基于转录组测序的玉米瘤黑粉菌UM01240过表达菌株诱导玉米抗病性分析

doi:10.3864/j.issn.0578-1752.2025.06.006

中国农业科学 ›› 2025, Vol. 58 ›› Issue (6): 1116-1130.doi: 10.3864/j.issn.0578-1752.2025.06.006

基于转录组测序的玉米瘤黑粉菌UM01240过表达菌株诱导玉米抗病性分析

邹晓威¹(), 夏蕾¹, 朱晓敏¹, 孙辉¹, 周琦³, 齐霁¹^,², 张亚封⁴, 郑岩¹(), 姜兆远¹()

¹ 吉林省农业科学院（中国农业科技东北创新中心）植物保护研究所/吉林省农业微生物重点实验室/农业农村部东北作物有害生物综合治理重点实验室，吉林公主岭 136100
² 吉林师范大学生命科学学院，吉林四平 136099
³ 靖宇县农业技术推广中心，吉林白山 135200
⁴ 吉林农业大学农学院，长春 130118

收稿日期:2024-11-11 接受日期:2025-01-09 出版日期:2025-03-25 发布日期:2025-03-25
通信作者:
姜兆远，E-mail：jzy_80@163.com。通信作者郑岩，E-mail：jlzhengyan@163.com
姜兆远，E-mail：jzy_80@163.com。通信作者郑岩，E-mail：jlzhengyan@163.com
联系方式: 邹晓威，E-mail：zouxiaowei2008@126.com。
基金资助:
吉林省农业科技创新项目(KYJF2021ZR105); 国家重点研发计划(2023YFD1401504)

Analysis of Disease Resistance Induced by Ustilago maydis Strain with Overexpressed UM01240 Based on Transcriptome Sequencing

ZOU XiaoWei¹(), XIA Lei¹, ZHU XiaoMin¹, SUN Hui¹, ZHOU Qi³, QI Ji¹^,², ZHANG YaFeng⁴, ZHENG Yan¹(), JIANG ZhaoYuan¹()

¹ Institute of Plant Protection, Jilin Academy of Agricultural Sciences (Northeast Agricultural Research Center of China)/Jilin Key Laboratory of Agricultural Microbiology/Key Laboratory of Integrated Pest Management on Crops in Northeast China, Ministry of Agriculture and Rural Affairs, Gongzhuling 136100, Jilin
² School of Life Sciences, Jilin Normal University, Siping 136099, Jilin
³ Agro-Tech Extension and Service Center of Jingyu County, Baishan 135200, Jilin
⁴ Faculty of Agronomy, Jilin Agricultural University, Changchun 130118

Received:2024-11-11 Accepted:2025-01-09 Published:2025-03-25 Online:2025-03-25

摘要/Abstract

摘要：

【目的】探究玉米瘤黑粉菌（Ustilago maydis）外分泌蛋白基因UM01240诱导玉米抗瘤黑粉病机制。【方法】将玉米瘤黑粉菌野生型菌株SG200、UM01240过表达菌株SG200-OE-UM01240及UM01240缺失菌株SG200ΔUM01240分别接种于高感瘤黑粉病玉米品种吉单209，接种样品分别命名为S1、S2及S3，7 d后统计供试菌株对玉米致病力差异。利用高通量RNA-Seq技术比较S2玉米叶片与S1、S3玉米叶片之间的差异表达基因，从植物-病原互作、黄酮类化合物生物合成、苯丙烷代谢及植物激素信号转导途径中筛选抗病相关的基因，并进行qRT-PCR验证。【结果】过表达菌株SG200-OE-UM01240相较SG200菌株致病力明显减弱，其对应S2玉米叶片病症最轻，而SG200ΔUM01240致病力较SG200菌株显著增强，其对应S3玉米叶片病症最重。S2玉米叶片相较S1、S3玉米叶片共表达差异基因1 613个，涉及植物-病原互作途径相关基因31个，主要为WRKY1、WRKY33、WRKY52、PR1及PIT5等蛋白基因；黄酮类化合物生物合成途径基因15个，主要为乔松素、柚皮素、木犀草素及二氢槲皮素等合成相关基因；苯丙烷代谢途径基因23个，主要为木质素、肉桂醛、对-香豆醛、松柏醛及芥子醛等合成相关基因；植物激素信号转导途径基因33个，主要为水杨酸、细胞分裂素、赤霉素及茉莉酸等合成相关基因。所选基因qRT-PCR分析结果与转录组数据相关性一致。【结论】外分泌蛋白基因UM01240在玉米瘤黑粉菌致病力中起着重要作用，其表达水平与玉米瘤黑粉菌的致病力负相关。UM01240可能通过调控植物-病原互作、类黄酮和苯丙素类化合物生物合成、植物激素信号转导等途径达到玉米瘤黑粉菌与玉米寄主平衡共生的目的。

关键词: 玉米瘤黑粉菌, 玉米, 抗病基因, 转录组测序

Abstract:

【Objective】 The objective of this study is to investigate the mechanism of maize resistance to corn smut disease induced by the secreted protein gene UM01240 of Ustilago maydis.【Method】 The wild-type strain SG200 of U. maydis, the UM01240 overexpression strain SG200-OE-UM01240, and the UM01240 deletion strain SG200ΔUM01240 were individually inoculated onto the maize variety Jidan209, which is highly susceptible to U. maydis. The three inoculated maize samples were named as S1, S2, and S3, respectively. After 7 d of inoculation, the pathogenicity differences among the tested strains on maize were evaluated. Using high-throughput RNA-Seq technology, the differential expression of genes between the S2 maize leaves and the S1 and S3 maize leaves was compared. Resistance-related genes involved in plant-pathogen interactions, flavonoid biosynthesis, phenylpropane metabolism, and plant hormone signal pathways were screened and subsequently validated through qRT-PCR.【Result】 The overexpression strain SG200-OE-UM01240 exhibited significantly reduced pathogenicity compared to the SG200 strain, with the corresponding maize sample S2 displaying the mildest leaf symptoms. In contrast, the SG200ΔUM01240 strain demonstrated significantly increased pathogenicity, with the maize sample S3 displaying the most severe leaf symptoms. In comparison to the S1 and S3 maize leaves, the S2 maize leaves exhibited 1 613 differentially expressed genes. Among these genes, 31 were associated with the plant-pathogen interaction pathway, primarily including protein-coding genes such as WRKY1, WRKY33, WRKY52, PR1, and PIT5. Additionally, 15 genes were linked to the flavonoid biosynthesis pathway, primarily including the synthesis of pinocembrin, naringenin, luteolin, and dihydroquercetin. Furthermore, 23 genes related to the phenylpropane metabolism pathway were identified, mainly associated with the synthesis of lignin, cinnamaldehyde, p-hydroxycinnamic acid, coniferylaldehyde, and sinapaldehyde. Lastly, 33 genes connected to plant hormone signal transduction pathways were also found, primarily concerning the synthesis of salicylic acid, cytokinins, gibberellins, and jasmonic acid. The results of qRT-PCR analysis for the selected genes were consistent with the transcriptome data.【Conclusion】 The secreted protein gene UM01240 plays a crucial role in the pathogenicity of U. maydis in maize. The expression level of UM01240 is negatively correlated with the pathogenicity of U. maydis in maize. UM01240 achieves a balanced symbiotic relationship between U. maydis and the maize host by regulating pathways including plant-pathogen interaction, flavonoid and phenylpropanoid compound biosynthesis, and plant hormone signal transduction.

Key words: Ustilago maydis, maize, resistance gene, transcriptome sequencing

邹晓威, 夏蕾, 朱晓敏, 孙辉, 周琦, 齐霁, 张亚封, 郑岩, 姜兆远. 基于转录组测序的玉米瘤黑粉菌UM01240过表达菌株诱导玉米抗病性分析[J]. 中国农业科学, 2025, 58(6): 1116-1130.

ZOU XiaoWei, XIA Lei, ZHU XiaoMin, SUN Hui, ZHOU Qi, QI Ji, ZHANG YaFeng, ZHENG Yan, JIANG ZhaoYuan. Analysis of Disease Resistance Induced by Ustilago maydis Strain with Overexpressed UM01240 Based on Transcriptome Sequencing[J]. Scientia Agricultura Sinica, 2025, 58(6): 1116-1130.

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表1

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图2

表2

表3

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表4

病原与植物互作途径中S1—S2与S3—S2共有差异基因"

基因ID Gene ID	差异表达比率 Differential expression ratio		表达变化 Expression change	Pfam功能注释 Pfam annotation
基因ID Gene ID	S1-S2	S3-S2	表达变化 Expression change	Pfam功能注释 Pfam annotation
LOC100147737	2.92	2.64	Up	WRKY转录因子DNA结合结构域WRKY DNA-binding domain
LOC100277272	2.24	2.18	Up	WRKY转录因子DNA结合结构域WRKY DNA-binding domain
LOC100281172	2.61	2.79	Up	AP2结构域AP2 domain
LOC100281244	3.10	5.02	Up	WRKY转录因子DNA结合结构域WRKY DNA-binding domain
LOC100382219	2.80	2.11	Up	豆科植物凝集素结构域Legume lectin domain
LOC103626179	2.27	3.04	Up	富含亮氨酸重复序列Leucine rich repeat
LOC103626398	2.12	2.60	Up	NB-ARC结构域NB-ARC domain
LOC103631918	2.02	2.73	Up	富含半胱氨酸分泌蛋白家族Cysteine-rich secretory protein family
LOC103633564	2.80	3.15	Up	WRKY转录因子DNA结合结构域WRKY DNA-binding domain
LOC103634641	2.98	3.72	Up	WRKY转录因子DNA结合结构域WRKY DNA-binding domain
LOC103636195	2.03	2.06	Up	酪氨酸蛋白和丝氨酸/苏氨酸蛋白激酶 Protein tyrosine and serine/threonine kinase
LOC103639215	2.44	2.89	Up	蛋白激酶结构域Protein kinase domain
LOC103641459	2.38	2.36	Up	蛋白激酶结构域Protein kinase domain
LOC103653766	2.13	2.61	Up	富含亮氨酸重复序列Leucine rich repeat
LOC103654233	2.36	3.25	Up	EF hand结构域EF hand domain
LOC109942268	2.73	3.44	Up	WRKY转录因子DNA结合结构域WRKY DNA-binding domain
LOC542352	2.65	2.78	Up	富含半胱氨酸分泌蛋白家族Cysteine-rich secretory protein family
LOC542671	2.07	2.09	Up	蛋白激酶结构域Protein kinase domain
LOC100191595	-2.04	-2.03	Down	脂肪酸链延长酶1/Ⅲ型聚酮合成酶类蛋白 FAE1/Type Ⅲ polyketide synthase-like protein
LOC100193715	-2.36	-3.48	Down	酪氨酸蛋白和丝氨酸/苏氨酸蛋白激酶 Protein tyrosine and serine/threonine kinase
LOC100274438	-2.52	-2.60	Down	蛋白激酶结构域Protein kinase domain
LOC100281769	-2.55	-2.63	Down	脂肪酸链延长酶1/Ⅲ型聚酮合成酶类蛋白 FAE1/Type Ⅲ polyketide synthase-like protein
LOC100283031	-2.45	-2.27	Down	脂肪酸链延长酶1/Ⅲ型聚酮合成酶类蛋白 FAE1/Type Ⅲ polyketide synthase-like protein
LOC100283804	-2.29	-2.44	Down	LysM结构域LysM domain
LOC100286138	-2.27	-2.57	Down	脂肪酸链延长酶1/Ⅲ型聚酮合成酶类蛋白 FAE1/Type Ⅲ polyketide synthase-like protein
LOC100381429	-2.68	-2.96	Down	酪氨酸蛋白和丝氨酸/苏氨酸蛋白激酶 Protein tyrosine and serine/threonine kinase
LOC100383536	-2.85	-3.57	Down	酪氨酸蛋白和丝氨酸/苏氨酸蛋白激酶 Protein tyrosine and serine/threonine kinase
LOC103639429	-2.02	-2.46	Down	脂肪酸链延长酶1/Ⅲ型聚酮合成酶类蛋白 FAE1/Type Ⅲ polyketide synthase-like protein
LOC103655094	-2.07	-2.09	Down	脂肪酸链延长酶1/Ⅲ型聚酮合成酶类蛋白 FAE1/Type Ⅲ polyketide synthase-like protein
LOC103656014	-2.40	-2.55	Down	酪氨酸蛋白和丝氨酸/苏氨酸蛋白激酶 Protein tyrosine and serine/threonine kinase
LOC542018	-2.31	-3.64	Down	脂肪酸链延长酶1/Ⅲ型聚酮合成酶类蛋白 FAE1/Type Ⅲ polyketide synthase-like protein

表4

表5

表6

表7

植物激素信号转导途径中S1—S2与S3—S2共有差异基因"

基因ID Gene ID	相关植物激素 Related plant hormone	差异表达比率 Differential expression ratio		表达变化 Expression change	Pfam功能注释 Pfam annotation
基因ID Gene ID	相关植物激素 Related plant hormone	S1-S2	S3-S2	表达变化 Expression change	Pfam功能注释 Pfam annotation
LOC100193646	茉莉酸 Jasmonic acid	3.02	2.18	Up	螺旋-环-螺旋DNA结合域 Helix-loop-helix DNA-binding domain
LOC100282558	生长素Auxin	3.97	2.36	Up	生长素应答蛋白Auxin responsive protein
LOC103626859	水杨酸Salicylic acid	3.14	2.09	Up	种子休眠控制Seed dormancy control
LOC103631918	水杨酸Salicylic acid	2.73	2.02	Up	富含半胱氨酸分泌蛋白家族 Cysteine-rich secretory protein family
LOC103635561	茉莉酸Jasmonic acid	3.81	2.39	Up	螺旋-环-螺旋DNA结合域 Helix-loop-helix DNA-binding domain
LOC103635662	赤霉素Gibberellin	2.38	2.06	Up	α/β水解酶折叠alpha/beta hydrolase fold
LOC103636195	水杨酸Salicylic acid	2.06	2.03	Up	酪氨酸蛋白和丝氨酸/苏氨酸蛋白激酶 Protein tyrosine and serine/threonine kinase
LOC103639215	油菜素甾醇Brassicasterol	2.89	2.44	Up	蛋白激酶结构域Protein kinase domain
LOC103641459	油菜素甾醇Brassicasterol	2.36	2.38	Up	蛋白激酶结构域Protein kinase domain
LOC103646635	细胞分裂素Cytokinin	2.36	2.30	Up	应答调控蛋白受体结构域 Response regulator receiver domain
LOC103649622	茉莉酸Jasmonic acid	3.10	2.59	Up	螺旋-环-螺旋DNA结合域 Helix-loop-helix DNA-binding domain
LOC103650261	油菜素甾醇Brassicasterol	2.69	2.33	Up	富含亮氨酸重复序列Leucine rich repeat
LOC103650987	生长素Auxin	2.42	2.04	Up	跨膜氨基酸转运蛋白 Transmembrane amino acid transporter protein
LOC542352	水杨酸 Salicylic acid	2.78	2.65	Up	富含半胱氨酸分泌蛋白家族 Cysteine-rich secretory protein family
LOC542671	油菜素甾醇Brassicasterol	2.09	2.07	Up	蛋白激酶结构域Protein kinase domain
LOC100191484	油菜素甾醇Brassicasterol	-3.23	-2.63	Down	酪氨酸蛋白和丝氨酸/苏氨酸蛋白激酶 Protein tyrosine and serine/threonine kinase
LOC100191784	生长素Auxin	-2.86	-2.94	Down	生长素应答因子Auxin response factor
LOC100194106	茉莉酸Jasmonic acid	-2.70	-2.13	Down	螺旋-环-螺旋DNA结合域 Helix-loop-helix DNA-binding domain
LOC100274111	油菜素甾醇Brassicasterol	-2.78	-2.17	Down	BES1/BZR1转录因子N末端 BES1/BZR1 plant transcription factor, N-terminal
LOC100274569	生长素Auxin	-2.22	-2.38	Down	Aux/IAA家族AUX/IAA family
LOC100282511	油菜素甾醇Brassicasterol	-2.38	-2.50	Down	蛋白激酶结构域Protein kinase domain
LOC100283579	生长素Auxin	-2.56	-2.78	Down	Aux/IAA家族AUX/IAA family
LOC100284259	生长素Auxin	-2.86	-2.63	Down	Aux/IAA家族AUX/IAA family
LOC100284262	生长素Auxin	-2.56	-2.94	Down	Aux/IAA家族AUX/IAA family
LOC100382395	油菜素甾醇Brassicasterol	-4.76	-4.76	Down	蛋白激酶结构域Protein kinase domain
LOC100384222	茉莉酸Jasmonic acid	-3.33	-2.22	Down	Jas基序Jas motif
LOC100384328	生长素Auxin	-2.86	-2.08	Down	生长素应答因子Auxin response factor
LOC100502480	生长素Auxin	-2.17	-2.13	Down	生长素应答因子Auxin response factor
LOC103633580	乙烯Ethylene	-4.76	-2.86	Down	乙烯不敏感因子3 Ethylene insensitive 3
LOC103636232	油菜素甾醇Brassicasterol	-2.13	-2.38	Down	蛋白激酶结构域Protein kinase domain
LOC103647498	茉莉酸Jasmonic acid	-2.78	-2.13	Down	功能未知蛋白质DUF547 Protein of unknown function, DUF547
LOC103650745	水杨酸Salicylic acid	-2.86	-2.08	Down	BTB/POZ蛋白质结构域BTB/POZ domain
LOC542195	脱落酸Abscisic acid	-16.67	-16.67	Down	病程相关蛋白Bet v 1家族 Pathogenesis-related protein Bet v 1 family

表7

图4

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基因ID Gene ID	正向引物Forward primer (5′-3′)	反向引物Reverse primer (5′-3′)	产物大小Product size (bp)
LOC100281769	AGATGGACGCCTTCTTCGAC	GGGAGAGCATGGAGACGTTG	105
LOC100281244	CCGAGATCCTACTTCCGCTG	GTTGCTCATGGTTGTGCTCG	124
LOC100284018	ACACCAGGTGAAAATGGGCT	ATGTCCGTGATACCTGTGCC	117
LOC100272560	GCCTTACATCTGGTCTCCGT	TGGATGTGGATGCAGCTCAG	87
LOC100192105	GCTCCAACAACGGACAGATAA	CAACGCGACGATCTCACATA	135
LOC100191539	CTACATCAAGGTGCGCAAGC	TGACGGCTTTGTAGACGGAC	122
LOC100502480	CAGGCACAGAGCTTCACAGA	ATGAGAACGGCCTCAGTGTG	88
LOC103635561	CTGTGACGACCATCAGTGCT	GTTCTTGTGCTGCGCTCTTT	112
U76259	GCCTGGTATGGTTGTTACT	CATACCCACGCTTCAGATCC	155

样品 Sample	纯净数据 Clean reads	纯净碱基 Clean bases	GC含量 GC content (%)	Q30含量 Q30 content (%)	总读取数 Total reads	映射总数 Total mapped
S1-1	36037010	10006195830	54.42	93.72	77753256	68092533 (87.58%)
S1-2	35371086	10756440588	55.18	93.16	72962066	64176012 (87.96%)
S1-3	34830256	10583818126	53.72	93.42	69103372	61019566 (88.30%)
S2-1	33467645	10338642702	53.43	93.79	66935290	58565018 (87.49%)
S2-2	37146447	11115049820	54.56	93.93	74292894	66251495 (89.18%)
S2-3	36998045	11070925930	55.14	93.41	73996090	66114684 (89.35%)
S3-1	38876628	11585600834	53.50	93.77	72074020	63135502 (87.60%)
S3-2	36481033	10911121802	55.12	93.68	70742172	62436983 (88.26%)
S3-3	34551686	10420004118	53.72	93.45	69660512	61419088 (88.17%)

注释数据库Annotation database	注释数Annotated number	注释百分比Annotated percent (%)
COG注释COG_Annotation	10556	27.21
GO注释GO_Annotation	29131	75.09
KEGG注释KEGG_Annotation	23944	61.72
KOG注释KOG_Annotation	17926	46.21
Pfam注释Pfam_Annotation	28286	72.91
Swiss注释Swiss-Prot_Annotation	23478	60.52
eggNOG注释eggNOG_Annotation	32786	84.51
NR注释NR_Annotation	38693	99.74
全部注释All_Annotation	38795	—

基因ID Gene ID	差异表达比率 Differential expression ratio		表达变化 Expression change	Pfam功能注释 Pfam annotation
基因ID Gene ID	S1-S2	S3-S2	表达变化 Expression change	Pfam功能注释 Pfam annotation
LOC100191539	2.58	2.10	Up	细胞色素P450 Cytochrome P450
LOC100191750	3.29	2.39	Up	转移酶家族Transferase family
LOC100191769	2.11	3.40	Up	过氧化物酶Peroxidase
LOC100273589	2.33	2.04	Up	细胞色素P450 Cytochrome P450
LOC100274269	4.40	3.33	Up	转移酶家族Transferase family
LOC100279348	2.95	2.02	Up	糖苷水解酶家族1 Glycosyl hydrolase family 1
LOC100280077	2.49	2.40	Up	过氧化物酶Peroxidase
LOC100284063	2.19	2.39	Up	转移酶家族Transferase family
LOC100383097	2.17	3.44	Up	转移酶家族Transferase family
LOC103632940	2.37	2.06	Up	依赖NAD的表异构酶/脱水酶家族 NAD dependent epimerase/dehydratase family
LOC103639086	3.45	2.45	Up	过氧化物酶Peroxidase
LOC103639152	4.11	2.31	Up	转移酶家族Transferase family
LOC100191905	-2.94	-2.70	Down	过氧化物酶Peroxidase
LOC100192105	-2.44	-2.17	Down	过氧化物酶Peroxidase
LOC100272560	-2.63	-2.50	Down	转移酶家族Transferase family
LOC100274288	-3.85	-3.85	Down	糖苷水解酶家族1 Glycosyl hydrolase family 1
LOC100281032	-6.25	-3.13	Down	过氧化物酶Peroxidase
LOC100283382	-3.85	-2.78	Down	过氧化物酶Peroxidase
LOC100284675	-2.17	-2.38	Down	过氧化物酶Peroxidase
LOC100381862	-2.86	-2.38	Down	糖苷水解酶家族1 Glycosyl hydrolase family 1
LOC100382272	-2.33	-2.17	Down	AMP结合酶AMP-binding enzyme
LOC103645956	-2.22	-2.38	Down	转移酶家族Transferase family
LOC541913	-4.55	-3.70	Down	乙醛脱氢酶家族Aldehyde dehydrogenase family

基于转录组测序的玉米瘤黑粉菌UM01240过表达菌株诱导玉米抗病性分析

Analysis of Disease Resistance Induced by Ustilago maydis Strain with Overexpressed UM01240 Based on Transcriptome Sequencing

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