玉米镰孢菌复合病原茎腐病抗性种质资源鉴定及抗性基因挖掘

doi:10.3864/j.issn.0578-1752.2024.13.002

中国农业科学 ›› 2024, Vol. 57 ›› Issue (13): 2509-2524.doi: 10.3864/j.issn.0578-1752.2024.13.002

• 作物遗传育种·种质资源·分子遗传学 • 上一篇下一篇

玉米镰孢菌复合病原茎腐病抗性种质资源鉴定及抗性基因挖掘

桂翠林(), 马亮(), 王银莹, 谢富贵, 赵彩宏, 王文淼, 李鑫, 王青(), 高夕全()

南京农业大学农学院/作物遗传与种质创新和利用全国重点实验室/江苏省现代作物生产协同创新中心，南京 210095

收稿日期:2023-07-11 接受日期:2023-11-10 出版日期:2024-07-09 发布日期:2024-07-09
通信作者:
王青，E-mail：qingwang@njau.edu.cn。
高夕全，E-mail：xgao@njau.edu.cn
联系方式: 桂翠林，E-mail：2020101079@stu.njau.edu.cn。马亮，E-mail：2019201077@njau.edu.cn。桂翠林和马亮为同等贡献作者。
基金资助:
江苏省种业振兴“揭榜挂帅”项目(JBGS[2021]002); 国家重点研发计划战略性科技创新合作专项(2020YFE0202900); 中央高校基本科研业务费专项资金(Y0202100126); 中央高校基本科研业务费专项资金(KYZZ2022001)

Identification of Resistant Germplasms and Mining of Candidate Genes Associated with Resistance to Stalk Rot Caused by Synergistic Infection with Fusarium spp. in Maize

GUI CuiLin(), MA Liang(), WANG YinYing, XIE FuGui, ZHAO CaiHong, WANG WenMiao, LI Xin, WANG Qing(), GAO XiQuan()

College of Agriculture, Nanjing Agricultural University/State Key Laboratory for Crop Genetics & Germplasm Enhancement and Utilization/Jiangsu Collaborative Innovation Center for Modern Crop Production, Nanjing 210095

Received:2023-07-11 Accepted:2023-11-10 Published:2024-07-09 Online:2024-07-09

摘要/Abstract

摘要：

【目的】玉米茎腐病是我国玉米主产区普遍发生的重要病害之一，自然条件下，玉米茎腐病多由多种病原菌共同侵染造成。筛选抗禾谷镰孢菌（Fusarium graminearum）和拟轮枝镰孢菌（Fusarium verticillioides）复合侵染的优异玉米种质，鉴定与复合病原引起的茎腐病抗性相关数量性状核苷酸（quantitative trait nucleotide，QTN），挖掘抗性候选基因，为玉米抗复合病原抗性分子育种提供基因资源和理论借鉴。【方法】以一个玉米自然群体为试验材料，接种F. graminearum和F. verticillioides复合病原菌，鉴定茎腐病表型；利用全基因组关联分析，筛选显著抗性SNP位点，预测抗病候选基因。【结果】通过田间和室内2个环境下接种复合病原后的茎腐病表型鉴定试验，发现不同来源和亚群的自交系对复合病原侵染的表型差异显著。田间表型鉴定结果表明，收集于中国的自交系普遍抗性较高，而美国的自交系普遍感病性较高；热带及亚热带亚群的自交系抗性较高，混合型亚群的自交系感病性较高。室内表型鉴定结果表明，收集于美国的自交系材料抗性较高，国际玉米小麦改良中心的自交系材料感病性高；硬秆亚群的玉米种质表现较高抗性，混合型亚群的种质表现较高感病性。于田间和室内2个环境下分别筛选出29份和16份对复合病原侵染具有较高抗性水平的种质，2个环境共同筛选到6份抗病种质。基于田间表型GWAS分析，鉴定到18个与复合病原茎腐病抗性显著相关的QTN，挖掘出93个抗病候选基因；有4个基因表现出单倍型变异，且接种后基因表达水平在抗病材料中呈上调趋势。【结论】利用遗传背景丰富的玉米自然群体，在2个环境中共同鉴定出6份玉米镰孢菌复合病原茎腐病抗性材料，可作为潜在的玉米抗茎腐病育种种质资源；挖掘出4个可能参与复合病原菌抗性的候选基因，为玉米镰孢菌复合病原茎腐病抗性育种提供基因资源。

关键词: 玉米茎腐病, 禾谷镰孢菌, 拟轮枝镰孢菌, 复合侵染, 全基因组关联分析, 抗性基因

Abstract:

【Objective】 Maize stalk rot is one of the common and most devastating diseases in major maize production areas in China. Under natural conditions, maize stalk rot is mostly caused by the synergistic infection of various pathogens. The purpose of this study was to screen elite maize germplasms resistant to the synergistic infection with F. graminearum and F. verticillioides. Meanwhile, QTN associated with resistance to the infection by synergistic infection of two Fusarium species and the candidate resistance genes were identified, which will provide gene resources and theoretical reference for molecular breeding of maize variety resistant to synergistic infection of different pathogens.【Method】 Using a maize natural population as experimental materials, the maize stalk rot phenotypes were investigated upon simultaneous infection with F. graminearum and F. verticillioides. Furthermore, GWAS analysis was conducted to identify significant resistance SNP and to predict candidate genes for stalk rot resistance.【Result】 Through the phenotypic analysis of stalk rot caused by synergistic infection under both field and laboratory conditions, it was found that inbred lines from different sources and subgroups showed significant phenotypic variation. More specifically, the field assay results showed that the inbred lines collected from China were more resistant and that from USA were more susceptible to synergistic infection. Moreover, the inbred lines of tropical and subtropical subgroup were more resistant, whereas the inbred lines of Mixed subgroup more susceptible. The seedling assay results under laboratory condition showed that the lines collected from USA were more resistant, whereas that from CIMMYT were more susceptible. The lines of SS subgroup were more resistant, and that of Mixed subgroup were more susceptible. By integrating field and laboratory phenotypic data, 29 and 16 lines with higher levels of resistance to synergistic infection were screened out respectively, and 6 resistant lines were identified under both conditions. Moreover, based on the field phenotype GWAS, 18 QTNs associated with the resistance were identified, and 93 candidate genes associated with stalk rot resistance to synergistic infection were mined. Among these candidate genes, four genes showed haplotype variation, whose expression levels were up-regulated in disease-resistant lines.【Conclusion】 Using the natural population of maize with great diversity in genetic background, 6 resistant lines to the synergistic infection with Fusarium spp. were identified under two conditions, which can be used as potential germplasm resources for maize stalk rot resistance in the future. Four candidate genes that might be involved in the resistance to synergistic infection were identified by GWAS, which will provide genetic resources for the breeding maize varieties with enhanced resistance to stalk rot caused by F. graminearum and F. verticillioides.

Key words: maize stalk rot, Fusarium graminearum, Fusarium verticillioides, synergistic infection, genome wide association study, resistance genes

桂翠林, 马亮, 王银莹, 谢富贵, 赵彩宏, 王文淼, 李鑫, 王青, 高夕全. 玉米镰孢菌复合病原茎腐病抗性种质资源鉴定及抗性基因挖掘[J]. 中国农业科学, 2024, 57(13): 2509-2524.

GUI CuiLin, MA Liang, WANG YinYing, XIE FuGui, ZHAO CaiHong, WANG WenMiao, LI Xin, WANG Qing, GAO XiQuan. Identification of Resistant Germplasms and Mining of Candidate Genes Associated with Resistance to Stalk Rot Caused by Synergistic Infection with Fusarium spp. in Maize[J]. Scientia Agricultura Sinica, 2024, 57(13): 2509-2524.

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田间复合病原茎腐病抗性的候选基因信息"

标记 Marker	Bin	<BOLD>P</BOLD>值 <BOLD>P</BOLD> value	位置 Position	基因 Gene	基因位置开始-结束 Gene start-end	注释 Annotation
Chr.1.S_37202321	1.03	2.67E-06	3′UTR	GRMZM2G408305	37202146-37215962	ARM重复超家族蛋白 ARM repeat superfamily protein
Chr.1.S_35134046	1.03	1.95E-06	外显子Exonic	GRMZM2G136513	35132532-35136898	抗病蛋白RPS2 Disease resistance protein RPS2
Chr.1.S_35136660	1.03	8.73E-06	外显子Exonic	GRMZM2G136513	35132532-35136898	抗病蛋白RPS2 Disease resistance protein RPS2
Chr.1.S_230178588	1.08	5.64E-06	外显子Exonic	GRMZM5G816209	230176955-30178674
Chr.3.S_6095672	3.02	8.22E-06	3′UTR	GRMZM2G468479	6088603-6096563	假定的MYB DNA结合域超家族蛋白 Putative MYB DNA-binding domain superfamily protein
Chr.3.S_198540836	3.07	6.03E-06	内含子Intronic	AC209455.3_FG009	198539184-198543636
Chr.4.S_226677337	4.09	6.23E-07	上游Upstream	GRMZM2G534064	226678246-226678352
Chr.5.S_110733295	5.04	8.23E-06	基因间区Intergenic	GRMZM2G052821 GRMZM5G810549	110462595-110515712 111031219-111031605	(6-4) DNA 光解酶 (6-4) DNA photolyase
Chr.6.S_16552209	6.01	3.09E-06	基因间区Intergenic	GRMZM2G357280 GRMZM2G519047	16469580-16476098 16592323-16592418‬
Chr.6.S_166899228	6.08	7.19E-07	3′UTR	GRMZM2G158998	166897023-166899522	Phox相关结构域 Phox-associated domain
Chr.7.S_13209638	7.01	5.63E-06	3′UTR	GRMZM2G150091	13208679-13209853	硫氧还蛋白 Thioredoxin
Chr.7.S_133361933	7.03	4.56E-06	外显子Exonic	GRMZM2G103902	133359936-133367491	EMSY-LIKE 4蛋白 Protein EMSY-LIKE 4
Chr.7.S_133367147	7.03	4.56E-06	外显子Exonic	GRMZM2G103902	133359936-133367491	EMSY-LIKE 4蛋白 Protein EMSY-LIKE 4
Chr.7.S_133367336	7.03	4.56E-06	外显子Exonic	GRMZM2G103902	133359936-133367491	EMSY-LIKE 4蛋白 Protein EMSY-LIKE 4
Chr.7.S_145977576	7.03	3.70E-06	外显子Exonic	GRMZM2G146240	145968303-145978114
Chr.7.S_173375841	7.05	5.90E-06	基因间区Intergenic	GRMZM2G349655 GRMZM5G867912	173327041-173328625 173447389-173451235	钙结合蛋白CAST Calcium-binding protein CAST
Chr.10.S_10615482	10.02	9.26E-07	外显子Exonic	GRMZM2G103662	10613555-10616571	天冬氨酰蛋白酶APCB1 Aspartyl protease APCB1
Chr.10.S_28599638	10.03	7.00E-06	基因间区Intergenic	GRMZM2G052606 GRMZM2G121031	28600793-28603531 28588781-28589630	次生壁MYB46转录因子Secondary wall MYB46 transcription factor

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病级指数 Disease index	室内 In the laboratory	田间 In the field	抗性评价 Resistance evaluation
1	茎秆未见明显菌丝和明显色泽变化 No obvious hyphae and color change were observed on the stem	发病面积占接种茎节总面积0%—10% The lesion area accounts for 0%-10% of the total area of inoculated stems	高抗 Highly resistant (HR)
2	接种部位出现稀疏菌丝，接种部位表面出现褶皱 The hyphae were sparse and the surface of inoculation site was wrinkled	发病面积占接种茎节总面积10%—20% The lesion area accounts for 10%-20% of the total area of inoculated stems	抗 Resistant (R)
3	有明显菌丝，接种部位颜色加深，出现腐烂变软，但茎秆仍可直立 There are obvious hyphae, the color of the inoculation site is deepened, and it decays and softens, but the stem can still stand upright	发病面积占接种茎节总面积20%—40% The lesion area accounts for 20%-40% of the total area of inoculated stems	中抗 Moderately resistant (MR)
4	菌丝扩展，接种部位腐烂变软出现明显水渍状，茎秆不能直立 The hyphae expanded, the inoculation site rotted and softened, and obvious water soak appeared, and the stems could not stand upright	发病面积占接种茎节总面积40%—60% The lesion area accounts for 40%-60% of the total area of inoculated stems.	感 Susceptible (S)
5	菌丝向上向下密集扩展，腐烂部位深褐色，茎秆倒伏 The hyphae spread densely upward and downward, the rotten parts were dark brown, and the stems were lodging	发病面积占接种茎节总面积60%—100% The lesion area accounts for 60%-100% of the total area of inoculated stems	高感 Highly susceptible (HS)

处理 Treatment	平均值 Mean	标准差 SD	最小值 Min	最大值 Max	偏度 Skew	峰度 Kurt	遗传率 H²	相关性 Correlation
重复1 Repeat 1	28.61	15.75	5.00	77.50	0.80	0.34		0.45**
重复2 Repeat 2	27.33	16.21	5.00	90.00	0.94	0.88		0.45**
最佳线性无偏预测BLUP	28.00	8.35	14.49	56.04	0.75	0.31	0.62

数量和百分比 Number and percentage	高抗 HR	抗 R	中抗 MR	感 S	高感 HS
重复1数量No. of repeat 1	22	46	97	38	10
重复1百分比Percentage of repeat 1 (%)	10.33	21.60	45.54	17.84	6.49
重复2数量No. of repeat 2	21	63	81	37	8
重复2百分比Percentage of repeat 2 (%)	10.00	30.00	38.57	17.62	3.81

处理 Treatment	平均值 Mean	标准差 SD	最小值 Min	最大值 Max	偏度 Skew	峰度 Kurt	遗传率 H²
重复1 Repeat 1	2.95	0.78	1.00	4.33	-0.60	-0.34
重复2 Repeat2	3.25	0.67	1.45	4.67	-0.57	-0.05
重复3 Repeat3	3.37	0.56	1.52	4.31	-0.91	0.83
最佳线性无偏预测BLUP	3.19	0.20	2.69	3.61	-0.37	-0.40	0.43

数量和百分比 Number and percentage	高抗HR	抗R	中抗MR	感S	高感HS
重复1数量No. of repeat 1	2	27	64	87	8
重复1百分比Percentage of repeat 1 (%)	1.06	14.36	34.04	46.28	4.26
重复2数量No. of repeat 2	0	10	47	109	22
重复2百分比Percentage of repeat 2 (%)	0.00	5.32	25.00	57.98	11.70
重复3数量No. of repeat 3	0	6	40	126	16
重复3百分比Percentage of repeat 3 (%)	0.00	3.19	21.28	67.02	8.51

玉米镰孢菌复合病原茎腐病抗性种质资源鉴定及抗性基因挖掘

Identification of Resistant Germplasms and Mining of Candidate Genes Associated with Resistance to Stalk Rot Caused by Synergistic Infection with Fusarium spp. in Maize

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