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Journal of Integrative Agriculture
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Eureka lemon zinc finger protein ClDOF3.4 interacts with citrus yellow vein clearing virus coat protein to inhibit viral infection
Ping Liao1, 2, Ting Zeng1, 2, Mengyang Huangfu1, 2, Cairong Zheng1, 2, Jiequn Ren3,  Changyong Zhou1, 2, Yan Zhou1, 2

1 Integrative Science Center of Germplasm Creation in Western China (CHONGQING) Science City, Chongqing 401329, China

2 National Citrus Engineering Research Center, Citrus Research Institute, Southwest University, Chongqing 400712, China

3 Chongqing Three Gorges Academy of Agricultural Science, Chongqing Three Gorges University, Chongqing 404020, China

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摘要  柑橘黄化脉明病毒(citrus yellow vein clearing virusCYVCV)是一种新型柑橘病毒,该病毒已对印度、伊朗、土耳其、中国、美国和韩国的柠檬、酸橙和部分宽皮等柑橘品种的种植生产造成了严重的损失。CYVCV外壳蛋白(CP)具有RNA沉默抑制子活性,与病毒致病性和症状密切相关。DOFDNA-binding with one finger)是高等植物特有的锌指蛋白,在植物生长发育和抗病原物侵染的过程中扮演着重要作用。然而,目前尚未开展尤力克柠檬锌指蛋白ClDOFCYVCV的互作研究。因此,本研究通过一系列体内和体外互作验证实验,以及基因瞬时表达、基因瞬时沉默和尤力克柠檬遗传转化等手段,验证了ClDOF3.4CYVCV CP之间的互作关系及其对尤力克柠檬响应CYVCV免疫应答的影响。试验结果表明,ClDOF3.4蛋白在体内和体外均与CP存在相互作用关系,且ClDOF3.4蛋白N端的104-280个氨基酸序列是与CP相互作用的关键区段。在尤力克柠檬叶片中瞬时表达ClDOF3.4可以诱导水杨酸通路相关基因和超敏反应标记基因的上调表达,造成接种部位活性氧爆发和离子渗透坏死、并引起H2O2和水杨酸积累;而ClDOF3.4基因瞬时沉默尤力克柠檬叶片中的水杨酸和超敏反应相关基因下调表达。此外,该研究进一步通过农杆菌接种分别在瞬时表达及沉默ClDOF3.4基因的尤力克柠檬叶片中瞬时表达CP,结果表明ClDOF3.4负向调控CP在尤力克柠檬中的表达和积累。接种CYVCV六个月后,ClDOF3.4转基因尤力克柠檬植株的CYVCV含量约为对照植株的69.4%,与对照植株相比,转基因植株感病后的症状明显减轻,仅出现轻度的叶片斑驳症状。上述研究表明,ClDOF3.4不仅与CYVCV-CP存在相互作用,还可以通过水杨酸信号通路诱导尤力克柠檬对CYVCV的免疫应答。这是首次关于锌指蛋白参与柑橘抗病毒病的报道,该研究结果为进一步研究柑橘抗CYVCV的分子机制奠定了基础。

Abstract  Citrus yellow vein clearing virus (CYVCV) is a new citrus virus that has become an important factor restricting the development of China’s citrus industry, and the CYVCV coat protein (CP) is associated with viral pathogenicity. In this study, the Eureka lemon zinc finger protein (ZFP) ClDOF3.4 was shown to interact with CYVCV CP in vivo and in vitro. Transient expression of ClDOF3.4 in Eureka lemon induced the expression of salicylic acid (SA)-related and hypersensitive response marker genes, and triggered a reactive oxygen species burst, ion leakage necrosis, and the accumulation of free SA. Furthermore, the CYVCV titer in ClDOF3.4 transgenic Eureka lemon plants was approximately 69.4% that in control plants 6 months after inoculation, with only mild leaf chlorotic spots observed in those transgenic plants. Taken together, the results indicate that ClDOF3.4 not only interacts with CP but also induces an immune response in Eureka lemon by inducing the SA pathways. This is the first report that ZFP is involved in the immune response of a citrus viral disease, which provides a basis for further study of the molecular mechanism of CYVCV infection.
Keywords:  citrus yellow vein clearing virus       coat protein              ClDOF3.4              plant immune response  
Online: 15 April 2024  
About author:  Ping Liao, E-mail: liaoping940324@163.com; Correspondence Yan Zhou, E-mail: zhouyan@cric.cn

Cite this article: 

Ping Liao, Ting Zeng, Mengyang Huangfu, Cairong Zheng, Jiequn Ren, Changyong Zhou, Yan Zhou. 2024. Eureka lemon zinc finger protein ClDOF3.4 interacts with citrus yellow vein clearing virus coat protein to inhibit viral infection. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2024.03.049

Afloukou F, Önelge N. 2021. Occurrence and molecular characterisation of citrus yellow vein clearing virus isolates in Adana province, Turkey. Physiological and Molecular Plant Pathology, 115, 101655.

Baxter A, Mittler R, Suzuki N. 2014. ROS as key players in plant stress signalling. Journal of Experimental Botany, 65, 1229-1240.

Bhattacharjee S. 2005. Reactive oxygen species and oxidative burst: Roles in stress, senescence and signal transduction in plants. Current Science, 89, 1113-1121.

Bin Y, Zhang Q, Su Y, Wang C Q, Jiang Q Q, Song Z, Zhou C Y. 2023. Transcriptome analysis of Citrus limon infected with citrus yellow vein clearing virus. BMC Genomics, 24, 65.

Bisht A, Eekhout T, Canher B, Lu R, Vercauteren I, De Jaeger G, Heyman J, De Veylder L. 2023. PAT1-type GRAS-domain proteins control regeneration by activating DOF3.4 to drive cell proliferation in Arabidopsis roots. The Plant Cell, 35, 1513-1531.

Burckhardt C J, Minna J D, Danuser G. 2021. Co-immunoprecipitation and semi-quantitative immunoblotting for the analysis of protein-protein interactions. STAR Protocols, 2, 100644.

Catara A, Azzaro A, Davino M, Polizzi G. 1993. Yellow vein clearing of lemon in Pakistan. Proc. 12th Conf. IOCV. IOCV, Riverside, CA, 364-367.

Chen H M, Zhou Y, Wang X F, Zhou C Y, Yang X Y, Li Z A. 2016. Detection of citrus yellow vein clearing virus based on a real-time RT-PCR approach. Acta Horticulturae Sinica, 43, 168-174.

Cheung M Y, Zeng N Y, Tong S W, Li F W Y, Zhao K J, Zhang Q, Sun S S M, Lam H M. 2007. Expression of a RING-HC protein from rice improves resistance to Pseudomonas syringae pv. tomato DC3000 in transgenic Arabidopsis thaliana. Journal of Experimental Botany, 58, 4147-4159.

Clamp M, Cuff J, Searle S M, Barton G J. 2004. The Jalview Java alignment editor. Bioinformatics, 20, 426-427.

Curin M, Ojangu E L, Trutnyeva K, Ilau B, Truve E, Waigmann E. 2007. MPB2C, a microtubule-associated plant factor, is required for microtubular accumulation of tobacco mosaic virus movement protein in plants. Plant Physiology, 143, 801-811.

Du J, Wang Q Y, Zeng C H, Zhou C Y, Wang X F. 2022. A prophage-encoded nonclassical secretory protein of "Candidatus Liberibacter asiaticus" induces a strong immune response in Nicotiana benthamiana and citrus. Molecular Plant Pathology, 23, 1022-1034.

Du X X, Huang Y Y, Ma C Q, Li H Y. 2021. Transcription factor BvM14-Dof 3.4 in response to salt stress: Functional study. Chinese Agricultural Science Bulletin, 37, 119-125. (in Chinese)

Hamdi J, Kmeli N, Bouktila D. 2021. Genome-wide survey of sugar beet (Beta vulgaris subsp. vulgaris) DOF transcription factors reveals structural diversity, evolutionary expansion and involvement in taproot development and biotic stress response. Biologia, 76, 2421-2436.

Hashmian S M B, Aghajanzadeh S. 2017. Occurrence of citrus yellow vein clearing virus in citrus species in Iran. Journal of Plant Pathology, 99, 290.

Hong X F, Qi F, Wang R, Jia Z Y, Lin F C, Yuan M H, Xin X F, Liang Y. 2023. Ascorbate peroxidase 1 allows monitoring of cytosolic accumulation of effector-triggered reactive oxygen species using a luminol-based assay. Plant Physiology, 191, 1416-1434.

Kang S H, Qu F, Morris T J. 2015. A nuclear fraction of turnip crinkle virus capsid protein is important for elicitation of the host resistance response. Virus Research, 210, 264-270.

Kumar D, Haq I, Chapagai D, Tripathi D, Donald D, Hossain, M, Devaiah S. 2015. Hormone signaling: Current perspectives on the roles of salicylic acid and its derivatives in plants. The Formation, Structure and Activity of Phytochemicals, Recent Advances in Phytochemistry, 45, 115-136.

Li J H, Yang Y Q, Sun K, Chen Y, Chen X, Li X H. 2019. Exogenous melatonin enhances cold, salt and drought stress tolerance by improving antioxidant defense in tea plant (Camellia sinensis (L.) O. Kuntze). Molecules, 24, 1826.

Li P B, Guo L M, Lang X Y, Li M J, Wu G T, Wu R, Wang L X, Zhao M S, Qing L. 2022. Geminivirus C4 proteins inhibit GA signaling via prevention of NbGAI degradation, to promote viral infection and symptom development in N. benthamiana. Plos Pathogens, 18, e1010217.

Li X T, Su H N, Tan K Z, Tong X N, Zhong B L. 2017. Fruit malformation of Satsuma mandarin (Citrus unshiu Marc.) infected by citrus yellow vein clearing virus. Journal of Phytopathology, 165, 283-288.

Liu C H, Liu H, Hurst J, Timko M P, Zhou C Y. 2020 a. Recent advances on citrus yellow vein clearing virus in citrus. Horticultural Plant Journal, 6, 216-222.

Liu C X, Atanasov K E, Arafaty N, Murillo E, Tiburcio A F, Zeier J, Alcázar R. 2020 b. Putrescine elicits ROS-dependent activation of the salicylic acid pathway in Arabidopsis thaliana. Plant Cell and Environment, 43, 2755-2768.

Liu H M, Xiao S Q, Sui S Z, Huang R W, Wang X, Wu H F, Liu X. 2022. A tandem CCCH type zinc finger protein gene CpC3G3 from Chimonanthus praecox promotes flowering and enhances drought tolerance in Arabidopsis. BMC Plant Biology, 22, 506.

Liu X L, Fan Y Y, Zhang C, Dai M X, Wang X F, Li W M. 2019. Nuclear import of a secreted "Candidatus Liberibacter asiaticus" protein is temperature dependent and contributes to pathogenicity in Nicotiana benthamiana. Frontiers in Microbiology, 10, 1684.

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

Loconsole G, Onelge N, Potere O, Giampetruzzi A, Bozan O, Satar S, De Stradis A, Savino V, Yokomi R K, Saponari M. 2012. Identification and characterization of citrus yellow vein clearing virus, a putative new member of the genus Mandarivirus. Phytopathology, 102, 1168-1175.

Lu P P, Yu T F, Zheng W J, Chen M, Zhou Y B, Chen J, Ma Y Z, Xi Y J, Xu Z S. 2018. The wheat BAX inhibitor-1 protein interacts with an aquaporin TaPIP1 and enhances disease resistance in Arabidopsis. Frontiers in Plant Science, 9, 20.

Luo Q, Liu R X, Zeng L G, Wu Y Y, Jiang Y, Yang Q, Nie Q. 2020. Isolation and molecular characterization of NtMYB4a, a putative transcription activation factor involved in anthocyanin synthesis in tobacco. Gene, 760, 144990.

Ma C Q, Huang Y Y, Li H Y. 2020. BvM14-Dof3.4 gene in sugar beet M14 line: Cloning and expression in response to salt stress. Chinese Agricultural Science Bulletin, 36, 36-41. (in Chinese)

Marash I, Leibman-Markus M, Gupta R, Avni A, Bar M. 2022. Tor inhibition primes immunity and pathogen resistance in tomato in a salicylic acid-dependent manner. Molecular Plant Pathology, 23, 1035-1047.

Newman L, Duffus A L J, Lee C. 2016. Using the free program MEGA to build phylogenetic trees from molecular data. The American Biology Teacher: Journal of the National Association of Biology Teachers, 78, 608-612.

Noguero M, Atif R M, Ochatt S, Thompson R D. 2013. The role of the DNA-binding one finger (DOF) transcription factor family in plants. Plant Science, 209, 32-45.

Noman A, Liu Z Q, Yang S, Shen L, Hussain A, Ashraf M F, Khan M I, He S L. 2018. Expression and functional evaluation of CaZNF830 during pepper response to Ralstonia solanacearum or high temperature and humidity. Microbial Pathogenesis, 118, 336-346.

Pitino M, Armstrong C M, Cano L M, Duan Y P. 2016. Transient expression of Candidatus Liberibacter asiaticus effector induces cell death in Nicotiana benthamiana. Frontiers in Plant Science, 7, 982.

Rehman A U, Li Z R, Yang Z K, Waqas M, Wang G P, Xu W X, Li F, Hong N. 2019. The coat protein of citrus yellow vein clearing virus interacts with viral movement proteins and serves as an RNA silencing suppressor. Viruses, 11, 329.

Santos L A, de Souza S R, Fernandes M S. 2012. OsDof25 expression alters carbon and nitrogen metabolism in Arabidopsis under high N-supply. Plant Biotechnology Reports, 6, 327-337.

Sasaki N, Matsumaru M, Odaira S, Nakata A, Nakata K, Nakayama I, Yamaguchi K, Nyunoya H. 2015. Transient expression of tobacco BBF1-related DOF proteins, BBF2 and BBF3, upregulates genes involved in virus resistance and pathogen defense. Physiological and Molecular Plant Pathology, 89, 70-77.

Senthil-Kumar M, Mysore K S. 2014. Tobacco rattle virus-based virus-induced gene silencing in Nicotiana benthamiana. Nature Protocols, 9, 1549-1562.

Shen P, Li X Y, Fu S M, Zhou C Y, Wang X F. 2022. A "Candidatus Liberibacter asiaticus"-secreted polypeptide suppresses plant immune responses in Nicotiana benthamiana and Citrus sinensis. Frontiers in Plant Science, 13, 997825.

Song Z, Kurth E G, Peremyslov V V, Zhou C Y, Dolja V V. 2015. Molecular characterization of a citrus yellow vein clearing virus strain from China. Archives of Virology, 160, 1811-1813.

Sun D Y, Zhang X G, Li S H, Jiang C Z, Zhang Y L, Niu L X. 2016. LrABCF1, a GCN-type ATP-binding cassette transporter from Lilium regale, is involved in defense responses against viral and fungal pathogens. Planta, 244, 1185-199.

Sun Y D, Folimonova S Y. 2019. The p33 protein of citrus tristeza virus affects viral pathogenicity by modulating a host immune response. New Phytologist, 221, 2039-2053.

Sun Y D, Yokomi R. 2023. Whole genome sequence of citrus yellow vein clearing virus CA1 isolate. BMC Research Notes, 16, 166.

Tian Y, Hao Z L, Zhu J Y, Yang J C, Shi L, Li Z, Chang Y Q. 2019. The complete mitochondrial genome of Boreotrophon candelabrum (Reeve, 1848). Mitochondrial DNA Part B-resources, 4, 1142-1143.

Tilsner J, Kriechbaumer V. 2022. Reticulons 3 and 6 interact with viral movement proteins. Molecular Plant Pathology, 23, 1807-1714.

Umemura Y, Ishiduka T, Yamamoto R, Esaka M. 2004. The DOF domain, a zinc finger DNA-binding domain conserved only in higher plants, truly functions as a Cys2/Cys2 Zn finger domain. Plant Journal, 37, 741-749.

Walter M, Chaban C, Schütze K, Batistic O, Weckermann K, Näke C, Blazevic D, Grefen C, Schumacher K, Oecking C, Harter K, Kudla J. 2004. Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant Journal, 40, 428-438.

Wang C H, Wang X Q, Li J X, Guan J H, Tan Z J, Zhang Z, Shi G R. 2022 b. Genome-wide identification and transcript analysis reveal potential roles of oligopeptide transporter genes in iron deficiency induced cadmium accumulation in peanut. Frontiers in Plant Science, 13, 894848.

Wang F S, Xu Y Y, Liu X N, Shen W X, Zhu S P, Zhao X C. 2019 a. Use of TRV-mediated VIGS for functional genomics research in citrus. Plant Cell, Tissue and Organ Culture, 139, 609-613.

Wang S, Han K L, Peng J J, Zhao J P, Jiang L L, Lu Y W, Zheng H Y, Lin L, Chen J P, Yan F. 2019 b. NbALD1 mediates resistance to turnip mosaic virus by regulating the accumulation of salicylic acid and the ethylene pathway in Nicotiana benthamiana. Molecular Plant Pathology, 20, 990-1004.

Wang Y, Liao P, Zhao J F, Zhang X K, Liu C, Xiao P A, Zhou C Y, Zhou Y. 2022 a. Comparative transcriptome analysis of the Eureka lemon in response to citrus yellow vein virus infection at different temperatures. Physiological and Molecular Plant Pathology, 119, 101832.

Wen C L, Cheng Q, Zhao L Q, Mao A J, Yang J J, Yu S C, Weng Y Q, Xu Y. 2016. Identification and characterisation of DOF transcription factors in the cucumber genome. Scientific Reports, 6, 23072.

Xu G J, Zhong X H, Shi Y L, Liu Z, Jiang N, Liu J, Ding B, Li Z Q, Kang H X, Ning Y S, Liu W D, Guo Z J, Wang G L, Wang X L. 2020. A fungal effector targets a heat shock-dynamin protein complex to modulate mitochondrial dynamics and reduce plant immunity. Science Advances, 6, eabb7719.

Yanagisawa S, Izui K. 1993. Molecular cloning of two DNA-binding proteins of maize that are structurally different but interact with the same sequence motif. Journal Biological Chemistry, 268, 16028-16036.

Yang M Z, Derbyshire M K, Yamashita R A, Marchler-Bauer A. 2020. NCBI's conserved domain database and tools for protein domain analysis. Current Protocols in Bioinformatics, 69, e90.

Yang T, Zhu L S, Meng Y, Lv R, Zhou Z, Zhu L, Lin H H, Xi D H. 2018. Alpha-momorcharin enhances tobacco mosaic virus resistance in tobaccoNN by manipulating jasmonic acid-salicylic acid crosstalk. Journal of Plant Physiology, 223, 116-126.

Yoshioka H, Adachi H, Nakano T, Miyagawa N, Asai S, Ishihama N, Yoshika M. 2016. Hierarchical regulation of NADPH oxidase by protein kinases in plant immunity. Physiological and Molecular Plant Pathology, 95, 20-26.

Yu Y H, Bian L, Wan Y T, Jiao Z L, Yu K K, Zhang G H, Guo D L. 2019. Grape (Vitis vinifera) VvDOF3 functions as a transcription activator and enhances powdery mildew resistance. Plant Physiology and Biochemistry, 143, 183-189.

Yuan W, Jiang T, Du K T, Chen H, Cao Y Y, Xie J P, Li M F, Carr J P, Wu B M, Fan Z F, Zhou T. 2019. Maize phenylalanine ammonia‐lyases contribute to resistance to sugarcane mosaic virus infection, most likely through positive regulation of salicylic acid accumulation. Molecular Plant Pathology, 20, 1365-1378.

Zhao C N, Liu X J, Gong Q, Cao J P, Shen W X, Yin X R, Grierson D, Zhang B, Xu C J, Li X, Chen K S, Sun C D. 2021. Three AP2/ERF family members modulate flavonoid synthesis by regulating type IV chalcone isomerase in citrus. Plant Biotechnology Journal, 19, 671-688.

Zhao L F, Su P S, Hou B Q, Wu H Y, Fan Y H, Li W, Zhao J X, Ge W Y, Xu S S, Wu S W, Ma X, Li A F, Bai G H, Wang H W, Kong L R. 2022. The black necrotic lesion enhanced Fusarium graminearum resistance in wheat. Frontiers in Plant Science, 13, 926621.

Zhao T T, Zhang Y H, Wang F M, Zhang B, Chen Q, Liu L P, Yan L, Yang Y, Meng Q M, Huang J A, Zhang M C, Lin J, Qin J. 2023. Transcriptome mapping related genes encoding PR1 protein involved in necrotic symptoms to soybean mosaic virus infection. Molecular Breeding, 43, 7.

Zhang C, Wang D, Li W M, Zhang B L, Ouf G M A F, Su X F, Li J. 2022. The coat protein p25 from maize chlorotic mottle virus involved in symptom development and systemic movement of tobacco mosaic virus hybrids. Frontiers in Microbiology13, 951479.

Zhang K, Wang Y, Sun W M, Han K M, Yang M, Si Z Z, Li G L, Qiao Y K. 2019 c. Effects of exogenous salicylic acid on the resistance response of wild soybean plants (Glycine soja) infected with soybean mosaic virus. Canadian Journal of Plant Pathology, 42, 84-93.

Zhang Y H, Liu C H, Wang Q, Wang Y L, Zhou C Y, Zhou Y. 2019 a. Identification of Dialeurodes citri as a vector of citrus yellow vein clearing virus in China. Plant Disease, 103, 65-68.

Zhang Y H, Liu Y J, Wang Y L, Wang Q, He S G, Li X Y, Zhou Y. 2019 b. Transmissibility of citrus yellow vein clearing virus by contaminated tools. Journal of Plant Pathology, 101, 169-171.

Zhang Y H, Wang Y L, Wang Q, Cao M J, Zhou C Y, Zhou Y. 2018. Identification of Aphis spiraecola as a vector of citrus yellow vein clearing virus. European Journal of Plant Pathology, 152, 841-844.

Zhang Y J, Zhang X F, Niu S F, Han C G, Yu J L, Li D W. 2011. Nuclear localization of beet black scorch virus capsid protein and its interaction with importin α. Virus Research, 155, 307-315.

Zhou M L, Zhang K X, Sun Z M, Yan M L, Chen C, Zhang X Q, Tang Y X, Wu Y M. 2017 b. LNK1 and LNK2 co-repressors interact with the MYB3 transcription factor in phenylpropanoid biosynthesis. Plant Physiology, 174, 1348-1358.

Zhou Y, Chen H M, Cao M J, Wang X F, Jin X, Liu K H, Zhou C Y. 2017 a. Occurrence, distribution and molecular characterization of citrus yellow vein clearing virus in China. Plant Disease, 101, 137-143.

Zhou Y, Ma D D, Chen H M, Wang X F, He S G, Zhou C Y. 2016. A rapid and efficient purification of citrus yellow vein clearing virus by sucrose cushion ultracentrifugation. Journal of Plant Pathology, 98, 159-161.

Zhou Z Y, Bi G Z, Zhou J M. 2018. Luciferase complementation assay for protein-protein interactions in plants. Current Protocols in Plant Biology, 3, 42-50.

Zou X M, Sun H M. 2023. DOF transcription factors: Specific regulators of plant biological processes. Frontiers in Plant Science, 14, 1044918.

Zou X P, Jiang X Y, Xu L Z, Lei T G, Peng A H, He Y R, Yao L X, Chen S C. 2017. Transgenic citrus expressing synthesized cecropin B genes in the phloem exhibits decreased susceptibility to Huanglongbing. Plant Molecular Biology, 93, 341-353.

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