Welcome to Acta Agronomica Sinica,

Acta Agronomica Sinica ›› 2020, Vol. 46 ›› Issue (9): 1303-1311.doi: 10.3724/SP.J.1006.2020.03004

• CROP GENETICS & BREEDING · GERMPLASM RESOURCES · MOLECULAR GENETICS •     Next Articles

Exploration of specific gene(s) for ear rot resistance to Fusarium verticilloides in maize

WEN Jing1, SHEN Yan-Qi1, HAN Si-Ping1, XING Yue-Xian2, ZHANG Ye1, WANG Zi-Yu1, LI Shi-Jie1, YANG Xiao-Hong3, HAO Dong-Yun1, ZHANG Yan1,*()   

  1. 1 Agro-Biotechnology Research Institute, Jilin Academy of Agricultural Sciences, Changchun 130033, Jilin, China
    2 Maize Research Institute, Jilin Academy of Agricultural Sciences, Gongzhuling 136100, Jilin, China
    3 College of Agronomy and Biotechnology, China Agricultural University, Beijing 100193, China
  • Received:2020-01-18 Accepted:2020-04-15 Online:2020-09-12 Published:2020-04-26
  • Contact: Yan ZHANG E-mail:zhangyan4023@163.com
  • Supported by:
    National Natural Science Foundation of China(31701504)

Abstract:

Ear rot in maize, caused by fungal pathogens, poses a grave threat to maize production, and current inbred lines in use generally lack resistance to ear rot. It is essential to explore the resistant loci and corresponding resistance genes for improvement of the resistance to ear rot in maize by molecular marker-assisted breeding and biotechnology breeding. The purpose of this study was to explore the resistance loci of ear rot caused by Fusarium verticilloides and preliminary identify candidate genes by transcriptome analysis and genome-wide association. The result of transcriptome analysis showed that there were 10,761 differentially expressed genes between inbred lines Fa A and Ye 81162 at seven days after artificial inoculation with Fusarium verticilloides. A total of five SNPs significantly associated with ear rot resistance were detected by genome-wide association analysis, and these SNPs were distributed on chromosomes 1 and 9. By comparing B73 RefGen_v3 and annotating, it was found that the genes involved near the SNP site included acyl activating enzyme 1 peroxisome, protein phosphatase 2C 48, magnesium transporter, receptor protein kinase CRINKLY4 and zinc finger CCCH domain protein 19. The zinc finger CCCH domain protein 19 detected in genome-wide association just was the differentially expressed gene from transcriptome analysis, indicating that Zinc finger CCCH domain protein 19 probably is related to resistance to Fusarium verticilloides ear rot in maize. The results not only provide theoretical basis and important genetic resources for resistance gene cloning and molecular breeding of maize, but also lay a foundation for analysing the interaction between maize and pathogen.

Key words: maize, Fusarium verticilloides, ear rot, resistance genes

Table 1

Classification criteria of Fusarium verticillioides ear rot in maize"

病情评级Disease severity 发病百分比Percentage of symptom
1 发病面积占雌穗总面积0~1% Percentages of lesion area: 0-1%
3 发病面积占雌穗总面积2%~10% Percentages of lesion area: 2%-10%
5 发病面积占雌穗总面积11%~25% Percentages of lesion area: 11%-25%
7 发病面积占雌穗总面积26%~50% Percentages of lesion area: 26%-50%
9 发病面积占雌穗总面积51%~100% Percentages of lesion area: 51%-100%

Table 2

Sequences of primers"

基因名称
Gene name
上游引物序列
Forward primer sequence (5'-3')
下游引物序列
Reverse primer sequence (5'-3')
产物长度
Product length (bp)
actin CCTTCATTGGCATGGAATCT GCAACCACCTTCACCTTCAT 128
β-tubulin2 AGACCGGTCAGTGCGGTAAC CGTGCTCGCCAGAGAGATGGT 70
CCCH domain protein 19 CAGGTGAGTTGTGGACATGG CTCCAAGCACAAGCAAACAA 197

Fig. 1

RT-PCR analysis of β-tubulin2 of Ye 81162 M: DL2000 marker; 1-6: Grain samples from ears before inoculation and at 1 d, 2 d, 3 d, 4 d, 7 d after inoculation."

Fig. 2

Relative expression of β-tubulin2 gene after artificial inoculation with Fusarium verticillium"

Fig. 3

Analysis of differentially expressed genes of Fa A and Ye 81162 after inoculation with Fusarium verticillium R: resistant; S: susceptible; R-0: Fa A before inoculation; R-7d: Fa A at seven days after inoculation; S-0: Ye 81162 before inoculation; S-7d: Ye 81162 at seven days after inoculation."

Fig. 4

Manhattan plot and QQ plot for genome-wide association analysis of resistance to ear rot caused by Fusarium verticillium in maize"

Table 3

Relative expression of β-tubulin2 gene after artificial inoculation with Fusarium verticillium"

自交系
Inbred line
β-tubulin2基因的相对表达量 Relative expression of β-tubulin2 gene
接菌前
Before inoculation
1 d 2 d 3 d 4 d 7 d
法A Fa A 0±0.00 0.0004±0.00 0.0002±0.00 0.0003±0.00 0.0002±0.00 1.006E-07±0.00
掖81162 Ye 81162 0±0.00 2.3894±0.93 0.6537±0.14 3.1675±0.38 3.0244±0.65 4.2477±0.26

Table 4

Gene information related to SNP loci associated with Fusarium verticillium ear rot resistance"

标记
Marker
注释
Annotation
染色体
Chromosome
描述
Description
chr1.S_7569254 GRMZM2G110616 1 酰基激活酶1过氧化物酶体
Probable acyl-activating enzyme 1 peroxisomal
chr1.S_8288770 GRMZM5G891266 1 蛋白磷酸酶2C 48 Probable protein phosphatase 2C 48
chr1.S_8353697 GRMZM2G018706 1 镁转运蛋白10 Magnesium transporter 10
chr9.S_154383692 GRMZM2G092776 9 受体蛋白激酶CRINKLY4 Receptor protein kinase CRINKLY4
chr9.S_154384544 GRMZM2G393471 9 锌指CCCH域蛋白19 Zinc finger CCCH domain-containing protein 19

Fig. 5

Relative expression of zinc finger CCCH domain-containing protein 19 gene after artificial inoculation with Fusarium verticillium"

[1] Ullstrup A J. An undescribed ear rot of corn caused by Physalospora zeae. Phytopathology, 1946,36:201-212.
[2] Bezuidenhout H, Maxasas W F O. Botryosphaeria zeae: the cause of gery ear rot of maize(Zea mays) in South Africa. Phytophylaetica, 1978,10:21-24.
[3] Kumar V, Shetty H S. A new ear and kernel rot of maize caused by Trichoderma viride pers. ex Fries. Curr Sci, 1982,51:620-621.
[4] 张艳, 谭静. 玉米穗粒腐病的研究进展. 现代农业科技, 2014, (21):121-122.
Zhang Y, Tan J. Research progress on ear rot in maize. Modern Agric Sci Technol, 2014, (21):121-122 (in Chinese with English abstract).
[5] 潘惠康, 张兰新. 玉米对穗粒腐病菌的抗病性. 华北农学报, 1987,2(3):86-89.
Pan H K, Zhang L X. Studies on kernel and ear rot of corm. Acta Agric Boreali-Sin, 1987,2(3):86-89 (in Chinese with English abstract).
[6] 任金平. 玉米穗腐病研究进展. 吉林农业科学, 1993, (3):39-43.
Ren J P. Progress in researching of ear rot of maize. J Jilin Agric Sci, 1993, (3):39-43 (in Chinese with English abstract).
[7] 胡南, 章红. 吉林省玉米穗腐病病原真菌中镰刀菌毒素的研究. 玉米科学, 1997,5(2):66-68.
Hu N, Zhang H. A study on production of three Fusarium mycotoxins of corn ear rot pathogenic fungi in Jilin province. J Maize Sci, 1997,5(2):66-68 (in Chinese with English abstract).
[8] 胡韬纲. 玉米穗腐病研究进展. 粮食科技与经济, 2015,40(3):50-52.
Hu T G. Research progress on maize ear rot. Grain Sci Technol Econ, 2015,40(3):50-52 (in Chinese with English abstract).
[9] 陈甲法, 丁俊强, 孙小东, 王爱东, 刘春元, 王瑞霞, 李晶晶, 王永霞, 马金亮, 韩娅楠, 吴建宇. 几种杀菌剂对玉米穗粒腐病主要病原菌的抑制作用. 河南农业科学, 2009, (4):81-83.
doi: 10.3969/j.issn.1004-3268.2009.04.022
Chen J F, Ding J Q, Sun X D, Wang A D, Liu C Y, Wang R X, Li J J, Wang Y X, Ma J L, Han Y N, Wu J Y. Inhibitory effects of several fungicides on the main pathogens of corn ear rot. J Henan Agric Sci, 2009, (4):81-83 (in Chinese).
[10] 刘春元, 李洪连, 吴建宇, 刘建华. 穗粒腐病菌对玉米幼苗的致病性研究. 河南农业科学, 2005, (11):60-63.
doi: 10.3969/j.issn.1004-3268.2005.11.019
Liu C Y, Li H L, Wu J Y, Liu J H. Studies on pathogenicity of pathogen of ear and seed rot in maize hybrids to maize seedling blight. J Henan Agric Sci, 2005, (11):60-63 (in Chinese with English abstract).
[11] 陈广泉. 河西走廊玉米穗粒腐病侵染规律及发病因子研究. 玉米科学, 2006,14(1):158-160.
Chen G Q. Study on infection law and disease factor of corn spike kernel rotten in Hexi corridor. J Maize Sci, 2006,14(1):158-160 (in Chinese with English abstract).
[12] 袁广胜, 杜娟, 高健, 张志明, 潘光堂. 玉米穗粒腐病差异表达基因的生物信息学分析. 玉米科学, 2013,21(5):46-51.
Yuan G S, Du J, Gao J, Zhang Z M, Pan G T. Bioinformation analysis on the differentially expressed genes in maize ear rot. J Maize Sci, 2013,21(5):46-51 (in Chinese with English abstract).
[13] Young N D. QTL mapping and quantitative disease resistance in plants. Annu Rev Phytopathol, 1996,34:479-501.
doi: 10.1146/annurev.phyto.34.1.479 pmid: 15012553
[14] Ding J Q, Wang X M, Chander S, Yan J B, Li J S. QTL mapping of resistance to Fusarium ear rot using a RIL population in maize. Mol Breed, 2008,22:395-403.
doi: 10.1007/s11032-008-9184-4
[15] Li Z M, Ding J Q, Wang R X, Chen J F, Sun X D, Chen W, Song W B, Dong H F, Dai X D, Xia Z L, Wu J Y. A new QTL for resistance to Fusarium ear rot in maize. J Appl Genet, 2011,52:403-406.
[16] Zila C T, Ogut F, Romay M C, Gardner C A, Buckler E S, Holland J B. Genome-wide association study of Fusarium ear rot disease in the U.S.A. maize inbred line collection. BMC Plant Biol, 2014,14:372.
doi: 10.1186/s12870-014-0372-6 pmid: 25547028
[17] Zila C T, Samayoa L F, Santiago R, Butron A, Holland J B. A genome-wide association study reveals genes associated with Fusarium ear rot resistance in a maize core diversity panel. Genes Genomes Genet, 2013,3:2095-2104.
[18] Kebede A Z, Woldemariam T, Reid L M, Harris L J. Quantitative trait loci mapping for Gibberella ear rot resistance and associated agronomic traits using genotyping-by-sequencing in maize. Theor Appl Genet, 2016,129:17-29.
doi: 10.1007/s00122-015-2600-3 pmid: 26643764
[19] Chen J F, Ding J Q, Li H M, Li Z M, Sun X D, Li J J, Wang R X, Dai X D, Dong H F, Song W B, Chen W, Xia Z L, Wu J Y. Detection and verification of quantitative trait loci for resistance to Fusarium ear rot in maize. Mol Breed, 2012,30:1649-1656.
[20] Perez-Brito S J D G D. QTL Mapping of Fusarium moniliforme ear rot resistance in highland maize, Mexico. Publicado como Articuloen Agrociencia, 2001,35:181-196.
[21] 张艳, 张叶, 王梓钰, 闻竞, 韩四平, 郭嘉, 邢跃先. 44份玉米自交系对镰孢穗腐病的抗性鉴定. 植物遗传资源学报, 2019,20:276-283
Zhang Y, Zhang Y, Wang Z Y, Wen J, Han S P, Guo J, Xing Y X. Evaluation of resistance to Fusarium ear rot in 44 maize inbred lines. J Plant Genet Resour, 2019,20:276-283 (in Chinese with English abstract).
[22] 邹成佳, 崔丽娜, 章振羽, 张小飞, 李荣进, 陈耕, 李晓. 玉米自交系对轮枝镰孢菌穗腐病的抗性评价, 西南农学报, 2017,30:1346-1349
Zou C J, Cui L N, Zhang Z Y, Zhang X F, Li R J, Chen G, Li X. Evaluation of maize inbred lines for resistance to Fusarium verticillioides ear rot. Southwest China J Agric Sci, 2017,30:1346-1349 (in Chinese with English abstract).
[23] 刘小艳, 孙艳侠, 王亚男, 刘晓楠, 刘坤, 郗冬梅. 水稻CCCH锌指蛋白亚家族I基因的表达分析. 山东农业科学, 2015,47(2):7-11
Liu X Y, Sun Y X, Wang Y N, Liu X N, Liu K, Xi D M. Expression analysis of CCCH-zinc finger protein subfamily I genes in rice. Shandong Agric Sci, 2015,47(2):7-11 (in Chinese with English abstract).
[24] 秦智慧, 杨青川, 晁跃辉, 康俊梅. CCCH型锌指蛋白研究进展. 生物技术通报, 2010, (8):1-6.
Qin Z H, Yang Q C, Chao Y H, Kang J M. Study of CCCH-type zinc finger protein. Biotechnol Bull, 2010, (8):1-6 (in Chinese with English abstract).
[25] Synan A Q, Chen X, Rahul D, Burton B, John S, Stephen L, Robert A, Tesfaye M. Expression profiling and mutant analysis reveals complex regulatory networks involved in Arabidopsis response to Botrytis infection. Plant J, 2006,48:28-44.
pmid: 16925600
[26] Sun J Q, Jiang H L, Xu Y X, Li H M, Wu X Y, Xie Q, Li C Y. The CCCH-type zinc finger proteins AtSZF1 and AtSZF2 regulate salt stress responses in Arabidopsis. Plant Cell Physiol, 2007,48:1148-1158.
doi: 10.1093/pcp/pcm088 pmid: 17609218
[27] Yao L S, Li Y M, Ma C Y, Tong L X, Du F L, Xu M L. Combined genome-wide association study and rtanscriptome analysis reveal candidate genes for resistance to Fusarium ear rot in maize. J Integr Plant Biol, published online, doi: 10.1111/ jipb.12911
[1] Liang Jin-Yu, Yin Jia-De, Wang Hong-Li, Zhang Guo-Ping, Hou Hui-Zhi, Dong Bo, Ma Ming-Sheng. Estimation of leaf nitrogen content in dryland forage maize using UAV-based hyperspectral imaging and machine learning [J]. Acta Agronomica Sinica, 2026, 52(6): 1788-1801.
[2] Yang Yang, Chang Shi-Hui, Tian Hong-Li, Yi Hong-Mei, Wang Lu, Ren Jie, Fan Ya-Ming, Liu Ya-Wei, Wang Feng-Ge, Zhao Jiu-Ran. Genetic diversity analysis of nationally approved maize varieties in different ecological regions [J]. Acta Agronomica Sinica, 2026, 52(5): 1352-1364.
[3] Zhang Hong-Rong, Wang Fei-Er, Li Pan, Qiu Hai-Long, Zhu Jing, Zhao Lian-Hao, Nan Yun-You, He Wei, Fan Zhi-Long, Hu Fa-Long, Chai Qiang, Yin Wen. Photosynthetic characteristics of 20% reduced irrigation combined with 25% organic substitution for chemical fertilizer in increasing silage maize yield [J]. Acta Agronomica Sinica, 2026, 52(5): 1487-1500.
[4] Yang Xin-Yu, Cui Wen-Tao, Dilinigeer Alimu, Wang Kai-Xiang, Wu Peng-Hao, Ren Jiao-Jiao. Genome-wide association and genomic selection analysis of the number of leaves above the ear in maize [J]. Acta Agronomica Sinica, 2026, 52(5): 1573-1590.
[5] Han Ya-Xin, He Guan-Hua, Zhang Xiao-Qiong, Zhang Deng-Feng, Li Yong-Xiang, Liu Xu-Yang, Wang Tian-Yu, Li Yu, Zou Hua-Wen, Li Chun-Hui. Identification of maize lateral root density genes resources through integrated RNA-seq and BSA-seq analyses [J]. Acta Agronomica Sinica, 2026, 52(5): 1341-1352.
[6] Sun Shu-Feng, Xu Zhen-Nan, Huang Jia-Xin, Weng Jian-Feng, Li Xin-Hai. Genome-wide identification of the maize MAPK gene family and its response to Fusarium verticillioides infection [J]. Acta Agronomica Sinica, 2026, 52(5): 1291-1308.
[7] Zhang Ning-Ning, Teng Yu-Fei, Ren Na-Na, Wei Xing-Zhuo, Yan Shu-Hao, Fan Ke-Xin, Wang Yong-Hong, Chen Wen-Kang, Zhang Xing-Hua, Zhu Wan-Chao, Xu Shu-Tu, Xue Ji-Quan. Phenotypic evaluation and plasticity analysis of drought resistance in 201 maize inbred lines [J]. Acta Agronomica Sinica, 2026, 52(5): 1309-1325.
[8] Cai Hong-Wei, Yu Ai-Zhong, Jiang Ke-Qiang, Wang Peng-Fei, Wang Yu-Long, Huo Jian-Zhe, Pang Xiao-Neng, Yin Bo, Shang Yong-Pan. Key mechanisms underlying the enhancement of sweet maize yield through partial substitution of chemical fertilizers with organic manure in arid irrigation districts [J]. Acta Agronomica Sinica, 2026, 52(4): 1166-1180.
[9] Tian Hong-Li, Yang Yang, Fan Ya-Ming, Yi Hong-Mei, Guo Dan-Dan, Wang Feng-Ge, Zhao Jiu-Ran. A novel set of tri-allelic variant SNP loci suitable for maize variety identification [J]. Acta Agronomica Sinica, 2026, 52(4): 993-1005.
[10] Guo Xiang-Yang, Tu Liang, Wang Dong, Liu Peng-Fei, Wang An-Gui, Yi Qiang, Ren Hong, Li Gang, Zhu Yun-Fang, Wu Xun, Jiang Yu-Lin, Tian Feng, Chen Ze-Hui. Application and prospects of Suwan germplasm in maize breeding in China [J]. Acta Agronomica Sinica, 2026, 52(3): 655-664.
[11] Meng Cheng, Wang Zhe. Genome-wide identification and expression analysis of the ZmPFK gene family under biotic and abiotic stresses in maize [J]. Acta Agronomica Sinica, 2026, 52(3): 764-779.
[12] Li Xin-Hao, Xing Meng-Ke, Zhou Zi-Hui, Li Si-Ye, Ren Hao, Wang Hong-Zhang, Lai Hua-Jiang. Exogenous melatonin enhances heat tolerance of maize at the seedling stage by coordinating light and dark reactions [J]. Acta Agronomica Sinica, 2026, 52(3): 839-856.
[13] Ma Liang, Ma Lu, Zhang Shu-Yu, Zhang Hui-Min, Wang Ren-Ming, Song Xu-Dong, Zhang Zhen-Liang, Mao Yu-Xiang, Lu Hu-Hua, Chen Guo-Qing, Hao De-Rong, Zhou Guang-Fei. Transcriptome analysis and identification of candidate genes associated with husk number in maize [J]. Acta Agronomica Sinica, 2026, 52(3): 790-801.
[14] Liu Ji-Chang, Li Si-Ye, Li Xue-Ting, Wang Hong-Zhang, Liu Peng, Zhang Ji-Wang, Zhao Bin, Ren Bai-Zhao, Ren Hao. Effects of salt stress on root growth and nutrient absorption efficiency of different salt-tolerant summer maize varieties [J]. Acta Agronomica Sinica, 2026, 52(2): 565-577.
[15] Lin Zi-Qing, Zhong Xing-Yu, Liu Fan, Ren Zi-Ao, Ma Rui, Deng Xiu-Feng, Wang Dong-Wei, Liu Shao-Peng, Chen Kang, Zhang Ming-Cai, Li Zhao-Hu, Zhou Yu-Yi, Duan Liu-Sheng. Development of ultra-high-yield technology for a wheat-maize double cropping system achieving a 2-ton annual grain yield per mu in the coastal plain of Northern Shandong peninsula, China [J]. Acta Agronomica Sinica, 2026, 52(2): 631-643.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
No Suggested Reading articles found!