabolic pathway genes in the quadruple mutant of GmLHY were significantly decreased in comparison to the WT. These results suggest that GmLHY encodes an MYB transcription factor that affects plant height through mediating the GA pathway in soybean. We also developed genetic markers for identifying mutants for application in breeding studies. Conclusions Our results indicate that CRISPR/Cas9-mediated targeted mutagenesis of four GmLHY genes reduces soybean plant height and shortens internodes from 20 to 35 days after emergence (DAE). These findings provide insight into the mechanisms underlying plant height regulatory networks in soybean.

Fanjiang Kong, Zhixi Tian, Xingliang Hou, Baohui Liu and colleagues report the cloning and functional characterization of J , the locus underlying the long-juvenile (LJ) trait that has enabled tropical cultivation of soybean. They show that J, an ortholog of Arabidopsis ELF3, downregulates the expression of E1 , thereby promoting flowering under short-day conditions. Soybean is a major legume crop originating in temperate regions, and photoperiod responsiveness is a key factor in its latitudinal adaptation. Varieties from temperate regions introduced to lower latitudes mature early and have extremely low grain yields. Introduction of the long-juvenile (LJ) trait extends the vegetative phase and improves yield under short-day conditions, thereby enabling expansion of cultivation in tropical regions. Here we report the cloning and characterization of J , the major classical locus conferring the LJ trait, and identify J as the ortholog of Arabidopsis thaliana EARLY FLOWERING 3 ( ELF3 ). J depends genetically on the legume-specific flowering repressor E1 , and J protein physically associates with the E1 promoter to downregulate its transcription, relieving repression of two important FLOWERING LOCUS T ( FT ) genes and promoting flowering under short days. Our findings identify an important new component in flowering-time control in soybean and provide new insight into soybean adaptation to tropical regions.

The basic leucine zipper (bZIP) family of transcription factors plays an important role in the growth and developmental process as well as responds to various abiotic stresses, such as drought and high salinity. Our previous work identified GmFDL19, a bZIP transcription factor, as a flowering promoter in soybean, and the overexpression of GmFDL19 caused early flowering in transgenic soybean plants. Here, we report that GmFDL19 also enhances tolerance to drought and salt stress in soybean. GmFDL19 was determined to be a group A member, and its transcription expression was highly induced by abscisic acid (ABA), polyethylene glycol (PEG 6000) and high salt stresses. Overexpression of GmFDL19 in soybean enhanced drought and salt tolerance at the seedling stage. The relative plant height (RPH) and relative shoot dry weight (RSDW) of transgenic plants were significantly higher than those of the WT after PEG and salt treatments. In addition, the germination rate and plant height of the transgenic soybean were also significantly higher than that of WT plants after various salt treatments. Furthermore, we also found that GmFDL19 could reduce the accumulation of Na+ ion content and up-regulate the expression of several ABA/stress-responsive genes in transgenic soybean. We also found that GmFDL19 overexpression increased the activities of several antioxidative enzyme and chlorophyll content but reduced malondialdehyde content. These results suggested that GmFDL19 is involved in soybean abiotic stress responses and has potential utilization to improve multiple stress tolerance in transgenic soybean.

FLOWERING LOCUS T (FT) is the key flowering integrator in Arabidopsis (Arabidopsis thaliana), and its homologs encode florigens in many plant species regardless of their photoperiodic response. Two FT homologs, GmFT2a and GmFT5a, are involved in photoperiod-regulated flowering and coordinately control flowering in soybean. However, the molecular and genetic understanding of the roles played by GmFT2a and GmFT5a in photoperiod-regulated flowering in soybean is very limited. In this study, we demonstrated that GmFT2a and GmFT5a were able to promote early flowering in soybean by overexpressing these two genes in the soybean cultivar Williams 82 under noninductive long-day (LD) conditions. The soybean homologs of several floral identity genes, such as GmAP1, GmSOC1 and GmLFY, were significantly upregulated by GmFT2a and GmFT5a in a redundant and differential pattern. A bZIP transcription factor, GmFDL19, was identified as interacting with both GmFT2a and GmFT5a, and this interaction was confirmed by yeast two-hybridization and bimolecular fluorescence complementation (BiFC). The overexpression of GmFDL19 in soybean caused early flowering, and the transcription levels of the flowering identity genes were also upregulated by GmFDL19, as was consistent with the upregulation of GmFT2a and GmFT5a. The transcription of GmFDL19 was also induced by GmFT2a. The results of the electrophoretic mobility shift assay (EMSA) indicated that GmFDL19 was able to bind with the cis-elements in the promoter of GmAP1a. Taken together, our results suggest that GmFT2a and GmFT5a redundantly and differentially control photoperiod-regulated flowering in soybean through both physical interaction with and transcriptional upregulation of the bZIP transcription factor GmFDL19, thereby inducing the expression of floral identity genes.

Adaptability of soybean [Glycine max (L.) Merr.] to a wide range of latitudes is attributed to the natural variation in the major genes and quantitative trait loci (QTL) that control flowering time and maturity. Identification of novel genes and understanding their molecular basis is critical to improving soybean productivity. We identified a new locus conditioning days to flowering and maturity that was detected in hybrid progeny between cultivated and wild soybeans. A backcross was made between the recurrent parent Tokei 780 and two early‐flowering recombinant inbred lines (RILs; from the cross Tokei 780 × Hidaka 4, a wild soybean accession, all of which possessed an identical genotype at the major four maturity loci, E1 to E4). The segregation patterns observed in the F2 and F3 progeny derived from the two crosses revealed that early‐flowering was controlled by a single dominant gene. The gene was fine‐mapped to a 245‐kb interval between markers M5 and M7 on Gm16. A tagging marker ID1 was significantly associated with the variation in days to flowering (0.82, p < 0.01) and maturity (0.76, p < 0.01) in the F2 population. The new early‐flowering gene and its tagging marker are very useful for molecular breeding towards early maturity and stable productivity of soybean under high‐latitude environments. The gene symbol E9e9 has been assigned. E9E9 results in early maturity and e9e9 results in late maturity.

Flowering time, as an important ecological trait related to photoperiod response, maturity, and final yield, is a complex trait conferred by multiple genes. To further elucidate the genetic mechanism for the flowering time, quantitative trait loci (QTLs) related to the flowering time and maturity were identified utilizing specific-locus amplified fragment sequencing (SLAF-Seq) technology. In total, we identified three QTLs on chromosomes 5, 6, and 7 from a recombinant inbred line (RIL) population of 171 individuals derived from a cross between Minsoy and Archer soybeans. Of these QTLs, one new QTL on chromosome 7, called E11 , was simultaneously detected in an ~ 1.03 Mb region from the F 6 and F 8 generations of the RIL population, and accounted for ~ 15% of the total phenotypic variation over 2 years. The gene symbol E11e11 had been approved by the soybean genetic committee. The segregation patterns observed in residual heterozygous lines (RHLs) at the E11 locus revealed that early flowering was controlled by a single dominant gene. The gene was fine-mapped to an ~ 138 kb interval, including 11 genes based on the reference genome. Through amino acid sequence analysis, three most likely candidate genes, Glyma.07 g048500 , Glyma.07 g049000 , and Glyma.07 g049200 , were identified. The phenotypes detected from two near-isogenic lines (NILs) revealed that NILs for E11 allele significantly promoted the flowering time and maturity than NILs for the e11 under the long-day (LD) conditions. These results suggest that E11 is a new flowering time gene that will be valuable in improving our understanding of the mechanism for the flowering time and molecular breeding.

Soybean cultivars are extremely diverse in time to flowering and maturation as a result of various photoperiod sensitivities. The underlying molecular genetic mechanism is not fully clear, however, four maturity loci E1, E2, E3 and E4 have been molecularly identified. In this report, cultivars were selected with various photoperiod sensitivities from different ecological zones, which covered almost all maturity groups (MG) from MG 000 to MG VIII and MG X adapted from latitude N 18° to N 53°. They were planted in the field under natural daylength condition (ND) in Beijing, China or in pots under different photoperiod treatments. Maturity-related traits were then investigated. The four E maturity loci were genotyped at the molecular level. Our results suggested that these four E genes have different impacts on maturity and their allelic variations and combinations determine the diversification of soybean maturity and adaptation to different latitudes. The genetic mechanisms underlying photoperiod sensitivity and adaptation in wild soybean seemed unique from those in cultivated soybean. The allelic combinations and functional molecular markers for the four E loci will significantly assist molecular breeding towards high productivity.

Soybean is an important crop used for oil production. Alterations of the fatty acids, especially increased oleic acid content, can improve the nutritional quality and oxidative stability of soybean oil. During seed development, two genes, encoding FAD2-1A and FAD2-1B, are mainly responsible for the transformation from oleic acid to linoleic acid, and the combination of fad2-1a and fad2-1b is the key factor for increasing oleic acid content. To breed high oleic acid varieties, we analyzed the haplotype of FAD2-1A and F AD2-1B among 1250 soybean accessions and detected a novel mutation in the FAD2-1A gene that we described as fad2-1a/W254Stop . By focusing on the mutation fad2-1a/W254Stop and the reported fad2-1b allele, we developed two molecular markers. Based on these markers, we selected one line (435) from a cross between the fad2-1a(W254Stop) allele and the existing fad2-1 allele . The oleic acid content of ‘435’ was 91.03%. The ‘435’ line was used as a donor parent, and an elite soybean cultivar ‘Heinong51’ was selected as the recurrent parent. After three backcrosses, we detected an individual with high oleic acid content (75%) and high yield. We named this individual ‘Fuhang3’. This study generated material for breeding high oleic acid soybean varieties and improved the rate of breeding novel soybean varieties.

Soybean ( L.) is a major legume crop that is mainly distributed in temperate regions. The adaptability of soybean to grow at relatively high latitudes is attributed to natural variations in major genes and quantitative trait loci (QTLs) that control flowering time and maturity. Identification of new QTLs and map-based cloning of candidate genes are the fundamental approaches in elucidating the mechanism underlying soybean flowering and adaptation. To identify novel QTLs/genes, we developed two F8:10 recombinant inbred lines (RILs) and evaluated the traits of time to flowering (R1), maturity (R8), and reproductive period (RP) in the field. To rapidly and efficiently identify QTLs that control these traits, next-generation sequencing (NGS)-based QTL analysis was performed. This study demonstrates that only one major QTL on chromosome 4 simultaneously controls R1, R8, and RP traits in the Dongnong 50 × Williams 82 (DW) RIL population. Furthermore, three QTLs were mapped to chromosomes 6, 11, and 16 in the Suinong 14 × Enrei (SE) RIL population. Two major pleiotropic QTLs on chromosomes 4 and 6 were shown to affect flowering time, maturity, and RP. A QTL influencing RP was identified on chromosome 11, and QTL on chromosome 16 was associated with time to flowering responses. All these QTLs contributed to soybean maturation. The QTLs identified in this study may be utilized in fine mapping and map-based cloning of candidate genes to elucidate the mechanisms underlying flowering and soybean adaptation to different latitudes and to breed novel soybean cultivars with optimal yield-related traits.