Genetic mechanisms underlying the expansion of soybean Glycine max (L.) Merr. cultivation to the north

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Abstract

Soybean [Glycine max (L.) Merr.] is produced in 93 countries of the world on 120.5 million hectares. The production area of the crop is located between 56°N. (Russian Federation) and 35-37°S (Argentina). In the gene pool of the crop, there is a wide variety of genotypes of different maturity groups, which every has a relatively narrow latitudinal adaptability, which depends on heat and moisture supply and the duration of photoperiod. An urgent problem of our time is the creation of early maturated varieties which allow to expand soybean cultivation to the north. In soybean 12 major loci (E1–E11 and J) have been identified, which control the flowering initiation and the response to the photoperiod. The time of maturation, photothermal response and, ultimately, the adaptation of the crop to different latitudes also depend on various allelic combinations and the interaction of these loci. All these loci have been mapped, and for some of them genes have been identified, their allelic diversity has been characterized and the mechanisms of their functioning and interaction have been described. But the molecular-genetic nature of the early maturity of soybean has not yet been revealed in detail. This review presents the current understanding of the structure and nature of the interaction of molecular genetic determinants of early maturity of soybean, which regulate the timing of its flowering and maturation at different photoperiods and their influence on other plant traits, including the type of growth and productivity. As a result, an idea of the optimal genotype for northern latitudes was proposed, with a combination of alleles providing the earliest flowering and maturation in relatively northern regions with a long day.

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BACKGROUND

Soybean [Glycine max (L.) Merr.] are grown in a wide range of geographic latitudes in both hemispheres of the globe, spanning more than 120.5 million hectares in 93 countries [1]. The modern boundaries of soybean range are 56° north in the Russian Federation and 35–37° south in Argentina. Soybean was first domesticated in Northeast China, in the southern part of its temperate climate zone [2]. From there, soybean cultivation spread to the north and south, with the species developing adaptations to different agro-climatic parameters

The main limiting factors affecting soybean production at different latitudes are temperature, moisture supply, and daylight hours [3–5]. Expansion of soybean to the north, termed northering, is the result of creation of early – matureted varieties. Northering poses a significant challenge because soybean is a short-day plant with a strong photoperiodic sensitivity (PS). Longer daylight exposures can cause delayed onset of flowering, especially in the most photoperiod-sensitive varieties. These plants remain at the vegetative stage, resulting in enhanced growth of the vegetative mass. In contrast, some varieties have a weak or almost absent PS [6].

The reverse of northering is the expansion of soybean into tropical latitudes, where most varieties have drastically reduced prebloom period, growth, and seed production. The introduction of the long juvenile (LJ) period trait into varieties in the late 1970s played a key role in the expansion of soybean in these regions [7, 8].

Therefore, when searching for soybean varieties for expansion to higher latitudes, it is necessary to identify the genetic determinants of photoperiod sensitivity / insensitvity. This work aimed to review the genetic mechanisms that determine soybean early maturation, which can guide the expansion of soybean cultivation to the north.

Diversity of the soybean gene pool coding for maturing terms and photoperiod sensitivity.

There are two main classification systems used to classify soybean varieties. The International Descriptor of the Council for Mutual Economic Assistance [9] and the United States classification. The former is used by N.I. Vavilov All-Russian Institute of Plant Genetic Resources (Russia). According to this scheme, soybean varieties take from 80 to 150 or more days from germination to maturation [9].

The US classification scheme recognizes 13 groups of soybeans varieties according to time to maturity, which corresponds to the latitudinal production of different varieties. Initially, only seven maturity groups (MGI–VII) were recognized based on the existing gene pool. Three more groups were added (MG0, MG00, MG000) as soon as early maturated varieties were created for northering in the US and Canada. For cultivation toward ower southern latitudes, the three maturity groups were introduced (MGVIII–X). In the US collection, MG000 included 147 accessions, 536 accessions in MG00, 1176 in MG0,1745 in MGI, 2071 in MGII, 1985 in MGIII, 4108 in MGIV, 2721 in MGV, 1551 in MGVI, 944 in MGVII, 913 in MGVIII, none in MGIX, and in MGX [10]. Identification of accessions that mature earlier than MG000 in North China and the Amur region of Russia led to the proposal of another early maturity rank, MG0000. It was proposed to call them as varieties of high-latitude cold regions [11].

It should be noted that it is not easy to reconcile the American and Russian classifications because specific varieties have a limited latitudinal range that depends on the photoperiod and the sum of active temperatures in a particular latitude. Furthermore, the northern limits of soybean cultivation in the US, China, and the Russian Federation are different. The soybean belt in the US ranges from latitudes 27–49° N, with its northern boundary located just at the latitude of Volgograd.

There is a great variation in the soybean gene pool for day length sensitivity. The International Descriptor distinguishes five groups of PS, from very high to very low [9]. The VIR soybean collection includes 7,000 accessions of cultivated soybean, with 2,500 accessions in the Krasnodar Territory characterized as early- maturated (maturing for a period of up to 110 days). Of these, more than 2,000 accessions from 43 countries of the world were tested in a field experiment in the Leningrad province. Only 400 accessions (from 33 countries) were able to form viable seeds under these conditions, indicating their weak PS and low heat requirements [6].

The PS coefficient is calculated as the ratio of the duration of the period from germination to flowering on a natural long day (LD) and the duration of the same transition on a short-day (SD). In a photoperiodic experiment performed in the Leningrad region, the PS coefficient varied from 1.0 to 2.4 (LD length can reach up to 18 h 46 min, while SDs last for 12h.). Of the 94 accessions studied, 35 had the lowest PS (1.0 to 1.15). These include the Svetlaya variety, which was created in the Ryazan region, and the experimental accessions PEP 17 and PEP 18, which were created in the Leningrad region as a result of repeated selections [12].

Genes that determine soybean early – maturity

To date, researchers have identified 12 loci that control the time of flowering and maturation in soybean: E1–E11 and J. E1, E2, and E3 were first described in the 1970s [13, 14], E4 and E5 in the 1980s [15, 16], E6 and J in the 1990s [17, 18]. At the beginning of the 2000s, the E7 gene was described [19], while the E8, E9, and E10 genes were later described from 2010 to 2017 [20–24]. E11 was reported only recently, in 2019 [25]. Their loci on the chromosomes have been mapped [26]. The alleles of E1–E4, E9, and E10 genes have been characterized and the molecular mechanisms of their functions have been described [24, 27, 28].

In 2010, the genome of the soybean (G. max) American variety Williams 82 was sequenced. It is contained in 20 chromosomes (2n = 40). The soybean genome size is 1115 Mb [29], with 85% of the base pairs annotated. About 78% of the genes are located in the distal regions of the chromosomes, which represents less than half of the entire genome but is responsible for almost all genetic recombination.

Sequencing revealed that soybean are paleopolyploid. The genome of the hypothetical soybean ancestor underwent two genome-wide duplications 59 and 13 million years ago, causing almost 75% of the genes to have several copies in the genome. Homologous blocks containing an average of 75 genes (8 to 1377) are noted in two or three chromosomes, with most genes having a homologous copy. Besides duplication, the soybean genome underwent diversification, gene loss, and numerous chromosomal rearrangements, resulting in a present genome organized as in diploid organisms [30]. Wild soybean (G. soja Sieb. et Zucc.) is paleopolyploid, with its genome differing from cultivated soybean by no more than 0.31% [31]. These duplication and diversification events in the genome are thought to have paved the way for the emergence of flexible and diverse phenotypes related to flowering onset under various environmental conditions.

In addition to annotated genes, numerous quantitative trait loci (QTLs) that control the timing of flowering and maturing have been identified. In the 1990s, the relationship of certain QTLs with the temporal regulation of soybean maturity was established [32, 33], with some of these QTLs possessing pleiotropic effects on flowering, maturing, and morphological traits [34]. These efforts were continued in the first decade of the 21st century, which revealed the QTLs that were critical in determining the timing of flowering and maturing [35] and other pleiotropic effects by QTLs QTLs binding to chromosome sites was show, as well as dependence of different traits (time of maturation, seed pigmentation, cleistogamous pollination in buds) from the same QTLs [36–42]. Other studies have shown the ability to compare genes оf PS and QTLs determining the flowering and maturing time [43–45]. It has been shown that different QTLs can perform similar control of flowering time in varieties of different origin [46–49]. The main QTL that determines the delay of flowering in wild soybean has the same effect in cultivated varieties (in interspecific cross-breeding) [50]. The corresponding QTLs for the gene extending the juvenile stage were also identified [51].

The set of genes that control flowering time is evolutionarily conserved. Using the model plants Arabidopsis and Oryza, great progress has been made in understanding the mechanisms that control flowering in response to seasonal changes in day length and temperature [52–54]. For Arabidopsis, a database has been created that includes more than 300 genes that regulate flowering time [55]. In the soybean genome, 844 genes were identified through their homology to Arabidopsis genes and candidate genes were revealed for QTLs that control flowering [26, 56, 57]. Analyses of nucleotide polymorphism were used to develop allele-specific markers for genotyping E1–E4 [58–62], E7 [63], E8 [64], E9 [22], E10 [24, 65], and J [66, 67] (Fig. 1).

 

Fig. 1. The distribution of candidate genes that determine the onset of flowering and associated QTLs in the soybean genome. Columns represent soybean chromosomes. Areas containing QTLs are marked in gray, whereas darker areas indicate overlaps between different QTLs. The E1, E2, E3, E7, E8, E9, and J loci are on the left side of the chromosomes, with the corresponding molecular markers in black. Question marks next to the loci indicate that the corresponding genes for these QTLs remain unknown. The blue lines on the chromosomes indicate the position of the soybean orthologs of flowering genes in Arabidopsis. Orthologs located in the QTL are labeled as Arabidopsis gene symbols in blue, and red letters denote the characterized genes corresponding to the QTL (according to Zhang et al., 2017 [26]).

 

These genes and QTLs have different effects on soybean flowering and play various roles in the photoperiodic response [68, 69]. Their interactions with each other and the environment strongly influence the temp of flowering and maturing, morphology, productivity, and tolerance to stressors. The vegetation period is the total time of plant development and is divided into the vegetative and reproductive stages. The duration of these individual stages varies with temperature and photoperiod [70, 71]. These indicate that adaptation to the place of cultivation involves fine-tuning of the soybean genetic apparatus. To precisely coordinate the soybean agricultural cycle to the duration of plant development specific to a local climate, it is necessary to take advantage of the genetic variability available in the gene pool.

In 2010, an atlas of the soybean transcriptome was created [72], cDNA of 57,352 genes from 14 different soybean tissues were sequenced, revealing tissue-specific differences in the expression levels of various genes. The soybean gene expression atlas is used in comparative studies with plant model organisms, such as Medicago truncatula Gaertn., Lotus japonicus (Regel) K. Larsen, Arabidopsis thaliana (L.) Heynh. [73].

Molecular genetic mechanisms that determine the time of flowering and maturation in soybean

Dominant alleles at the E1–E4, E7, E8, and E10 loci delay flowering and maturation, while dominant alleles at the E6, E9, E11, and J loci, on the contrary, promote early flowering.

E1 gene. Among the identified genes, E1 exhibits the most pronounced effect on the initiation of flowering [28, 68, 74]. It is located on chromosome 6 and encodes a legume-specific transcription factor containing a B3 domain that acts as a repressor of flowering. Six E1 alleles, e1-as, e1-fs, e1-n1, e1-re, and e1-p [27, 28], have been identified. Two of these, e1-nl and e1-fs, are non-functional alleles associated with early flowering under LD conditions [27, 75]. On the other hand, the effects of e1-re and e1-p alleles on flowering have not been determined [28]. Non-functional E1 alleles were intensively selected in the northern latitudes of Asia, particularly in northern and northeastern China and northern USA [27, 76].

In a study by Z.Xia et al. [27], accessions with the e1-as allele exhibited a flowering period intermediate between the active E1 and the inactive e1 alleles. Thus, e1-as was determined as partially preserved E1 allele function. The partially functional e1-as allele has consistently been detected in early- and mid- maturated cultivars (MG000–MGIV), including cultivars adapted to northern latitudes [77].

In the soybean genome, two E1 homologs were revealed (E1-La and E1-Lb). These are located in the centromeric region of chromosome 4, a region homologous to chromosome 6. The E1-L genes inhibit flowering by downregulating FT (Flowering locus T) gene. The E1-L genes expression exert weaker effects than E1 [78]. The non-functional e1-lb allele carries a single nucleotide deletion in the coding region and determines insensitivity to photoperiod independently of the E1 gene. This allele is present among varieties of the Russian Far East that are weakly sensitive to photoperiod [79].

The expression of E1, E1La, and E1Lb are activated under LD conditions and strongly inactivated under SD. SD-induced down regulation of these genes depends on the duration of the dark phase. This interruption leads to gene reactivation and, as a result, late flowering [27, 78, 80].

In Arabidopsis and Oryza, E1 homologs have not been identified [27]. Meanwhile, the E1 homolog in M. truncatula (MtEL1) was shown to inhibit flowering but another homolog in Phaseolus vulgaris L. (PvE1L) does not affect blooming [81].

E2 gene. E2 is the second most important gene for regulating the PS of flowering. It is one of three soybean orthologs of the Arabidopsis GIGANTEA gene (GmGIa, GmGIb, andGmGIc) [60]. GmGIa (E2) is involved in the regulation of the circadian rhythm and flowering processes, causing late flowering during LD [60, 82].

The recessive allele e2-ns has a nonsense mutation, resulting in a premature stop codon. In varieties with the e2e2 genotype, a response to light exposure was noted. This can be interpreted as a compensatory function of the other orthologs or the non-involvement of E2 in the light-sensitive control of photoperiodism [78]. In population genetic studies done in China, three E2 haplotypes (non-functional H1 and functional H2 and H3) were identified in both G. max (GmGIa) breeding varieties and G. soja (GsGIa) wild soybean accessions. The H1 haplotype bears a stop codon in exon 10 and is the most common haplotype in China [82]. This haplotype showed the greatest effect in early flowering and may have contributed to the spread of the domesticated soybean.

E3 and E4 genes. The E3 and E4 genes encode the phytochrome A isoforms GmPhyA3 and GmPhyA2. These control flowering at high and low red light to far red (R/FR) ratios, respectively. High R/FR ratios occur under direct sunlight, while low R/FR ratios occur at dusk, sunset, and sunrise or under a shade. A high R/FR value under LD conditions increases the effects of E3 alleles, while a low R/FR activates E4 [19, 58, 59, 83]. Non-functional alleles of the E3 and E4 loci emerged recently and independently in different East Asian soybean cultivars [61, 84].

The dominant alleles E3 and E4 activate the expression of E1 and cause late flowering under both SD and LD conditions. The recessive alleles e3 and e4 control insensitivity to LD and lead to an increase in the expression of FT genes, which contributes to flowering under LD [58, 59, 78].

GmPHYA4, E3 homolog, and GmPHYA1, E4 homolog, are genes in the phytochrome A (PHYA) family that have been identified in the soybean [26, 58, 59, 85]. Their functions are not completely understood. Inactive GmphyA1 alleles have been shown to control photoperiod insensitivity under LD conditions [58, 86].

E5 locus. The E5 locus slows down flowering and maturation during LD [16]. Based on QTL analysis, E5 shares a similar location as E2. When mapping the E5 locus, the F2 population did not split in an expected manner, casting doubt on the existence of the E5 gene and supporting the argument that it is merely E2 [87].

E6 and J loci. The E6 and J loci are mapped on chromosome 4 and are closely linked [66, 67, 88]. The dominant E6E6 genotype codes early flowering and maturation. The mechanisms of E6 function are poorly understood and a candidate gene has not yet been identified. The E6 locus downregulates E1expression, affecting the active E1 allele more than the e1-as allele. In turn, the E6 activity depends on the active E1 allele (that is, the dominant E1 allele has an epistatic effect on E6). In plants with the e1-ts/e1-fsge no type, the E6-mediated control over flowering is lost [22, 88].

The J locus is an ortholog of the Arabidopsis Early Flowering 3 (ELF3) gene [66, 89]. ELF3 is a highly conserved plant nuclear protein that is crucial in maintaining circadian rhythms and controlling flowering time in several species, including Arabidopsis and various crops. In LD plants, such as Arabidopsis, the ELF3 gene delays flowering by indirectly downregulating the key flowering activator FT and its main targets [90]. In comparison, ELF3 induces flowering in SD plants by decreasing the expression of key FT repressors (primarily E1 in soybean).

The active J allele controls early flowering of soybean. The inactive allele j is responsible for the LJ trait, which is characterized by late flowering and high productivity under SD conditions. J has six non-functional alleles, j1–6, and two weak alleles, j7–8. The ELF3 protein binds to the E1 gene promoter and represses E1 transcription. This weakens the repression of two important FT genes (GmFT2a, GmFT5a) and promotes early flowering under SD conditions. When the J allele is attenuated, E1 expression becomes unrepressed, resulting in FT downregulation and a prolonged vegetative phase. J functions in the signalling cascade downstream of E3 and E4. In turn, phytochrome proteins PHYA (E3, E4) downregulate J expression in SD [66].

E7 locus. E7 is a late flowering and maturation locus. However, it has the weakest effect on delayed flowering. It was identified under LD condition, with the E7E7 plants characterized by late flowering. E7 has been mapped to chromosome 6, 6.2 cM away from the E1 locus [19, 26]. Markers for the E7 locus are Satt100, Satt319, and Satt460 [63]. This region contains eight homologs of flowering genes, including two homologs of SPA1, a key regulator of the PHYA signal transduction pathway. These two homologs, Glyma06G241900 and Glyma06G242100, are presumed to be candidates for the E7 gene [26].

E8 locus. The e8 locus contributes to the inhibition of flowering. Varieties with the E8E8 genotype exhibit late maturation, while varieties with inactive e8e8 alleles are characterized by early – maturation. E8 is mapped to the pericentromeric region of chromosome 4 [26, 65]. This region contains six flowering genes, including the homolog of the E1 gene (E1Lb). These genes are suitable candidates for E8. This region also contains the QTL responsible for the duration of the reproductive period (QTL 3–4, QTL 2–2), whose phenotypic expression can be influenced by E8 [20, 78].

E8 may also be associated with the expression of the qRP-c-1 locus, located in a small region of 1.8 cM in the C1 linkage group between the markers Sat_404 and Satt136. The closest marker to both loci is Sat_085 [20, 38], which, in turn, is closely associated with the GmCRY1a gene [91, 92]. GmCRY1a controls the production of cryptochromes, which presumably mediate light-regulated plant development and growth and is involved in the regulation of soybean flowering onset [93]. Therefore, qRP-c-1 is most probably associated with GmCRY1a and plays an important role in soybean development during the reproductive period [45].

E9 gene. E9 causes early flowering and maturation. It was mapped to chromosome 16 and identified as an ortholog of the Arabidopsis FT (GmFT2a) gene. In Arabidopsis, FT is a key flowering activator. Soybean has twelve FT homologs [94, 95]. Six of these genes have been experimentally shown to activate flowering in the ft-mutant of Arabidopsis. Their expression profiles vary by tissue and growth stage, indicating their functional specialization during soybean flowering.

Two of these homologs, FT2a and FT5a, were studied for their role in photoperiod changes. GmFT5a promotes early flowering in LD, while GmFT2a promotes early flowering in SD [94–96]. Different levels of FT2a and FT5a co-expression directly regulate the natural variation in soybean flowering time [96]. A total of 17 polymorphic sites were revealed in GmFT2a (10 SNPs, 2 insertions, 5 SSRs). In early-maturated varieties, three alleles were identified (FT2a-TO, FT2a-HA, FT2a-HY). The FT2a-TO allele has a 10-bp deletion in the 5'-UTR promoter region, and SNP do not affect expression levels. In the first intron, an insertion of the SORE-1 retrotransposon weakens gene expression and delays flowering [22]. CRISPR-induced mutants of GmFT2a show delayed flowering under both LD and SD conditions [97]. Thirteen GmFT5a haplotypes and seven GmFT2a haplotypes were identified, of which GmFT5a-Hap2/GmFT2a-Hap2 plants exhibited the earliest flowering [96]. Nevertheless, flowering induction by FT proteins can start regardless of the amount of GmFT2a and GmFT5a transcripts.

The GmFT2a and GmFT5a photoperiod responses occur via distinct mechanisms. GmFT2a expression is strictly regulated by photoperiodic changes and is activated immediately in SD. In contrast, GmFT5a expression changes in response to the photoperiod are gradual. GmFT5a expression is initially retained at a low level, even under conditions of LD and is activated only later during development [21, 94].

Products of GmFT2a and GmFT5a have florigen-like functions, i.e., they accelerate the onset of flowering. The GmFT2a and GmFT5a proteins interact with the bZIP GmFDL19 transcription factor, which can bind to the ACGT cis-element of the GmAP1 promoter. Furthermore, the FT/FD complex triggers the transformation of the vegetative meristem into the floral meristem by activating the expression of the flower formation gene homologs APETALA1 (GmAP1) and LEAFY (GmLFY) and GmSOC1. The soybean homolog GmAP1 is expressed in the flower, especially in the sepals and petals. GmFDL19 may function as a key component in the photoperiod-regulated flowering pathway controlled by GmFT2a and GmFT5a. Expression of FT2aand FT5a is regulated by the E1 locus (PHYA-mediated photoperiod-dependent regulation, E1-PHYA pathway) and its homologs (E1La, E1Lb), which, in turn, are controlled by the E3 and E4 loci [23, 27, 78, 94].

Under LD conditions, E2 inhibits FT2a expression, probably through the GI-Co pathway, resulting in late flowering. Soybean has 26 Co-like genes (CONSTANS), of which four (GmCOL1a, GmCOL1b, GmCOL2a, GmCOL2b) have the greatest sequence similarity with Arabidopsis Co-genes [23]. GmCOL1a and GmCOL1b are key activators of flowering in SD, while they increase the expression of GmFT5a in the morning hours and are repressors in LD [98]. The mechanisms of GI–Co module function in the regulation of FT genes are poorly understood. E2 was shown to have no influence on the expression of GmFT5a. Thus, GmFT2a and GmFT5a show both similarities and differences in their regulatory pathways [96, 98].

The GmFT1a gene is expressed in leaves and is activated under LD conditions to inhibit flowering and maturation [50]. It supports vegetative growth in soybean, an effect that is diametrically opposed to that of GmFT2a and GmFT5a.

The GmFT2b gene has a high homology with GmFT2a. Its overexpression promotes flowering under LD conditions, while the inactive allele inhibits flowering only under LD conditions. For GmFT2b, 4 haplotypes (Hap1–4) were identified, with Hap3 showing the earliest flowering. GmFT2b activates GmFT2a and GmFT5a under conditions of LD [99].

Recently, a clear role of GmFT2b-ox in accelerating the onset of flowering in soybeans was demonstrated under LD conditions [99]. It has been posited that this stimulating effect occurs by upregulating the flowering activating genes GmFT2a/2b.

E10 locus. The E10 locus was mapped to chromosome 8. A candidate gene, FT4, was revealed in the E10 locus [24]. FT4 is expressed in parallel with E1 but functions downstream of E1 as a repressor of soybean flowering [100]. It is activated by LD, resulting in late flowering, while it is blocked under SD conditions, resulting in early flowering.

Several SNPs in the FT4 gene were identified between the recessive and dominant alleles in introns, 5'-UTR (GM08:44608620), 3'-UTR (GM08:46607056), and exon 4. The exon 4 SNP (Е10: ACT, е10: ATT) results in the replacement of threonine by isoleucine. This amino acid substitution is located very close to the outer loop encoded by exon 4 and affects protein function. This substitution in the FT and TFL1 genes (flowering end gene) has been observed in all flowering plant species [101]. This substitution in the inactive e10 allele induces early flowering. However, the e10e10 genotype was rarely detected in 300 Canadian early maturated soybean accessions and the mechanisms contributing to their flowering have not been identified [24].

E11 locus. The E11 locus induces early flowering and maturation under LD conditions. It plays an important role in the regulation of flowering, independent of E1. It was mapped to chromosome 7. Possible candidate genes were identified as Glyma07g48500, Glyma07g049000, and Glyma07g049200, homologs of LHY (LATEELONGATEDHYPOCOTYL), CURT1B (CURVATURETHYLAKOID1B), and MTP3 (METALTOLERANCEPROTEIN3) of Arabidopsis, respectively [25].

Identification of QTLs that affect the timing of flowering onset

There are several pieces of evidence that document the role of QTLs in regulating soybean flowering onset [38, 40, 102]. There is a possibility that some of the detected QTLs and known E1 [41, 102], E3 [42, 43], E4 [42], E7 [44], E11 [25], and LJ [51] genes are identical. Soybean QTL data are stored in the SoyBase database [103].

The QTL qDTF-J was detected on chromosome 16, near the GmFT5a locus, and contains ef (early flowering), a rare allele that occurs in both cultivated and wild soybean populations. It activates the expression of GmFT5a under conditions of LD, regardless of the allelic state of the E1 locus. It contributes to the adaptation of soybean to northern latitudes. Presumably, the GmFT5a gene may be a candidate for qDTF-J [104].

The GmPRR37 gene (qFT12-2) on chromosome 12, a homolog of the Arabidopsis APRR7 gene, is involved in the regulation of flowering time. In LD, the GmPRR37 gene downregulates GmFT2a and GmFT5a and activates GmFT1a, leading to a delay in flowering. However, it does not affect the expression of the J (GmELF3), E2 (GmGIa), GmCOL1a, and GmCOL1b genes in LD. CRISPR/cas9-induced knockout of this gene resulted in early flowering during LD. During SD, there were no phenotypic differences in flowering time observed between active and inactive alleles. Furthermore, GmFT2a, GmFT5a, GmFT1a, J (GmELF3), E2 (GmGIa), GmCOL1a, and GmCOL1b gene expression are unaffected in SD. Among Chinese varieties, accessions with recessive alleles that carry a nonsense mutation in the CCT domain are characterized by early flowering [105].

Key genes and QTLs that control flowering time often have pleiotropic effects on other agriculturally important traits, such as plant height and productivity [37, 39, 65], degree of self-pollination [42], pigmentation, and cold stress-induced seed coat cracking [41, 106]. A recent study identified new loci that act in a non-pleiotropic manner, namely R1-1 on chromosome 9, which controls flowering, and R8-1 and R8-2 on chromosomes 13 and 18, respectively, which control maturation. However, R1-1 also overlapped with QTLs controlling other agronomic traits. The pleiotropy of flowering and maturing may be genetically separate; however, artificial selection during soybean cultivation may have favoured pleiotropic loci such as E, which control both flowering and maturation processes [107].

In total, 228 QTLs controlling PS have been registered in soybean [25, 51, 88, 103]. The genetic system that determines the flowering time involves complex QTL-gene networks that include a number of biological processes that are directly or indirectly related to flowering time [108].

Promising genotypes for soybean northering

Graphical models have been proposed to describe the transition from vegetative to reproductive development in soybean [99, 109]. In these models, the E1 locus acts as a photoperiod-dependent modulator that can upregulate the expression of flowering inhibitor genes (GmFT1a and GmFT4) and downregulate the expression of flowering activator genes (GmFT2a and GmFT5a). Figure 2 presents our own modification of these models.

 

Fig. 2. Regulation of the transition from vegetative phase to reproductive phase in soybean during long days (LD) and short days (SD). Arrows: stimulation of gene expression. Gray T-shaped arrow: inhibition of gene expression. Crossed-out black arrow: absence of gene stimulation. Crossed-T-shaped line: absence of gene inhibition. Black T-shaped line: no effect of SD. Broad arrows: over all influence of genes on plant development

 

In soybean, genetic control of flowering time has been used in classical breeding programs for many years and is important for the effective creation of varieties that can thrive in higher latitudes, mainly in Northeast China, Northern Russia, and North America [11, 65, 110].

Soybean cultivars adapted to northern latitudes are known to be weakly sensitive to the photoperiod, which is determined by various combinations of mutant alleles at the E1, E2, E3, and E4 loci [11, 28, 62, 111].

Active alleles in the E1–E4 loci were consistently observed in mid- and late- maturated accessions. Recessive alleles e1–e4 were more common in early – maturated varieties developed for the northern parts of cultivation areas [77, 88, 112]. Photoperiod sensitivity decreases as the number of recessive alleles is increased. When comparing different genotypes, E1/E2/E3/E4 showed maximal PS, e1-as/E2/E3/E4, e1-as/e2/E3/E4, and e1-as/e2/e3/E4 genotypes exhibit decreased PS. In the E1/e2/E3/E4, e1-as/E2/E3/E4, and E1/E2/E3/E4 genotypes, the non-functional e1 allele reduces the PS more significantly than the non-functional e2 allele, indicating a more profound role of E1 in controlling flowering time [112].

Three allelic combinations have been identified, which determine the decrease in PS, namely e2/e3/e4, e1/e3, or e1/e2/e4, e1-as/e2/e3/E4. Among low-sensitivity genotypes, the variant with two inactive alleles е3 and е4, was the most common; i.e., the dysfunction of phytochrome PHYA proteins is probably the most crucial mechanism of photoperiod insensitivity in soybean. Non-functional alleles of E1 play a similar role in attenuating or deactivating the photoperiodic responses regulated by the E3 and E4 alleles.

Among the analysed accessions insensitive to the pre-bloom photoperiod, inactive alleles were generally observed in the E3 or E4 loci (e3 and e4). If one of these alleles was active (E3/E4), then the inactive allele e1-fs/e1-nl or hypomorphic allele e1-as was always revealed in the E1 locus. In the case of the active E1 allele, it was in combination with inactive e3 and e4. For the e1-as/e2/e3/E4 allele combination, photoperiod insensitivity is determined by unknown genes [62]. Thus, the photoperiod-insensitive Japanese variety Sakamotowase has the same genotype as the isogenic line of the variety Harosoy, NIL-е3, e1e1e2e2e3e3E4E4 [113]. However, unlike Sakamotowase, NIL-e3 does not form buds under LD conditions since the non-functional e1 allele in the presence of the functional E4 allele cannot induce photoperiod insensitivity [86]. Based on the differences between Sakamotowase and NIL-e3, it was suggested that there is another locus that functions independently or jointly with the e1 allele to promote the flowering of soybean with the e1e1e2e2e3e3E4E4 genotype under LD conditions [44, 62, 114].

In several studies, early-maturated accessions have the same duration of vegetation period but differed in the duration of their reproductive periods [11, 62]. It was suggested that post-flowering photoperiodic responses play the most important role in the maturing of soybean seeds under LD conditions and that the duration of the reproductive stage is rather independent of the time of flowering [11, 115, 116].

Photoperiod responses during the flowering and maturation stages are controlled by the phytochrome-coding (PHY) E3 and E4 loci, whereas the E1 and E2 loci have a significant effect on the pre-flowering phase. The E3 and E4 genes also activate the expression of the Dt1 gene (in the dominant state, which determines the indeterminate type of growth) at the stage after the onset of flowering. This leads to an increase in the time of pod formation, the number of nodes and pods per shoot, and the formation of a longer main shoot [62]. Thus, the E3 and E4 loci are of great importance for increasing soybean productivity.

Varieties with the same E1–E4 genotypes differed in flowering time and maturing rate. This suggests either the contribution of other E loci to these differences or may be due to the influence of environmental factors, such as temperature [117]. In varieties grown in relatively northern latitudes, E3 and E4 have opposite effects on the rate of maturation, probably due to low average temperatures. The active E3 allele activates maturation but slows down the onset of flowering, e3 promotes flowering. E4 slows down maturing, but both E4/e4 alleles in the heterozygote do not affect flowering [11]. Among photoperiod-insensitive lines, the temperature has been suggested to play an important role in the regulation of GmFT2a expression. The expression of GmFT2a in the photoperiod-insensitive Heihe 27 cultivar was significantly higher at high temperatures and under LD conditions. For cultivars sensitive to the photoperiod, on the contrary, high temperature suppressed GmFT2a expression [118].

Thus, we can conclude that the genotypes with the largest number of inactive alleles (е1, е2, е3, е4, е7, е9) provide the earliest flowering and maturation in relatively northern areas with LD. Combinations of е9(FT2a-ТО)/ е1-nl/е2/e3/e4 alleles can be considered the best genotype for soybean selection under LD conditions [28, 77, 88, 119]. The replacement of functional E3E3 and E4E4 alleles with non-functional ones, which can be achieved by marker-based selection and site-directed mutagenesis, can be a promising approach for the northering of soybean varieties with the most common genotypes e1e1e2e2E3E3E4E4, e1e1E2E2e3e3E4E4, and e1e1E2E2E3E3E4E4 [120].

CONCLUSION

Over the past decade, significant progress has been made in elucidating the molecular-genetic mechanisms underlying the photoperiod-dependent regulation of flowering and maturation in soybean. From the Williams 82 variety genome sequence, the critical genes and QTLs associated with flowering and maturation times were identified. However, the precise mechanisms of gene-QTL networks have not been fully elucidated. Experiments are currently being performed around the world to determine the PS of soybean genotypes grown in various photoperiodic and temperature regimes at different latitudes, as well as in simulations of different day lengths. A specific gene pool has been identified, which is characterized by a reduced PS, early flowering, and maturation. A hypothetical genotype optimal for northern latitudes was proposed, namely е9 (FT2a-ТО)/е1-nl/е 2/e3/e4.

Future studies to better understand the regulatory mechanisms controlling PS and flowering time in soybean are warranted. Further characterization of identified soybean genes and search for novel loci are needed. Findings from these studies can help optimize highly adapted and productive varieties for different local conditions and can help expand the soybean gene pool to promote its cultivation in northern regions.

ADDITIONAL INFORMATION

Author contributions. All authors made a significant contribution to the conceptualization, research, and preparation of the article. All authors read and approved the final version before its publication.

Conflicts of interest. The authors declare no conflict of interest.

Funding. This work was conducted within the state task according to the VIR thematic plan under project No. 0481-2022-0007 “Identification of new genetic markers of selectively significant properties and new allelic variants of economically valuable genes in the gene pool of cultivated plants and their wild relatives using genomic and post-genomic technologies.”

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About the authors

Jaroslava V. Fedorina

Sirius University of Science and Technology

Email: f.jaroslava@gmail.com
ORCID iD: 0000-0003-0215-7928
SPIN-code: 7993-4540
Scopus Author ID: 57105740200

Researcher

Russian Federation, Sochi

Elena K. Khlestkina

N.I. Vavilov All-Russian Institute of Plant Genetic Resources

Email: director@vir.nw.ru
ORCID iD: 0000-0002-8470-8254
SPIN-code: 3061-1429
Scopus Author ID: 6603368411
ResearcherId: T-2734-2017

Dr. Sci. (Biol.), Professor, Director

Russian Federation, Saint Petersburg

Irina V. Seferova

N.I. Vavilov All-Russian Institute of Plant Genetic Resources

Author for correspondence.
Email: i.seferova@vir.nw.ru
SPIN-code: 5061-9712
Scopus Author ID: 57144617000

Cand. Sci. (Biol.), Researcher

Russian Federation, Saint Petersburg

Margarita A. Vishnyakova

N.I. Vavilov All-Russian Institute of Plant Genetic Resources

Email: m.vishnyakova@vir.nw.ru
ORCID iD: 0000-0003-2808-7745
SPIN-code: 2802-9614
Scopus Author ID: 6603209207

Dr. Sci. (Biol.), Chief Researcher, Head of Department

Russian Federation, Saint Petersburg

References

  1. Faostat [Internet]. Crops and livestock products [cited: 2021 Jan 1]. Available from: www.fao.org/faostat/en/#data/QCL
  2. Vavilov NI. Botaniko-geograficheskie osnovy selektsii. Moscow; Leningrad: Sel’khozgiz, 1935. 60 p. (In Russ.)
  3. Garner WW, Allard HA. Photoperiodic response of soybeans in relation to temperature and other environmental factors. J Agric Res. 1930;41(10):719–735.
  4. Board JE, Hall W. Premature flowering in soybean yield reductions at non optimal planting dates as influenced by temperature and photoperiod. Agron J. 1984;76(4):700–704. doi: 10.2134/agronj1984.00021962007600040043x
  5. Seddigh M, Jolliff GD, Orf JH. Night temperature effects on soybean phenology. Crop Sci. 1989;29(2):400–406. doi: 10.2135/cropsci1989.0011183X002900020033x
  6. Seferova IV. Soybean in the north-west of the Russian Federation. Maslichnye kul’tury. Nauchno-tekhnicheskii byulleten’ VNIIMK. 2016;(3):101–105. (In Russ.)
  7. Neumaier N, James AT. Exploiting the long-juvenile trait to improve adaptation of soybeans to the tropics. ACIAR Food Legume Newsletter. 1993;18:12–14.
  8. Destro D, Carpentieri-Pipolo V, Kiihl RAS, Almeida LA. Photoperiodism and genetic control of the long juvenile period in soybean: a review. Crop Breed Appl Technol. 2001;1(1):72–92. doi: 10.13082/1984-7033.v01n01a10
  9. Shchelko L, Sedova T, Korneichuk V, et al. Mezhdunarodnyi klassifikator SEHV roda Glycine Willd. Leningrad: VIR, 1990. 38 p. (In Russ.)
  10. Training.ars-grin.gov [Internet]. Soybean. Descriptor: Maturity group (MATGROUP). Agricultural Research Service. United States Department of Agriculture [cited: 2021 Jul 12]. Available from: training.ars-grin.gov/gringlobal/descriptordetail?id=51055
  11. Jia H, Jiang B, Wu C, et al. Maturity group classification and maturity locus genotyping of early-maturing soybean varieties from high-latitude cold regions. PLoS One. 2014;9(4):1–9. doi: 10.1371/journal.pone.0094139
  12. Seferova IV. Ultra early soybean cultivars on the northern border of potentially possible seed maturation. Book of abstracts of the International Conference “125 Years of Applied Botany in Russia”. 25–28 Nov 2019; Saint Petersburg. Saint Petersburg: VIR, 2019. P. 186. (In Russ.) doi: 10.30901/978-5-907145-39-9
  13. Bernard RL. Two major genes for time of flowering and maturity in soybeans. Crop Sci. 1971;11(2):242–244. doi: 10.2135/cropsci1971.0011183X001100020022x
  14. Buzzell RI. Inheritance of a soybean flowering response to fluorescent day length conditions. Can J Genet Cytol. 1971;13(4):703–707. doi: 10.1139/g71-100
  15. Buzzel RI, Voldeng HD. Inheritance of insensitivity to long day length. Soybean Genet Newsl. 1980;7(1):26–29.
  16. McBlain BA, Bernard RL. A new gene affecting the time of flowering maturity in soybeans. J Hered. 1987;178(3):160–162. doi: 10.1093/oxfordjournals.jhered.a110349
  17. Ray JD, Hinson K, Mankono JEB, Malo MF. Genetic control of a long-juvenile trait in soybean. Crop Sci. 1995;35(4):1001–1006. doi: 10.2135/cropsci1995.0011183X003500040012x
  18. Bonato ER, Vello NA. E6 a dominant gene conditioning early flowering and maturity in soybeans. Genet Mol Biol. 1999;22(2): 229–232. doi: 10.1590/s1415-47571999000200016
  19. Cober ER, Voldeng HD. A new soybean maturity and photoperiod-sensitivity locus linked to E1 and T. Crop Sci. 2001;41(3): 698–701. doi: 10.2135/cropsci2001.413698x
  20. Cober ER, Molnar SJ, Charette M, Voldeng HD. A New Locus for Early Maturity in Soybean. Crop Sci. 2010;50(2):524–527. doi: 10.2135/cropsci2009.04.0174
  21. Kong F, Nan H, Cao D, et al. A new dominant gene E9 conditions early flowering and maturity in soybean. Crop Sci. 2014;54(6): 2529–2535. doi: 10.2135/cropsci2014.03.0228
  22. Zhao C, Takeshima R, Zhu J, et al. A recessive allele for delayed flowering at the soybean maturity locus E9 is a leaky allele of FT2a, a Flowering Locus T ortholog. BMC Plant Biol. 2016;16(1):20. doi: 10.1186/s12870-016-0704-9
  23. Cao D, Takeshima R, Zhao C, et al. Molecular mechanisms of flowering under long days and stem growth habit in soybean. J Exp Bot. 2017;68(8):1873–1884. doi: 10.1093/jxb/erw394
  24. Samanfar B, Molnar SJ, Charette M, et al. Mapping and identification of a potential candidate gene for a novel maturity locus, E10, in soybean. Theor Appl Genet. 2017;130:377–390. doi: 10.1007/s00122-016-2819-7
  25. Wang F, Nan H, Chen L, et al. A new dominant locus, E11, controls early flowering time and maturity in soybean. Mol Breed. 2019;39:70. doi: 10.1007/s11032-019-0978-3
  26. Zhang S-R, Wang H, Wang Z, et al. Photoperiodism dynamics during the domestication and improvement of soybean. Sci China Life Sci. 2017;60:1416–1427. doi: 10.1007/s11427-016-9154-x
  27. Xia Z, Watanabe S, Yamada T, Harada K. Positional cloning and characterization reveal the molecular basis for soybean maturity locus E1 that regulates photoperiodic flowering. Proc Natl Acad Sci USA. 2012;109(32): E2155–E2164. doi: 10.1073/pnas.1117982109
  28. Tsubokura Y, Watanabe S, Xia Z, et al. Natural variation in the genes responsible for maturity loci E1, E2, E3 and E4 in soybean. Ann Bot. 2014;113(3):429–441. doi: 10.1093/aob/mct269
  29. Sequence Read Archive [Internet]. National Center for Biotechnology Information [cited: 2021 Jul 12]. Available from: https://www.ncbi.nlm.nih.gov/sra/
  30. Schmutz J, Cannon SB, Schlueter J, et al. Genome sequence of the palaeopolyploid soybean. Nature. 2010;463(7278): 178–183. doi: 10.1038/nature08670
  31. Kim MY, Lee S, Van K, et al. Whole-genome sequencing and intensive analysis of the undomesticated soybean (Glycine soja Sieb. and Zucc.) genome. Proc Natl Acad Sci USA. 2010;107(51): 22032–22037. doi: 10.1073/pnas.1009526107
  32. Keim P, Diers BW, Olson TC, Shoemaker RC. RFLP mapping in soybean: association between marker loci and variation in quantitative traits. Genetics. 1990;126(3):735–742. doi: 10.1093/genetics/126.3.735
  33. Orf JH, Chase K, Jarvik T, et al. Genetics of soybean agronomic traits: I. Comparison of three related recombinant inbred populations. Crop Sci. 1999;39(6):1642–1651. doi: 10.2135/cropsci1999.3961642x
  34. Lee SH, Bailey MA, Mian MAR, et al. Molecular markers associated with soybean plant height, lodging, and maturity across locations. Crop Sci. 1996;36(3):728–735. doi: 10.2135/cropsci1996.0011183x003600030035x
  35. Tasma IM, Lorenzen LL, Green DE, Shoemaker RC. Mapping genetic loci for flowering time, maturity, and photoperiod insensitivity in soybean. Mol Breed. 2001;8(1):25–35. doi: 10.1023/A:1011998116037
  36. Yamanaka N, Ninomiy S, Hoshi M, et al. An informative linkage map of soybean reveals QTLs for flowering time, leaflet morphology and regions of segregation distortion. DNA Res. 2001;8(2):61–72. doi: 10.1093/dnares/8.2.61
  37. Wang D, Graef GL, Procopiuk AM, Diers WB. Identification of putative QTL that underlie yield in interspecific soybean backcross populations. Theor Appl Genet. 2004;108:458–467. doi: 10.1007/s00122-003-1449-z
  38. Watanabe S, Tadjuddin T, Yamanaka N, et al. Analysis of QTLs for reproductive development and seed quality traits in soybean using recombinant inbred lines. Breed Sci. 2004;54(4):399–407. doi: 10.1270/jsbbs.54.399
  39. Zhang W-K, Wang Y-J, Luo G-Z, et al. QTL mapping of ten agronomic traits on the soybean (Glycine max L. Merr.) genetic map and their association with EST markers. Theor Appl Genet. 2004;108:1131–1139. doi: 10.1007/s00122-003-1527-2
  40. Funatsuki H, Kawaguchi K, Matsuba S, et al. Mapping of QTL associated with chilling tolerance during reproductive growth in soybean. Theor Appl Genet. 2005;111:851–861. doi: 10.1007/s00122-005-0007-2
  41. Githiri SM, Yang D, Khan NA, et al. QTL analysis of low temperature induced browning in soybean seed coats. J Hered. 2007;98(4):360–366. doi: 10.1093/jhered/esm042
  42. Khan NA, Githiri SM, Benitez ER, et al. QTL analysis of cleistogamy in soybean. Theor Appl Genet. 2008;117:479–487. doi: 10.1007/s00122-008-0792-5
  43. Liu B, Fujita T, Yan Z-H, et al. QTL Mapping of Domestication-related Traits in Soybean (Glycine max). Ann Bot. 2007;100(5): 1027–1038. doi: 10.1093/aob/mcm149
  44. Liu B, Abe J. QTL mapping for photoperiod insensitivity of a Japanese soybean landrace Sakamotowase. J Hered. 2010;101(2): 251–256. doi: 10.1093/jhered/esp113
  45. Cheng L, Wang Y, Zhang C, et al. Genetic analysis and QTL detection of reproductive period and post-flowering photoperiod responses in soybean. Theor Appl Genet. 2011;123:421–429. doi: 10.1007/s00122-011-1594-8
  46. Liu W, Kim MY, Kang YJ, et al. QTL identification of flowering time at three different latitudes reveals homeologous genomic regions that control flowering in soybean. Theor Appl Genet. 2011;123: 545–553. doi: 10.1007/s00122-011-1606-8
  47. Komatsu K, Hwang T-Y, Takahashi M, et al. Identification of QTL controlling post-flowering period in soybean. Breed Sci. 2012;61(5):646–652. doi: 10.1270/jsbbs.61.646
  48. Lu S, Li Y, Wang J, et al. QTL mapping for flowering time in different latitude in soybean. Euphytica. 2015;206:725–736. doi: 10.1007/s10681-015-1501-5
  49. Kong L, Lu S, Wang Y, et al. Quantitative trait locus mapping of flowering time and maturity in soybean using next-generation sequencing-based analysis. Front Plant Sci. 2018;9:1–20. doi: 10.3389/fpls.2018.00995
  50. Liu D, Yan Y, Fujita Y, et al. A major QTL (qFT12.1) allele from wild soybean delays flowering time // Mol Breed. 2018;38:4. doi: 10.1007/s11032-018-0808-z
  51. Fang C, Chen L, Nan H, et al. Rapid identification of consistent novel QTLs underlying long-juvenile trait in soybean by multiple genetic populations and genotyping-by-sequencing. Mol Breed. 2019;39:80. doi: 10.1007/s11032-019-0979-2
  52. Hayama R, Coupland G. The Molecular Basis of Diversity in the Photoperiodic Flowering Responses of Arabidopsis and Rice. Plant Physiol. 2004;135(2):677–684. doi: 10.1104/pp.104.042614
  53. Valverde F, Mouradov A, Soppe W, et al. Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science. 2004;303(5660):1003–1006. doi: 10.1126/science.109176
  54. Tsuji H, Taoka K-I, Shimamoto K. Regulation of flowering in rice: two florigen genes, a complex gene network, and natural variation. Curr Opin Plant Biol. 2011;14(1):45–52. doi: 10.1016/j.pbi.2010.08.016
  55. Bouche F, Lobet G, Tocquin P, Perilleux C. FLOR-ID: an interactive database of flowering-time gene networks in Arabidopsis thaliana. Nucleic Acids Res. 2016;44(D1):D1167–D1171. doi: 10.1093/nar/gkv1054
  56. Jung C-H, Wong CE, Singh MB, Bhalla PL. Comparative genomic analysis of soybean flowering genes. PLoS One. 2012;7(6): e38250. doi: 10.1371/journal.pone.0038250
  57. Kim MY, Shin JH, Kang YJ, et al. Divergence of flowering genes in soybean. J Biosci. 2012;37:857–870. doi: 10.1007/s12038-012-9252-0
  58. Liu B, Kanazawa A, Matsumura H, et al. Genetic redundancy in soybean photoresponses associated with duplication of phytochrome A gene. Genetics. 2008;180(2):996–1007. doi: 10.1534/genetics.108.092742
  59. Watanabe S, Hideshima R, Xia Z, et al. Map-based cloning of the gene associated with the soybean maturity locus E3. Genetics. 2009;182(4):1251–1262. doi: 10.1534/genetics.108.098772
  60. Watanabe S, Xia Z, Hideshima R, et al. A map-based cloning strategy employing a residual heterozygous line reveals that the GIGANTEA gene is involved in soybean maturity and flowering. Genetics. 2011;188(2):395–407. doi: 10.1534/genetics.110.125062
  61. Tsubokura Y, Matsumura H, Xu M, et al. Genetic variation in soybean at the maturity locus E4 is involved in adaptation to long days at high latitudes. Agronomy. 2013;3(1):117–134. doi: 10.3390/agronomy3010117
  62. Xu M, Xu Z, Liu B, et al. Genetic variation in four maturity genes affects photoperiod insensitivity and PHYA-regulated post-flowering responses of soybean. BMC Plant Biol. 2013;13:91. doi: 10.1186/1471-2229-13-91
  63. Molnar SJ, Rai S, Charette M, Cober ER. Simple sequence repeat (SSR) markers linked to E1, E3, E4, and E7 maturity genes in soybean. Genome. 2003;46(6):1024–1036. doi: 10.1139/g03-079
  64. Watanabe S, Tsukamoto C, Oshita T, et al. Identification of quantitative trait loci for flowering time by a combination of restriction site-associated DNA sequencing and bulked segregant analysis in soybean. Breed Sci. 2017;67(3):277–285. doi: 10.1270/jsbbs.17013
  65. Cober E.R., Morrison M.J. Regulation of seed yield and agronomic characters by photoperiod sensitivity and growth habit genes in soybean. Theor Appl Genet. 2010;120(5):1005–1012. doi: 10.1007/s00122-009-1228-6
  66. Lu S, Zhao X, Hu Y, et al. Natural variation at the soybean J locus improves adaptation to the tropics and enhances yield. Nat Genet. 2017;49:773–779. doi: 10.1038/ng.3819
  67. Yue Y, Liu N, Jiang B, et al. A single nucleotide deletion in J encoding GmELF3 confers long juvenility and is associated with adaption of tropic soybean. Molecular Plant. 2017;10(4):656–658. doi: 10.1016/j.molp.2016.12.004
  68. McBlain BA, Hesketh JD, Bernard RL. Genetic effect on reproductive phenology in soybean isolines differing in maturity genes. Can J Plant Sci. 1987;67(1):105–115. doi: 10.4141/cjps87-012
  69. Wang Y, Wu CX, Zhang XM, et al. Effects of soybean major maturity genes under different photoperiods. Acta agronomica sinica. 2008;34(7):1160–116. doi: 10.3724/SP.J.1006.2008.01160
  70. Whigham DK, Minor HC, Carmen SG. Effects of environment and management on soybean performance in the tropics1. Agronomy J. 1978;70(4):587–592. doi: 10.2134/agronj1978.00021962007000040017x
  71. Egli DB. Seed biology and the yield of grain crops. Wallingford, UK: CAB International, 1998.
  72. Severin AJ, Woody JL, Bolon Y-T, et al. RNA-Seq Atlas of Glycine max: A guide to the soybean transcriptome. BMC Plant Biol. 2010;10:160. doi: 10.1186/1471-2229-10-160
  73. Libault M, Farmer A, Joshi T, et al. An integrated transcriptome atlas of the crop model Glycine max, and its use in comparative analyses in plants. Plant J. 2010;63(1):86–99. doi: 10.1111/j.1365-313X.2010.04222.x
  74. Upadhyay AP, Ellis RH, Summerfield RJ, et al. Characterization of photothermal flowering responses in maturity isolines of soyabean [Glycine max (L.) Merrill] cv. Clark. Ann Bot. 1994;74(1):87–96. doi: 10.1006/anbo.1994.1097
  75. Thakare D, Kumudini S, Dinkins RD. Expression of flowering- time genes in soybean E1 near-isogenic lines under short and long day conditions. Planta. 2010;231:951–963. doi: 10.1007/s00425-010-1100-6
  76. Zhou Z, Jiang Y, Wang Z, et al. Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean. Nat Biotechnol. 2015;33:408–414. doi: 10.1038/nbt.3096
  77. Langewisch T, Zhang H, Vincent R, et al. Major soybean maturity gene haplotypes revealed by SNPViz analysis of 72 sequenced soybean genomes. PLoS One. 2014;9(4): e94150. doi: 10.1371/journal.pone.0094150
  78. Xu M, Yamagishi N, Zhao C, et al. The soybean-specific maturity gene E1 family of floral repressors controls night-break responses through down-regulation of Flowering Locus T orthologs. Plant Physiol. 2015;168(4):1735–1746. doi: 10.1104/pp.15.00763
  79. Zhu J, Takeshima R, Harigai K, et al. Loss of function of the E1-Like-b gene associates with early flowering under long-day conditions in soybean. Front Plant Sci. 2019;9:1867. doi: 10.3389/fpls.2018.01867
  80. Zhai H, Lü S, Wu H, et al. Diurnal expression pattern, allelic variation, and association analysis reveal functional features of the E1 gene in control of photoperiodic flowering in soybean. PLoS One. 2015;10(8): e0135909. doi: 10.1371/journal.pone.0135909
  81. Zhang X, Zhai H, Wang Y, et al. Functional conservation and diversification of the soybean maturity gene E1 and its homologs in legumes. Sci Rep. 2016;6:29548. doi: 10.1038/srep29548
  82. Wang Y, Gu Y, Gao H, et al. Molecular and geographic evolutionary support for the essential role of GIGANTEAa in soybean domestication of flowering time. BMC Evol Biol. 2016;16:79. doi: 10.1186/s12862-016-0653-9
  83. Cober ER, Tanner JW, Voldeng HD. Soybean photoperiod-sensitivity loci respond differentially to light quality. Crop Sci. 1996;36(3): 606–610. doi: 10.2135/cropsci1996.0011183x003600030014x
  84. Kanazawa A, Liu B, Kong F, et al. Adaptive evolution involving gene duplication and insertion of a novel Ty1/copia-like retrotransposon in soybean. J Mol Evol. 2009;69:164–175. doi: 10.1007/s00239-009-9262-1
  85. Li Y-H, Zhou G, Ma J, et al. De novo assembly of soybean wild relatives for pan-genome analysis of diversity and agronomic traits. Nat Biotechnol. 2014;32:1045–1052. doi: 10.1038/nbt.2979
  86. Cober ER, Tanner JW, Voldeng HD. Genetic control of photoperiod response in early-maturing near-isogenic soybean lines. Crop Sci. 1996;36(3):601–605. doi: 10.2135/cropsci1996.0011183x003600030013x
  87. Dissanayaka A, Rodriguez TO, Di S, et al. Quantitative trait locus mapping of soybean maturity gene E5. Breed Sci. 2016;66(3): 407–415. doi: 10.1270/jsbbs.15160
  88. Li X, Fang C, Xu M, et al. Quantitative trait locus mapping of soybean maturity gene E6. Crop Sci. 2017;57(5):2547–2554. doi: 10.2135/cropsci2017.02.0106
  89. Zagotta MT, Hicks KA, Jacobs CI, et al. The Arabidopsis ELF3 gene regulates vegetative photomorphogenesis and the photoperiodic induction of flowering. Plant J. 1996;10(4):691–702. doi: 10.1046/j.1365-313x.1996.10040691.x
  90. Yu J-W, Rubio V, Lee N-Y, et al. COP1 and ELF3 control circadian function and photoperiodic flowering by regulating GI stability. Mol Cell. 2008;32(5):617–630. doi: 10.1016/j.molcel.2008.09.026
  91. Matsumura H, Kitajima H, Akada S, et al. Molecular cloning and linkage mapping of cryptochrome multigene family in soybean. The Plant Genome. 2009;2(3):271. doi: 10.3835/plantgenome.2009.06.0018
  92. Zhang Q, Li H, Li R, et al. Association of the circadian rhythmic expression of GmCRY1a with a latitudinal cline in photoperiodic flowering of soybean. Proc Natl Acad Sci USA. 2008;105(52): 21028–21033. doi: 10.1073/pnas.0810585105
  93. Guo H, Yang H, Mockler TC, Lin C. Regulation of flowering time by Arabidopsis photoreceptors. Science. 1998;279(5355):1360–1363. doi: 10.1126/science.279.5355.1360
  94. Kong F, Liu B, Xia Z, et al. Two coordinately regulated homologs of FLOWERING LOCUS Tare involved in the control of photoperiodic flowering in soybean. Plant Physiol. 2010;154(3):1220–1231. doi: 10.1104/pp.110.160796
  95. Wu F, Sedivy EJ, Price WB, et al. Evolutionary trajectories of duplicated FT homologues and their roles in soybean domestication. Plant J. 2017;90(5):941–953. doi: 10.1111/tpj.13521
  96. Cai Y, Wang L, Chen L, et al. Mutagenesis of GmFT2a and GmFT5a mediated by CRISPR/Cas9 contributes for expanding the regional adaptability of soybean. Plant Biotechnol J. 2020;18(1): 298–309. doi: 10.1111/pbi.13199
  97. Cai Y, Chen L, Liu X, et al. CRISPR/Cas9-mediated targeted mutagenesis of GmFT2a delays flowering time in soya bean. Plant Biotechnol J. 2018;16(1):176–185. doi: 10.1111/pbi.12758
  98. Cao D, Li Y, Lu S, et al. GmCOL1a and GmCOL1b function as flowering repressors in soybean under long-day conditions. Plant Cell Physiol. 2015;56(12):2409–2422. doi: 10.1093/pcp/pcv152
  99. Chen L, Cai Y, Qu M, et al. Soybean adaption to high-latitude regions is associated with natural variations of GmFT2b, an ortholog of Flowering Locus T. Plant Cell Environ. 2020;43(4):934–944. doi: 10.1111/pce.13695
  100. Zhai H, Lü S, Liang S, et al. GmFT4, a homolog of Flowering Locus T, is positively regulated by E1 and functions as a flowering repressor in soybean. PLoS One. 2014;9(2): e89030. doi: 10.1371/journal.pone.0089030
  101. Wickland DP, Hanzawa Y. The Flowering Locus T/Terminal Flower 1 gene family: functional evolution and molecular mechanisms. Mol Plant. 2015;8(7):983–997. doi: 10.1016/j.molp.2015.01.007
  102. Yamanaka N, Watanabe S, Toda K, et al. Fine mapping of the FT1 locus for soybean flowering time using a residual heterozygous line derived from a recombinant inbred line. Theor Appl Genet. 2005;110:634–639. doi: 10.1007/s00122-004-1886-3
  103. Soybase.org [Internet]. SoyBase, Integrating Genetics and Genomics to Advance Soybean Research [cited: 2021 Jul 12]. Available from: https://www.soybase.org/soybaselist/index.php
  104. Takeshima R, Hayashi T, Zhu J, et al. A soybean quantitative trait locus that promotes flowering under long days is identified as FT5a, a Flowering Locus T ortholog. J Exp Bot. 2016;67(17): 5247–5258. doi: 10.1093/jxb/erw283
  105. Wang L, Sun S, Wu T, et al. Natural variation and СRISPR/Cas9-mediated mutation in GmPRR37 affect photoperiodic flowering and contribute to regional adaptation of soybean. Plant Biotechnol J. 2020;18(9):1869–1881. doi: 10.1111/pbi.13346
  106. Takahashi R, Abe J. Soybean maturity genes associated with seed coat pigmentation and cracking in response to low temperatures. Crop Sci. 1999;39(6):1657–1662. doi: 10.2135/cropsci1999.3961657x
  107. Sedivy EJ, Akpertey A, Vela A, et al. Identification of non-pleiotropic loci in flowering and maturity control in soybean. Agronomy. 2020;10(8):1204. doi: 10.3390/agronomy10081204
  108. Pan L, He J, Zhao T, et al. Efficient QTL detection of flowering date in a soybean RIL population using the novel restricted two-stage multi-locus GWAS procedure. Theor Appl Genet. 2018;131: 2581–2599. doi: 10.1007/s00122-018-3174-7
  109. Liu W, Jiang B, Ma L, et al. Functional diversification of Flowering Locus T homologs in soybean: GmFT1a and GmFT2a/5a have opposite roles in controlling flowering and maturation. New Phytologist. 2017;217(3):1335–1345. doi: 10.1111/nph.14884
  110. Saindon G, Beversdorf WD, Voldeng HD. Adjustment of the soybean phenology using the E4 locus. Crop Sci. 1989;29(6):1361–1365. doi: 10.2135/cropsci1989.0011183x002900060006x
  111. Zhai H, Lü S, Wang Y, et al. Allelic variations at four major maturity e genes and transcriptional abundance of the E1 gene are associated with flowering time and maturity of soybean cultivars. PLoS One. 2014;9(5): e97636. doi: 10.1371/journal.pone.0097636
  112. Jiang B, Nan H, Gao Y, et al. Allelic combinations of soybean maturity loci E1, E2, E3 and E4 result in diversity of maturity and adaptation to different latitudes. PLoS One. 2014;9(8):e106042. doi: 10.1371/journal.pone.0106042
  113. Voldeng HD, Saindon G. Registration of seven long-daylength insensitive soybean genetic stocks. Crop Sci. 1991;31(5):1399. doi: 10.2135/cropsci1991.0011183x003100050095x
  114. Abe J, Xu D, Miyano A, et al. Photoperiod-insensitive Japanese soybean landraces differ at two maturity loci. Crop Sci. 2003;43(4):1300–1304. doi: 10.2135/cropsci2003.1300
  115. Han TF, Wang JL. Studies on the post flowering photoperiodic responses in soybean. Acta Bot Sin. 1995;37(11):863–869.
  116. Egli DB. Time and the productivity of agronomic crops and cropping systems. Agron J. 2011;103(3):743–750. doi: 10.2134/agronj2010.0508
  117. Kurasch AK, Hahn V, Leiser WL, et al. Identification of mega-environments in Europe and effect of allelic variation at maturity E loci on adaptation of European soybean. Plant Cell Environ. 2017;40(5):765–778. doi: 10.1111/pce.12896
  118. Sun H, Jia Z, Cao D, et al. GmFT2a, a soybean homolog of Flowering Locus T, is involved in flowering transition and maintenance. PLoS One. 2011;6(12):18–20. doi: 10.1371/journal.pone.0029238
  119. Kumawat G, Yadav A, Satpute GK, et al. Genetic relationship, population structure analysis and allelic characterization of flowering and maturity genes E1, E2, E3 and E4 among 90 Indian soybean landraces. Physiol Mol Biol Plants. 2019;25:387–398. doi: 10.1007/s12298-018-0615-3
  120. Gerasimova SV, Khlestkina EK, Kochetov AV, Shumny VK. Genome editing system CRISPR/CAS9 and peculiarities of its application in monocots. Fiziologiya rastenij. 2017;64(2):92–108. (In Russ.) doi: 10.1134/S1021443717010071

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2. Fig. 1. The distribution of candidate genes that determine the onset of flowering and associated QTLs in the soybean genome. Columns represent soybean chromosomes. Areas containing QTLs are marked in gray, whereas darker areas indicate overlaps between different QTLs. The E1, E2, E3, E7, E8, E9, and J loci are on the left side of the chromosomes, with the corresponding molecular markers in black. Question marks next to the loci indicate that the corresponding genes for these QTLs remain unknown. The blue lines on the chromosomes indicate the position of the soybean orthologs of flowering genes in Arabidopsis. Orthologs located in the QTL are labeled as Arabidopsis gene symbols in blue, and red letters denote the characterized genes corresponding to the QTL (according to Zhang et al., 2017 [26]).

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3. Fig. 2. Regulation of the transition from vegetative phase to reproductive phase in soybean during long days (LD) and short days (SD). Arrows: stimulation of gene expression. Gray T-shaped arrow: inhibition of gene expression. Crossed-out black arrow: absence of gene stimulation. Crossed-T-shaped line: absence of gene inhibition. Black T-shaped line: no effect of SD. Broad arrows: over all influence of genes on plant development

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