Understanding the molecular mechanisms of flowering and maturity is important for improving the adaptability and yield of seed crops in different environments. In soybean, a facultative short-day plant, genetic variation at four maturity genes, E1 to E4, plays an important role in adaptation to environments with different photoperiods. However, the molecular basis of natural variation in time to flowering and maturity is poorly understood. Using a cross between early-maturing soybean cultivars, we performed a genetic and molecular study of flowering genes. The progeny of this cross segregated for two maturity loci, E1 and E9. The latter locus was subjected to detailed molecular analysis to identify the responsible gene. Fine mapping, sequencing, and expression analysis revealed that E9 is FT2a, an ortholog of Arabidopsis FLOWERING LOCUS T. Regardless of daylength conditions, the e9 allele was transcribed at a very low level in comparison with the E9 allele and delayed flowering. Despite identical coding sequences, a number of single nucleotide polymorphisms and insertions/deletions were detected in the promoter, untranslated regions, and introns between the two cultivars. Furthermore, the e9 allele had a Ty1/copia–like retrotransposon, SORE-1, inserted in the first intron. Comparison of the expression levels of different alleles among near-isogenic lines and photoperiod-insensitive cultivars indicated that the SORE-1 insertion attenuated FT2a expression by its allele-specific transcriptional repression. SORE-1 was highly methylated, and did not appear to disrupt FT2a RNA processing. The soybean maturity gene E9 is FT2a, and its recessive allele delays flowering because of lower transcript abundance that is caused by allele-specific transcriptional repression due to the insertion of SORE-1. The FT2a transcript abundance is thus directly associated with the variation in flowering time in soybean. The e9 allele may maintain vegetative growth in early-flowering genetic backgrounds, and also be useful as a long-juvenile allele, which causes late flowering under short-daylength conditions, in low-latitude regions.

Photoperiodism is a rhythmic change of sensitivity to light, which helps plants to adjust flowering time according to seasonal changes in daylength and to adapt to growing conditions at various latitudes. To reveal the molecular basis of photoperiodism in soybean (Glycine max), a facultative short-day plant, we analyzed the transcriptional profiles of the maturity gene E1 family and two FLOWERING LOCUS T (FT) orthologs (FT2a and FT5a). E1, a repressor for FT2a and FT5a, and its two homologs, E1-like-a (E1La) and E1Lb, exhibited two peaks of expression in long days. Using two different approaches (experiments with transition between light and dark phases and night-break experiments), we revealed that the E1 family genes were expressed only during light periods and that their induction after dawn in long days required a period of light before dusk the previous day. In the cultivar Toyomusume, which lacks the E1 gene, virus-induced silencing of E1La and E1Lb up-regulated the expression of FT2a and FT5a and led to early flowering. Therefore, E1, E1La, and E1Lb function similarly in flowering. Regulation of E1 and E1L expression by light was under the control of E3 and E4, which encode phytochrome A proteins. Our data suggest that phytochrome A-mediated transcriptional induction of E1 and its homologs by light plays a critical role in photoperiodic induction of flowering in soybean.

Precise timing of flowering is critical to crop adaptation and productivity in a given environment. A number of classical E genes controlling flowering time and maturity have been identified in soybean [Glycine max (L.) Merr.]. The public availability of the soybean genome sequence has accelerated the identification of orthologues of Arabidopsis flowering genes and their functional analysis, and has allowed notable progress towards understanding the molecular mechanisms of flowering in soybean. Great progress has been made particularly in identifying genes and modules that inhibit flowering in long-day conditions, because a reduced or absent inhibition of flowering by long daylengths is an essential trait for soybean, a short-day (SD) plant, to expand its adaptability toward higher latitude environments. In contrast, the molecular mechanism of floral induction by SDs remains elusive in soybean. Here we present an update on recent work on molecular mechanisms of flowering under long days and of stem growth habit, outlining the progress in the identification of genes responsible, the interplay between photoperiod and age-dependent miRNA-mediated modules, and the conservation and divergence in photoperiodic flowering and stem growth habit in soybean relative to other legumes, Arabidopsis, and rice (Oryza sativa L.).

FLOWERING LOCUS T (FT) is an important floral integrator whose functions are conserved across plant species. In soybean, two orthologs, FT2a and FT5a, play a major role in initiating flowering. Their expression in response to different photoperiods is controlled by allelic combinations at the maturity loci E1 to E4, generating variation in flowering time among cultivars. We determined the molecular basis of a quantitative trait locus (QTL) for flowering time in linkage group J (Chromosome 16). Fine-mapping delimited the QTL to a genomic region of 107kb that harbors FT5a. We detected 15 DNA polymorphisms between parents with the early-flowering (ef) and late-flowering (lf) alleles in the promoter region, an intron, and the 3′ untranslated region of FT5a, although the FT5a coding regions were identical. Transcript abundance of FT5a was higher in near-isogenic lines for ef than in those for lf, suggesting that different transcriptional activities or mRNA stability caused the flowering time difference. Single-nucleotide polymorphism (SNP) calling from re-sequencing data for 439 cultivated and wild soybean accessions indicated that ef is a rare haplotype that is distinct from common haplotypes including lf. The ef allele at FT5a may play an adaptive role at latitudes where early flowering is desirable.

Photoperiod response of flowering determines plant adaptation to different latitudes. Soybean, a short-day plant, has gained the ability to flower under long-day conditions during the growing season at higher latitudes, mainly through dysfunction of phytochrome A genes (E3 and E4) and the floral repressor E1. In this study, we identified a novel molecular genetic basis of photoperiod insensitivity in Far-Eastern Russian soybean cultivars. By testcrossing these cultivars with a Canadian cultivar Harosoy near-isogenic line for a recessive e3 allele, followed by association tests and fine mapping, we determined that the insensitivity was inherited as a single recessive gene located in an 842-kb interval in the pericentromeric region of chromosome 4, where E1-Like b (E1Lb), a homoeolog of E1, is located. Sequencing analysis detected a single-nucleotide deletion in the coding sequence of the gene in insensitive cultivars, which generated a premature stop codon. Near-isogenic lines (NILs) for the loss-of-function allele (designated e1lb) exhibited upregulated expression of soybean FLOWERING LOCUS T (FT) orthologs, FT2a and FT5a, and flowered earlier than those for E1Lb under long-day conditions in both the e3/E4 and E3/E4 genetic backgrounds. These NILs further lacked the inhibitory effect on flowering by far-red light–enriched long-day conditions, which is mediated by E4, but not that of red-light–enriched long-day conditions, which is mediated by E3. These findings suggest that E1Lb retards flowering under long-day conditions by repressing the expression of FT2a and FT5a independently of E1. This loss-of-function allele can be used as a new resource in breeding of photoperiod-insensitive cultivars, and may improve our understanding of the function of the E1 family genes in the photoperiod responses of flowering in soybean.