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Acta Agronomica Sinica ›› 2021, Vol. 47 ›› Issue (12): 2299-2313.doi: 10.3724/SP.J.1006.2021.14022

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Research progress on genetic regulatory mechanism of seed color in soybean (Glycine max)

QIU Hong-Mei1(), CHEN Liang1, HOU Yun-Long1, WANG Xin-Feng1, CHEN Jian1, MA Xiao-Ping1, CUI Zheng-Guo1, ZHANG Ling1, HU Jin-Hai1, WANG Yue-Qiang1,*(), QIU Li-Juan2,*()   

  1. 1Jilin Academy of Agricultural Sciences / National Engineering Research Center for Soybean, Changchun 130033, Jilin, China
    2National Key Facility for Crop Gene Resources and Genetic Improvement (NFCRI) / Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China
  • Received:2021-01-24 Accepted:2021-05-17 Online:2021-12-12 Published:2021-05-26
  • Contact: WANG Yue-Qiang,QIU Li-Juan E-mail:qhm2001-2005@163.com;825164942@qq.com;qiulijuan@caas.cn
  • Supported by:
    National Key R&D Program for Crop Breeding(2016YFD01100201)

Abstract:

The color of soybean seeds is an important morphological marker and evolutionary trait. During the process of domestication, seed coat has gradually evolved from black to yellow, green, black, brown, and bicolor, and cotyledons has evolved from green to yellow. The dark seed coat contains anthocyanins, which are natural pigments with medicinal and nutritional values. Therefore, it is of great importance to study the genetic regulation mechanism of seed color for evolutionary theory, variety breeding, and practical application. The pigment content and composition of seeds result in diverse seed coat colors through complex molecular regulatory mechanisms. In this paper, we described the research progress on genetic loci, related genes, regulatory mechanisms, and flavonoid biosynthesis pathways that controlling the color of soybean seeds. Specifically, we introduced the 9 classical genetic loci I, R, T, O, W1, K1, G, D1, D2, and related molecular markers, as well as the interactions between the loci; 22 related genes that controlling seed color, and the regulatory mechanisms of some allelic variants; as well as the physiological functions of the flavonoid biosynthesis pathways and major metabolites involved in the related genes. The progress of researches on genetic regulation of the color of seed coat, seed hilum, and cotyledon in soybean was reviewed, in addition the regulatory network was mapped with genetic loci, genes, allelic regulatory mechanisms, and flavonoid metabolic pathways, in order to provide references for the quality of seed appearance and genetic improvement of anthocyanin components.

Key words: soybean, seed color, genetic regulation, related gene, flavonoid biosynthesis pathway

Table 1

Information of classical genetic loci controlling seed color"

遗传位点
Genetic locus
连锁群
Linkage group
染色体
Chromosome
控制性状
Character
等位
基因
Allele
表型
Phenotype
参考文献
Reference
I A2 8 种皮、种脐是否含有花色素
The seed coat and hilum were controlled to contain anthocyanins.
I 黄种皮黄脐
Fully yellow seed coat and hilum
Terao[9], Todd et al.[26]
ii 黄种皮黑脐
Yellow seed coat with black hilum
Terao[9], Tuteja et al.[27]
ik 鞍挂Black saddle Terao[9], Tuteja et al.[27]
i 黑种皮或褐种皮
Black or brown seed coat
Terao[9], Clough et al.[28]
R K 9 种皮为黑色或褐色
The seed coat was black or brown.
R 黑种皮Black seed coat Owen[10], Song et al.[29]
R* 黑种皮Black seed coat Zabala et al.[57]
r 褐种皮Brown seed coat Zabala et al.[57]
rm 虎斑Black spots or concentric rings of black pigment superimposed on an otherwise brown seed coat Zabala et al.[57]
T C2 6 种皮的着色程度及茸毛颜色
Control the pigmentation degree of seed coat and the color of trichomes.
T 深褐种皮、棕色茸毛
Dark brown seed coat, tawny trichomes
Owen[10], Zabala et al.[29,30]
t 褐种皮、灰色茸毛
Brown seed coat, gray trichomes
Owen[10], Zabala et al.[29,30]
tm 深褐和褐色种皮、棕和灰色茸毛
Dark brown and brown seed coat, tawny and gray trichomes
Zabala et al.[29,30]
O A2 8 种皮的褐色程度
Control the brown degree of seed coat.
O 褐种皮Brown seed coat Owen[10], Yang et al.[32]
o 红褐种皮Red-brown seed coat Owen[10], Yang et al.[32]
W1 G 13 种皮着色程度及花的颜色
Control the pigmentation degree of seed coat and the color of flowers.
W1 黑种皮、紫花
Black seed coat and purple flowers
Owen[10], Zabala et al.[33]
w1 浅褐种皮、白花
Buff seed coat and white flowers
Owen[10], Zabala et al.[33]
K1 B1 11 控制色素在鞍区的分布
Control the distribution of pigment in saddle region.
K1 黄种皮Yellow seed coat Cho et al.[34]
k1 鞍挂Black saddle Cho et al.[34]
G D1a 1 种皮、子叶是否含有叶绿素
The seed coat and cotyledon were controlled to contain chlorophyll.
G 绿种皮、绿子叶
Green seed coat and cotyledon
Owen[10], Song et al.[21]
g 黄种皮、黄子叶
Yellow seed coat and cotyledon
Owen[10], Song et al.[21]
D1 D1a 1 种皮、子叶是否含有叶绿素
The seed coat and cotyledon were controlled to contain chlorophyll.
D1 黄种皮、黄子叶
Yellow seed coat and cotyledon
Fang et al.[35], Song J [12]
d1 绿种皮、绿子叶
Green seed coat and cotyledon
Fang et al.[35], Song J [12]
D2 B1 11 种皮、子叶是否含有叶绿素
The seed coat and cotyledon were controlled to contain chlorophyll.
D2 黄种皮、黄子叶
Yellow seed coat and cotyledon
Fang et al.[35], Song J [12]
d2 绿种皮、绿子叶
Green seed coat and cotyledon
Fang et al.[35], Song J [12]
CytG 种皮、子叶是否含有叶绿素
The seed coat and cotyledon were controlled to contain chlorophyll.
CytG 黄种皮、黄子叶
Yellow seed coat and cotyledon
Guiamét et al.[39]
cytG 绿种皮、绿子叶
Green seed coat and cotyledon
Guiamét et al.[39]

Fig. 1

Seed color of different genotypes a: fully yellow seed coat and hilum; b: yellow seed coat with black hilum; c: black saddle; d: black seed coat; e: brown seed coat; f: black spots or concentric rings of black pigment superimposed on an otherwise brown seed coat; g: dark brown seed coat; h: red-brown seed coat; i: buff seed coat; j: green seed coat; k: yellow cotyledon; l: green cotyledon."

Fig. 2

Genetic loci and molecular markers of controlling seed coat color This map was modified on the basis of the genetic map published by Song et al. [29]"

Table 2

Genetic information related to seed color regulation"

序号
No.
基因编号(v2.1)
Gene ID (v2.1)
基因名称
Gene name
英文缩写
Abbreviation
遗传位点
Genetic locus
编码产物注释
Annotation of coding products
参考文献
Reference
1 Glyma.08G109500 查尔酮合成酶1
Chalcone synthase 1
CHS1 I 类黄酮合成途径酶:合成柚皮苷查尔酮
Flavonoid biosynthesis pathway enzyme: synthesis of naringin chalcone
Akada et al.[51]
2 Glyma.08G110300 查尔酮合成酶3
Chalcone synthase 3
CHS3 I 类黄酮合成途径酶:合成柚皮苷查尔酮
Flavonoid biosynthesis pathway enzyme: synthesis of naringin chalcone
Senda et al.[52]
Cho et al.[53]
3 Glyma.08G109200 查尔酮合成酶4
Chalcone synthase 4
CHS4 I 类黄酮合成途径酶:合成柚皮苷查尔酮
Flavonoid biosynthesis pathway enzyme: synthesis of naringin chalcone
Liu et al.[54]
Tuteja et al.[55]
4 Glyma.11G190900 Argonaute 5蛋白
Argonaute 5 protein
AGO5 K1 调控CHS siRNAs在种皮的分布
Regulation of CHS siRNAs distribution in seed coat
Rogers et al.[58]
Song et al.[59]
5 Glyma.09G025300 内啡肽酶同源物2a
Endorphinase homolog 2a
DCL2a 切割含长LIR的转录本,生成22nt siRNA
LIR-derived transcripts are predominately processed by GmDCL2 into 22-nt siRNAs
Jia et al.[60]
6 Glyma.09G025400 内啡肽酶同源物2b
Endorphinase homolog 2a
DCL2b 切割含长LIR的转录本,生成22nt siRNA
LIR-derived transcripts are predominately processed by GmDCL2 into 22-nt siRNAs
Jia et al.[60]
7 Glyma.06G202300 黄烷酮3’-羟化酶
Flavanone 3’-hydroxylase
F3’H T 类黄酮合成途径酶:催化黄烷酮羟基化
Flavonoid biosynthesis pathway enzymes: catalyzing the hydroxylation of flavanones
Toda et al.[61]
Guo et al.[62]
8 Glyma.13G072100 黄烷酮3’,5’-羟化酶
Flavanone 3’,5’-hydroxylase
F3’5’H W1 类黄酮合成途径酶:催化黄烷酮羟基化
Flavonoid biosynthesis pathway enzymes: catalyzing the hydroxylation of flavanones
Zabala et al.[33]
9 Glyma.08G062000 花青素还原酶
Anthocyanidin reductase
ANR1 O 类黄酮合成途径酶:形成原花青素
Flavonoid biosynthesis pathway enzymes: procyanidins production
Yang et al.[32]
10 Glyma.08G062100 花青素还原酶
Anthocyanidin reductase
ANR2 O 类黄酮合成途径酶:形成原花青素
Flavonoid biosynthesis pathway enzymes: procyanidins production
Yang et al.[32]
11 Glyma.09G235100 R2R3 MYB转录因子
Transcripion foctor R2R3 MYB
R2R3 MYB R 转录因子:调控ANS基因的表达
Transcription factors: regulation of ANS gene expression
Yan et al.[63]
Zabala et al.[64]
12 Glyma.01G198500 CAAX自身免疫蛋白酶
CAAX protease self-immunity
CPSI G 防止叶绿素降解使成熟种皮保持绿色
Prevent chlorophyll degradation to keep the mature seed coat green
Xie et al.[65]
Wang et al.[66]
13 Glyma.01g214600 保持绿色蛋白1
Protein stay-green 1
SGR1 D1 使成熟种子保持绿色
Mature seeds stay-green
Fang et al.[34]
宋健[12]
Fang et al.[34]
Song J[12]
14 Glyma.11g027400 保持绿色蛋白2
Protein stay-green 2
SGR2 D2 使成熟种子保持绿色
Mature seeds stay-green
Fang et al.[34]
宋健[12]
Fang et al.[34]
Song J[12]
15 Glyma.20G241500 查尔酮异构酶1A
Chalcone isomerase 1A
CHI1A 类黄酮合成途径酶:催化分子内环化反应
Flavonoid synthesis pathway enzymes: catalyzing intramolecular cyclization
Kovinich et al.[63]
16 Glyma.20G241700 查尔酮异构酶2
Chalcone isomerase 2
CHI2 类黄酮合成途径酶:催化分子内环化反应
Flavonoid synthesis pathway enzymes: catalyzing intramolecular cyclization
Kovinich et al.[63]
17 Glyma.02G048400 黄烷酮3-羟化酶
Naringenin 3-dioxygenase
F3H Wp 类黄酮合成途径酶:催化黄烷酮羟基化
Flavonoid biosynthesis pathway enzymes: catalyzing the hydroxylation of flavanones
Zabala et al.[64]
18 Glyma.14G072700 二氢黄酮醇还原酶1
Dihydroflavonol 4-reductase 1
DFR1 W3 类黄酮合成途径酶:形成无色花青素
Flavonoid synthesis pathway enzymes: formation of colorless anthocyanins
Xu et al.[65]
19 Glyma.17G252200 二氢黄酮醇还原酶2
Dihydroflavonol 4-reductase 2
DFR2 W4 类黄酮合成途径酶:形成无色花青素
Flavonoid synthesis pathway enzymes: formation of colorless anthocyanins
Xu et al.[65]
20 Glyma.01G214200 花青素合成酶2
Anthocyanidin synthase 2
ANS2 类黄酮合成途径酶:形成花色素
Flavonoid biosynthesis pathway enzymes: anthocyanin formation
Kovinich et al.[68]
21 Glyma.11G027700 花青素合成酶3
Anthocyanidin synthase 3
ANS3 类黄酮合成途径酶:形成花色素
Flavonoid biosynthesis pathway enzymes: anthocyanin formation
Kovinich et al.[68]
22 Glyma.08G066800 UDP类黄酮葡萄糖基转移酶
UDP-flavonoid 3-O-glucosyltransferase
UF3GT 类黄酮合成途径酶:形成花色苷
Flavonoid biosynthesis pathway enzymes: anthocyanin formation
Kovinich et al.[68]
23 光系统Ⅱ反应中心M亚基
Photosystem II reaction center M subunit
Psbm 具有叶绿素b降解功能
Degradation of chlorophyll b
Kohzuma et al.[40]

Table 3

Regulation mechanism of alleles controlling seed color"

基因/编号
Gene ID
突变基因型
Mutant genotype
种子颜色
Seed color
变异方式
Variation
检测方法
Detection method
参考文献
Reference
I
Glyma.08G109500
Glyma.08G110300
Glyma.08G109200
ii 黄种皮黑脐 Yellow seed coat with black hilum CHS基因的拷贝数增加 The copy number of CHS gene increased BAC重测序 BAC resequencing Cho et al.[53]
ik 鞍挂 Black saddle 基因间序列缺失 Deletion of intergenic sequencesl BAC重测序 BAC resequencing Cho et al.[53]
i 深色种皮 Dark pigment seed coat 基因及基因间序列大片段缺失
Large deletions of genes and intergenic sequences
BAC重测序 BAC resequencing Cho et al.[53]
R
Glyma.09G235100
R* 黑种皮 Black seed coat 第2内含子插入CACTA转座子及CACTA序列的甲基化
Insertion of the second intron into the CACTA transposon and methylation of the CACTA sequence
长片段PCR扩增、表达谱分析、甲基化检测
Long fragment PCR amplification, expression profile analysis, methylation detection
Zabala et al.[64]
r 褐种皮 Brown seed coat 第2外显子单碱基C缺失 Single base C deletion in exon 2 克隆测序 Cloning and sequencing Zabala et al.[64]
rm 虎斑
Black spots or concentric rings of black pigment superimposed on an otherwise brown seed coat
第2内含子插入CACTA转座子
Insertion of the second intron into the CACTA transposon
长片段PCR扩增、表达谱分析、甲基化检测
Long fragment PCR amplification, expression profile analysis, methylation detection
Zabala et al.[64]
T
Glyma.06G202300
t 褐种皮 Brown seed coat 第3外显子单碱基A的缺失或非同义突变或单碱基C的缺失
Deletion of single base A or non synonymous mutation or deletion of single base C in exon 3
PCR测序 PCR sequencing Guo et al.[62]
tm 深褐和褐色种皮
Dark brown and brown seed coat,
第1内含子插入CACTA转座子
The first intron was inserted into the CACTA transposon
长片段PCR扩增
Long fragment PCR amplification
Zabala et al.[31]
W1
Glyma.13G072100
w1 淡褐种皮 Buff seed coat 第3外显子插入53 bp
The third exon was inserted 53 bp sequence
克隆测序
Cloning and sequencing
Guo et al.[62]
K1
Glyma.11G190900
k1 鞍挂 Black saddle 第7外显子129 bp的缺失
Deletion of 129 bp sequence in exon 7
转录组与小RNA测序、PCR测序、全基因组深度重测序
Ranscriptome and micro RNA sequencing, PCR sequencing, whole genome deep resequencing
Cho et al.[34]
G
Glyma.01G198500
g 黄种皮 Yellow seed coat 第8内含子末端发生碱基突变
A base mutation occurred at the end of intron 8
克隆测序
Cloning and sequencing
Wang et al.[66]
D1
Glyma.01g214600
d1 绿种皮、绿子叶
Green seed coat and cotyledon
第2外显子单碱基T缺失
Single base T deletion in exon 2
基因组重测序、克隆测序
Genome resequencing, cloning and sequencing
Fang et al.[35], Song J[12]
D2
Glyma.11g027400
d2 绿种皮、绿子叶
Green seed coat and cotyledon
322 bp重复插入
322 bp sequence repeated insertion
基因组重测序、克隆测序
Genome resequencing, cloning and sequencing
Fang et al.[35], Song J[12]
CytG
cytG 绿种皮、绿子叶
Green seed coat and cotyledon
5 bp插入 5 bp sequence insertion 对叶绿体基因组广泛的测序
Extensively sequenced the chloroplast genome
Kohzuma et al.[40]

Fig. 3

Flavonoid biosynthesis pathway regulated by seed coat color related genes in legumes The above figure was modified from Zabala et al. [64] "

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