Welcome to Acta Agronomica Sinica,

Acta Agron Sin ›› 2016, Vol. 42 ›› Issue (08): 1122-1133.doi: 10.3724/SP.J.1006.2016.01122

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

Transcriptional Analysis of Maize Resistance against Fusarium graminearum

LIU Yong-Jie,MA Chuan-Yu,MA Xue-Na,XU Ming-Liang*   

  1. National Maize Improvement Center of China, China Agricultural University, Beijing 100193, China
  • Received:2016-01-11 Revised:2016-05-09 Online:2016-08-12 Published:2016-05-30
  • Contact: 徐明良, E-mail: mxu@cau.edu.cn, Tel: 010-62733166 E-mail:liu_yongj@126.com
  • Supported by:

    This study was supported by the Program of Introducing International Super Agricultural Science and Technology(948 Program) (2011-G15).

Abstract:

Gibberella stalk rot, caused by Fusarium graminearum (teleomorph, Gibberella zeae), is one of the most devastating soil-borne diseases in maize. It seriously decreases maize yield and quality. Molecular mapping  led to the identification of twoQTLs, qRfg1 and qRfg2, on chromosomes 10 and 1 respectively, conferring resistance to Gibberella stalk rot. In order to characterize the defense mechanism of maize against F. graminearum, NIL-R with resistant alleles at both QTLs and NIL-S with the susceptible alleles at both QTLs were generated and used in transcriptome analysis. After inoculation of young seedling roots of both NILs with the F. graminearum spores, the inoculated roots were sampled at 0, 6, and 18 hours after inoculation (hai) for transcriptome analysis using RNAseq. The basal difference was achieved by the comparison between control samples. In total, 2958 genes were differentially expressed between control samples of NIL-R and NIL-S, among which 1170 genes were more abundant in NIL-R. GO analysis revealed that genes involved in biological processes related to JA/ET and SA biosynthesis, JA/ET mediated signaling pathway and SA mediated signaling pathway were significantly enriched. Phenylpropanoid biosynthesis process was enriched in the genes more abundant in NIL-R and genes encoding enzymes involved in phenylpropanoid biosynthesis like PAL, 4CL2, CAD, and HCTwere more abundant in NIL-R. There were 431 genes differentially expressed between NIL-R and NIL-S at 6 hai, among which 83 genes were more abundant in NIL-R. Genes encoding pathogenesis-related (PR) proteins like lipid-transfer protein and germin-like proteinwere more abundant in NIL-R. Among the 1292 genes differentially expressed between NIL-R and NIL-S. At 18 hai, 291 genes were more abundant in NIL-R. Genes involved in ET biosynthesis like ACO and JA biosynthesis like LOX were more abundant in NIL-R. Genes involved in DON detoxification like PDR1 and MDR2 were more abundant in NIL-R. After inoculation with F. graminearum, 428 genes were exclusively up-regulated in NIL-R at 6 hai compared with control. Genes involved in ET biosynthesis and ET-mediated signaling pathway like ACO, ERF, EBF1, and EIL1 and pathogenesis-related genes like PR1, OSM34, and germin-like protein were exclusively up-regulated in NIL-R. At 18 hai, 359 genes were exclusively up-regulated in NIL-R compared with control. Pathogenesis-related genes like PR1, PR4, and genes encoding the transporters of DON out of cytoplasm likeABC transport family protein, heavy metal transport protein and MATE efflux family protein were exclusively up-regulated in NIL-R. All these results indicate that NIL-R can increase the resistance of maize to F. graminearum by the constitutive resistance characterized by the higher expression of genes related to defense responses. Genes involved in defense responses exclusively up-regulated in NIL-R and higher expression level of disease resistance genes in NIL-R at 6 and 18 hai may restrict the pathogen invasion after infection. The phenylpropanoid biosynthesis pathway and DON-detoxification proteins identified in this study are important for the resistance against F. graminearum infection.



 本研究由引进国际先进农业科学技术计划(948计划)项目(2003-Q04)资助。
This study was supported by the Program of Introducing International Super Agricultural Science and Technology(948 Program) (2011-G15).
* 通讯作者(Corresponding author): 徐明良, E-mail: mxu@cau.edu.cn, Tel: 010-62733166
第一作者联系方式: E-mail: liu_yongj@126.com
Received(收稿日期): 2016-01-11; Accepted(接受日期): 2016-05-09; Published online(网络出版日期):2016-05-30.
URL: http://www.cnki.net/kcms/detail/11.1809.S.20160530.0905.008.html

Key words: Maize, Stalk rot, Transcriptome, Resistance, JA/ET, Phenylpropanoid

[1] Yang Q, Yin G M, Guo Y L, Zhang D F, Chen S J, Xu M L. A major QTL for resistance to Gibberella stalk rot in maize. Theor Appl Genet, 2010, 121: 673–687
[2] Ali M L, Taylor J H, Jie L, Sun G L, William M, Kasha K J, Reid L M, Pauls K P. Molecular mapping of QTLs for resistance to Gibberella ear rot, in corn, caused by Fusarium graminearum. Genome, 2005, 48: 521–533
[3] Schweiger W, Steiner B, Ametz C, Siegwart G, Wiesenberger G, Berthiller F, Lemmens M, Jia H Y, Adam G, Muehlbauer G J. Transcriptomic characterization of two major Fusarium resistance quantitative trait loci (QTLs), Fhb1 and Qfhs. Ifa-5A, identifies novel candidate genes. Mol Plant Pathol, 2013, 14: 772–785
[4] Boddu J, Cho S, Kruger W M, Muehlbauer G J. Transcriptome analysis of the barley-Fusarium graminearum interaction. Mol Plant-Microbe Interact, 2006, 19: 407–417
[5] Goswami R S, Kistler H C. Pathogenicity and in planta mycotoxin accumulation among members of the Fusarium graminearum species complex on wheat and rice. Phytopathology, 2005, 95: 1397–1404
[6] Urban M, Daniels S, Mott E, Hammond-Kosack K. Arabidopsis is susceptible to the cereal ear blight fungal pathogens Fusarium graminearum and Fusarium culmorum. Plant J, 2002, 32: 961–973
[7] McMullen M, Jones R, Gallenberg D. Scab of wheat and barley: a re-emerging disease of devastating impact. Plant Dis, 1997, 81: 1340–1348
[8] Rocha O, Ansari K, Doohan F M. Effects of trichothecene mycotoxins on eukaryotic cells: a review. Food Addit Contam, 2005, 22: 369–378
[9] Pestka J J, Zhou H R, Moon Y, Chung Y J. Cellular and molecular mechanisms for immune modulation by deoxynivalenol and other trichothecenes: unraveling a paradox. Toxicol Lett, 2004, 153: 61–73
[10] Pestka J J. Deoxynivalenol-induced proinflammatory gene expression: Mechanisms and pathological sequelae. Toxins, 2010, 2: 1300–1317
[11] Miller J D, Ewen M A. Toxic effects of deoxynivalenol on ribosomes and tissues of the spring wheat cultivars Frontana and Casavant. Nat Toxins, 1997, 5: 234–237
[12] Desjardins A E, Proctor R H, Bai G H, McCormick S P, Shaner G, Buechley G, Hohn T M. Reduced virulence of trichothecene-nonproducing mutants of Gibberella zeae in wheat field tests. Mol Plant-Microbe Interact, 1996, 9: 775–781
[13] Langevin F, Eudes F, Comeau A. Effect of trichothecenes produced by Fusarium graminearum during Fusarium head blight development in six cereal species. Eur J Plant Pathol, 2004, 110: 735–746
[14] Harris L, Desjardins A E, Plattner R, Nicholson P, Butler G, Young J, Weston G, Proctor R, Hohn T. Possible role of trichothecene mycotoxins in virulence of Fusarium graminearum on maize. Plant Dis, 1999, 83: 954–960
[15] Desmond O J, Manners J M, Stephens A E, Maclean D J, Schenk P M, Gardiner D M, Munn A M, Kazan K. The Fusarium mycotoxin deoxynivalenol elicits hydrogen peroxide production, programmed cell death and defence responses in wheat. Mol Plant Pathol, 2008, 9: 435–445
[16] Jia H Y, Cho S, Muehlbauer G J. Transcriptome analysis of a wheat near-isogenic line pair carrying Fusarium head blight-resistant and-susceptible alleles. Mol Plant-Microbe Interact, 2009, 22: 1366–1378
[17] Poppenberger B, Berthiller F, Lucyshyn D, Sieberer T, Schuhmacher R, Krska R, Kuchler K, Glossl J, Luschnig C, Adam G. Detoxification of the Fusarium mycotoxin deoxynivalenol by a UDP-glucosyltransferase from Arabidopsis thaliana. J Biol Chem, 2003, 278: 47905–47914
[18] Muhitch M J, McCormick S P, Alexander N J, Hohn T M. Transgenic expression of the TRI101 or PDR5 gene increases resistance of tobacco to the phytotoxic effects of the trichothecene 4,15-diacetoxyscirpenol. Plant Sci, 2000, 157: 201–207
[19] Boddu J, Cho S, Muehlbauer G J. Transcriptome analysis of trichothecene-induced gene expression in barley. Mol Plant-Microbe Interact, 2007, 20: 1364–1375
[20] Gardiner S A, Boddu J, Berthiller F, Hametner C, Stupar R M, Adam G, Muehlbauer G J. Transcriptome analysis of the barley-deoxynivalenol interaction: evidence for a role of glutathione in deoxynivalenol detoxification. Mol Plant-Microbe Interact, 2010, 23: 962–976
[21] Schweiger W, Boddu J, Shin S, Poppenberger B, Berthiller F, Lemmens M, Muehlbauer G J, Adam G. Validation of a candidate deoxynivalenol-inactivating UDP-glucosyltransferase from barley by heterologous expression in yeast. Mol Plant-Microbe Interact, 2010, 23: 977–986
[22] Kruger W M, Pritsch C, Chao S, Muehlbauer G J. Functional and comparative bioinformatic analysis of expressed genes from wheat spikes infected with Fusarium graminearum. Mol Plant-Microbe Interact, 2002, 15: 445–455
[23] Zhu Q H, Stephen S, Kazan K, Jin G, Fan L, Taylor J, Dennis E S, Helliwell C A, Wang M B. Characterization of the defense transcriptome responsive to Fusarium oxysporum-infection in Arabidopsis using RNA-seq. Gene, 2013, 512: 259–266
[24] Lanubile A, Ferrarini A, Maschietto V, Delledonne M, Marocco A, Bellin D. Functional genomic analysis of constitutive and inducible defense responses to Fusarium verticillioides infection in maize genotypes with contrasting ear rot resistance. BMC Genomics, 2014, 15: 710
[25] Buerstmayr H, Steiner B, Lemmens M, Ruckenbauer P. Resistance to Fusarium head blight in winter wheat: heritability and trait associations. Crop Sci, 2000, 40: 1012–1018
[26] Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley D R, Pimentel H, Salzberg S L, Rinn J L, Pachter L. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protocols, 2012, 7: 562–578
[27] Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol, 2010, 11: R106
[28] Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 2005, 21: 3674–3676
[29] Ashburner M, Ball C A, Blake J A, Botstein D, Butler H, Cherry J M, Davis A P, Dolinski K, Dwight S S, Eppig J T. Gene Ontology: tool for the unification of biology. Nat Genet, 2000, 25: 25–29
[30] Gimenez-Ibanez S, Solano R. Nuclear jasmonate and salicylate signaling and crosstalk in defense against pathogens. Front Plant Sci, 2013, 4: 7
[31] Xiao J, Jin X H, Jia X P, Wang H Y, Cao A Z, Zhao W P, Pei H Y, Xue Z K, He L Q, Chen Q G, Wang X. Transcriptome-based discovery of pathways and genes related to resistance against Fusarium head blight in wheat landrace Wangshuibai. BMC Genomics, 2013, 14: 197
[32] Li G L, Yen Y. Jasmonate and ethylene signaling pathway may mediate Fusarium head blight resistance in wheat. Crop Sci, 2008, 48: 1888–1896
[33] Ding L N, Xu H B, Yi H Y, Yang L M, Kong Z X, Zhang L X, Xue S L, Jia H Y, Ma Z Q. Resistance to hemi-biotrophic F. graminearum infection is associated with coordinated and ordered expression of diverse defense signaling pathways. PloS One, 2011, 6: e19008
[34] Steiner B, Kurz H, Lemmens M, Buerstmayr H. Differential gene expression of related wheat lines with contrasting levels of head blight resistance after Fusarium graminearum inoculation. Theor Appl Genet, 2009, 118: 753–764
[35] Ye J R, Guo Y L, Zhang D F, Zhang N, Wang C, Xu M L. Cytological and molecular characterization of quantitative trait locus qRfg1, which confers resistance to Gibberella stalk rot in maize. Mol Plant-Microbe Interact, 2013, 26: 1417–1428
[36] Hamzehzarghani H, Kushalappa A C, Dion Y, Rioux S, Comeau A, Yaylayan V, Marshall W D, Mather D E. Metabolic profiling and factor analysis to discriminate quantitative resistance in wheat cultivars against Fusarium head blight. Physiol Mol Plant Pathol, 2005, 66: 119–133
[37] Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones J D, Felix G, Boller T. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature, 2007, 448: 497–500

 
[1] Mao Jia-Qi, Huang Peng-Yu, Zhao Jia-Jia, Zheng Xing-Wei, Wu Bang-Bang, Hao Yu-Qiong, Qu Fei, Liu Cheng, Ma Peng-Tao, Zheng Jun. Evaluation of powdery mildew resistance in wheat cultivars and molecular detection of resistance genes in Shanxi province, China [J]. Acta Agronomica Sinica, 2026, 52(6): 1669-1681.
[2] Chen Xue-Yan, He Hua-Chuan, Li Zheng-Jia, Dong Xin-Pan, Li Ou-Qi, Liu Xiao-Yun, Li Dan-Ping, Chen Zhi-Wei, Liu Guo-Xia, Lyu Sheng-Yuan, Wu Yin-Ying, Zhao Zhen-Dong, Cao Xin-You, Wan He-Ping. Dynamic changes in root organic acid secretion and its transcriptional regulatory mechanisms in ‘Jimai 60’ seedlings under combined salinity-alkalinity stress in hydroponics [J]. Acta Agronomica Sinica, 2026, 52(6): 1859-1875.
[3] 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.
[4] Zou Yi-Mei, Xu Min, Wang Hai-Yang, Yao Hui, Wang Jia-Feng, Liu Hao, Ren Dai-Sheng. Analysis of transcription factor regulatory networks in two-line male sterile rice seedling roots in response to salt stress [J]. Acta Agronomica Sinica, 2026, 52(6): 1728-1742.
[5] 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.
[6] 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.
[7] 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.
[8] Cai Zhao-Qin, He Guan-Yong, He Wen, Ruan Li-Xia, Liang Zhen-Hua, Li Yong-Zhen, Li Heng-Rui, Chen Hui-Xian. Dynamic transcriptome analysis and key gene discovery during cassava branching development [J]. Acta Agronomica Sinica, 2026, 52(5): 1430-1441.
[9] 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.
[10] 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.
[11] Zhang Xi, Wang Guang-En, Li Shao-Qi, Liu Yi, Li Jun-Lan, Qian Yu-Yuan. Transcriptome sequencing-based analysis on the formation mechanism of fiber micronaire differences between two sister lines derived from Gossypium hirsutum-G. barbadense hybrid [J]. Acta Agronomica Sinica, 2026, 52(5): 1442-1458.
[12] 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.
[13] 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.
[14] 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.
[15] Yu Yong-Chao, Liu Ming, Jin Rong, Zhao Peng, Zhang Qiang-Qiang, Wang Jing, Zhu Xiao-Ya, Tang Zhong-Hou. Physiological mechanism and transcriptome analysis of sweet potato overgrowth under high-nitrogen conditions [J]. Acta Agronomica Sinica, 2026, 52(3): 813-824.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
No Suggested Reading articles found!