84个苹果栽培品种对斑点落叶病的抗性评价和全基因组关联分析

doi:10.3864/j.issn.0578-1752.2022.18.011

Abstract

Abstract:

【Objective】 Alternaria alternata f. sp. mali is a main disease occurring in the apple orchards in China, which seriously threatens the yield and quality of apples. The aim of this research was to identify apple cultivars and genes responsible for high resistance to Alternaria alternata f. sp. mali, thus providing the basis for disease resistance breeding of apples.【Method】 In this study, the isolated Alternaria alternata f. sp. mali strain was used to inoculate leaves of 84 apple cultivars. To evaluate the resistance of apple cultivars to Alternaria alternata f. sp. mali, the cluster analysis was carried out from two aspects including lesion area and lesion area growth rate. The genome-wide association study was performed based on the lesion area. The disease spot area of the inoculated leaves was used as a phenotypic trait, and the 1243071 high-quality SNP loci obtained by whole genome deep resequencing were used as genetic markers. Genome wide association analysis was performed by EMMAX method.【Result】The statistical analysis of lesion area showed significant diversity of 84 apple cultivars in resistance to Alternaria alternata f. sp. mali. Most apple cultivars were susceptible or resistant to Alternaria alternata f. sp. mali, while only a few cultivars were highly resistant and highly susceptible. The disease resistance of Alternaria alternata f. sp. mali has the characteristics of normal distribution, showing the genetic characteristics of quantitative characters. The genome-wide association trait analysis finally obtained 6 SNP loci with a significant level of P≤0.0000001 (-LgP≥7), and in-depth analysis linked them to 7 key candidate genes, including Integrin-linked protein kinase, FMN-linked oxidoreductase superfamily protein, B-box zinc finger family protein, GATA type transcription factor, etc. The biological function of Integrin-linked protein kinase in disease resistance was further verified. 【Conclusion】After two years of comprehensive analysis of data, 7 stable resistant varieties and 2 stable susceptible varieties were identified from 84 apple cultivars. Through genome-wide association trait analysis, six SNP loci and seven genes significantly related to the disease resistance of apple leaf spot were identified, and function of one gene was verified.

Key words: apple cultivars, Alternaria alternata f.sp. mali, disease resistance, genome-wide association study

BaoHua CHU,FuGuo CAO,NingNing BIAN,Qian QIAN,ZhongXing LI,XueWei LI,ZeYuan LIU,FengWang MA,QingMei GUAN. Resistant Evaluation of 84 Apple Cultivars to Alternaria alternata f. sp. mali and Genome-Wide Association Analysis[J].Scientia Agricultura Sinica, 2022, 55(18): 3613-3628.

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Figures/Tables 10

Table 1

Table 2

Lesion area and its growth rate of 84 apple cultivars inoculated with Alternaria alternata f. sp. Mali"

品种名称 Cultivar resource	病斑面积 Lesion area (cm²)	增长率 Growth rate (%)	品种名称 Cultivar resource	病斑面积 Lesion area (cm²)	增长率 Growth rate (%)
凯密欧 Cameo	0.76±0.14	15.00	红露 Hongro	2.2±0.27	45.00
Kiku	0.90±0.17	15.75	斯派克 Spike	2.25±0.24	29.25
JA	0.95±0.21	19.50	平成 Heisei	2.31±0.19	48.75
皇家嘎啦 Royal Gala	0.99±0.13	16.75	阿肯色黑 Arkansasblack	2.38±0.24	50.25
秋光 Qiu Guang	1.01±0.33	19.50	布瑞本 Braeburn	2.4±0.18	53.25
蜜脆 Honeycrisp	1.03±0.32	19.50	Ce2	2.46±0.49	50.25
蓝皮尔曼 Blue Pearman	1.05±0.20	19.00	凉香 Ryoka	2.47±0.31	53.50
福拉瑞娜 Florina	1.14±0.33	19.00	Chenago Strawberry	2.49±0.17	54.75
Roho3615	1.20±0.14	23.25	秦阳 Qin Yang	2.51±0.21	50.25
艾达红 Idared	1.29±0.16	24.25	阿莱特 Arlet	2.51±0.32	55.00
威廉姆斯女士 Lady Williams	1.29±0.19	27.00	富红早嘎 Fu Hong Zao Ga	2.56±0.26	52.00
弘前富士 Hirosakifuji	1.33±0.17	22.25	Redcord	2.58±0.35	53.50
Fujiko	1.35±0.16	18.75	红勋1号 Hong Xun No.1	2.6±0.32	59.75
红盖露 Gale Gala	1.38±0.16	25.50	Ruby Mac	2.6±0.33	53.50
Gloster69	1.40±0.29	28.50	陆奥 Mutsu	2.61±0.34	60.00
长富2号 NaganofujiNo.2	1.42±0.27	26.25	秦冠 Qin Guan	2.69±0.32	60.75
早红1号 Early red one	1.45±0.20	25.00	Maririi Red	2.74±0.2	57.75
Challenger	1.61±0.18	29.50	千秋 Senshu	2.88±0.66	55.75
王林 Orin	1.62±0.30	31.00	新乔纳金 New Jonagold	2.88±0.91	61.50
鲁宾斯 Rubens	1.64±0.25	34.50	丽嘎 Li Ga	2.92±0.25	62.75
皮诺娃 Pinova	1.65±0.31	34.25	信浓甜 Cinano Sweet	2.93±0.65	61.00
N2	1.67±0.21	34.00	魔笛 Modi	3±0.36	66.50
无锈金冠 Reinders	1.68±0.36	35.00	富士冠军 Fuji Champion	3.05±0.06	62.00
坎兹 Kanzi	1.73±0.21	35.25	晨雾 Morning Mist	3.13±0.4	67.75
早红霞 Zao Hong Xia	1.74±0.32	30.25	金红 Jin Hong	3.14±0.27	63.25
玫瑰光芒 Rosy Glow	1.76±0.33	37.25	Northfield Beauty	3.17±0.21	69.50
美味 Ambrosia	1.77±0.18	36.25	北斗 Hokudo	3.26±0.98	66.75
宝罗红 PaulaRed	1.78±0.19	36.25	Yellow Transparent	3.29±0.68	67.50
Halerstadter Jungfermapfe	1.81±0.55	32.50	瑞林 Jude-line	3.37±0.08	71.75
北海道9号 HokkaidoNo.9	1.82±0.38	35.25	粉红女士 Pink Lady	3.42±0.16	70.25
夕阳 Sundowner	1.85±0.31	39.50	Su	3.45±0.3	65.50
巴克艾 Buckeye	1.86±0.15	35.00	K296	3.47±0.27	58.75
寒富 Han Fu	1.88±0.55	37.00	署红 James Grieve	3.64±0.29	68.00
荷斯坦 Holstein	1.90±0.12	39.75	茜 Akane	3.75±0.53	74.00
Unknown	1.90±0.25	41.75	Pound Sweet	3.83±0.16	80.75
瑞星 Judestar	1.92±0.23	36.00	2001富士 Fuji2001	4.12±0.47	81.25
昂林 Korin	1.93±0.21	34.25	阿丽亚娜 Ariane	4.24±0.49	80.75
瑞莲娜 Juliana	2.00±0.32	43.25	赫拉森 Haralson	4.32±0.68	75.50
津轻 Tsugaru	2.01±0.30	43.75	信浓红 CinanoRed	4.38±0.22	88.75
甘红 Gan Hong	2.07±0.33	38.00	比蒂格海姆 Bietigheimer	5.31±0.25	114.00
NJ-90	2.17±0.26	45.00	埃德尔博斯多夫 Edelborsdorfer	5.49±0.67	128.25
Ce1	2.19±0.27	47.00	Chanterler	6.02±0.23	95.75

Table 2

Fig. 1

Table 3

Lesion area and its growth rate of 84 apple cultivars inoculated with Alternaria alternata f. sp. mali"

品种名称 Cultivar resource	病斑面积 Lesion areas (cm²)	增长率 Growth rate (%)	品种名称 Cultivar resource	病斑面积 Lesion area (cm²)	增长率 Growth rate (%)
蓝皮尔曼 Blue Pearman	0.30±0.11	4.75	寒富 Han Fu	1.12±0.23	24.75
艾达红 Idared	0.36±0.19	8.00	坎兹 Kanzi	1.13±0.33	22.00
平成 Heisei	0.40±0.09	7.25	粉红女士 Pink Lady	1.17±0.35	22.25
Yellow Transparent	0.49±0.24	8.50	Maririi Red	1.18±0.23	26.25
Ce1	0.50±0.07	9.75	威廉姆斯女士 Lady Williams	1.20±0.28	23.50
皮诺娃 Pinova	0.60±0.27	13.00	瑞莲娜 Juliana	1.21±0.24	22.50
秦冠 Qin Guan	0.61±0.11	12.25	北海道9号 HokkaidoNo.9	1.21±0.25	22.50
NJ-90	0.62±0.22	11.50	红盖露 Gale Gala	1.23±0.26	25.00
无锈金冠 Reinders	0.63±0.10	12.00	2001富士 Fuji2001	1.23±0.34	26.75
宝罗红 PaulaRed	0.65±0.22	14.75	瑞林 Jude-line	1.23±0.36	25.75
皇家嘎啦 Royal Gala	0.65±0.33	13.00	巴克艾 Buckeye	1.30±0.12	25.25
玫瑰光芒 Rosy Glow	0.68±0.10	13.50	津轻 Tsugaru	1.33±0.27	28.25
夕阳 Sundowner	0.70±0.32	14.00	弘前富士 Hirosakifuji	1.37±0.25	30.75
Kiku	0.74±0.17	15.25	福拉瑞娜 Florina	1.37±0.29	28.25
信浓甜 Cinano Sweet	0.77±0.20	14.75	Chenago Strawberry	1.37±0.30	28.75
蜜脆 Honeycrisp	0.78±0.11	16.00	鲁宾斯 Rubens	1.37±0.32	27.50
阿莱特 Arlet	0.78±0.14	16.00	赫拉森 Haralson	1.41±0.10	22.75
Northfield Beauty	0.78±0.20	14.50	金红 Jin Hong	1.48±0.31	30.25
美味 Ambrosia	0.79±0.19	17.50	Unknown	1.50±0.61	30.25
凯密欧 Cameo	0.80±0.11	16.75	红勋1号 Hong Xun No.1	1.52±0.14	32.00
Challenger	0.80±0.13	16.50	魔笛 Modi	1.54±0.33	31.50
秦阳 Qin Yang	0.80±0.23	17.25	Pound Sweet	1.55±0.35	33.00
Su	0.81±0.28	18.25	早红1号 Early red one	1.55±0.43	33.25
Gloster69	0.82±0.17	15.50	比蒂格海姆 Bietigheimer	1.57±0.07	30.75
Ce2	0.83±0.20	17.75	K296	1.66±0.26	35.75
署红 James Grieve	0.87±0.10	17.25	北斗 Hokudo	1.69±0.34	31.25
凉香 Ryoka	0.90±0.25	19.75	N2	1.71±0.47	34.00
Fujiko	0.91±0.17	18.00	早红霞 Zao Hong Xia	1.75±0.16	37.00
丽嘎 Li Ga	0.92±0.20	18.50	斯派克 Spike	1.75±0.21	35.25
红露 Hongro	0.92±0.37	19.50	王林 Orin	1.80±0.41	37.75
陆奥 Mutsu	0.94±0.17	18.50	Redcord	1.80±0.73	38.25
秋光 Qiu Guang	0.94±0.21	17.75	埃德尔博斯多夫 Edelborsdorfer	1.84±0.2	34.25
富士冠军 Fuji Champion	0.95±0.40	19.00	昂林 Korin	1.86±0.07	36.00
瑞星 Judestar	0.96±0.15	19.25	富红早嘎 Fu Hong Zao Ga	1.87±0.16	41.00
布瑞本 Braeburn	0.99±0.13	17.75	甘红 Gan Hong	1.90±0.46	37.25
信浓红 CinanoRed	1.00±0.16	21.75	Chanterler	1.98±0.33	42.00
Roho3615	1.00±0.19	20.00	长富2号 NaganofujiNo.2	2.00±0.30	41.75
JA	1.01±0.18	20.75	新乔纳金 New Jonagold	2.05±0.44	42.75
阿肯色黑 Arkansasblack	1.03±0.21	20.25	千秋 Senshu	2.13±0.46	35.00
Halerstadter Jungfermapfe	1.08±0.18	20.00	Ruby Mac	2.14±0.49	44.75
晨雾 Morning Mist	1.10±0.25	23.50	荷斯坦 Holstein	2.37±0.48	44.00
阿丽亚娜 Ariane	1.12±0.20	24.00	茜 Akane	2.83±0.47	56.25

Table 3

Fig. 2

Fig. 3

Table 4

Table 5

Fig. 4

Fig. 5

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引物名称 Primer name	引物序列 Primer sequence (5' to 3')	目的 Purpose
MdMDH-qpcr-F	CGTGATTGGGTACTTGGAAC	荧光定量PCR qRT-PCR
MdMDH-qpcr-R	TGGCAAGTGACTGGGAATGA
MD05G1054300-qpcr-F	CCGTACGGCAGCTGTAGAT
MD05G1054300-qpcr-R	GGAACTTCTCGAGGATTCGCA
MD05G1054400-qpcr-F	CGGAGGGGAAATCAAAGGCT
MD05G1054400-qpcr-R	TTGTACGGGCACCGACTAAC
MD05G1054500-qpcr-F	CCCATTTCGCCCTGTTCTGA
MD05G1054500-qpcr-R	AACACGCACCTACATCACCA
MD05G1048600-qpcr-F	GCAGGCCCAAGGACACTATG
MD05G1048600-qpcr-R	GCTACAACATCGGAATCCTGTT
MD05G1048700-qpcr-F	ACTCAACCATACGAGGCTCC
MD05G1048700-qpcr-R	ATTGCATGGGCAGCATGTTC
MD00G1039900-qpcr-F	GCTGCCCGATGTAAAACCAAA
MD00G1039900-qpcr-R	CCCACACCTTGTTCCTGGTT
MD00G1066800-qpcr-F	CAGAGTGGCAATGGTGGCTA
MD00G1066800-qpcr-R	TGCAAGTCGGTGGAGACTTC
MD05G1054300-attb-F	GGGGACAAGTTTGTACAAAAAAGCAGGCTGCatggagaacatcgcggcg	表达载体构建 Plasmid constructure of PK7-203
MD05G1054300-attb-R	GGGGACCACTTTGTACAAGAAAGCTGGGTCttatttccaaggaagcttaaacgtgt	表达载体构建 Plasmid constructure of PK7-203

染色体 Chromosome	显著关联SNP位置 Leading SNP position (bp)	基因型 Genotype	位置类型 Position type	-log10（P）值 -log10 (P)
Chr5	9339654	[T/C]	基因间区 Intergenic region	4.05E-08
Chr5	9357320	[T/C]	基因间区 Intergenic region	3.86E-08
Chr5	8263898	[T/C]	基因间区 Intergenic region	3.37E-08
Chr0	6821757	[A/G]	内含子 Intron	2.14E-08
Chr0	12882138	[T/C]	内含子 Intron	1.40E-08
Chr5	9336893	[C/G]	基因间区 Intergenic region	1.21E-08

SNP位置 SNP position (bp)	候选基因 Candicate gene	同源拟南芥 Homolog Arabidopsis	距离 Distance (bp)	基因功能 Gene function
9339654	MD05G1054300	AT2G43850	204058	整合素连接蛋白激酶 Integrin-linked protein kinase
9339654	MD05G1054400	AT4G38890	1049	FMN连锁氧化还原酶类超家族蛋白 FMN linked oxidoreductase superfamily protein
9357320	MD05G1054400	AT4G38890	3882	FMN连锁氧化还原酶类超家族蛋白 FMN linked oxidoreductase superfamily protein
9357320	MD05G1054500	AT4G38900	7806	碱性亮氨酸拉链（bZIP）转录因子家族蛋白 Basic leucine zipper (bZIP) transcription factor family protein
8263898	MD05G1048600	AT3G21175	12639	植物特异性GATA型转录因子的一个新家族成员 GATA-type transcription factor
8263898	MD05G1048700	AT1G21280	14343	多蛋白/逆转录转座子Multiprotein/retrotransposon
6821757	MD00G1039900	AT4G38960		B-box型锌指家族蛋白 B-box zinc finger family protein
12882138	MD00G1066800	AT4G34730		核糖体结合因子A家族蛋白 Ribosome-binding factor A family protein
9336893	MD05G1054300	AT2G43850	201297	整合素连接蛋白激酶 Integrin-linked protein kinase
	MD05G1054400	AT4G38890	3810	FMN连锁氧化还原酶类超家族蛋白 FMN-linked oxidoreductase superfamily protein

Resistant Evaluation of 84 Apple Cultivars to Alternaria alternata f. sp. mali and Genome-Wide Association Analysis

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