Scientia Agricultura Sinica ›› 2023, Vol. 56 ›› Issue (18): 3642-3654.doi: 10.3864/j.issn.0578-1752.2023.18.012

• HORTICULTURE • Previous Articles     Next Articles

Genome Wide Association Study for Resistance to Citrus Brown Spot Disease

YANG ShengNan(), CHENG Li, TAN YueXia, ZHU YanSong, JIANG Dong()   

  1. Citrus Research Institute of Southwest University, Chongqing 400712
  • Received:2023-02-14 Accepted:2023-05-04 Online:2023-09-16 Published:2023-09-21
  • Contact: JIANG Dong

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Abstract:

【Objective】The study objective was to explore candidate genes associated with resistance to Alternaria brown spot disease in citrus mandarin, so as to provide the basis for developing suitable molecular markers for further citrus resistance breeding work. 【Method】In summer and autumn of 2022, the young leaves of 136 citrus mandarin accessions were picked and inoculated with the fungus mycelium of Alternaria alternata in the laboratory. The combined results of two experiments were used to obtain the reliable results of 121 citrus mandarins responding to Alternaria brown spot. The phenotypes of 121 citrus mandarins were selected to verify the effectiveness of the CAPS marker developed in a previous study. Then, in order to obtain the candidate SNPs related to Alternaria brown spot resistance, the phenotypes of 121 citrus mandarins and corresponding SNP genotype data from GBS sequencing were analyzed with PCA, GWAS, and Fst methods, respectively. Candidate genes had been selected from the flanking region of 25 kb sequences surrounding the candidate SNPs site, and then they were screened out according to phytozome annotations. The expressions of candidate genes were analyzed after inoculating with the pathogen fungus on leave of Chengtuo hongju and Clementina (Algeria) for 24, 48, and 72 h. 【Result】Among 121 citrus mandarins, 67 varieties such as Clementine and Satsuma were resistant to Alternaria brown spot disease, whereas 54 varieties such as Hong Ju and Ponkan were susceptible. Some varieties resistance to Alternaria brown spot disease could discriminated by CAPS, but its accuracy only accounted for 76.86% in the study. GWAS analysis identified six significant SNPs highly associated with disease resistance, among which SNP1 located in Ciclev10021676 at 24 838 146 bp of chromosome 3 could be used to predicate the resistance of varieties, and their genotype showed a strong correlation with phenotype. Eight significant SNPs highly associated with disease resistance selected by Fst analysis. Finally, five genes of Ciclev10018604, Ciclev10023485, Ciclev10023486, Ciclev10024586 and Ciclev10019874 were screened out. The expression levels of these five genes in Chengtuo Hongju were up-regulated extensively after inoculating leaves with the pathogen fungus, and their expression levels reached the highest 48 hours later. 【Conclusion】Through GWAS, the SNP at 24 838 146 bp on chromosome 3 was found to be the most significant one with high resistance correlation to Alternaria brown spot disease, and the genotype at this location could be effectively used to distinguish the resistant varieties. The candidate genes responding to Alternaria brown spot disease in mandarin were discussed, i.e., Ciclev10019874, Ciclev10018604, Ciclev10023485, Ciclev10024586, and Ciclev10023486.

Key words: citrus mandarin, Alternaria brown spot, molecular marker, genome-wide association study, fixation index

Table 1

Primer of CAPS"

引物名称
Primer name		 序列
Primer sequence		 扩增长度
Length (bp)
SNP08-spare-F AGGATTGTGAGGTGACGCTT 747
SNP08-spare-R GCAACATATCCAAATGCGCC

Table 2

Primers for real-time fluorescence quantification of candidate genes"

基因名称
Gene name		 引物名称
Primer name		 序列
Primer sequence
β-Actin F CCCCATCGTTACCGTCCAG
R CGCCTTGCCAGTTGAATATCC
Ciclev10018604 F GGGAGCTTGTGGCACTGTAT
R TCCTTCACCACGCAACTTGA
Ciclev10019874 F GAATCCCTTCTCTCCGGCTG
R GTGGTGGAGTGATGAGGTGG
Ciclev10023485 F GAGTCACCTGACAAGAGAATGC
R ACTTGCAGCAACATCATCCAAG
Ciclev10024586 F GCATAGGCCTTGCCAATGTT
R CGATAATCAACGACACGGGC
Ciclev10023486 F AAACAGCATTCCAAGCGTGC
R AATCCCATCCGCATAGGTCG

Fig. 1

Example diagram of resistance to citrus brown spot disease A: Symptom of Alternaria alternata inoculated young leaves of Da Xianggan in summer; B: Symptom of Alternaria alternata inoculated young leaves of Guiping Zhushaju in summer; C: Symptom of Alternaria alternata inoculated young leaves of Da Xianggan in autumn; D: Symptom of Alternaria alternata inoculated young leaves of Guiping Zhushaju in autumn. The left three leaves of Fig. 1-A and Fig. 1-B were inoculated leaves, and the right three leaves were control leaves; The first 15 leaves in Fig. 1-C and Fig. 1-D were inoculated leaves, and the last 15 leaves were control leaves"

Fig. 2

esistance prediction results of CAPS A: CAPS results of 20 citrus mandarin; 1: 2000DNA marker; the varieties from 2 to 21 lane are as follow: Minneola Tangelo, Tangor 22-53, Yuanhong Xianggan, Clementina (Algeria), Anjiang Hongju, Jinju, Suanganzi, Wilking Mandarin, Apireno, Shagan, Clementina×Bendizao, Tsunonozomi, 1-26, Duong Mandarin, Kiyomi×Minneola, Ortanique, Calamondin, Seedless W. murcott, Seedless Zaoju, Huapi Ju. B: Pie chart of CAPS accuracy"

Fig. 3

Results of PCA, GWAS and Fst A: Principal component analysis of 121 citrus mandarins; B: Manhattan plot of GWAS for displaying SNPs related to resistance to Alternaria brown spot; C: QQ plot of GWAS for resistance to Alternaria brown spot; D: Manhattan plot of Fst for displaying SNPs related to resistance to Alternaria brown spot"

Table 3

The information of 14 SNPs from GWAS analysis and Fst analysis"

来源
Source		 编号
Code		 染色体
Chromosome		 位置
Location (bp)		 P值/Fst值
P value/ Fst value
GWAS筛选 Screening of GWAS SNP1 3 24838146 7.742227
GWAS筛选 Screening of GWAS SNP2 3 29033460 6.01147
GWAS筛选 Screening of GWAS SNP3 2 9623685 5.404526
GWAS筛选 Screening of GWAS SNP4 3 10912656 4.899702
GWAS筛选 Screening of GWAS SNP5 3 29379604 4.524974
GWAS筛选 Screening of GWAS SNP6 3 29379461 4.504927
Fst筛选 Screening of Fst SNP7 5 9384031 0.427099
Fst筛选 Screening of Fst SNP8 3 21846432 0.407686
Fst筛选 Screening of Fst SNP9 3 30824581 0.402405
Fst筛选 Screening of Fst SNP10 2 32716438 0.400017
Fst筛选 Screening of Fst SNP11 3 11889486 0.395677
Fst筛选 Screening of Fst SNP12 3 30230610 0.391282
Fst筛选 Screening of Fst SNP13 3 30132014 0.381140
Fst筛选 Screening of Fst SNP14 3 33601151 0.380600

Table 4

The information of 6 SNPs genotype from GWAS analysis"

SNP编号
SNP code		 基因型
genotype		 感病资源数量
Number of susceptible varieties		 抗病资源数量
Number of resistant varieties		 感病资源占比
The proportion of susceptible varieties (%)		 抗病资源占比
The proportion of resistant varieties (%)
SNP1 G/G 13 0 100 0
G/A 45 14 76 24
A/A 7 39 15 85
SNP2 C/C 13 0 100 0
C/T 37 11 77 23
T/T 14 42 25 75
SNP3 C/C 33 4 89 11
C/A 28 16 64 36
A/A 5 33 13 87
SNP4 G/G 13 0 100 0
G/T 36 10 78 22
T/T 16 43 27 73
SNP5 A/A 19 1 5 95
A/T 24 21 47 53
T/T 37 13 74 26
SNP6 C/C 12 0 100 0
C/T 35 11 76 24
T/T 15 42 26 74

Table 5

Functional annotation of five candidate genes"

基因
Gene		 注释
Annotation		 连锁SNP编号
Chain SNP code
Ciclev10019874 丝氨酸/苏氨酸-蛋白激酶wag1
Serine/threonine-protein kinase wag1		 SNP2
Ciclev10023485 非特异性丝氨酸/苏氨酸蛋白激酶；苏氨酸特异性蛋白激酶
Non-specific serine/threonine protein kinase; Threonine-specific protein kinase		 SNP14
Ciclev10018604 蛋白激酶结构域；富含亮氨酸重复序列N端结构域（LRRNT_2）；富含亮氨酸重复序列（LRR_8）
Protein kinase domain; Leucine rich repeat N-terminal domain (LRRNT_2); Leucine rich repeat (LRR_8)		 SNP2
Ciclev10024586 富含亮氨酸重复序列（LRR_1）；富含亮氨酸重复序列N端结构域（LRRNT_2）
Leucine Rich Repeat (LRR_1); Leucine rich repeat N-terminal domain (LRRNT_2)		 SNP14
Ciclev10023486 富含亮氨酸重复序列的蛋白
Leucine-rich repeat-containing protein		 SNP8

Fig. 4

Analysis of relative expression levels of five candidate genes *, ** and *** indicate significant difference at 0.05, 0.01 and 0.001 level, respectively. CTHJ-24, CTHJ-48 and CTHJ-72 represent Chengtuo Hongju after inoculating with Alternaria alternata 24, 48 and 72 h, respectively. XKLMD-24, XKLMD-48, and XKLMD-72 represent Clementina (Algeria) after inoculating with Alternaria alternata 24, 48 and 72 h, respectively"

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