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Acta Agronomica Sinica ›› 2023, Vol. 49 ›› Issue (7): 1829-1842.doi: 10.3724/SP.J.1006.2023.24188


Genome-wide identification and functional analysis of SGR gene family in Brassica napus L.

TANG Yu-Feng(), YAO Min, HE Xin, GUAN Mei, LIU Zhong-Song, GUAN Chun-Yun, QIAN Lun-Wen*()   

  1. College of Agronomy, Hunan Agricultural University / Collaborative Innovation Center of Grain and Oil Crops in South China, Changsha 410128, Hunan, China
  • Received:2022-08-11 Accepted:2022-11-25 Online:2023-07-12 Published:2022-12-06
  • Contact: *E-mail: qianlunwen@163.com E-mail:tyf331213@163.com;qianlunwen@163.com
  • Supported by:
    The National Natural Science Foundation of China(31801399);The Research Foundation of Education Bureau of Hunan Province(21A0135)


Chlorophyll is a kind of green pigment for plant photosynthesis, which has a direct effect on plant growth. In this study, bioinformatics methods were used to identify the members of SGR gene family in Brassica napus, Brassica rapa, Brassica oleracea, and Arabidopsis thaliana. Most of the 28 SGR genes contained four exons, encoding basic proteins. Chromosome mapping and syntenic analysis showed that there was no tandem duplication in the SGR gene family members of Brassica napus. SGR gene family members had a linear relationship, highly homologous in evolution, and very conserved in the evolutionary process. Moreover, a genome-wide association study (GWAS) of chlorophyll content was performed using a Brassica 60K Illumina Infinium SNP array in 203 Brassica napus accessions. Two haplotype regions (Chr.A01: 6,193,165-6,317,757 bp and Chr.C01: 9,059,861-9,906,618 bp) carrying two SGR genes (BnaSGR1a-A01 and BnaSGR1-C01) were detected, which were significantly associated with chlorophyll content. Meanwhile, the regional association analysis of 50 resequenced rapeseed inbred lines revealed that a SNP located in exon 2 of BnaSGR1a-A01 significantly associated with chlorophyll content. Co-expression network analysis revealed that BnaSGR1a-A01 were directly linked with BnaSGR2-A03, and indirectly linked with BnaSGR1-C01, BnaSGR1-A08, BnaSGR2-C03, BnaSGR1-C07, BnaSGRL-C06, and BnaSGRL-A10, thus forming a molecular network involved in the potential regulation of chlorophyll content. Chlorophyll a, chlorophyll b, and the total chlorophyll content of T2 Arabidopsis transgenic plants overexpressing BnasSGR1a-A01 were significantly lower than wild type, indicating that BnaSGR1a-A01 regulated chlorophyll degradation. This study laid a foundation for the functional research and utilization of SGR gene in Brassica napus L.

Key words: Brassica napus, STAY-GREEN gene, GWAS, chlorophyll content

Table 1

Primers used in this study"

Primer name
Sequence (5°-3°)

Table 2

SGR gene information"

Arabidopsis thaliana
Gene ID
Gene name
Gene length
Length of amino acids
Molecular weight (kD)
No. of introns
No. of exons
Predicted subcellular localization
甘蓝型油菜 Brassica napus BnaA01g12570D BnaSGR1a-A01 1874 332 9.35 37.82 5 6 叶绿体Chloroplast
甘蓝型油菜 Brassica napus BnaA01g22870D BnaSGR1b-A01 1063 114 9.86 13.18 2 3 叶绿体Chloroplast
甘蓝型油菜 Brassica napus BnaA03g45630D BnaSGR1-A03 1484 266 8.67 29.83 3 4 叶绿体Chloroplast
甘蓝型油菜 Brassica napus BnaA08g10510D BnaSGR1-A08 1341 273 8.32 30.67 3 4 叶绿体Chloroplast
甘蓝型油菜 Brassica napus BnaCnng29210D BnaSGR1-Cnn 1378 264 8.85 29.57 3 4 叶绿体Chloroplast
甘蓝型油菜 Brassica napus BnaC01g14360D BnaSGR1-C01 5975 999 8.65 112.40 11 12 质膜Plasma membrane
甘蓝型油菜 Brassica napus BnaC07g37710D BnaSGR1-C07 1616 266 8.60 29.92 3 4 叶绿体Chloroplast
白菜 Brassica rapa Bra013656 BraSGR1a-A01 5705 950 8.48 106.87 10 11 质膜Plasma membrane
白菜 Brassica rapa Bra028385 BraSGR1b-A01 804 113 10.02 13.00 1 2 叶绿体Chloroplast
白菜 Brassica rapa Bra019346 BraSGR1-A03 1125 264 8.60 29.73 3 4 叶绿体Chloroplast
白菜 Brassica rapa Bra020829 BraSGR1-A08 982 254 8.57 28.55 3 4 叶绿体Chloroplast
甘蓝Brassica oleracea Bol014983 BoSGR1-C01 1252 269 9.01 30.49 3 4 叶绿体Chloroplast
甘蓝Brassica oleracea Bol010654 BoSGR1-C03 1018 264 8.85 29.57 3 4 叶绿体Chloroplast
甘蓝Brassica oleracea Bol042063 BoSGR1-C07 1106 266 8.41 29.78 3 4 叶绿体Chloroplast
甘蓝型油菜 Brassica napus BnaA03g24900D BnaSGR2-A03 1776 262 9.28 29.96 4 5 叶绿体Chloroplast
甘蓝型油菜 Brassica napus BnaC03g72930D BnaSGR2-C03 1654 274 9.00 31.14 3 4 叶绿体Chloroplast
白菜 Brassica rapa Bra000755 BraSGR2-A03 1335 274 9.22 31.08 3 4 叶绿体Chloroplast
甘蓝Brassica oleracea Bol030516 BoSGR2-C03 1194 263 8.94 30.15 3 4 叶绿体Chloroplast
甘蓝型油菜 Brassica napus BnaA10g08850D BnaSGRL-A10 1387 257 9.15 29.28 3 4 叶绿体Chloroplast
甘蓝型油菜 Brassica napus BnaC06g00560D BnaSGRL-C06 1455 257 9.15 29.17 3 4 叶绿体Chloroplast
白菜 Brassica rapa Bra036938 BraSGRL-Scaffold000123 1067 257 9.24 29.34 3 4 叶绿体Chloroplast
甘蓝Brassica oleracea Bol006958 BoSGRL-Scaffold000269 1096 259 8.40 29.29 3 4 叶绿体Chloroplast
甘蓝型油菜 Brassica napus BnaCnng70460D BnaSGLP-Cnn 983 246 7.99 28.05 3 4 叶绿体Chloroplast
甘蓝Brassica oleracea Bol044955 BoSGLP-C02 982 267 8.44 28.13 3 4 叶绿体Chloroplast

Fig. 1

Phylogenetic tree of SGR gene family in Brassica napus, Brassica rapa, Brassica oleracea, and Arabidopsis thaliana"

Fig. 2

Systematic comparative analysis of SGR genes of Arabidopsis thaliana, Brassica rapa, Brassica oleracea, and Brassica napus chromosomes"

Fig. 3

Distribution of SGR genes in Brassica rapa, Brassica oleracea, and Brassica napus chromosomes The numbers of chromosomes are labeled on the left side of each chromosome. A and C are the chromosomes from Brassica rapa and Brassica oleracea; chrA and chrC are the chromosomes of the A-subgenomes and C-subgenomes from Brassica napus, respectively. Random means genes are distributed randomly to the specific chromosome, and chrCnn is unanchored scaffold that cannot be mapped to a specific chromosome from the C-subgenomes."

Fig. 4

Syntenic analysis of SGR genes in Brassica napus, Brassica oleracea, Brassica rapa, and Arabidopsis thaliana Syntenic analysis between Brassica napus showed by pink lines. Syntenic analysis between Brassica napus, Brassica rapa, and Brassica oleracea are indicated by green lines. Syntenic analysis among Arabidopsis thaliana, Brassica napus, Brassica rapa, and Brassica oleracea are indicated by brown lines."

Fig. 5

Genome-wide association study of chlorophyll content at seedling and bolting stages in 203 rapeseed accessions Haplotype region (6,193,165-6,317,757 bp) and haplotype region (9,059,861-9,906,618 bp) were significant association with chlorophyll content. In these haplotype regions carrying two orthologues of Arabidopsis gene BnaSGR1a-A01 (BnaA01g12570D) and BnaSGR1-C01 (BnaC01g14360D) are involved in chlorophyll biosynthesis process. The heat map spans the SNP markers in LD with the most strongly associated SNPs. The horizontal red dotted line represents the significant threshold (-log10(P)=4). ss_GH: chlorophyll content index in seedling stage (glasshouse experiments, 2012), bs_GH: chlorophyll content index in bolting stage (glasshouse experiments, 2012)."

Fig. 6

Association analysis of candidate genes for chlorophyll content within whole-genome resequencing of 50 accessions A: the regional association analysis of chlorophyll content in haplotype region (6,193,165-6,312,172 bp; r2=0.55). The blue dotted line indicates a threshold P-value of 1.0×10-3 for genome-wide significance. B: SNP chrA01:6306874 locates in exon two region of BnaSGR1a-A01 gene showed associated with chlorophyll content. C and D: the comparative analysis of allele G and T related to gene expression and chlorophyll content. Allele frequency greater than 0.05 in the population will be used for this analysis. The box plot showed that the allele G corresponding to inbred lines had higher chlorophyll content and gene expression level."

Fig. 7

Overexpression of BnaSGR1a-A01 in Arabidopsis A: the schematic diagram of the overexpresed vector backbone; B: the comparison of one-month seedling age true leaves (No. 4-6) of Col-0 and OE lines, bar:5 mm; C: the qRT-PCR detection of Col-0 and OE lines; D-F: the determination of chlorophyll a, chlorophyll b and total chlorophyll in Col-0 and OE lines; Col-0: non-transgenic plant; OE-BnaSGR1-13,OE-BnaSGR1-14: transgenic plant. *: P < 0.05; **: P < 0.01. Error bars indicate the standard derivations."

Fig. 8

Co-expression network analysis of BnaSGR1a-A01 genes A: the co-expression network of BnaSGR1a-A01 in the silique of Brassica napus. Red nodes represent BnaSGR genes, turquoise triangle node represent these genes directly correlation with BnaSGR genes. B: the partly co-expression network of BnaSGR1a-A01 in the silique of Brassica napus. Based on the functional annotation, the genes in the BnaSGR1a-A01 co-expression network are classified into the following three groups: chlorophyll (light blue nodes), photosystem (turquoise nodes), and transcription factors (darkolivegreen nodes). C: GO pathway of BnaSGR1a-A01 co-expression networks. Deep yellow represents that BnaSGR1a-A01 is significant correlation with these metabolism process."

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