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Summary: Photoperiod‐mediated flowering determines the phenological adaptability of crops including soybean (Glycine max). A genome‐wide association study (GWAS) identified a new flowering time locus, Time of flowering 13 (Tof13), which defined a gene encoding an AP2/ERF transcription factor. This new transcription factor, which we named TOE4b, is localized in the nucleus. TOE4b has been selected for soybean latitude adaptability. The existing natural variant TOE4bH4 was rare in wild soybean accessions but occurred more frequently in landraces and cultivars. Notably, TOE4bH4 improved high‐latitude adaptation of soybean to some extent. The gene‐edited TOE4b knockout mutant exhibited earlier flowering, conversely, TOE4b overexpression delayed flowering time. TOE4b is directly bound to the promoters and gene bodies of the key flowering integration factor genes FT2a and FT5a to inhibit their transcription. Importantly, TOE4b overexpression lines in field trials not only showed late flowering but also altered plant architecture, including shorter internode length, more internodes, more branches and pod number per plant, and finally boosted grain yield per plant by 60% in Guangzhou and 87% in Shijiazhuang. Our findings therefore identified TOE4b as a pleiotropic gene to increase yield potential per plant in soybean, and these results provide a promising option for breeding a soybean variety with an idealized plant architecture that promotes high yields. [ABSTRACT FROM AUTHOR]

Summary: Soybean (Glycine max) is a major source of protein and edible oil world‐wide and is cultivated in a wide range of latitudes. However, it is extremely sensitive to photoperiod, which influences flowering time, maturity, and yield, and severely limits soybean latitude adaptation.In this study, a genome‐wide association study (GWAS) identified a novel locus in accessions harboring the E1 allele, called Time of flowering 8 (Tof8), which promotes flowering and enhances adaptation to high latitude in cultivated soybean. Gene functional analyses showed that Tof8 is an ortholog of Arabidopsis FKF1.We identified two FKF1 homologs in the soybean genome. Both FKF1 homologs are genetically dependent on E1 by binding to E1 promoter to activate E1 transcription, thus repressing FLOWERING LOCUS T 2a (FT2a) and FT5a transcription, which modulate flowering and maturity through the E1 pathway.We also demonstrate that the natural allele FKF1bH3 facilitated adaptation of soybean to high‐latitude environments and was selected during domestication and improvement, leading to its rapid expansion in cultivated soybean. These findings provide novel insights into the roles of FKF1 in controlling flowering time and maturity in soybean and offer new means to fine‐tune adaptation to high latitudes and increase grain yield. [ABSTRACT FROM AUTHOR]

Summary: Flowering time is one of important agronomic traits determining the crop yield and affected by high temperature. When facing high ambient temperature, plants often initiate early flowering as an adaptive strategy to escape the stress and ensure successful reproduction. However, here we find opposing ways in the short‐day crop soybean to respond to different levels of high temperatures, in which flowering accelerates when temperature changes from 25 to 30 °C, but delays when temperature reaches 35 °C under short day. phyA‐E1, possibly photoperiodic pathway, is crucial for 35 °C‐mediated late flowering, however, does not contribute to promoting flowering at 30 °C. 30 °C‐induced up‐regulation of FT2a and FT5a leads to early flowering, independent of E1. Therefore, distinct responsive mechanisms are adopted by soybean when facing different levels of high temperatures for successful flowering and reproduction. [ABSTRACT FROM AUTHOR]

Soybean (Glycine max L.) is a typical photoperiod‐sensitive crop, such that photoperiod determines its flowering time, maturity, grain yield, and phenological adaptability. During evolution, the soybean genome has undergone two duplication events, resulting in about 75% of all genes being represented by multiple copies, which is associated with rampant gene redundancy. Among duplicated genes, the important soybean maturity gene E2 has two homologs, E2‐Like a (E2La) and E2‐Like b (E2Lb), which encode orthologs of Arabidopsis GIGANTEA (GI). Although E2 was cloned a decade ago, we still know very little about its contribution to flowering time and even less about the function of its homologs. Here, we generated single and double mutants in E2, E2La, and E2Lb by genome editing and determined that E2 plays major roles in the regulation of flowering time and yield, with the two E2 homologs depending on E2 function. At high latitude regions, e2 single mutants showed earlier flowering and high grain yield. Remarkably, in terms of genetic relationship, genes from the legume‐specific transcription factor family E1 were epistatic to E2. We established that E2 and E2‐like proteins form homodimers or heterodimers to regulate the transcription of E1 family genes, with the homodimer exerting a greater function than the heterodimers. In addition, we established that the H3 haplotype of E2 is the ancestral allele and is mainly restricted to low latitude regions, from which the loss‐of‐function alleles of the H1 and H2 haplotypes were derived. Furthermore, we demonstrated that the function of the H3 allele is stronger than that of the H1 haplotype in the regulation of flowering time, which has not been shown before. Our findings provide excellent allelic combinations for classical breeding and targeted gene disruption or editing. [ABSTRACT FROM AUTHOR]

Salt stress and flowering time are major factors limiting geographic adaptation and yield productivity in soybean (Glycine max). Although improving crop salt tolerance and latitude adaptation are essential for efficient agricultural production, whether and how these two traits are integrated remains largely unknown. Here, we used a genome‐wide association study to identify a major salt‐tolerance locus controlled by E2, an ortholog of Arabidopsis thaliana GIGANTEA (GI). Loss of E2 function not only shortened flowering time and maturity, but also enhanced salt‐tolerance in soybean. E2 delayed soybean flowering by enhancing the transcription of the core flowering suppressor gene E1, thereby repressing Flowering Locus T (FT) expression. An E2 knockout mutant e2CR displayed reduced accumulation of reactive oxygen species (ROS) during the response to salt stress by releasing peroxidase, which functions in ROS scavenging to avoid cytotoxicity. Evolutionary and population genetic analyses also suggested that loss‐of‐function e2 alleles have been artificially selected during breeding for soybean adaptation to high‐latitude regions with greater salt stress. Our findings provide insights into the coupled selection for adaptation to both latitude and salt stress in soybean; and offer an ideal target for molecular breeding of early‐maturing and salt‐tolerant cultivars. [ABSTRACT FROM AUTHOR]

Photoperiod responsiveness is a key factor limiting the geographic distribution of cultivated soybean and its wild ancestor. In particular, the genetic basis of the adaptation in wild soybean remains poorly understood. In this study, by combining whole-genome resequencing and genome-wide association studies we identified a novel locus, Time of Flowering 5 (Tof5), which promotes flowering and enhances adaptation to high latitudes in both wild and cultivated soybean. By genomic, genetic and transgenic analyses we showed that Tof5 encodes a homolog of Arabidopsis thaliana FRUITFULL (FUL). Importantly, further analyses suggested that different alleles of Tof5 have undergone parallel selection. The Tof5 H1 allele was strongly selected by humans after the early domestication of cultivated soybean, while Tof5 H2 allele was naturally selected in wild soybean, and in each case facilitating adaptation to high latitudes. Moreover, we found that the key flowering repressor E1 suppresses the transcription of Tof5 by binding to its promoter. In turn, Tof5 physically associates with the promoters of two important FLOWERING LOCUS T (FT), FT2a and FT5a, to upregulate their transcription and promote flowering under long photoperiods. Collectively, our findings provide insights into how wild soybean adapted to high latitudes through natural selection and indicate that cultivated soybean underwent changes in the same gene but evolved a distinct allele that was artificially selected after domestication. This study reveals that different alleles of Tof5 have undergone parallel selection in wild and cultivated soybean. The transcription of Tof5 is directly regulated by soybean key flowering suppressor E1. In turn, Tof5 protein physically associates with the promoters of FT homologs to enhance their transcription and improve adaptation to high latitudes in both wild and cultivated soybean. [ABSTRACT FROM AUTHOR]

Soybean (Glycine max) serves as a major source of protein and edible oils worldwide. The genetic and genomic bases of the adaptation of soybean to tropical regions remain largely unclear. Here, we identify the novel locus Time of Flowering 16 (Tof16), which confers delay flowering and improve yield at low latitudes and determines that it harbors the soybean homolog of LATE ELONGATED HYPOCOTYL (LHY). Tof16 and the previously identified J locus genetically additively but independently control yield under short-day conditions. More than 80% accessions in low latitude harbor the mutations of tof16 and j, which suggests that loss of functions of Tof16 and J are the major genetic basis of soybean adaptation into tropics. We suggest that maturity and yield traits can be quantitatively improved by modulating the genetic complexity of various alleles of the LHY homologs, J and E1. Our findings uncover the adaptation trajectory of soybean from its temperate origin to the tropics. How soybean, a temperate origin crop, adapted to a tropical environment remains unclear. Here, the authors report Tof16, an ortholog of LHY, and the previously identified J locus, control soybean yield under short-day condition and loss of function of these two genes contributes to the adaptation to tropics. [ABSTRACT FROM AUTHOR]

Flowering time and stem growth habit determine inflorescence architecture in soybean, which in turn influences seed yield. Dt1, a homolog of Arabidopsis TERMINAL FLOWER 1 (TFL1), is a major controller of stem growth habit, but its underlying molecular mechanisms remain unclear. Here, we demonstrate that Dt1 affects node number and plant height, as well as flowering time, in soybean under long‐day conditions. The bZIP transcription factor FDc1 physically interacts with Dt1, and the FDc1‐Dt1 complex directly represses the expression of APETALA1 (AP1). We propose that FT5a inhibits Dt1 activity via a competitive interaction with FDc1 and directly upregulates AP1. Moreover, AP1 represses Dt1 expression by directly binding to the Dt1 promoter, suggesting that AP1 and Dt1 form a suppressive regulatory feedback loop to determine the fate of the shoot apical meristem. These findings provide novel insights into the roles of Dt1 and FT5a in controlling the stem growth habit and flowering time in soybean, which determine the adaptability and grain yield of this important crop. [ABSTRACT FROM AUTHOR]

Flowering time and plant height are key agronomic traits that directly affect soybean (Glycine max) yield. APETALA1 (AP1) functions as a class A gene in the ABCE model for floral organ development, helping to specify carpel, stamen, petal, and sepal identities. There are four AP1 homologs in soybean, all of which are mainly expressed in the shoot apex. Here, we used clustered regularly interspaced short palindromic repeats (CRISPR) – CRISPR‐associated protein 9 technology to generate a homozygous quadruple mutant, gmap1, with loss‐of‐function mutations in all four GmAP1 genes. Under short‐day (SD) conditions, the gmap1 quadruple mutant exhibited delayed flowering, changes in flower morphology, and increased node number and internode length, resulting in plants that were taller than the wild type. Conversely, overexpression of GmAP1a resulted in early flowering and reduced plant height compared to the wild type under SD conditions. The gmap1 mutant and the overexpression lines also exhibited altered expression of several genes related to flowering and gibberellic acid metabolism, thereby providing insight into the role of GmAP1 in the regulatory networks controlling flowering time and plant height in soybean. Increased node number is the trait with the most promise for enhancing soybean pod number and grain yield. Therefore, the mutant alleles of the four AP1 homologs described here will be invaluable for molecular breeding of improved soybean yield. [ABSTRACT FROM AUTHOR]

Flowering time is an important factor that controls crop yield and latitudinal adaptation. Soybean is a facultative short-day (SD) plant, and cultivars that originate from temperate regions generally undergo a very short juvenile phase and early flowering when grown in low-latitude regions, thereby resulting in extremely low grain yield. However, introduction of the long-juvenile (LJ) trait, which extends the vegetative phase and improves yield under SD environments, has largely overcome this constraint and has enabled the expansion of soybean production to tropical regions. Quantitative trait locus (QTL) mapping is a fundamental approach to the identification of new loci related to LJ trait, while conventional strategy takes lots of time to verify the findings. Here, we provide a new strategy to rapidly identify consistent novel QTLs by using multiple genetic populations and genotyping-by-sequencing (GBS) approach. In this study, we developed six F2 populations and grew them under SD conditions. A total of seven QTLs related to the LJ trait were identified by integrating flowering time (R1) and high-density genetic maps. There were three consistent QTLs repeatedly detected in different populations and one of them has been previously reported, yet two are novel. This research not only provides fundamental resources for fine-mapping candidate genes associated to the LJ trait, but also provides new insights to QTL mapping. [ABSTRACT FROM AUTHOR]

In many plants, flowering time is influenced by daylength as an adaptive response. In soybean (Glycine max) cultivars, however, photoperiodic flowering reduces crop yield and quality in high-latitude regions. Understanding the genetic basis of wild soybean (Glycine soja) adaptation to high latitudes could aid breeding of improved cultivars. Here, we identify the Tof4 (Time of flowering 4) locus, which encodes by an E1-like protein, E1La, that represses flowering and enhances adaptation to high latitudes in wild soybean. Moreover, we found that Tof4 physically associates with the promoters of two important FLOWERING LOCUS T (FT2a and FT5a) and with Tof5 to inhibit their transcription under long photoperiods. The effect of Tof4 on flowering and maturity is mediated by FT2a and FT5a proteins. Intriguingly, Tof4 and the key flowering repressor E1 independently but additively regulate flowering time, maturity, and grain yield in soybean. We determined that weak alleles of Tof4 have undergone natural selection, facilitating adaptation to high latitudes in wild soybean. Notably, over 71.5% of wild soybean accessions harbor the mutated alleles of Tof4 or a previously reported gain-of-function allele Tof5 H2 , suggesting that these two loci are the genetic basis of wild soybean adaptation to high latitudes. Almost no cultivated soybean carries the mutated tof4 allele. Introgression of the tof4-1 and Tof5 H2 alleles into modern soybean or editing E1 family genes thus represents promising avenues to obtain early-maturity soybean, thereby improving productivity in high latitudes. [Display omitted] • A new locus Tof4 controlling flowering time in wild soybean was identified by GWAS • Mutant alleles of Tof4 facilitate the adaptation of wild soybean to high latitudes • Tof4 directly binds to the promoters of FT2a and FT5a to control maturity in soybean • Tof4 and Tof5 H2 form the genetic basis of wild soybean adaptation to high latitudes Identification of genes or alleles from wild soybean to introgress into modern elite cultivars will improve soybean productivity. Dong et al. show that Tof4 has undergone natural selection in wild soybean and facilitated adaptation to high latitudes. This study provides a new approach for precision breeding of early-maturity soybean varieties. [ABSTRACT FROM AUTHOR]