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Journal of Integrative Agriculture  2024, Vol. 23 Issue (10): 3328-3342    DOI: 10.1016/j.jia.2023.07.022
Section 1: Cotton functional genomics Advanced Online Publication | Current Issue | Archive | Adv Search |
Cotton ethylene response factor GhERF91 is involved in the defense against Verticillium dahliae
Nurimanguli Aini1, Yuanlong Wu1, Zhenyuan Pan1, Yizan Ma2, Qiushuang An1, Guangling Shui1, Panxia Shao1, Dingyi Yang2, Hairong Lin1, Binghui Tang3, Xin Wei4, Chunyuan You2, 3, Longfu Zhu2#, Dawei Zhang4#, Zhongxu Lin2#, Xinhui Nie1#
1 Key Laboratory of Oasis Eco-agriculture, Xinjiang Production and Construction Group/Agricultural College, Shihezi University, Shihezi 832003, China
2 National Key Laboratory of Crop Genetic Improvement/College of Plant Sciences & Technology, Huazhong Agricultural University, Wuhan 430070, China
3 Cotton Research Institute, Shihezi Academy of Agricultural Science, Shihezi 832011, China
4 Institute of Economic Crops, Xinjiang Academy of Agricultural Sciences, Urumqi 830091, China
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摘要  

棉花黄萎病使棉花生产受到重大损失。为了揭示棉花响应黄萎病的防御机制,本研究利用棉花品系M138(抗黄萎病)和P2(感黄萎病)进行了转录组分析。结果显示,在M138和P2中分别有11076个和6640个差异表达基因响应黄萎病菌的侵染。利用加权基因共表达网络分析方法对4633个差异表达转录因子进行共表达分析发现,一个与黄萎病菌的抗性反应密切相关的“MEblue”模块,该模块包含654个转录因子。并在这些差异表达转录因子中,发现了参与黄萎病防御反应的关键基因乙烯转录因子GhERF91。进一步,通过病毒诱导的基因沉默实验和外源乙烯利处理分析发现,GhERF91受乙烯诱导表达,并正调控棉花对黄萎病菌的响应。本研究提供了棉花响应黄萎病侵染的转录组数据,同时鉴定了与黄萎病抗性相关的关键基因GhERF91,为选育抗黄萎病的棉花品种提供了的遗传资源。



Abstract  
Verticillium dahliae causes significant losses in cotton production.  To reveal the mechanism of the defense response to V. dahliae in cotton, transcriptomic analyses were performed using cotton cultivars M138 (V. dahliae-resistant) and P2 (V. dahliae-susceptible).  The results revealed 11,076 and 6,640 differentially expressed genes (DEGs) in response to V. dahliae, respectively.  The weighted gene co-expression network analysis of 4,633 transcription factors (TFs) indicated a “MEblue” module containing 654 TFs that strongly correlate with resistance to V. dahliae.  Among these TFs, the ethylene response factor Ghi_A05G10166 (GhERF91) was identified as a putative hub gene with a defense response against V. dahliae.  A virus-induced gene silencing assay and exogenous application of ethephon showed that GhERF91 is activated by ethylene and positively regulates the response to V. dahliae exposure in cotton.  This study provides fundamental transcriptome data and a putative causal gene (GhERF91) associated with resistance to V. dahliae, as well as genetic resources for breeding V. dahliae-resistant cotton.


Keywords:  cotton        Verticillium wilt        RNA-sequencing        GhERF91        virus-induced gene silencing  
Received: 10 April 2023   Accepted: 03 July 2023
Fund: 
This work was supported by the fund for National Key Research and Development Program of China (2023YFD2301203-05), the BTNYGG, China (NYHXGG, 2023AA102) and the Key Programs for Science and Technology Development of Shihezi City, Xinjiang Production and Construction Corps, China (2022NY01).
About author:  #Correspondence Longfu Zhu, Tel: +86-27-87283955, E-mail: lfzhu@mail.hzau.edu.cn; Dawei Zhang, Tel: +86-571-63370369, E-mail: zbzdw012@126.com; Zhongxu Lin, E-mail: linzhongxu@mail.hzau.edu.cn; Xinhui Nie, Tel: +86-993-2058970, E-mail: xjnxh2004130@126.com

Cite this article: 

Nurimanguli Aini, Yuanlong Wu, Zhenyuan Pan, Yizan Ma, Qiushuang An, Guangling Shui, Panxia Shao, Dingyi Yang, Hairong Lin, Binghui Tang, Xin Wei, Chunyuan You, Longfu Zhu, Dawei Zhang, Zhongxu Lin, Xinhui Nie. 2024. Cotton ethylene response factor GhERF91 is involved in the defense against Verticillium dahliae. Journal of Integrative Agriculture, 23(10): 3328-3342.

An J P, Zhang X W, Bi S Q, You C X, Wang X F, Hao Y J. 2020. The ERF transcription factor MdERF38 promotes drought stress-induced anthocyanin biosynthesis in apple. Plant Journal, 101, 573–589.

Arlotta C, Puglia G D, Genovese C, Toscano V, Karlova R, Beekwilder J, De Vos R C H, Raccuia S A. 2020. MYB5-like and bHLH influence flavonoid composition in pomegranate. Plant Science, 298, 110563.

Berrocal-Lobo M, Molina A, Solano R. 2002. Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. The Plant Journal, 29, 23–32.

Cai Y F, He X H, Mo J C, Sun Q, Yang J P, Liu J G. 2009. Molecular research and genetic engineering of resistance to Verticillium wilt in cotton: A review. African Journal of Biotechnology, 8, 7363–7372.

Chen W Q, Provart N J, Glazebrook J, Katagiri F, Chang H S, Eulgem T, Mauch F, Luan S, Zou G Z, Whitham S A, Budworth P R, Tao Y, Xie Z Y, Chen X, Lam S, Kreps J A, Harper J F, Si-Ammour A, Mauch-Mani B, Heinlein M, et al. 2002. Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell, 14, 559–574.

Cheng M C, Liao P M, Kuo W W, Lin T P. 2013. The Arabidopsis ETHYLENE RESPONSE FACTOR1 regulates abiotic stress-responsive gene expression by binding to different cis-acting elements in response to different stress signals. Plant Physiology, 162, 1566–1582.

Deokar A A, Kondawar V, Kohli D, Aslam M, Jain P K, Karuppayil S M, VarshneyR K, Srinivasan R. 2015. The CarERF genes in chickpea (Cicer arietinum L.) and the identification of CarERF116 as abiotic stress responsive transcription factor. Functional & Integrative Genomics, 15, 27–46.

Dubois M, Skirycz A, Claeys H, Maleux K, Dhondt S, Bodt S D, Bossche R V, Milde L D, Yoshizumi T, Inzé M. 2013. ETHYLENE RESPONSE FACTOR6 acts as a central regulator of leaf growth under water-limiting conditions in Arabidopsis. Plant Physiology, 162, 319–332.

Fischer U, Droge-Laser W. 2004. Overexpression of NtERF5, a new member of the tobacco ethylene response transcription factor family enhances resistance to Tobacco mosaic virus. Molecular Plant-Microbe Interactions, 17, 1162–1171.

Fradin E F, Thomma B. 2010. Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. alboatrum. Molecular Plant Pathology, 7, 71–86.

Galindo-Gonzalezi L, Deyholos M K. 2016. RNA-seq transcriptome response of flax (Linum usitatissimum L.) to the pathogenic fungus Fusarium oxysporum f. sp lini. Frontiers in Plant Science, 7, 1766.

Gao W, Long L, Zhu L F, Xu L, Gao W H, Sun L Q, Liu L L, Zhang X L. 2013. Proteomic and virus-induced gene silencing (VIGS) analyses reveal that gossypol, brassinosteroids, and jasmonic acid contribute to the resistance of cotton to Verticillium dahliae. Molecular & Cellular Proteomics, 12, 3690–3703.

Guo W F, Jin L, Miao Y H, He X, Hu Q, Guo K, Zhu L F, Zhang X L. 2016. An ethylene response-related factor, GbERF1-like, from Gossypium barbadense improves resistance to Verticillium dahliae via activating lignin synthesis. Plant Molecular Biology, 91, 305–318.

Hou Y J, Yu X Y, Chen W P, Wang S H, Cao L F, Geng X Y, Sun C, Qu. S C. 2021a. Transcriptome sequencing, data-based screening, and functional investigation of MdWRKY75d and MdWRKY75e in disease-resistant apples. Journal of Plant Interactions, 16, 462–473.

Hou Y J, Yu X Y, Chen W P, Zhuang W B, Wang S H, Sun C, Cao L F, Zhou T T, Qu S C. 2021b. MdWRKY75e enhances resistance to Alternaria alternata in Malus domestica. Horticulture Research, 8, 225.

Huang G, Wu Z G, Percy R G, Bai M Z, Li Y, Frelichowski J E, Hu J, Wang K, Yu J Z, Zhu Y X. 2020. Genome sequence of Gossypium herbaceum and genome updates of Gossypium arboreum and Gossypium hirsutum provide insights into cotton A-genome evolution. Nature Genetics, 52, 516–524.

Jiang J J, Ma S H, Ye H, Jiang M, Cao J S, Zhang J H. 2017. WRKY transcription factors in plant responses to stresses. Journal of Integrative Plant Biology, 59, 86–101.

Kang C Y, Darwish O, Geretz A, Shahan R, Alkharouf N, Liu Z C. 2013. Genome-scale transcriptomic insights into early-stage fruit development in woodland strawberry Fragaria vesca. Plant Cell, 25, 1960–1978.

Lai Y, Dang F F, Lin J, Yu L, Shi Y L, Xiao Y H, Huang M K, Lin J H, Chen C C, Qi A H, Liu Z Q, Guan D Y, Mou S L, Qiu A L, He S L. 2013. Overexpression of a Chinese cabbage BrERF11 transcription factor enhances disease resistance to Ralstonia solanacearum in tobacco. Plant Physiology and Biochemistry, 62, 70–78.

Langfelder P, Horvath S. 2008. WGCNA: An R package for weighted correlation network analysis. BMC Bioinformatics, 9, 559.

Li X, Kong X Q, Zhou J Y, Luo Z, Lu H Q, Li W J, Tang W, Zhang D M, Ma C L, Zhang H, Dong H Z. 2021. Seeding depth and seeding rate regulate apical hook formation by inducing GhHLS1 expression via ethylene during cotton emergence. Plant Physiology and Biochemistry, 164, 92–100.

Liang H X, Liu Y, Liu H X, Wang F D, Xin Z Y, Zhang Z Y. 2008. A novel activator-type ERF of Thinopyrum intermedium, TiERF1, positively regulates defence responses. Journal of Experimental Botany, 59, 3111–3120.

Licausi F, Giorgi F M, Zenoni S, Osti F, Pezzotti M, Perata P. 2010. Genomic and transcriptomic analysis of the AP2/ERF superfamily in Vitis vinifera. BMC Genomics, 11, 719.

Licausi F, Ohme-Takagi M, Perata P. 2013. APETALA2/Ethylene responsive factor (AP2/ERF) transcription factors: Mediators of stress responses and developmental programs. New Phytologist, 199, 639–649.

Liu J G, Wang Y Q, Zhao G Y, Zhao J L, Du H Y, He X L, Zhang H S. 2017. A novel Gossypium barbadense ERF transcription factor, GbERFb, regulation host response and resistance to Verticillium dahliae in tobacco. Physiology and Molecular Biology of Plants, 23, 125–134.

Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2–∆∆CT method. Methods, 25, 402–408.

Lorenzo O, Piqueras R, Sanchez-Serrano J J, Solano R. 2003. ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell, 15, 165–178.

Ma Z M, Wu T, Huang K, Jin Y M, Li Z, Chen M J, Yun S, Zhang H J, Yang X, Chen H Y, Bai H J, Du L, Ju S S, Guo L P, Bian M D, Hu L J, Du X L, Jiang W Z. 2020. A novel AP2/ERF transcription factor, OsRPH1, negatively regulates plant height in rice. Frontiers in Plant Science, 11, 709.

Meng X P, Li F G, Liu C L, Zhang C J, Wu Z X, Chen Y J. 2010. Isolation and characterization of an ERF transcription factor gene from cotton (Gossypium barbadense L.). Plant Molecular Biology Reporter, 28, 176–183.

Moffat C S, Ingle R A, Wathugala D L, Saunders N J, Heather K, Knight M R, Wu K. 2012. ERF5 and ERF6 play redundant roles as positive regulators of JA/Et-mediated defense against Botrytis cinerea in Arabidopsis. PLoS ONE, 7, e35995.

Otasek D, Morris J H, Boucas J, Pico A R, Demchak B. 2019. Cytoscape automation: Empowering workflow-based network analysis. Genome Biology, 20, 185.

Pantelides I S, Tjamos S E, Paplomatas E J. 2010. Ethylene perception via ETR1 is required in Arabidopsis infection by Verticillium dahliae. Molecular Plant Pathology, 11, 191–202.

Qiao Z X, Huang B, Liu J H. 2008. Molecular cloning and functional analysis of an ERF gene from cotton (Gossypium hirsutum). Biochimica Et Biophysica Acta-Gene Regulatory Mechanisms, 1779, 122–127.

Quan R D, Hu S J, Zhang Z L, Zhang H W, Zhang Z J, Huang R F. 2010. Overexpression of an ERF transcription factor TSRF1 improves rice drought tolerance. Plant Biotechnology Journal, 8, 476–488.

Sakuma Y, Liu Q, Dubouzet J G, Abe H, Shinozaki K, Yamaguchi-Shinozaki K. 2002. DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochemical & Biophysical Research Communications, 290, 998–1009.

Son G H, Wan J R, Kim J, Nguyen X C, Chung W S, Hong J C, Stacey G. 2012. Ethylene-responsive element-binding factor 5, ERF5, is involved in chitin-induced innate immunity response. Molecular Plant-Microbe Interactions, 25, 48–60.

Song R R, Li J P, Xie C J, Jian W, Yang X Y. 2020. An Overview of the molecular genetics of plant resistance to the Verticillium wilt pathogen Verticillium dahliae. International Journal of Molecular Sciences, 21, 1120.

Song C P, Agarwal M, Ohta M, Guo Y, Halfter U, Zhu W. 2005. Role of an arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses. Plant Cell, 17, 2384–2396.

Tian X M, Han P, Wang J, Shao P X, An Q S, Aini N, Yang Q Y, You C Y, Lin H R, Zhu L F, Pan Z Y, Nie X. 2022. Association mapping of lignin response to Verticillium wilt through eight-way MAGIC population in upland cotton. Journal of Integrative Agriculture, 22, 1324–1337.

Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley D R, Pimentel H, Salzberg S L, Rinn J L, Pachter L. 2012. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nature Protocols, 7, 562–578.

Tu L L, Zhang X L, Liu D Q, Jin S X, Cao J L, Zhu F, Deng F L, Tan J F, Zhang C B. 2007. Suitable internal control genes for qRT-PCR normalization in cotton fiber development and somatic embryogenesis. Chinese Science Bulletin, 52, 3110–3117.

Wang F X, Ma Y P, Yang C L, Zhao P M, Yao Y, Jian G L, Luo Y M, Xia G X. 2011. Proteomic analysis of the sea-island cotton roots infected by wilt pathogen Verticillium dahliae. Proteomics, 11, 4296–4309.

Xiao S H, Hu Q, Zhang X J, Si H, Liu S M, Chen L, Chen K S, Berne S, Yuan D J, Lindsey K, Zhang X L, Zhu L F. 2021. Orchestration of plant development and defense by indirect crosstalk of salicylic acid and brassinosteorid signaling via transcription factor GhTINY2. Journal of Experimental Botany, 72, 4721–4743.

Xie Z L, Nolan T M, Jiang H, Yin Y H. 2019. AP2/ERF transcription factor regulatory networks in hormone and abiotic stress responses in Arabidopsis. Frontiers in Plant Science, 10, 228.

Xiong X P, Sun S C, Li Y J, Zhang X Y, Sun J, Xue F. 2019. The cotton WRKY transcription factor GhWRKY70 negatively regulates the defense response against Verticillium dahliae. Crop Journal, 7, 393–402.

Xiong X P, Sun S C, Zhang X Y, Li Y J, Liu F, Zhu Q H, Xue F, Sun J. 2020. GhWRKY70D13 regulates resistance to Verticillium dahliae in cotton through the ethylene and jasmonic acid signaling pathways. Frontiers in Plant Science, 11, 69.

Xu J, Wang X, Li Y, Zeng J, Wang G, Deng C, Guo W. 2018. Host-induced gene silencing of a regulator of G protein signalling gene (VdRGS1) confers resistance to Verticillium wilt in cotton. Plant Biotechnology Journal, 16, 1629–1643.

Yang C L, Liang S, Wang H Y, Han L B, Wang F X, Cheng H Q, Wu X M, Qu Z L, Wu J H, Xia G X. 2015. Cotton major latex protein 28 functions as a positive regulator of the ethylene responsive factor 6 in defense against Verticillium dahliae. Molecular Plant, 8, 399–411.

Yang Z, Tian L, Latoszek-Green M, Brown D, Wu K. 2005. Arabidopsis ERF4 is a transcriptional repressor capable of modulating ethylene and abscisic acid responses. Plant Molecular Biology, 58, 585–596.

Yang Z R, Qanmber G, Wang Z, Yang Z E, Li F G. 2020. Gossypium genomics: Trends, scope, and utilization for cotton improvement. Trends in Plant Science, 25, 488–500.

Yu G C, Wang L G, Han Y Y, He Q Y. 2012. clusterProfiler: An R package for comparing biological themes among gene clusters. Omics-A Journal of Integrative Biology, 16, 284–287.

Zhao L, Chang X, Qi D Y, Dong L D, Wang G J, Fan S J, Jiang L Y, Cheng Q, Chen X, Han D, Xu P F, Zhang S Z. 2017. A novel soybean ERF transcription factor, GmERF113, increases resistance to Phytophthora sojae infection in soybean. Frontiers in Plant Science, 8, 299.

Zhou B, Zhang L, Ullah A, Jin X, Yang X Y, Zhang X L 2016. Identification of multiple stress responsive genes by sequencing a normalized cDNA library from sea-land cotton (Gossypium barbadense L.). PLoS ONE, 11, e0152927.

Zhu Z G, Shi J L, Xu W R, Li H E, He M Y, Xu Y, Xu T F, Yang Y Z, Cao J L, Wang Y J. 2013. Three ERF transcription factors from Chinese wild grapevine Vitis pseudoreticulata participate in different biotic and abiotic stress-responsive pathways. Journal of Plant Physiology, 170, 923–933.

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