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. 2022 Mar 17;13:817544. doi: 10.3389/fpls.2022.817544

CONSTANS Polymorphism Modulates Flowering Time and Maturity in Soybean

Mohammad Abdul Awal Khan 1,†, Shouwei Zhang 1,†, Reza Mohammad Emon 1,2,†, Fulu Chen 1,†, Wenwen Song 1, Tingting Wu 1, Shan Yuan 1, Cunxiang Wu 1, Wensheng Hou 1, Shi Sun 1, Yongfu Fu 1, Bingjun Jiang 1,*, Tianfu Han 1,*
PMCID: PMC8969907  PMID: 35371153

Abstract

CONSTANS (CO) plays a critical role in the photoperiodic flowering pathway. However, the function of soybean CO orthologs and the molecular mechanisms in regulating flowering remain largely unknown. This study characterized the natural variations in CO family genes and their association with flowering time and maturity in soybeans. A total of 21 soybean CO family genes (GmCOLs) were cloned and sequenced in 128 varieties covering 14 known maturity groups (MG 0000-MG X from earliest to latest maturity). Regarding the whole genomic region involving these genes, GmCOL1, GmCOL3, GmCOL8, GmCOL9, GmCOL10, and GmCOL13 were conserved, and the remaining 15 genes showed genetic variation that was brought about by mutation, namely, all single-nucleotide polymorphisms (SNPs) and insertions-deletions (InDels). In addition, a few genes showed some strong linkage disequilibrium. Point mutations were found in 15 GmCOL genes, which can lead to changes in the potential protein structure. Early flowering and maturation were related to eight genes (GmCOL1/3/4/8/13/15/16/19). For flowering and maturation, 11 genes (GmCOL2/5/6/14/20/22/23/24/25/26/28) expressed divergent physiognomy. Haplotype analysis indicated that the haplotypes of GmCOL5-Hap2, GmCOL13-Hap2/3, and GmCOL28-Hap2 were associated with flowering dates and soybean maturity. This study helps address the role of GmCOL family genes in adapting to diverse environments, particularly when it is necessary to regulate soybean flowering dates and maturity.

Keywords: soybean, GmCOL orthologue, natural variation, flowering time, maturity group

Introduction

Plants can adapt to different environmental conditions in response to various day lengths (photoperiods). In the photoperiodic flowering pathway, CONSTANS (CO), which is a B-box-containing transcription factor (Robson et al., 2001; Gangappa and Botto, 2014), plays a key role (Putterill et al., 1995; Suarez-Lopez et al., 2001). CO also possesses a CONSTANS, CONSTANS-LIKE, TIMING OF CAB1 (CCT) domain at its C-terminus involved in DNA binding (Strayer et al., 2000; Robson et al., 2001). CYCLING DOF FACTOR (CDF) family proteins bind to the CO promoter to repress its transcription in the morning (Imaizumi et al., 2005; Fornara et al., 2009). FLAVIN-BINDING, KELCH REPEAT, and F-BOX1 (FKF1) interact with GIGANTEA (GI) to degrade the CDF1 protein, which results in the elevation of CO mRNA (Sawa et al., 2007). CO acts in the phloem of leaf vascular tissues to activate FLOWERING LOCUS T (FT) expression, which causes flowering under linkage disequilibrium (LD) conditions (Takada and Goto, 2003; An et al., 2004). SUPPRESSOR OF PHYTOCHROME A-105 (SPA) proteins interact with the CCT domain of CO (Laubinger et al., 2006). CO is ubiquitinated by CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1) and degraded by the 26S proteasome (Jang et al., 2008; Liu L. J. et al., 2008). HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENES1 (HOS1) interacts with CO and participates in the degradation of CO mediated by red light (Lazaro et al., 2012, 2015). Nucleoporin96 (Nup96) interacts with HOS1 to gate CO protein levels (Cheng et al., 2020). CO protein is stable under the light in the evening but degraded in the morning or in the dark under LD conditions (Valverde et al., 2004). All of the abovementioned comments are based on studies in Arabidopsis.

As a short-day plant (SDP) distributed over a vast range of latitudes, soybean is characterized as having 14 maturity groups from MG 0000 to MG X (Liu et al., 2017; Jiang et al., 2019). There are hundreds of genetic loci associated with flowering time and maturity in soybean, among which E1 (Xia et al., 2012), E2 (Watanabe et al., 2011), E3 (Watanabe et al., 2009), E4 (Liu B. et al., 2008), E6 (Fang C. et al., 2021), E9 (Kong et al., 2014), E10 (Samanfar et al., 2017), E11 (Wang et al., 2019), J (Lu et al., 2017; Yue et al., 2017) and Tof11/GmPRR37/GmPRR3b (Li et al., 2020; Lu et al., 2020; Wang et al., 2020), GmTof16 (Dong et al., 2021b), GmFUL (Dong et al., 2021a; Sun et al., 2021; Yue et al., 2021), and GmLUX (Bu et al., 2021; Fang X. et al., 2021) are molecularly identified. There are 28 CO orthologs in soybean (Fan et al., 2014), but the functions of most of the CO orthologs remain uncharacterized. It has been shown that GmCOL1a and GmCOL1b can fully complement the late-flowering phenotype of the co1 mutant in Arabidopsis (Wu et al., 2014). In contrast, GmCOL1a and GmCOL1b repressed flowering in soybean under long-day conditions (Cao et al., 2015; Wu et al., 2019).

Natural variation is associated with photoperiodic flowering and adaptation in different species (Alonso-Blanco et al., 2005; Balasubramanian et al., 2006; Rosas et al., 2014; Li et al., 2017; Lu et al., 2017; Bao et al., 2019; Jiang et al., 2019; Wu et al., 2020). In this study, 128 soybean varieties were selected and planted, covering all 14 maturity groups from MG 0000 to MG X with a continuous distribution in maturity groups (Jiang et al., 2019). Due to the short duration of the project, 21 of the 28 soybean COL genes (Fan et al., 2014) were sequenced, and their sequence polymorphisms were analyzed. Furthermore, we studied the haplotypes of these soybean GmCOL genes to discover their natural variations in association with flowering time and maturity. These results suggested that some natural variations in 21 soybean GmCOL genes were associated with flowering date and maturity.

Materials and Methods

Plant Materials

Soybean varieties covering all 14 maturity groups (MG 0000-MG X) were assessed in this study (Jiang et al., 2019). In this study, 64 Chinese and Russian soybean varieties and 64 North American maturity group standard varieties were included, covering MG 0000-MG X, for a total of 128 accessions analyzed (Table 1).

TABLE 1.

Soyabean varieties and maturity groups.

MGR (maturity group reference) varieties
Maturity
group		 North American
varieties		 Chinese-Russian
varieties
MG 0000 Star4/75, Hujiao07-2479, Hujiao07-2123, Dongnong 36, Paula, R-4, Dongnong 41, Lingbei 8
MG 000 Maple Presto, OAC Vision, Rassvet, Jug 30, Mageva R-2, Heihe 35
MG 00 Canatto, Maple Ridge, Daksoy, McCall, Agassiz Mengdou 32, Beidou 16, Dongnong 44, Mengdou 11
MG 0 Traill, Chico, Barnes, Norpro, Dawson Jiangmodou 1, Heihe 18, Heihe 43, Heihe 27, Beidou 37, Dengke 1, Fengshou 12, Dongnong 4, Hefeng 25
MG I Haroson, Kato, Parker, Granite, NE1900 Heinong 16, Taixingheidou, Heinong 26, Suinong 14
MG II Holt, Olympus, Century 84, IL1, LN92-7369 Jilin 20, Yongchengzihuadou, Xiangchundou 24, Tiefeng 19
MG III Athow, LN89-5699, KS3494, IL2, Williams 82 Zhonghuang 13, Zhonghuang 30, Tiefeng 33, Zhongdou 39, Xudou 9, Tiefeng 31, Jindou 19, Huachun 6, Huaidou 9
MG IV Flyer, Omaha, Calhoun, CF461, UA-4805 Zheng 92116, Guandou 2, Jindou 39, Shanning 16, Houzimao
MG V Nathan, Hollady, Hutcheson, R01-3474F, TN04-5321 Shangdou 14, Dian 86-4, Diandou 7
MG VI Desha, Musen, D95-6271, G01-PR16, Boggs Zhongdou 38, Wuhuasiyuehuang, Suxiandou 19, Nannong 493-1
MG VII Stonewall, Benning, Santee, Hagood Huangfengwo, Tongshanbopihuang, Hengyangbayueqing, Nanxiadou 25
MG VIII Motte, Dowling, Crockett, Prichard, IAC-8, CIGRAS-51, CIGRAS-06 Aijiaoqing, Pingguohuangdou, Nandou 12, Shangraodaqingsi, Lanxidaqingdou, Qiudou 1, Nandou 17, Jiangledaqingdou, Guixia 3
MG IX Jupiter, Alamo, FT-15, UFV-3
MG X I.C. 192 Zigongdongdou
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Investigation of Flowering and Maturity Dates

The soybeans were planted in soil in 10-L pots and grown under natural conditions in Haidian District, Beijing (39.95°N, 116.32°E) on May 27, 2015, and May 18, 2016 (Jiang et al., 2019). After emergence (VE), seedlings of similar size were selected so that each pot contained five uniform plants. Each variety was planted in three pots. The four developmental stages of soybean, namely, VE, R1, R7, and R8 (Fehr and Caviness, 1977), were investigated, and the average value of three pots for each variety was used for statistical analysis.

DNA Isolation, PCR, and Sequencing

Genomic DNA was extracted from fresh trifoliolate leaves using the standard cetyltrimethylammonium bromide (CTAB) method (Jiang et al., 2019). To amplify the 21 soybean GmCOL genes, 36 PCR primer pairs were used. GmCOL9/15/16/20/28 was amplified with 2 primer pairs: GmCOL4 with 11 primer pairs and GmCOL1/2/3/5/6/8/10/13/14/19/22/23/24/25/26 with 1 primer pair. The sequences of these primers and the template designation are listed in Supplementary Table 1. Target regions were amplified with the high-fidelity polymerase of KOD-Plus-Neo and KOD-FX. Their reaction conditions were 94°C for 2 min (98°C for 10 s, 68°C for 3 min), 35 cycles, and 68°C for 10 min. The PCR products were directly sequenced using the Sanger method (TSINGKE Biological Technology Company, BGI and Omega Genetics, Beijing, China). The polymorphic site information of the 21 soybean GmCOL family genes is listed in Supplementary Table 2.

Data Mining and Sequence Analysis

The annotated soybean COL gene sequence was downloaded from the Joint Genome Institute (JGI) Phytozome website1. The protein sequences of the annotated Arabidopsis genes (TAIR9 release) were downloaded from the Arabidopsis Information Resource (TAIR) website2. The CO-like gene sequence data were also collected from the USDA-ARS Soybean Genetics and Genomics Database (SoyBase Database3). The reference sequence of the soybean variety Williams 82 was obtained from the Phytozome (version 12.0) database4 as a reference design for the amplification and sequencing primers of the COL genes.

Sequencing was performed using an ABI3730 sequencer. Multiple sequence alignment, editing, and stitching were carried out using ClustalW in MEGA5 with default parameters. Single-nucleotide polymorphism (SNP) analysis was carried out using TASSEL5 software. The haplotype analysis of the sequencing results was conducted by DNAsp to determine whether the protein coding was affected. LD was also evaluated using TASSEL5 software. The statistical analysis was performed using “R” software.

Results

Diversity of Soybean Varieties in Flowering Time and Maturity

The results of the growth traits are presented in Table 2. The varieties utilized in this experiment exhibited significant diversity in flowering time and maturity (Table 2). In 2015, 19 varieties, namely, MC119, MC63, MC69, MC70, MC54, MC121, MC122, MC123, MC72, MC124, MC125, MC126, MC48, MC64, MC65, MC66, MC67, MC68, and MC71, flowered but failed to reach R7. In 2016, 50 varieties did not reach R7 (Table 2). In 2015, the days to R1 from emergence (VE) ranged from 21 (MC82, MG 0) to 121 days (MC72, MG VIII) with a span of 100 days. In 2016, the span time was 96 days between MG 0000 (MC05, 13 days) and MG VIII (MC129, 109 days). In 2016, the days to R7 ranged from 68 (MC05 and MC74, MG 0000) to 144 days (MC42, MG IV), and the days to R8 ranged from 76 (MC05, MG 0000) to 109 days (MC37, MG III). The combination of maturity group information for the days of flowering time from the emergence and the days of beginning maturity from emergence in 2016 is plotted in a box diagram (Figure 1).

TABLE 2.

Phenotypic variation of soybean varieties at Beijing.

Code Variety name MG Phenotype in 2016
VE-R1 VE-R7 VE-R8
MC01 Star 4/75 0000 15.4 ± 1.2 70.6 ± 1.3 80.6 ± 0.61
MC02 Hujiao 07-2479 0000 16.4 ± 0.82 72.06 ± 1.27 81.26 ± 0.45
MC03 Hujiao 07-2123 0000 15.6 ± 0.50 71.13 ± 0.35 80.8 ± 0.41
MC04 Dongnong 36 0000 14.13 ± 0.51 69.13 ± 0.51 79.66 ± 0.97
MC05 Paula 0000 13.66 ± 0.48 68.4 ± 0.82 76.66 ± 0.48
MC06 R-4 0000 25.86 ± 0.74 71.46 ± 0.91 82.6 ± 0.82
MC07 Dongnong 41 0000 14.33 ± 0.48 69.46 ± 0.51 79.53 ± 0.91
MC74 Lingbei 8 0000 18.9 ± 1.0 68.4 ± 1.2 80.2 ± 1.5
MC75 Dongnong 41-C 0000 25.7 ± 1.4 70.5 ± 0.9 80.9 ± 1.0
MC08 Maple-Presto 000 15.53 ± 0.51 69.2 ± 1.01 77.66 ± 0.97
MC09 OAC-Vision 000 16.73 ± 0.79 69.8 ± 1.52 77.53 ± 0.91
MC10 Rassvet 000 17.33 ± 0.48 71.53 ± 0.91 79.8 ± 0.41
MC11 Jug-30 000 24.33 ± 0.48 71.2 ± 0.41 79.8 ± 0.67
MC12 Mageva 000 25.73 ± 0.45 75.66 ± 0.97 83.8 ± 0.86
MC73 R2 000 14.6 ± 0.9 70.6 ± 1.4 80.8 ± 2.1
MC76 Heihe 35 000 25.4 ± 1.5 73.5 ± o.5 87.5 ± 0.5
MC13 Canatto 00 18.2 ± 0.4 72.8 ± 1.8 85.2 ± 0.4
MC14 Maple-Ridge 00 18.4 ± 0.5 72.0 ± 1.0 84.7 ± 0.4
MC15 Daksoy 00 24.3 ± 0.4 71.3 ± 0.4 80.8 ± 0.3
MC16 McCall 00 23.6 ± 0.8 73.4 ± 1.2 85.8 ± 1.5
MC17 Agassiz 00 25.2 ± 0.4 71.6 ± 0.8 81.2 ± 0.4
MC77 Mengdou 32 00 22.6 ± 2.4 73.2 ± 1.0 86.3 ± 0.9
MC78 Beidou 16 00 19.9 ± 0.7 73.4 ± 1.5 85.4 ± 0.5
MC80 Dongnong 44 00 24.8 ± 1.0 71.3 ± 1.4 81.3 ± 0.9
MC81 Mengdou 11 00 24.3 ± 0.4 71.2 ± 1.3 81.6 ± 1.5
MC26 Traill 0 27.3 ± 0.4 73.3 ± 0.9 82.26 ± 0.7
MC27 Chico 0 26.4 ± 0.9 70.8 ± 1.5 81.4 ± 1.5
MC28 Barnes 0 26.5 ± 0.7 68.8 ± 1.3 78.4 ± 0.5
MC29 Norpro 0 25.3 ± 0.9 71.4 ± 0.50 82.1 ± 1.2
MC30 Dawson 0 23.6 ± 0.4 70.2 ± 1.37 80.4 ± 1.2
MC31 Jiangmodou 1 0 23.4 ± 0.9 69.7 ± 1.1 80.5 ± 0.9
MC82 Heihe 18 0 25.2 ± 1.5 72.0 ± 1.0 80.8 ± 1.3
MC83 Heihe 43 0 26.4 ± 0.5 71.9 ± 1.6 82.6 ± 0.7
MC84 Heihe 27 0 23.6 ± 0.4 70.8 ± 1.0 81.6 ± 0.5
MC85 Beidou 37 0 21.5 ± 0.9 69.5 ± 0.9 80.2 ± 1.2
MC86 Dengke1 0 23.8 ± 0.4 69.6 ± 0.4 80.4 ± 0.5
MC97 Fengshou 12 0 24.6 ± 0.9 71.0 ± 1.0 80.8 ± 1.0
MC88 Dongnong-4 0 32.2 ± 1.0 74.1 ± 0.8 85.8 ± 0.6
MC89 Hefeng 25 0 32.7 ± 0.4 75.5 ± 0.9 85.7 ± 0.7
MC23 Haroson I 25.2 ± 0.45 71.2 ± 0.4 82.2 ± 0.4
MC24 Kato I 27.5 ± 0.9 72.2 ± 0.4 81.5 ± 0.9
MC25 Parker I 25.4 ± 0.9 71.4 ± 0.9 80.3 ± 0.9
MC26 Granite I 25.3 ± 0.9 71.3 ± 0.9 78.4 ± 0.9
MC27 NE1900 I 35.2 ± 0.4 70.7 ± 1.0 80.1 ± 0.3
MC90 Heinong 16 I 28.5 ± 0.9 71.6 ± 0.9 79.4 ± 0.5
MC91 Taixingheidou I 26.6 ± 0.9 72.73 ± 1.6 79.3 ± 1.7
MC92 Heinong 26 I 29.4 ± 0.5 70.8 ± 0.6 78.8 ± 0.9
MC93 Suinong 14 I 27.2 ± 1.5 69.4 ± 1.3 78.2 ± 1.3
MC28 Holt II 30.3 ± 2.4 70.8 ± 0.8 81.8 ± 1.5
MC29 Olympus II 27.7 ± 0.9 72.3 ± 0.4 82.0 ± 1.0
MC30 Century-84 II 26.6 ± 0.4 71.6 ± 0.8 81.0 ± 1.2
MC31 IL1 II 30.4 ± 5.5 70.2 ± 1.7 79.6 ± 2.5
MC32 LN92-7369 II 30.4 ± 1.4 76.2 ± 1.0 107.9 ± 1.6
MC94 Jilin 20 II 25.2 ± 1.0 70.3 ± 0.9 78.2 ± 1.0
MC95 Yongchengzihuadou II 41.3 ± 1.2 72.1 ± 1.2 87.7 ± 1.2
MC96 Xiangchundou 24 II 43.8 ± 1.0 77.4 ± 0.5 86.6 ± 1.2
MC98 Tiefeng 19 II 24.4 ± 0.5 71.2 ± 1.2 81.2 ± 1.7
MC33 Athow III 30.3 ± 0.9 76.3 ± 0.9 106.3 ± 0.9
MC34 Zhonghuang 13 III 43.3 ± 0.4 78.4 ± 0.9 106.4 ± 0.9
MC35 Zhonghuang 30 III 37.8 ± 0.9 78.3 ± 0.9 105.5 ± 1.4
MC36 LN89-5699 III 32.3 ± 0.9 80.2 ± 1.5 108.2 ± 0.4
MC37 KS3494 III 37.4 ± 0.5 79.8 ± 0.9 109.4 ± 1.5
MC38 IL2 III 42.1 ± 0.8 105.2 ± 2.3 105.3 ± 5.1
MC39 Williams 82 III 36.8 ± 0.3 107.3 ± 0.8 108.1 ± 2.3
MC97 Tiefeng 33 III 29.5 ± 0.5 78.7 ± 0.4 106.8 ± 1.2
MC99 Zhongdou 39 III 44.5 ± 0.5 77.4 ± 0.5 105.2 ± 1.8
MC100 Xudou 9 III 37.9 ± 0.7 78.0 ± 1.0 106.4 ± 1.5
MC101 Tiefeng 31 III 24.2 ± 1.1 77.2 ± 1.3 105.2 ± 1.1
MC102 Jindou 19 III 25.8 ± 1.3 77.4 ± 1.5 104.8 ± 1.5
MC103 Huachun 6 III 31.4 ± 0.5 77.3 ± 0.4 105.6 ± 0.9
MC104 Huaidou 9 III 34.3 ± 0.4 ND ND
MC40 Flyer IV 35.5 ± 1.4 143.0 ± 1.4 ND
MC41 Omaha IV 38.0 ± 1.0 143.4 ± 1.4 ND
MC42 Calhoun IV 37.3 ± 0.4 144.4 ± 0.5 ND
MC43 CF461 IV 31.8 ± 1.0 143.7 ± 0.4 ND
MC44 UA-4805 IV 61.2 ± 0.4 ND ND
MC105 Zheng 92116 IV 37.2 ± 0.4 ND ND
MC106 Guandou 2 IV 35.8 ± 1.0 ND ND
MC107 Jindou 39 IV 36.2 ± 1.3 142.9 ± 1.0 ND
MC108 Shanning 16 IV 43.4 ± 0.8 142.3 ± 0.4 ND
MC109 Houzimao IV 43.7 ± 1.4 143.3 ± 1.1 ND
MC45 Nathan V 60.2 ± 1.0 ND ND
MC46 Holladay V 62.2 ± 1.5 ND ND
MC47 Hutcheson V 63.2 ± 1.0 ND ND
MC48 R01-3474F V 62.2 ± 1.5 ND ND
MC49 TN04-5321 V 63.6 ± 1.5 ND ND
MC110 Shangdou 14 V 44.7 ± 0.4 ND ND
MC111 Dian 86-4 V 43.6 ± 1.5 ND ND
MC113 Diandou 7 V 88.3 ± 0.9 ND ND
MC50 Desha VI 48.0 ± 0.8 ND ND
MC51 Musen VI 80.0 ± 1.0 ND ND
MC52 D95-6271 VI 82.3 ± 1.5 ND ND
MC53 G01-PR16 VI 81.6 ± 0.9 ND ND
MC54 Boggs VI 79.8 ± 1.5 ND ND
MC112 Zhongdou 38 VI 83.6 ± 2.5 ND ND
MC114 Wuhuasiyuehuang VI 86.3 ± 0.9 ND ND
MC108 Suxiandou 19 VI 85.8 ± 1.2 ND ND
MC116 Nannong 493-1 VI 91.2 ± 0.4 ND ND
MC55 Stonewall VII 81.4 ± 0.5 ND ND
MC57 Santee VII 82.6 ± 1.8 ND ND
MC58 Hagood VII 94.6 ± 1.2 ND ND
MC56 Benning VII 93.3 ± 0.9 ND ND
MC117 Hunagfengwu VII 93.7 ± 0.4 ND ND
MC118 Tongshanbopihuang VII 93.2 ± 1.2 ND ND
MC60 Motte VIII 93.3 ± 0.9 ND ND
MC61 Dowling VIII 95.8 ± 1.5 ND ND
MC62 Crockett VIII 65.4 ± 0.2 142.2 ± 0.5 158.0 ± 1.0
MC128 Hengyangbayueqing VII 96.9 ± 1.0 ND ND
MC119 Nanxiadou 25 VII 92.6 ± 0.9 ND ND
MC63 Prichard VIII 94.8 ± 1.0 ND ND
MC69 CIGRAS-51 VIII 81.4 ± 0.5 ND ND
MC70 CIGRAS-06 VIII 81.5 ± 0.9 ND ND
MC54 Aijiaoqing VIII 94.3 ± 0.4 ND ND
MC121 Pingguohuangdou VIII 92.9 ± 1.0 ND ND
MC122 Nandou 12 VIII 91.3 ± 0.4 ND ND
MC123 Shangraodaqingsi VIII 92.8 ± 1.0 ND ND
MC72 Zigongdongdou VIII 73.4 ± 1.5 ND ND
MC124 Lanxidaqingdou VIII 91.6 ± 0.5 ND ND
MC125 Qiudou 1 VIII 94.3 ± 0.4 ND ND
MC126 Nandou 17 VIII 91.6 ± 0.4 ND ND
MC48 Jiangledaqingdou VIII 99.5 ± 0.9 ND ND
MC129 Guixia 3 VIII 109.2 ± 1.0 118.4 ± 0.2 ND
MC64 Jupiter IX 96.3 ± 0.9 ND ND
MC65 Alamo IX 96.0 ± 1.3 ND ND
MC66 FT-15 IX 94.2 ± 1.3 ND ND
MC67 UFV-3 IX 96.2 ± 1.0 ND ND
MC68 IAC-8 IX 90.0 ± 1.0 ND ND
MC71 I.C.-192 X 80.4 ± 1.5 ND ND
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ND, Not available data; VE, Variation after emergence.

FIGURE 1.

FIGURE 1

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(A,B) Flowering time and maturity of soybean varieties from different maturity groups. Flowering time and maturity data were collected in 2016 from 128 soybean varieties covering 14 maturity groups. DAE, days after emergence.

GmCOL Gene Sequencing and Mutation Study

A large number of mutated sites were found in GmCOL2, GmCOL5, GmCOL14, GmCOL16, GmCOL20, and GmCOL28 (Figures 2B1,D1 and Supplementary Figures 1G1,I1, 2B1,H1). A majority of the mutation sites were in gene intron regions, but a few were located in protein-coding regions caused by insertions-deletions (InDels) and substitutions. In addition, GmCOL6, GmCOL22, GmCOL23, GmCOL24, GmCOL25, and GmCOL26 showed high mutation frequencies in the protein-coding regions (Supplementary Figures 1, 2). In contrast, GmCOL4, GmCOL15, and GmCOL19 expressed lower mutational occurrences (Supplementary Figures 1A1,H1, 2A1). The exception was GmCOL3, which did not show mutations (Figure 2C) in either the intron or exon region of the entire gene. GmCOL3 is a highly conserved gene with no change in sequence. However, the amino acid sequences encoded by GmCOL1, GmCOL8, GmCOL9, GmCOL10, and GmCOL13 were not affected (Figure 2A and Supplementary Figures 1C1-F1).

FIGURE 2.

FIGURE 2

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Haplotype analysis, distribution in different maturity groups, and flowering time (VE-R1) in the main haplotypes of approximately four GmCOL family genes. (A) Haplotype of GmCOL1. (B,B1) Haplotypes of GmCOL2. The haplotype is shown as a linear combination of alleles. The site combination labeled with the yellow outline represents the tagging haplotype (the composition of the haplotype depends on fewer and critical variation sites). (B2) Haplotype distribution of GmCOL2 in different maturity groups. (B3) Flowering time (VE-R1) of the main haplotypes of GmCOL2 in 2015. (B4) Flowering time (VE-R1) of the main haplotypes of GmCOL2 in 2016. (C) Gene structure of GmCOL3. (D,D1) Haplotypes of GmCOL5 (1) and GmCOL5 (2). (D2) Haplotype distribution of GmCOL5 in different maturity groups. (D3) Flowering time (VE-R1) of the main haplotypes of GmCOL5 in 2015. (D4) Flowering time (VE-R1) of the main haplotypes of GmCOL5 in 2016.

Soybean COL Gene Family Exhibited Different Linkage Disequilibrium

Linkage and association mapping were drawn among the SNPs of the gene via TASSEL5. GmCOL5 across the region almost from the starting to the end site presented a strong LD by completing the haplotype block (Figure 3D). GmCOL20, GmCOL24, and GmCOL25 across the region expressed strong LD as a haplotype block (Figures 3N,Q,R), and the polymorphic sites of GmCOL6, GmCOL8, GmCOL10, GmCOL13, and GmCOL19 showed a strong LD, with almost the entire region being a haplotype block (Figures 3E,F,H,I,M). Although GmCOL2, GmCOL16, GmCOL22, GmCOL26, and GmCOL28 had a high-sequence polymorphism, the entire region distributed a few LDs (Figures 3B,L,O,S,T) with the same high-sequence polymorphism of GmCOL4, GmCOL9, and GmCOL23, and quite a few strong LDs were distributed broadly (Figures 3C,G,P). GmCOL1, GmCOL14, and GmCOL15 did not reveal any LD (Figures 3A,J,K). GmCOL3 was the most conserved gene, showing no polymorphic site(s).

FIGURE 3.

FIGURE 3

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Linkage disequilibrium of GmCOL family genes in soybean. (A) Linkage disequilibrium (LD) of GmCOL1. (B) LD of GmCOL2. (C) LD of GmCOL4. (D) LD of GmCOL5. (E) LD of GmCOL6. (F) LD of GmCOL8. (G) LD of GmCOL9. (H) LD of GmCOL10. (I) LD of GmCOL13. (J) LD of GmCOL14. (K) LD of GmCOL15. (L) LD of GmCOL16. (M) LD of GmCOL19. (N) LD of GmCOL20. (O) LD of GmCOL22. (P) LD of GmCOL23. (Q) LD of GmCOL24. (R) LD of GmCOL25. (S) LD of GmCOL26. (T) LD of GmCOL28.

Haplotype Analysis and Its Association With Maturity Groups of Soybean Varieties

Based on LD and sequence clustering, haplotype definition was analyzed for the 21 soybean GmCOL gene families in the 128 varieties investigated. A total of 21 haplotypes of the GmCOL gene family variation types and polymorphic sites used for composing haplotypes are listed in Figure 2 and Supplementary Tables 3, 4 (Supplementary Figures 1, 2), respectively. Supplementary Table 5 shows 21 GmCOL protein groups associated with haplotypes.

GmCOL2-Hap2 was dominant in the 41 accessions covering all maturity groups, except MG X. GmCOL2-Hap4 showed early flowering compared with the other haplotype groups (Figures 2B3,B4, Table 2, and Supplementary Table 3). GmCOL4-Hap1 accounted for 99 varieties, with all maturity groups excluding MG X (Supplementary Figure 1A2). GmCOL4-Hap1 had an earlier flowering date in 2016. GmCOL5-Hap2 was present in 56 accessions, covering all maturity groups (Figure 2D1). GmCOL6-Hap1 was the most abundant in 70 varieties from different maturity groups, including MG 0000-MG V and MG VIII-MG X (Supplementary Figure 1B1). Among the 11 haplotypes, GmCOL9-Hap1 was dominant in 67 varieties from maturity groups MG 0000-MG X (Supplementary Figures 1D1,D2). GmCOL9-Hap3 and GmCOL9-Hap4 were distributed in a few varieties, and the flowering time for both haplotypes was early. GmCOL10-Hap1 was the most abundantly expressed in 91 varieties from all maturity groups except MG X (Supplementary Figures 1E1,E2). GmCOL16-Hap1 was rich in accessions distributed in the maturity groups MG 0000-MG VIII (Supplementary Figures 1I1,I2). GmCOL20-Hap2 was present in 52 varieties from all maturity groups (MG 0000-MG X) (Supplementary Figures 2B1,B2). Among all the haplotypes of GmCOL28, GmCOL28-Hap1 was the most common, accounting for 59 accessions, and was distributed in the maturity groups MG 0000, MG 00, MG 0, MG I-MG VIII, and MG X (Supplementary Figures 2H1,H2). In this experiment, no haplotype variants were found in GmCOL1 and GmCOL3 (Figures 2A,C). The Hap1 series of haplotypes of GmCOL8/13/14/15/19/22/23/24/25/26 was the most abundant in the varieties and was distributed in all 14 maturity groups (Supplementary Figures 1C1,F1,G1,H1, 2A1,C1,D1,E1,F1,G1).

Haplotypes Associated With Flowering Time

The haplotype groups of 21 gene families are presented in Table 3. An analysis of variance (ANOVA) was performed to elucidate the natural variations in flowering time (VE-R1) of the GmCOL gene families based on haplotype groups. In this analysis, eight genes (GmCOL2/5/9/13/15/16/25/28) showed significant results from the first emergence to the first flowering date (VE-R1) in both years, and three genes [GmCOL8 (2015), GmCOL22 (2015), and GmCOL26 (2016)] exhibited significant results in a single year (Supplementary Table 6). The remaining genes (GmCOL4/6/10/14/19/20/23/24) did not show significant results in these years. Notably, GmCOL1 and GmCOL3 were the most conserved, and no polymorphisms in the coding region were observed.

TABLE 3.

Haplotype frequency of GmCOL family genes.

Haplotype
GmCOL2 Hap1 Hap2 Hap3 Hap4 Hap5 Hap6 Hap7 Hap8 Hap9 Hap10 Hap11
Accessions 18 41 20 17 3 3 3 3 1 1 1
GmCOL4 Hap1 Hap2 Hap3 Hap4 Hap5
Accessions 99 7 4 4 1
GmCOL5 Hap1 Hap2 Hap3 Hap4 Hap5
Accessions 51 56 1 1 1
GmCOL6 Hap1 Hap2 Hap3 Hap4 Hap5
Accessions 70 46 5 1 1
GmCOL8 Hap1 Hap2
Accessions 88 11
GmCOL9 Hap1 Hap2 Hap3 Hap4 Hap5 Hap6 Hap7 Hap8 Hap9 Hap10 Hap11
Accessions 67 25 4 4 3 1 1 1 1 1 1
GmCOL10 Hap1 Hap2 Hap3 Hap4
Accessions 91 16 1 1
GmCOL13 Hap1 Hap2 Hap3
Accessions 122 5 1
GmCOL14 Hap1 Hap2 Hap3
Accessions 114 1 1
GmCOL15 Hap1 Hap2 Hap3 Hap4
Accessions 107 5 2 1
GmCOL16 Hap1 Hap2 Hap3 Hap4 Hap5 Hap6 Hap7 Hap8 Hap9
Accessions 54 25 24 6 5 4 2 2 1
GmCOL19 Hap1 Hap2 Hap3 Hap4 Hap5
Accessions 99 17 2 2 1
GmCOL20 Hap1 Hap2 Hap3 Hap4 Hap5 Hap6 Hap7 Hap8 Hap9 Hap10
Accessions 19 52 27 8 2 2 1 1 1 1
GmCOL22 Hap1 Hap2 Hap3 Hap4 Hap5 Hap6
Accessions 110 7 4 3 2 1
GmCOL23 Hap1 Hap2 Hap3 Hap4 Hap5 Hap6 Hap7 Hap8 Hap9 Hap10
Accessions 80 4 3 2 1 1 1 1 1 1
GmCOL24 Hap1 Hap2 Hap3 Hap4 Hap5
Accessions 88 5 3 1 1
GmCOL25 Hap1 Hap2 Hap3 Hap4 Hap5
Accessions 89 9 6 6 1
GmCOL26 Hap1 Hap2 Hap3 Hap4
Accessions 61 56 7 2
GmCOL28 Hap1 Hap2 Hap3
Accessions 59 29 22
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Among the 11 haplotype groups of GmCOL2, 4 were analyzed, and GmCOL2-Hap3 was significantly different from every other haplotype group (Figure 4A). The GmCOL2-Hap1/2/4 haplotype groups, which appeared in the above haplotype group, were not significantly different from each other. Analysis of GmCOL5 showed that in both years two major haplotypes showed significant differences from each other, and Hap2 was related to late flowering compared with Hap1 (Figure 4B). In terms of GmCOL5 Hap2 (S999), the original nucleotide (A499) was mutated to G499 in the coding sequence, resulting in a missense mutation in the amino acid sequence (K167 to E167). K167 was located between the B-box and the CCT domain. In comparison, GmCOL9, Hap1, and Hap2 (Figure 4C) did not show significant differences from each other, and both were significantly different from GmCOL9-Hap3 and GmCOL9-Hap4 only in 2015. Likewise, GmCOL13-Hap2/3 (Figure 4D) was closely associated with flowering time because both were significantly different from GmCOL13-Hap1 in both years.

FIGURE 4.

FIGURE 4

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Haplotypes of GmCOL genes in relation to flowering time (2015–2016). The relationship between flowering time and haplotype of GmCOL2 (A), GmCOL5 (B), GmCOL9 (C), GmCOL13 (D), GmCOL15 (E), GmCOL16 (F), GmCOL25 (G), and GmCOL28 (H).

For GmCOL13 Hap2/3 (S584), the original nucleotide (G84) was mutated to A84 in the coding sequence, resulting in a silent mutation in the no. 28 amino acid sequence, which was located in the first B-box. In both years, GmCOL15-Hap3/4 (Figure 4E) showed a significant difference compared with GmCOL15-Hap1/2. For GmCOL16, the haplotypes showed non-significant results among the four haplotypes (Hap1, Hap2, Hap3, and Hap4) (Figure 4F). In the first year, five haplotypes of GmCOL25 (Hap1, Hap2, Hap3, Hap4, and Hap5) were not significantly different from each other, whereas Hap3 and Hap4 were significantly different from Hap1, Hap2, and Hap5 in the second year (Figure 4G). Hap2 of GmCOL28 was significantly different from Hap1 and Hap3 in both years (Figure 4H). For GmCOL28 Hap2 (S1066), the original nucleotide (T263) was mutated to C263 in the coding sequence, resulting in a missense mutation in the amino acid sequence (V88 to A88), which was located in the first B-box, and may affect the protein and protein interaction. Thus, the results revealed that Hap2 of GmCOL28 was closely associated with flowering time.

Discussion

Selected Soybean Varieties Showed Diversity in Flowering Time and Maturity

The varieties analyzed in this study showed the diversity of flowering time and maturity, which indicated that the flowering time (VE-R1) and the days from emergence to physiological maturity (VE-R7) were related to the variety trait and natural environment (Jiang et al., 2019). According to the photoperiod responses, many soybean varieties have evolved to adapt to a broad range of growing areas in China (Wang et al., 2016). The flowering time of the selected varieties ranged from 21 to 121 days and 13.66 to 109.2 days, and the maturity time ranged from 61.2 to 150.7 days and 68.4 to 144.4 days, respectively, for two consecutive years (2015 and 2016) (Jiang et al., 2019), indicating high diversity (Table 2). However, Paula showed the shortest VE-R1 in the 2nd year, with the maturity group MG 0000. Paula is recognized as a high-latitude cold region (HCR) soybean variety and HCR soybean, which typically matures early (Jia et al., 2014). This observation suggested that the maturity group MG 0000 was relatively stable for days to start flowering from emergence.

GmCOL Orthologs Showed Divergence in Sequence Polymorphism

It has been shown that GmCOL1a (Glyma08g28370) and GmCOL1b (Glyma18g51320) in soybean are the closest Arabidopsis COL2 orthologs to CO (Thakare et al., 2010). The transgenic soybean line overexpressing GmCOL1a flowered late under long-day or natural conditions (Cao et al., 2015). There is a single-nucleotide substitution at the GmCOL1b CCT domain in the gmcol1b mutant, leading to the mutagenesis of conserved threonine at amino acid 314 into isoleucine, which results in early flowering of the gmcol1b mutant (Cao et al., 2015). In this study, the varieties that were taken for the observation of natural variations regarding flowering time and maturation showed divergent characteristics in flowering time (Jiang et al., 2019). Allelic variation can have an effect on flowering time (Irwin et al., 2016). In this study, the insertion and single-nucleotide substitution (InDel918, InDel919, InDel920, s958, s1138, s1139, s1218, and s1260) found in the first exon in GmCOL2 led to missense mutations, which might have an effect on flowering time and maturity. The other genes in the GmCOL family showed various types of point mutations (Figure 2 and Supplementary Figures 1–5). The loss of functions may have an impact on gene function, and the presence of these mutations suggested that polymorphism could be the main cause of the diversity of soybean flowering time.

Polymorphism of GmCOL Family Genes Was Associated With Flowering Time and Maturity

Haplotype-based analyses have been successfully carried out in different crops, such as maize (Zea mays L.) (Weber et al., 2009; Van Inghelandt et al., 2012; Lipka et al., 2013), rice (Oryza sativa L.) (Lestari et al., 2011; Yonemaru et al., 2012, 2014; Shao et al., 2013; Wu et al., 2020), and soybean (Choi et al., 2007; Li et al., 2009; Langewisch et al., 2014; Patil et al., 2016; Jiang et al., 2019). In this study, some polymorphic sites were identified and utilized by conducting a haplotype analysis of 21 soybean GmCOL gene families. Based on LD analysis and polymorphic sites, tagging haplotypes composed of some SNPs and InDels indicated that there were 7 polymorphic sites in GmCOL2 and just 3 polymorphic sites in GmCOL10 and 46 and 10 polymorphic sites in GmCOL2 and GmCOL10, respectively (Supplementary Table 4). In addition, some haplotypes associated with flowering date and maturity (such as GmCOL2-Hap1, Hap2, and Hap4; GmCOL9-Hap1, Hap2, Hap3, and Hap4; GmCOL13-Hap1, Hap2, and Hap3; GmCOL15-Hap1, Hap2, Hap3, and Hap4; GmCOL16-Hap1, Hap2, Hap3, Hap4, and Hap5; and GmCOL25-Hap1, Hap2, Hap3, Hap4, and Hap5) were distributed in varieties with different maturity groups. The LD differences among the 21 soybean COL gene families may reflect selection pressure and, to some extent, the process of natural selection and domestication.

Conclusion

In summary, 21 GmCOL genes exhibited natural divergence in association with flowering and growth periods. Significant changes were found in 21 COL genome sequences, among which GmCOL1, GmCOL3, GmCOL8, GmCOL9, GmCOL10, and GmCOL13 were conserved, but the sequences of the remaining COL genes showed a wide range of changes that could alter their function. In this study, it was noticed that additional polymorphisms linked to the 21 GmCOL gene families in trait-controlling regions might have a significant impact on flowering time and maturity.

Data Availability Statement

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found in the article/Supplementary Material.

Author Contributions

MA conducted the major phenotypic and genotypic works. SZ, RE, WS, TW, and BJ joined the experiments. SY, CW, WH, SS, and YF provided the materials and technical supports. MA, RE, and BJ prepared the initial draft of the manuscript. FC rewrote the manuscript. FC, BJ, MA, RE, and TH revised the manuscript. TH coordinated and supervised the project. All authors read and approved the final manuscript.

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher’s Note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Footnotes

Funding

This work was supported by grants from the National Key R&D Program of China (2021YFF1001203 and 2017YFD0101400), China Agriculture Research System (CARS-04), and CAAS Agricultural Science and Technology Innovation Project.

Supplementary Material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fpls.2022.817544/full#supplementary-material

Supplementary Figure 1

Haplotype analysis, distribution in different maturity groups, and flowering time (VE-R1) in the main haplotypes of approximately nine GmCOL family genes. (A,A1) Haplotypes of GmCOL4. (A2) Haplotype distribution of GmCOL4 in different maturity groups. (A3) Flowering time (VE-R1) of the main haplotypes of GmCOL4 in 2015. (A4) Flowering time (VE-R1) of the main haplotypes of GmCOL4 in 2016. (B,B1) Haplotypes of GmCOL6. (B2) Haplotype distribution of GmCOL6 in different maturity groups. (B3) Flowering time (VE-R1) of the main haplotypes of GmCOL6 in 2015. (B4) Flowering time (VE-R1) of the main haplotypes of GmCOL6 in 2016. (C,C1) Haplotypes of GmCOL8. (C2) Haplotype distribution of GmCOL8 in different maturity groups. (C3) Flowering time (VE-R1) of the main haplotypes of GmCOL8 in 2015. (C4) Flowering time (VE-R1) of the main haplotypes of GmCOL8 in 2016. (D,D1) Haplotypes of GmCOL9 (1) and GmCOL9 (2). (D2) Haplotype distribution of GmCOL9 in different maturity groups. (D3) Flowering time (VE-R1) of the main haplotypes of GmCOL9 in 2015. (D4) Flowering time (VE-R1) of the main haplotypes of GmCOL9 in 2016. (E,E1) Haplotypes of GmCOL10. (E2) Haplotype distribution of GmCOL10 in different maturity groups. (E3) Flowering time (VE-R1) of the main haplotypes of GmCOL10 in 2015. (E4) Flowering time (VE-R1) of the main haplotypes of GmCOL10 in 2016. (F,F1) Haplotypes of GmCOL13. (F2) Haplotype distribution of GmCOL13 in different maturity groups. (F3) Flowering time (VE-R1) of the main haplotypes of GmCOL13 in 2015. (F4) Flowering time (VE-R1) of the main haplotypes of GmCOL13 in 2016. (G,G1) Haplotypes of GmCOL14. (G2) Haplotype distribution of GmCOL14 in different maturity groups. (G3) Flowering time (VE-R1) of the main haplotypes of GmCOL14 in 2015. (G4) Flowering time (VE-R1) of the main haplotypes of GmCOL14 in 2016. (H,H1) Haplotypes of GmCOL15. (H2) Haplotype distribution of GmCOL15 in different maturity groups. (H3) Flowering time (VE-R1) of the main haplotypes of GmCOL15 in 2015. (H4) Flowering time (VE-R1) of the main haplotypes of GmCOL15 in 2016. (I,I1) Haplotypes of GmCOL16 (1), GmCOL16 (2), GmCOL16 (3), and GmCOL16 (4). (I2) Haplotype distribution of GmCOL16 in different maturity groups. (I3) Flowering time (VE-R1) of the main haplotypes of GmCOL16 in 2015. (I4) Flowering time (VE-R1) of the main haplotypes of GmCOL16 in 2016.

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Supplementary Figure 2

Haplotype analysis, distribution in different maturity groups, and flowering time (VE-R1) in the main haplotypes of approximately eight GmCOL family genes. (A,A1) Haplotypes of GmCOL19. (A2) Haplotype distribution of GmCOL19 in different maturity groups. (A3) Flowering time (VE-R1) of the main haplotypes of GmCOL19 in 2015. (A4) Flowering time (VE-R1) of the main haplotypes of GmCOL19 in 2016. (B,B1) Haplotypes of GmCOL20 (1), GmCOL20 (2), and GmCOL20 (3). (B2) Haplotype distribution of GmCOL20 in different maturity groups. (B3) Flowering time (VE-R1) of the main haplotypes of GmCOL20 in 2015. (B4) Flowering time (VE-R1) of the main haplotypes of GmCOL20 in 2016. (C,C1) Haplotypes of GmCOL22 (1) and GmCOL22 (2). (C2) Haplotype distribution of GmCOL22 in different maturity groups. (C3) Flowering time (VE-R1) of the main haplotypes of GmCOL22 in 2015. (C4) Flowering time (VER1) of the main haplotypes of GmCOL22 in 2016. (D,D1) Haplotypes of GmCOL23 (1) and GmCOL23 (2). (D2) Haplotype distribution of GmCOL23 in different maturity groups. (D3) Flowering time (VE-R1) of the main haplotypes of GmCOL23 in 2015. (D4) Flowering time (VE-R1) of the main haplotypes of GmCOL23 in 2016. (E,E1) Haplotypes of GmCOL24. (E2) Haplotype distribution of GmCOL24 in different maturity groups. (E3) Flowering time (VE-R1) of the main haplotypes of GmCOL24 in 2015. (E4) Flowering time (VE-R1) of the main haplotypes of GmCOL24 in 2016. (F,F1) Haplotypes of GmCOL25. (F2) Haplotype distribution of GmCOL25 in different maturity groups. (F3) Flowering time (VE-R1) of the main haplotypes of GmCOL25 in 2015. (F4) Flowering time (VE-R1) of the main haplotypes of GmCOL25 in 2016. (G,G1) Haplotypes of GmCOL26. (G2) Haplotype distribution of GmCOL26 in different maturity groups. (G3) Flowering time (VE-R1) of the main haplotypes of GmCOL26 in 2015. (G4) Flowering time (VE-R1) of the main haplotypes of GmCOL26 in 2016. (H,H1) Haplotypes of GmCOL28 (1) and GmCOL28 (2). (H2) Haplotype distribution of GmCOL28 in different maturity groups. (H3) Flowering time (VE-R1) of the main haplotypes of GmCOL28 in 2015. (H4) Flowering time (VE-R1) of the main haplotypes of GmCOL28 in 2016.

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References

  1. Alonso-Blanco C., Mendez-Vigo B., Koornneef M. (2005). From phenotypic to molecular polymorphisms involved in naturally occurring variation of plant development. Int. J. Dev. Biol. 49 717–732. 10.1387/ijdb.051994ca [DOI] [PubMed] [Google Scholar]
  2. An H., Roussot C., Suarez-Lopez P., Corbesier L., Vincent C., Pineiro M., et al. (2004). CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. Development 131 3615–3626. 10.1242/dev.01231 [DOI] [PubMed] [Google Scholar]
  3. Balasubramanian S., Sureshkumar S., Agrawal M., Michael T. P., Wessinger C., Maloof J. N., et al. (2006). The PHYTOCHROME C photoreceptor gene mediates natural variation in flowering and growth responses of Arabidopsis thaliana. Nat. Genet. 38 711–715. 10.1038/ng1818 [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bao S., Hua C., Huang G., Cheng P., Gong X., Shen L., et al. (2019). Molecular Basis of Natural Variation in Photoperiodic Flowering Responses. Dev. Cell 50 90–101e103. 10.1016/j.devcel.2019.05.018 [DOI] [PubMed] [Google Scholar]
  5. Bu T., Lu S., Wang K., Dong L., Li S., Xie Q., et al. (2021). A critical role of the soybean evening complex in the control of photoperiod sensitivity and adaptation. Proc. Natl. Acad. Sci. U S A 118 e2010241118. 10.1073/pnas.2010241118 [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cao D., Li Y., Lu S., Wang J., Nan H., Li X., et al. (2015). GmCOL1a and GmCOL1b Function as Flowering Repressors in Soybean Under Long-Day Conditions. Plant Cell Physiol. 56 2409–2422. 10.1093/pcp/pcv152 [DOI] [PubMed] [Google Scholar]
  7. Cheng Z., Zhang X., Huang P., Huang G., Zhu J., Chen F., et al. (2020). Nup96 and HOS1 Are Mutually Stabilized and Gate CONSTANS Protein Level, Conferring Long-Day Photoperiodic Flowering Regulation in Arabidopsis. Plant Cell 32 374–391. 10.1105/tpc.19.00661 [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Choi I. Y., Hyten D. L., Matukumalli L. K., Song Q., Chaky J. M., Quigley C. V., et al. (2007). A soybean transcript map: gene distribution, haplotype and single-nucleotide polymorphism analysis. Genetics 176 685–696. 10.1534/genetics.107.070821 [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dong L., Fang C., Cheng Q., Su T., Kou K., Kong L., et al. (2021b). Genetic basis and adaptation trajectory of soybean from its temperate origin to tropics. Nat. Commun. 12:5445. 10.1038/s41467-021-25800-3 [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dong L., Cheng Q., Fang C., Kong L., Yang H., Hou Z., et al. (2021a). Parallel selection of distinct Tof5 alleles drove the adaptation of cultivated and wild soybean to high latitude. Mol. Plant 15 308–321. 10.1016/j.molp.2021.10.004 [DOI] [PubMed] [Google Scholar]
  11. Fan C., Hu R., Zhang X., Wang X., Zhang W., Zhang Q., et al. (2014). Conserved CO-FT regulons contribute to the photoperiod flowering control in soybean. BMC Plant Biol. 14:9. 10.1186/1471-2229-14-9 [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fang C., Liu J., Zhang T., Su T., Li S., Cheng Q., et al. (2021). A recent retrotransposon insertion of J caused E6 locus facilitating soybean adaptation into low latitude. J. Integr. Plant Biol. 63 995–1003. 10.1111/jipb.13034 [DOI] [PubMed] [Google Scholar]
  13. Fang X., Han Y., Liu M., Jiang J., Li X., Lian Q., et al. (2021). Modulation of evening complex activity enables north-to-south adaptation of soybean. Sci. China Life Sci. 64 179–195. 10.1007/s11427-020-1832-2 [DOI] [PubMed] [Google Scholar]
  14. Fehr W. R., Caviness C. E. (1977). Stages of Soybean Development. Special Report No.80. Cooperative Extension Service, Agriculture and Home Economic Experiment Station Ames. Iowa: Iowa State University. [Google Scholar]
  15. Fornara F., Panigrahi K. C., Gissot L., Sauerbrunn N., Ruhl M., Jarillo J. A., et al. (2009). Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response. Dev. Cell 17 75–86. 10.1016/j.devcel.2009.06.015 [DOI] [PubMed] [Google Scholar]
  16. Gangappa S. N., Botto J. F. (2014). The BBX family of plant transcription factors. Trends Plant Sci. 19 460–470. 10.1016/j.tplants.2014.01.010 [DOI] [PubMed] [Google Scholar]
  17. Imaizumi T., Schultz T. F., Harmon F. G., Ho L. A., Kay S. A. (2005). FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science 309 293–297. 10.1126/science.1110586 [DOI] [PubMed] [Google Scholar]
  18. Irwin J. A., Soumpourou E., Lister C., Ligthart J. D., Kennedy S., Dean C. (2016). Nucleotide polymorphism affecting FLC expression underpins heading date variation in horticultural brassicas. Plant J. 87 597–605. 10.1111/tpj.13221 [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Jang S., Marchal V., Panigrahi K. C., Wenkel S., Soppe W., Deng X. W., et al. (2008). Arabidopsis COP1 shapes the temporal pattern of CO accumulation conferring a photoperiodic flowering response. EMBO J. 27 1277–1288. 10.1038/emboj.2008.68 [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Jia H., Jiang B., Wu C., Lu W., Hou W., Sun S., et al. (2014). Maturity group classification and maturity locus genotyping of early-maturing soybean varieties from high-latitude cold regions. PLoS One 9:e94139. 10.1371/journal.pone.0094139 [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Jiang B., Zhang S., Song W., Khan M. A. A., Sun S., Zhang C., et al. (2019). Natural variations of FT family genes in soybean varieties covering a wide range of maturity groups. BMC Genom. 20:230. 10.1186/s12864-019-5577-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kong F. J., Nan H. Y., Cao D., Li Y., Wu F. F., Wang J. L., et al. (2014). A New Dominant Gene E9 Conditions Early Flowering and Maturity in Soybean. Crop Sci. 54 2529–2535. [Google Scholar]
  23. Langewisch T., Zhang H., Vincent R., Joshi T., Xu D., Bilyeu K., et al. (2014). Major soybean maturity gene haplotypes revealed by SNPViz analysis of 72 sequenced soybean genomes. PLoS One 9:e94150. 10.1371/journal.pone.0094150 [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Laubinger S., Marchal V., Le Gourrierec J., Wenkel S., Adrian J., Jang S., et al. (2006). Arabidopsis SPA proteins regulate photoperiodic flowering and interact with the floral inducer CONSTANS to regulate its stability. Development 133 3213–3222. 10.1242/dev.02481 [DOI] [PubMed] [Google Scholar]
  25. Lazaro A., Mouriz A., Pineiro M., Jarillo J. A. (2015). Red Light-Mediated Degradation of CONSTANS by the E3 Ubiquitin Ligase HOS1 Regulates Photoperiodic Flowering in Arabidopsis. Plant Cell 27 2437–2454. 10.1105/tpc.15.00529 [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lazaro A., Valverde F., Pineiro M., Jarillo J. A. (2012). The Arabidopsis E3 ubiquitin ligase HOS1 negatively regulates CONSTANS abundance in the photoperiodic control of flowering. Plant Cell 24 982–999. 10.1105/tpc.110.081885 [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Lestari P., Lee G., Ham T. H., Reflinur Woo M. O., Piao R. (2011). Single nucleotide polymorphisms and haplotype diversity in rice sucrose synthase 3. J. Hered. 102 735–746. 10.1093/jhered/esr094 [DOI] [PubMed] [Google Scholar]
  28. Li C., Li Y. H., Li Y., Lu H., Hong H., Tian Y., et al. (2020). A Domestication-Associated Gene GmPRR3b Regulates the Circadian Clock and Flowering Time in Soybean. Mol. Plant 13 745–759. 10.1016/j.molp.2020.01.014 [DOI] [PubMed] [Google Scholar]
  29. Li J., Wang X., Song W., Huang X., Zhou J., Zeng H., et al. (2017). Genetic variation of maturity groups and four E genes in the Chinese soybean mini core collection. PLoS One 12:e0172106. 10.1371/journal.pone.0172106 [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Li Y. H., Zhang C., Gao Z. S., Smulders M. J. M., Ma Z. L., Liu Z. X., et al. (2009). Development of SNP markers and haplotype analysis of the candidate gene for rhg1, which confers resistance to soybean cyst nematode in soybean. Mol. Breeding 24 63–76. 10.3389/fpls.2019.00401 [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Lipka A. E., Gore M. A., Magallanes-Lundback M., Mesberg A., Lin H., Tiede T., et al. (2013). Genome-wide association study and pathway-level analysis of tocochromanol levels in maize grain. G3 3 1287–1299. 10.1534/g3.113.006148 [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Liu B., Kanazawa A., Matsumura H., Takahashi R., Harada K., Abe J. (2008). Genetic redundancy in soybean photoresponses associated with duplication of the phytochrome A gene. Genetics 180 995–1007. 10.1534/genetics.108.092742 [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Liu L. J., Zhang Y. C., Li Q. H., Sang Y., Mao J., Lian H. L., et al. (2008). COP1-mediated ubiquitination of CONSTANS is implicated in cryptochrome regulation of flowering in Arabidopsis. Plant Cell 20 292–306. 10.1105/tpc.107.057281 [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Liu X., Wu J. A., Ren H., Qi Y., Li C., Cao J., et al. (2017). Genetic variation of world soybean maturity date and geographic distribution of maturity groups. Breed. Sci. 67 221–232. 10.1270/jsbbs.16167 [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Lu S., Dong L., Fang C., Liu S., Kong L., Cheng Q., et al. (2020). Stepwise selection on homeologous PRR genes controlling flowering and maturity during soybean domestication. Nat. Genet. 52 428–436. 10.1038/s41588-020-0604-7 [DOI] [PubMed] [Google Scholar]
  36. Lu S., Zhao X., Hu Y., Liu S., Nan H., Li X., et al. (2017). Natural variation at the soybean J locus improves adaptation to the tropics and enhances yield. Nat. Genet. 49 773–779. 10.1038/ng.3819 [DOI] [PubMed] [Google Scholar]
  37. Patil G., Do T., Vuong T. D., Valliyodan B., Lee J. D., Chaudhary J., et al. (2016). Genomic-assisted haplotype analysis and the development of high-throughput SNP markers for salinity tolerance in soybean. Sci. Rep. 6:19199. 10.1038/srep19199 [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Putterill J., Robson F., Lee K., Simon R., Coupland G. (1995). The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80 847–857. 10.1016/0092-8674(95)90288-0 [DOI] [PubMed] [Google Scholar]
  39. Robson F., Costa M. M., Hepworth S. R., Vizir I., Pineiro M., Reeves P. H., et al. (2001). Functional importance of conserved domains in the flowering-time gene CONSTANS demonstrated by analysis of mutant alleles and transgenic plants. Plant J. 28 619–631. 10.1046/j.1365-313x.2001.01163.x [DOI] [PubMed] [Google Scholar]
  40. Rosas U., Mei Y., Xie Q., Banta J. A., Zhou R. W., Seufferheld G., et al. (2014). Variation in Arabidopsis flowering time associated with cis-regulatory variation in CONSTANS. Nat. Commun. 5:3651. 10.1038/ncomms4651 [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Samanfar B., Molnar S. J., Charette M., Schoenrock A., Dehne F., Golshani A., et al. (2017). Mapping and identification of a potential candidate gene for a novel maturity locus. E10, in soybean Theor. Appl. Genet. 130 377–390. 10.1007/s00122-016-2819-7 [DOI] [PubMed] [Google Scholar]
  42. Sawa M., Nusinow D. A., Kay S. A., Imaizumi T. (2007). FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science 318 261–265. 10.1126/science.1146994 [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Shao G., Tang S., Chen M., Wei X., He J., Luo J., et al. (2013). Haplotype variation at Badh2, the gene determining fragrance in rice. Genomics 101 157–162. 10.1016/j.ygeno.2012.11.010 [DOI] [PubMed] [Google Scholar]
  44. Strayer C., Oyama T., Schultz T. F., Raman R., Somers D. E., Mas P., et al. (2000). Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science 289 768–771. 10.1126/science.289.5480.768 [DOI] [PubMed] [Google Scholar]
  45. Suarez-Lopez P., Wheatley K., Robson F., Onouchi H., Valverde F., Coupland G., et al. (2001). CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410 1116–1120. 10.1038/35074138 [DOI] [PubMed] [Google Scholar]
  46. Sun J., Wang M., Zhao C., Liu T., Liu Z., Fan Y., et al. (2021). GmFULc Is Induced by Short Days in Soybean and May Accelerate Flowering in Transgenic Arabidopsis thaliana. Int. J. Mol. Sci. 22:10333. 10.3390/ijms221910333 [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Takada S., Goto K. (2003). Terminal flower2, an Arabidopsis homolog of heterochromatin protein1, counteracts the activation of flowering locus T by constans in the vascular tissues of leaves to regulate flowering time. Plant Cell 15 2856–2865. 10.1105/tpc.016345 [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Thakare D., Kumudini S., Dinkins R. D. (2010). Expression of flowering-time genes in soybean E1 near-isogenic lines under short and long day conditions. Planta 231 951–963. 10.1007/s00425-010-1100-6 [DOI] [PubMed] [Google Scholar]
  49. Valverde F., Mouradov A., Soppe W., Ravenscroft D., Samach A., Coupland G., et al. (2004). Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303 1003–1006. 10.1126/science.1091761 [DOI] [PubMed] [Google Scholar]
  50. Van Inghelandt D., Melchinger A. E., Martinant J. P., Stich B. (2012). Genome-wide association mapping of flowering time and northern corn leaf blight (Setosphaeria turcica) resistance in a vast commercial maize germplasm set. BMC Plant Biol. 12:56. 10.1186/1471-2229-12-56 [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Wang F. F., Nan H. Y., Chen L. Y., Fang C., Zhang H. Y., Su T., et al. (2019). A new dominant locus, E11, controls early flowering time and maturity in soybean. Mol. Breeding 39:70. [Google Scholar]
  52. Wang L., Sun S., Wu T., Liu L., Sun X., Cai Y., et al. (2020). Natural variation and CRISPR/Cas9-mediated mutation in GmPRR37 affect photoperiodic flowering and contribute to regional adaptation of soybean. Plant Biotechnol. J. 18 1869–1881. 10.1111/pbi.13346 [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Wang X. B., Liu Z. X., Yang C. Y., Xu R., Lu W. G., Zhang L. F., et al. (2016). Stability of growth periods traits for soybean cultivars across multiple locations. J. Integr. Agr. 15 963–972. 10.1016/s2095-3119(15)61152-2 [DOI] [Google Scholar]
  54. Watanabe S., Hideshima R., Xia Z., Tsubokura Y., Sato S., Nakamoto Y., et al. (2009). Map-based cloning of the gene associated with the soybean maturity locus E3. Genetics 182 1251–1262. 10.1534/genetics.108.098772 [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Watanabe S., Xia Z., Hideshima R., Tsubokura Y., Sato S., Yamanaka N., et al. (2011). A map-based cloning strategy employing a residual heterozygous line reveals that the GIGANTEA gene is involved in soybean maturity and flowering. Genetics 188 395–407. 10.1534/genetics.110.125062 [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Weber A. L., Zhao Q., McMullen M. D., Doebley J. F. (2009). Using association mapping in teosinte to investigate the function of maize selection-candidate genes. PLoS One 4:e8227. 10.1371/journal.pone.0008227 [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Wu C. C., Wei F. J., Chiou W. Y., Tsai Y. C., Wu H. P., Gotarkar D., et al. (2020). Studies of rice Hd1 haplotypes worldwide reveal adaptation of flowering time to different environments. PLoS One 15:e0239028. 10.1371/journal.pone.0239028 [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Wu F., Kang X., Wang M., Haider W., Price W. B., Hajek B., et al. (2019). Transcriptome-Enabled Network Inference Revealed the GmCOL1 Feed-Forward Loop and Its Roles in Photoperiodic Flowering of Soybean. Front. Plant Sci. 10:1221. 10.3389/fpls.2019.01221 [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Wu F., Price B. W., Haider W., Seufferheld G., Nelson R., Hanzawa Y. (2014). Functional and evolutionary characterization of the CONSTANS gene family in short-day photoperiodic flowering in soybean. PLoS One 9:e85754. 10.1371/journal.pone.0085754 [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Xia Z., Watanabe S., Yamada T., Tsubokura Y., Nakashima H., Zhai H., et al. (2012). Positional cloning and characterization reveal the molecular basis for soybean maturity locus E1 that regulates photoperiodic flowering. Proc. Natl. Acad. Sci. U S A 109 E2155–E2164. 10.1073/pnas.1117982109 [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Yonemaru J., Ebana K., Yano M. (2014). HapRice, an SNP haplotype database and a web tool for rice. Plant Cell Physiol. 55 e9. 10.1093/pcp/pct188 [DOI] [PubMed] [Google Scholar]
  62. Yonemaru J., Yamamoto T., Ebana K., Yamamoto E., Nagasaki H., Shibaya T., et al. (2012). Genome-wide haplotype changes produced by artificial selection during modern rice breeding in Japan. PLoS One 7:e32982. 10.1371/journal.pone.0032982 [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Yue Y., Liu N., Jiang B., Li M., Wang H., Jiang Z., et al. (2017). A Single Nucleotide Deletion in J Encoding GmELF3 Confers Long Juvenility and Is Associated with Adaptation of Tropic Soybean. Mol. Plant 10 656–658. 10.1016/j.molp.2016.12.004 [DOI] [PubMed] [Google Scholar]
  64. Yue Y. L., Sun S., Li J. W., Yu H. D., Wu H. X., Sun B. Q., et al. (2021). GmFULa improves soybean yield by enhancing carbon assimilation without altering flowering time or maturity. Plant Cell Rep. 40 1875–1888. 10.1007/s00299-021-02752-y [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplementary Figure 1

Haplotype analysis, distribution in different maturity groups, and flowering time (VE-R1) in the main haplotypes of approximately nine GmCOL family genes. (A,A1) Haplotypes of GmCOL4. (A2) Haplotype distribution of GmCOL4 in different maturity groups. (A3) Flowering time (VE-R1) of the main haplotypes of GmCOL4 in 2015. (A4) Flowering time (VE-R1) of the main haplotypes of GmCOL4 in 2016. (B,B1) Haplotypes of GmCOL6. (B2) Haplotype distribution of GmCOL6 in different maturity groups. (B3) Flowering time (VE-R1) of the main haplotypes of GmCOL6 in 2015. (B4) Flowering time (VE-R1) of the main haplotypes of GmCOL6 in 2016. (C,C1) Haplotypes of GmCOL8. (C2) Haplotype distribution of GmCOL8 in different maturity groups. (C3) Flowering time (VE-R1) of the main haplotypes of GmCOL8 in 2015. (C4) Flowering time (VE-R1) of the main haplotypes of GmCOL8 in 2016. (D,D1) Haplotypes of GmCOL9 (1) and GmCOL9 (2). (D2) Haplotype distribution of GmCOL9 in different maturity groups. (D3) Flowering time (VE-R1) of the main haplotypes of GmCOL9 in 2015. (D4) Flowering time (VE-R1) of the main haplotypes of GmCOL9 in 2016. (E,E1) Haplotypes of GmCOL10. (E2) Haplotype distribution of GmCOL10 in different maturity groups. (E3) Flowering time (VE-R1) of the main haplotypes of GmCOL10 in 2015. (E4) Flowering time (VE-R1) of the main haplotypes of GmCOL10 in 2016. (F,F1) Haplotypes of GmCOL13. (F2) Haplotype distribution of GmCOL13 in different maturity groups. (F3) Flowering time (VE-R1) of the main haplotypes of GmCOL13 in 2015. (F4) Flowering time (VE-R1) of the main haplotypes of GmCOL13 in 2016. (G,G1) Haplotypes of GmCOL14. (G2) Haplotype distribution of GmCOL14 in different maturity groups. (G3) Flowering time (VE-R1) of the main haplotypes of GmCOL14 in 2015. (G4) Flowering time (VE-R1) of the main haplotypes of GmCOL14 in 2016. (H,H1) Haplotypes of GmCOL15. (H2) Haplotype distribution of GmCOL15 in different maturity groups. (H3) Flowering time (VE-R1) of the main haplotypes of GmCOL15 in 2015. (H4) Flowering time (VE-R1) of the main haplotypes of GmCOL15 in 2016. (I,I1) Haplotypes of GmCOL16 (1), GmCOL16 (2), GmCOL16 (3), and GmCOL16 (4). (I2) Haplotype distribution of GmCOL16 in different maturity groups. (I3) Flowering time (VE-R1) of the main haplotypes of GmCOL16 in 2015. (I4) Flowering time (VE-R1) of the main haplotypes of GmCOL16 in 2016.

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Supplementary Figure 2

Haplotype analysis, distribution in different maturity groups, and flowering time (VE-R1) in the main haplotypes of approximately eight GmCOL family genes. (A,A1) Haplotypes of GmCOL19. (A2) Haplotype distribution of GmCOL19 in different maturity groups. (A3) Flowering time (VE-R1) of the main haplotypes of GmCOL19 in 2015. (A4) Flowering time (VE-R1) of the main haplotypes of GmCOL19 in 2016. (B,B1) Haplotypes of GmCOL20 (1), GmCOL20 (2), and GmCOL20 (3). (B2) Haplotype distribution of GmCOL20 in different maturity groups. (B3) Flowering time (VE-R1) of the main haplotypes of GmCOL20 in 2015. (B4) Flowering time (VE-R1) of the main haplotypes of GmCOL20 in 2016. (C,C1) Haplotypes of GmCOL22 (1) and GmCOL22 (2). (C2) Haplotype distribution of GmCOL22 in different maturity groups. (C3) Flowering time (VE-R1) of the main haplotypes of GmCOL22 in 2015. (C4) Flowering time (VER1) of the main haplotypes of GmCOL22 in 2016. (D,D1) Haplotypes of GmCOL23 (1) and GmCOL23 (2). (D2) Haplotype distribution of GmCOL23 in different maturity groups. (D3) Flowering time (VE-R1) of the main haplotypes of GmCOL23 in 2015. (D4) Flowering time (VE-R1) of the main haplotypes of GmCOL23 in 2016. (E,E1) Haplotypes of GmCOL24. (E2) Haplotype distribution of GmCOL24 in different maturity groups. (E3) Flowering time (VE-R1) of the main haplotypes of GmCOL24 in 2015. (E4) Flowering time (VE-R1) of the main haplotypes of GmCOL24 in 2016. (F,F1) Haplotypes of GmCOL25. (F2) Haplotype distribution of GmCOL25 in different maturity groups. (F3) Flowering time (VE-R1) of the main haplotypes of GmCOL25 in 2015. (F4) Flowering time (VE-R1) of the main haplotypes of GmCOL25 in 2016. (G,G1) Haplotypes of GmCOL26. (G2) Haplotype distribution of GmCOL26 in different maturity groups. (G3) Flowering time (VE-R1) of the main haplotypes of GmCOL26 in 2015. (G4) Flowering time (VE-R1) of the main haplotypes of GmCOL26 in 2016. (H,H1) Haplotypes of GmCOL28 (1) and GmCOL28 (2). (H2) Haplotype distribution of GmCOL28 in different maturity groups. (H3) Flowering time (VE-R1) of the main haplotypes of GmCOL28 in 2015. (H4) Flowering time (VE-R1) of the main haplotypes of GmCOL28 in 2016.

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Data Availability Statement

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found in the article/Supplementary Material.

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