柑橘黄龙病对果实症状与品质的影响及分子机制研究进展

doi:10.16420/j.issn.0513-353x.2024-0296

摘要/Abstract

摘要：

柑橘黄龙病（Citrus Huanglongbing，HLB）是由韧皮部限制性病原菌‘Candidatus Liberibacter asiaticus’（CLas）引起的毁灭性病害，通过柑橘木虱（Diaphorina citri）传播，导致果实发育停滞、畸形及典型“红鼻子”果症状。由于CLas侵染显著干扰果实糖酸代谢、挥发性物质合成及次生代谢通路，造成可溶性固形物下降、柠檬苦素积累，并诱发特征性风味劣变。近年研究表明，CLas效应蛋白（如SDE1、SDE3）通过靶向宿主免疫相关蛋白酶及自噬通路，协同调控细胞程序性死亡与活性氧稳态，进而介导果实表型异常。本文中系统综述了CLas诱导的果实症状—品质—分子机制三联调控网络，并探讨多组学技术驱动下的致病机制解析策略，为柑橘黄龙病抗病育种与绿色防控提供理论依据。

关键词: 柑橘黄龙病, 果实, 症状, 品质, 病菌分布, 分子机制

Abstract:

Citrus Huanglongbing（HLB），caused by the phloem-restricted bacterium‘Candidatus Liberibacter asiaticus’（CLas） and transmitted by the Asian citrus psyllid（Diaphorina citri），leads to severe fruit developmental defects including asymmetrical shaping，abnormal coloration（“red nose”symptom），and drastic quality deterioration. CLas infection disrupts sugar-acid metabolism，volatile compound biosynthesis，and secondary metabolic pathways，resulting in accumulation of limonoids and characteristic flavor loss. Recent advances reveal that CLas-secreted effector proteins（e.g.，SDE1，SDE3）manipulate host immune proteases and autophagy pathways to coordinately regulate programmed cell death and ROS homeostasis，thereby driving fruit symptomatology. This review synthesizes the tripartite regulatory network linking fruit phenotype，quality traits，and molecular mechanisms under HLB pathogenesis，highlighting multi-omics approaches as pivotal tools for deciphering CLas virulence strategies，which may inform future resistant cultivar development and sustainable management practices.

Key words: citrus Huanglongbing, fruit, symptom, quality, distribution of CLas, mechanism

方芳, 陈晓虹, 王成, 郑正, 邓晓玲. 柑橘黄龙病对果实症状与品质的影响及分子机制研究进展[J]. 园艺学报, 2025, 52(8): 2046-2058.

FANG Fang, CHEN Xiaohong, WANG Cheng, ZHENG Zheng, and DENG Xiaoling. Research Advances on Citrus Huanglongbing-induced Fruit Symptomatology，Quality Deterioration，and Underlying Molecular Mechanisms[J]. Acta Horticulturae Sinica, 2025, 52(8): 2046-2058.

图/表 1

参考文献 96

[1]	Albrech U, Bowman K D. 2009. Candidatus Liberibacter asiaticus and Huanglongbing effects on citrus seeds and seedlings. HortScience, 44 (7):1967-1973.
[2]	Bai J, Baldwin E A, McCollum G, Plotto A, Manthey J A, Widmer W W, Luzio G, Cameron R. 2016. Changes in volatile and non-volatile flavor chemicals of‘Valencia’orange juice over the harvest seasons. Foods, 5 (4):4-10.
[3]	Baldwin E, Manthey J, McCollum G, Bai J, Irey M, Cameron R, Luzio G. 2010. Effect of Liberibacter infection(Huanglongbing disease)of citrus on orange fruit physiology and fruit/fruit juice quality:chemical and physical analyses. Journal of Agricultural and Food Chemistry, 58 (2):1247-1262.
[4]	Bassanezi R B, Montesino L H, Stuchi E S. 2009. Effects of Huanglongbing on fruit quality of sweet orange cultivars in Brazil. European Journal of Plant Pathology, 125 (4):565-572.
[5]	Batool A, Iftikhar Y, Mughal S M, Khan M M, Jaskani M J, Abbas M, Khan I A. 2007. Citrus greening disease-a major cause of citrus decline in the world-a review. Horticultural Science, 34 (4):159-166.
[6]	Bemer M, Karlova R, Ballester A R, Tikunov Y M, Bovy A G, Wolters-Arts M, Rossetto P D B, Angenent G C, de Maagd R A. 2012. The tomato FRUITFULL homologs TDR4/FUL1 and MBP7/FUL 2 regulate ethylene-independent aspects of fruit ripening. Plant Cell,24:4437-4451.
[7]	Bové J M. 2006. Huanglongbing:a destructive,newly-emerging,century-old disease of citrus. Journal of Plant Pathology,88:7-37.
[8]	Brunings A M, Gabriel D W. 2003. Xanthomonas citr:Breaking the surface. Molecular Plant Patholog, 4 (3):141-157.
[9]	Cen H, Weng H, Yao J, He M, Lv J, Hua S, Li H, He Y. 2017. Chlorophyll fluorescence imaging uncovers photosynthetic fingerprint of citrus Huanglongbing. Frontiers in Plant Science,8:1509.
[10]	Chen Chuanwu, Fu Huimin, Deng Chongling, Li Xianliang, Deng Guangzhou, Lou Binghai. 2015. Dynamic variation of huanglongbing pathogen content in citrus and wampee. Journal of Southern Agriculture, 46 (6):1024-1028. (in Chinese)
	陈传武, 付慧敏, 邓崇岭, 李贤良, 邓光宙, 娄兵海. 2015. 柑橘和黄皮中黄龙病菌含量动态变化. 南方农业学报, 46 (6):1024-1028.
[11]	Chin E L, Mishchuk D O, Breksa A P, Slupsky C M. 2014. Metabolite signature of Candidatus Liberibacter asiaticus infection in two citrus varieties. Journal of Agricultural and Food Chemistry, 62 (28):6585-6591.
[12]	Cirmi S, Navarra M, Woodside J V, Cantwell M M. 2018. Citrus fruits intake and oral cancer risk:a systematic review and meta-analysis. Pharmacological Research,133:187-194.
[13]	Clark K J, Pang Z, Trinh J, Wang N, Ma W. 2020. Sec-delivered effector 1(SDE1)of‘Candidatus Liberibacter asiaticus’promotes citrus huanglongbing. Molecular Plant-Microbe Interactions, 33 (12):1394-1404.
[14]	Cui X, Zhan X, Liu Y, Huang Z, Deng X, Zheng Z, Xu M. 2022. Integrated transcriptome and metabolome analysis reveals phenylpropanoid biosynthesis and phytohormone signaling contribute to‘Candidatus Liberibacter asiaticus’accumulation in citrus fruit piths(fluffy albedo). International Journal of Molecular Sciences, 23 (24):15648.
[15]	Dagulo L, Danyluk M D, Spann T M, Valim M F, Goodrich‐Schneider R, Sims C, Rouseff R. 2010. Chemical characterization of orange juice from trees infected with citrus greening(Huanglongbing). Journal of Food Science, 75 (2) :C199-C207.
[16]	Dala-Paula B M, Plotto A, Bai J, Manthey J A, Baldwin E A, Ferrarezi R S. 2019. Effect of Huanglongbing or greening disease on orange juice quality,a review. Frontiers in Plant Science,9:415137.
[17]	Dea S, Plotto A, Manthey J A, Raithore S, Irey M, Baldwin E. 2013. Interactions and thresholds of limonin and nomilin in bitterness perception in orange juice and other matrices. Journal of Sensory Studies, 28 (4):311-323.
[18]	Deng Xiaoling, Zheng Yongqin, Zheng Zheng, Xu Meirong. 1996. Current research on genomic analysis of‘Candidatus Liberibacter spp.’. Journal of South China Agricultural University, 40 (5):12-22. (in Chinese)
	邓晓玲, 郑永钦, 郑正, 许美容. 2019. 柑橘黄龙病菌基因组学的研究进展. 华南农业大学学报, 40 (5):12-22.
[19]	Deng Yunshuang, Li Tao, Deng Xiaoling, Zheng Zheng. 2023. Symptoms of Citrus reticulata cv. chachiensis infected with Huanglongbing and Candidatus liberibacter asiaticus distribution in branches and fruit pith. Chinese Journal of Tropical Crops, 44 (9):1854-1859. (in Chinese)
	邓云双, 李桃, 邓晓玲, 郑正. 2023. 感染黄龙病茶枝柑的症状表现及其病原在枝条与果实橘络中的分布规律. 热带作物学报, 44 (9):1854-1859.
[20]	Ding F, Duan Y, Paul C, Brlansky R H, Hartung J S. 2015. Localization and distribution of‘Candidatus Liberibacter asiaticus’in citrus and periwinkle by direct tissue blot immune assay with an anti-OmpA polyclonal antibody. Public Library of Science One, 10 (5):e0123939.
[21]	Du J, Wang Q, Shi H, Zhou C, He J, Wang X. 2023. A prophage-encoded effector from‘Candidatus Liberibacter asiaticus’targets ASCORBATE PEROXIDASE 6 in citrus to facilitate bacterial infection. Molecular Plant Pathology, 24 (4):302-316.
[22]	Du J, Wang Q, Zeng C, Zhou C, Wang X. 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 (7):1022-1034.
[23]	Du Meixia, Pang Shuwei, Dong Liting, Mo Kaiqin, Hou Mengyuan, Wang Shuai, Zou Xiuping. 2024. Research progress on the molecular mechanisms of interactions between Candidatus liberibacter and citrus. Acta Horticulturae Sinica, 51 (7):1623-1638. (in Chinese)
	杜美霞, 庞淑玮, 董丽婷, 莫凯琴, 候梦圆, 王帅, 邹修平. 2024. 柑橘黄龙病菌与寄主互作的分子机制研究进展. 园艺学报, 51 (7):1623-1638.
[24]	Du P, Zhang C, Zou X, Zhu Z, Yan H, Wuriyanghan H, Li W. 2021. ‘Candidatus Liberibacter asiaticus’secretes nonclassically secreted proteins that suppress host hypersensitive cell death and induce expression of plant pathogenesis-related proteins. Applied and Environmental Microbiology, 87 (8):e00019-21.
[25]	Duan Y, Zhou L, Hall D G, Li W, Doddapaneni H, Lin H, Liu L, Vahling C M, Gabriel D W, Williams K P, Dickerman A, Sun Y, Gottwald T. 2009. Complete genome sequence of citrus Huanglongbing bacterium,‘Candidatus Liberibacter asiaticus’obtained through metagenomics. Molecular Plant Microbe Interactions, 22 (8):1011-1020.
[26]	Fan J, Chen C, Brlansky R H, Gmitter Jr F G, Li Z. 2010. Changes in carbohydrate metabolism in Citrus sinensis infected with‘Candidatus Liberibacter asiaticus’. Plant Pathology, 59 (6):1037-1043.
[27]	Fang F, Guo H, Zhao A, Li T, Liao H, Deng X, Xu M, Zheng Z. 2021. A significantly high abundance of‘Candidatus Liberibacter asiaticus’in citrus fruit pith:in planta transcriptome and anatomical analyses. Frontiers in Microbiology,12:681251.
[28]	Feng G, Ai X, Yi H, Guo W, Wu J. 2021. Genomic and transcriptomic analyses of Citrus sinensis varieties provide insights into Valencia orange fruit mastication trait formation. Horticulture Research, 8 (1):218.
[29]	Fu S M, Liu H W, Liu Q H, Zhou C Y, Hartung J S. 2019. Detection of‘Candidatus Liberibacter asiaticus’in citrus by concurrent tissue print based qPCR and immunoassay. Plant Pathology, 68 (4):796-803.
[30]	Gao C, Li C, Li Z, Liu X, Li J, Guo J, Mao J, Fang F, Wang C, Deng X, Zheng Z. 2023. Comparative transcriptome profiling of susceptible and tolerant citrus species at early and late stage of infection by‘Candidatus Liberibacter asiaticus’. Frontiers in Plant Science,14:1191029.
[31]	Garcia-Luis A, Fornes F, Sanz A, Guardiola J L. 1988. The regulation of flowering and fruit set in Citrus:relationship with carbohydrate levels. Israel Journal of Botany, 37 (2-4):189-201.
[32]	Goldschmidt E E. 1999. Carbohydrate supply as a critical factor for citrus fruit development and productivity. HortScience, 34 (6):1020-1024.
[33]	Grafton-Cardwell E E, Stelinski L L, Stansly P A. 2013. Biology and management of Asian citrus psyllid,vector of the Huanglongbing pathogens. Annual Review of Entomology,58:413-432.
[34]	Guo Hengyu, Luo Xiaoling, Li Tao, Deng Xiaoling, Zheng Zheng. 2020. Distribution of‘Candidatus Liberibacter asiaticus’in huanglongbing-affected Citrus reticulata Blanco cv Gongkan branches and the fruit pith. Acta Phytopathologica Sinica, 50 (5):543-548. (in Chinese)
	郭亨玉, 罗小玲, 李桃, 邓晓玲, 郑正. 2020. 柑橘黄龙病菌在染病贡柑枝条和果实橘络内的分布规律. 植物病理学报, 50 (5):543-548.
[35]	González-Mas M C, Rambla J L, Alamar M C, Gutiérrez A, Granell A. 2011. Comparative analysis of the volatile fraction of fruit juice from different Citrus species. Public Library of Science One, 6 (7):e22016.
[36]	Hao G, Ammar D, Duan Y, Stover E. 2019. Transgenic citrus plants expressing a‘Candidatus Liberibacter asiaticus’prophage protein LasP235 display Huanglongbing-like symptoms. Agri Gene, 235,12:100085.
[37]	Hartung J S, Paul C, Achor D, Brlansky R H. 2010. Colonization of dodder,Cuscuta indecora,by‘Candidatus Liberibacter asiaticus’and‘Ca. L. americanus’. Phytopathology, 100 (8):756-762.
[38]	Heo J, Blob B, Helariutta Y. 2017. Differentiation of conductive cells:a matter of life and death. Current Opinion in Plant Biology,35:23-29.
[39]	Hijaz F M, Manthey J A, Folimonova S Y, Davis C L, Jones S E, Reyes-De-Corcuera J I. 2013. An HPLC-MS characterization of the changes in sweet orange leaf metabolite profile following infection by the bacterial pathogen Candidatus Liberibacter asiaticus. Public Library of Science One, 8 (11):e79485.
[40]	Huang M, Roose M L, Yu Q B, Stover E, Hall D G, Deng Z N, Frederick G, Gmitter J. 2023. Mapping of QTLs and candidate genes associated with multiple phenotypic traits for Huanglongbing tolerance in citrus. Horticultural Plant Journal, 9 (4):705-719.
[41]	Huang Zhenhui, Wang Juan, Gao Jie, Zheng Zheng, Deng Xiaoling, Xu Meirong. 2022. Distribution of‘Candidatus Liberibacter asiaticus’in the fruit branches of four citrus cultivars. Journal of South China Agricultural University, 43 (5):35-42. (in Chinese)
	黄桢辉, 王娟, 高洁, 郑正, 邓晓玲, 许美容. 2022. 黄龙病菌在4个品种柑橘果枝内的时空分布. 华南农业大学学报, 43 (5):35-42.
[42]	Hung W, Wang Y. 2018. A targeted mass spectrometry-based metabolomics approach toward the understanding of host responses to Huanglongbing disease. Journal of Agricultural and Food Chemistry, 66 (40):10651-10661.
[43]	Iglesias D J, Tadeo F R, Primo-Millo E, Talon M. 2003. Fruit set dependence on carbohydrate availability in citrus trees. Tree physiology, 23 (3):199-204.
[44]	Jagoueix S, Bové J M, Garnier M. 1994. The phloem-limited bacterium of greening disease of citrus is a member of the α subdivision of the Proteobacteria. International Journal of Systematic and Evolutionary Microbiology, 44 (3):379-386.
[45]	Jaakola L, Poole M, Jones M O, Kämäräinen-Karppinen T, Koskimäki J J, Hohtola A, Häggman H, Fraser P D, Manning K, King G J, Thomson H, Seymour G B. 2010. A SQUAMOSA MADS box gene involved in the regulation of anthocyanin accumulation in bilberry fruits. Plant Physiology, 153 (4):1619-1629.
[46]	Jain M, Fleites L A, Gabriel D W. 2015. Prophage-encoded peroxidase in‘Candidatus Liberibacter asiaticus’is a secreted effector that suppresses plant defenses. Molecular Plant-Microbe Interactions, 28 (12):1330-1337.
[47]	Jain M, Munoz-Bodnar A, Gabriel D W. 2019. ‘Candidatus Liberibacter asiaticus’peroxiredoxin(LasBCP)suppresses oxylipin-mediated defense signaling in citrus. Journal of plant physiology,236:61-65.
[48]	Jain M, Munoz-Bodnar A, Zhang S, Gabriel D W. 2018. A secreted‘Candidatus Liberibacter asiaticus’peroxiredoxin simultaneously suppresses both localized and systemic innate immune responses in planta. Molecular Plant-Microbe Interactions, 31 (12):1312-1322.
[49]	Kiefl J, Kohlenberg B, Hartmann A, Obst K, Paetz S, Krammer G, Trautzsch S. 2018. Investigation on key molecules of Huanglongbing(hlb)-induced orange juice off-flavor. Journal of Agricultural and Food Chemistry, 66 (10):2370-2377.
[50]	Kvittingen L, Sjursnes B J, Schmid R. 2021. Limonene in Citrus: a string of unchecked literature citings? Journal of Chemical Education, 98 (11):3600-3607.
[51]	Lado J, Gambetta G, Zacarias L. 2018. Key determinants of citrus fruit quality:metabolites and main changes during maturation. Scientia Horticulturae,233:238-248.
[52]	Li Y, Ma R, Gao C, Li Z, Zheng Y, Fang F,Wang, Li G, Du X, Xu C, Xu M, Liu R, Deng X, Zheng Z. 2024. Integrated bacterial transcriptome and host metabolome analysis reveals insights into‘Candidatus Liberibacter asiaticus’population dynamics in the fruit pith of three citrus cultivars with different tolerance. Microbiology Spectrum, 12 (4):e04052-23.
[53]	Li L, Tan W, Li W, Zhu Y, Cheng Y, Ni H. 2019. Citrus taste modification potentials by genetic engineering. International Journal of Molecular Sciences, 20 (24):6194.
[54]	Li Y, Yang X, Zhang J, Dai J, Liu L, Lin J, Benshui S. 2022. Transcriptome analyses reveal the potential mechanisms for color changes of a sweet orange peel induced by Candidatus Liberibacter asiaticus. Gene,839:146736.
[55]	Liao H L, Burns J K. 2012. Gene expression in Citrus sinensis fruit tissues harvested from huanglongbing-infected trees:comparison with girdled fruit. Journal of Experimental Botany, 63 (8):3307-3319.
[56]	Liu X, Fan Y, Zhang C, Dai M, Wang X, Li W. 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.
[57]	Lü Ruoya, Li Yun, Zheng Yongqin, Deng Xiaoling, Zheng Zheng. 2023. The distribution pattern of Candidatus Liberibacter asiaticus in fruit pith. Acta Horticulturae Sinica, 50 (5):1110-1117. (in Chinese)
	吕若亚, 李云, 郑永钦, 邓晓玲, 郑正. 2023. 黄龙病菌在柑橘果实橘络中的分布. 园艺学报, 50 (5):1110-1117.
[58]	Lu X, Zhao C, Shi H, Liao Y, Xu F, Du H, Zheng J. 2023. Nutrients and bioactives in citrus fruits:Different citrus varieties,fruit parts,and growth stages. Critical Reviews in Food Science and Nutrition, 63 (14):2018-2041.
[59]	Martinelli F, Uratsu S L, Albrecht U, Reagan R L, Phu M L., Britton M, Buffalo V, Fass J, Leicht E, Zhao W, Lin D. 2012. Transcriptome profiling of citrus fruit response to Huanglongbing disease. Public Library of Science One, 7 (5):e38039.
[60]	Massenti R, Lo Bianco R, Sandhu A K, Gu L, Sims C. 2016. Huanglongbing modifies quality components and flavonoid content of‘Valencia’oranges. Journal of the Science of Food and Agriculture, 96 (1):73-78.
[61]	Pang Z, Zhang L, Coaker G, Ma W, He S Y, Wang N. 2020. Citrus CsACD 2 is a target of Candidatus Liberibacter asiaticus in Huanglongbing disease. Plant physiology, 184 (2):792-805.
[62]	Pitino M, Armstrong C M, Cano L M, Duan Y. 2016. Transient expression of Candidatus Liberibacter asiaticus effector induces cell death in Nicotiana benthamiana. Frontiers in Plant Science,7:982.
[63]	Pitino M, Allen V, Duan Y. 2018. LasΔ5315 effector induces extreme starch accumulation and chlorosis as Ca. Liberibacter asiaticus infection in Nicotiana benthamiana. Frontiers in Plant Science,9:113.
[64]	Plotto A, Margaría C A, Goodner K L, Goodrich R, Baldwin E A. 2004. Odour and flavour thresholds for key aroma components in an orange juice matrix:terpenes and aldehydes. Flavour and Fragrance Journal, 19 (6):491-498.
[65]	Plotto A, Margarí C A, Goodner K L, Baldwin E A. 2008. Odour and flavour thresholds for key aroma components in an orange juice matrix:esters and miscellaneous compounds. Flavour and fragrance journal, 23 (6):398-406.
[66]	Poiroux‐Gonord F, Santini J, Fanciullin A L, Lopez‐Lauri F, Giannettini J, Sallanon H, Berti L, Urban L. 2013. Metabolism in orange fruits is driven by photooxidative stress in the leaves. Physiologia Plantarum, 149 (2):175-187.
[67]	Porat R, Deterre S, Giampaoli P, Plotto A. 2016. The flavor of citrus fruit. Biotechnology in flavor production,1:31.
[68]	Putnik P, Barba F J, Lorenzo J M, Gabrić D, Shpigelman A, Cravotto G, Bursać Kovačević D. 2017. An integrated approach to mandarin processing:food safety and nutritional quality,consumer preference,and nutrient bioaccessibility. Comprehensive Reviews in Food Science and Food Safety, 16 (6):1345-1358.
[69]	Reinking O A. 1919. Diseases of economic plants in southern China. Philippine Agriculturist, 8 (4):109-135.
[70]	Rosales R, Burns J K. 2011. Phytohormone changes and carbohydrate status in sweet orange fruit from Huanglongbing-infected trees. Journal of Plant Growth Regulation,30:312-321.
[71]	Sink Jr,K C Herner R C,Knowlton L L, 1974. Chlorophyll and carotenoids of the rin tomato mutant. Canadian Journal of Botany, 52 (7):1657-1660.
[72]	Slisz A M, Breksa A R, Mishchuk D O, McCollum G, Slupsky C M. 2012. Metabolomic analysis of citrus infection by‘Candidatus Liberibacter asiaticus’reveals insight into pathogenicity. Journal of Proteome Research, 11 (8):4223-4230.
[73]	Shen P, Li X, Fu S, Zhou C, Wang X. 2022. A‘Candidatus Liberibacter asiaticus’-secreted polypeptide suppresses plant immune responses in Nicotiana benthamiana and Citrus sinensis. Frontiers in Plant Science,13:997825.
[74]	Shi J, Gong Y, Shi H, Ma X, Zhu Y, Yang F, Wang D, Fu Y, Lin Y, Yang N, Yang Z, Zeng C, Li W, Zhou C, Wang X, Qiao Y. 2023a. ‘Candidatus Liberibacter asiaticus’secretory protein SDE 3 inhibits host autophagy to promote Huanglongbing disease in citrus. Autophagy, 19 (9):2558-2574.
[75]	Shi H, Yang Z, Huang J, Wu H, Fu S, Li W, Zou X, Zhou C, Wang X. 2023b. An effector of‘Candidatus Liberibacter asiaticus’manipulates autophagy to promote bacterial infection. Journal of Experimental Botany, 74 (15):4670-4684.
[76]	Tatineni S, Sagaram U S, Gowda S, Robertson C J, Dawson W O, Iwanami T, Wang N. 2008. In planta distribution of‘Candidatus Liberibacter asiaticus’as revealed by polymerase chain reaction(pcr)and real-time pcr. Phytopathology, 98 (5):592-599.
[77]	Teixeira D D C, Saillard C, Eveillard S, Danet J L, Costa P I D, Ayres A J, Bové J. 2005. ‘Candidatus Liberibacter asiaticus’,associated with citrus Huanglongbing(greening disease)in São Paulo State,Brazil. International Journal of Systematic and Evolutionary Microbiology,55:1857-1862.
[78]	Wang F, Huang Y, Wu W, Zhu C, Zhang R, Chen J, Zeng J. 2020. Metabolomics analysis of the peels of different colored citrus fruits(Citrus reticulata cv.‘Shatangju’)during the maturation period based on UHPLC-QQQ-MS. Molecules, 25 (2):396.
[79]	Wang F, Wu Y, Wu W, Huang Y, Zhu C, Zhang R, Chen J, Zeng J. 2021. Integrative analysis of metabolome and transcriptome profiles provides insight into the fruit pericarp pigmentation disorder caused by‘Candidatus Liberibacter asiaticus’infection. BMC Plant Biology, 21 (1):1-16.
[80]	Wang S, Du M, Dong L, Qu R, Ran D, Ma J, Wang X, Xu L, Li W, He Y, Zou X. X. 2023. Function and molecular mechanism analysis of CaLasSDE 460 effector involved in the pathogenesis of‘Candidatus Liberibacter asiaticus’in citrus. Molecular Horticulture, 3 (1):14.
[81]	Wang Shengtong, Zheng Zheng, Bao Minli, Xu Meirong, Deng Xiaoling. 2016. Effects of Huanglongbing on fruit quality of Shatangju(Citrus reticulata Blanco). Acta Agriculturae Zhejiangensis, 28 (1):145-149. (in Chinese)
	王圣通, 郑正, 鲍敏丽, 许美容, 邓晓玲. 2016. 柑橘黄龙病对砂糖橘果实品质的影响. 浙江农业学报, 28 (1):145-149.
[82]	Wang Xuefeng, Lei Tiangang, Zhou Changyong. 2023. Occurrence and control of citrus Huanglongbing. Modern Agrochemicals, 22 (6):13-16,21. (in Chinese)
	王雪峰, 雷天刚, 周常勇. 2023. 柑橘黄龙病的发生与防治. 现代农药, 22 (6):13-16,21.
[83]	Wang Feiyan, Zhang Ruiming, Wu Wen, Zhu Congyi, Huang Yongjing, Cheng Jiezhong, Zeng Jiwu. 2020. Effects of citrus Huanglongbing on tree traits and fruit quality of Citrus maxima(Burm.) Merr. cv. Shatian Yu. Chinese Journal of Tropical Crops, 41 (9):1847-1855. (in Chinese)
	王飞燕, 张瑞敏, 吴文, 朱从一, 黄永敬, 陈杰忠, 曾继吾. 2020. 柑橘黄龙病对沙田柚树体特性和果实品质的影响. 热带作物学报, 41 (9):1847-1855. (in Chinese).
[84]	Wang N, Pierson E A, Setubal J C, Xu J, Levy J G, Zhang Y, Li J, Rangel L T, Martins J J. 2017. The Candidatus Liberibacter-host interface:insights into pathogenesis mechanisms and disease control. Annual. Review of Phytopathology,55:451-482.
[85]	Wu Fengnian, Dai Zehan, Zheng Yu, Chen Yanghong, Xu Mengrong, Ceng Yijing, Deng Xiaoling. 2020. Effects of citrus Huanglongbing pathogen on agronomic characteristic and fruit quality of Citrus maxima cv. Shatian Yu. Journal of South China Agricultural University, 41 (3):63-71. (in Chinese)
	吴丰年, 戴泽翰, 郑昱, 陈仰泓, 许美容, 岑伊静, 邓晓玲. 2020. 柑橘黄龙病菌对沙田柚田间性状和果实品质的影响. 华南农业大学学报, 41 (3):63-71.
[86]	Xiong Zhiwei, Li Zhilong, Yin Hui, Gao Yuxia. 2024. Pan-genome analysis of Candidatus Liberibacter asiaticus causing Huanglongbing of citrus. Acta Horticulturae Sinica, 51 (4):737-747. (in Chinese)
	熊志伟, 李智龙, 尹晖, 高玉霞. 2024. 柑橘黄龙病菌亚洲种的泛基因组分析. 园艺学报, 51 (4):737-747.
[87]	Yao L, Yu Q, Huang M, Hung W, Grosser J, Chen S, Wang Y, Gmitter F G. 2019. Proteomic and metabolomic analyses provide insight into the off-flavour of fruits from citrus trees infected with‘Candidatus Liberibacter asiaticus’. Horticulture Research,6:31.
[88]	Yue M, Jiang L, Zhang N, Zhang L, Liu Y, Lin Y, Zhang Y, Luo Y, Zhang Y, Wang Y, Li M. 2023. Regulation of flavonoids in strawberry fruits by FaMYB5/FaMYB10 dominated MYB-bHLH-WD40 ternary complexes. Frontiers in Plant Science,14:1145670.
[89]	Zeng Danting, Zheng Yongqin, Li Wenting, Deng Xiaoling, Zheng Zheng. 2024. Distribution and prophage analysis of Candidatus Liberibacter asiaticus in Leibo navel orange. China Fruits,(1):97-102. (in Chinese)
	曾丹婷, 郑永钦, 李文婷, 邓晓玲, 郑正. 2024. 柑橘黄龙病菌在雷波脐橙中的分布规律及其原噬菌体类型分析. 中国果树,(1):97-102.
[90]	Zhang C, Wang X, Liu X, Fan Y, Zhang Y, Zhou X, Li W. 2019. A novel ‘Candidatus Liberibacter asiaticus’-encoded Sec-dependent secretory protein suppresses programmed cell death in Nicotiana benthamiana. International Journal of Molecular Sciences, 20 (22):5802.
[91]	Zhang J, Zhao H, Chen L, Lin J, Wang Z, Pan J, Yang F, Ni X, Wang Y, Wang Y, Li R. 2023. Multifaceted roles of WRKY transcription factors in abiotic stress and flavonoid biosynthesis. Frontiers in Plant Science,14:1303667.
[92]	Zhang S, Wang X, He J, Zhang S, Zhao T, Fu S, Zhou C. 2023. A Sec-dependent effector,CLIBASIA_04425,contributes to virulence in‘Candidatus Liberibacter asiaticus’. Frontiers in Plant Science, 14:1224736.
[93]	Zhao W, Baldwin E A, Bai J, Plotto A, Irey M. 2019. Comparative analysis of the transcriptomes of the calyx abscission zone of sweet orange insights into the huanglongbing-associated fruit abscission. Horticulture Research,6:71.
[94]	Zhao X, Yuan X, Chen S, Meng L, Fu D. 2018. Role of the tomato TAGL 1 gene in regulating fruit metabolites elucidated using RNA sequence and metabolomics analyses. PLoS ONE, 13 (6):e0199083.
[95]	Zheng Z, Bao M, Wu F, Van Horn C, Chen J, Deng X. 2018. A type 3 prophage of‘Candidatus Liberibacter asiaticus’carrying a restriction-modification system. Phytopathology, 108 (4):454-461.
[96]	Zhou Y, Wei X, Li Y, Liu Z, Duan Y, Zou H. 2020. ‘Candidatus Liberibacter asiaticus’SDE 1 effector induces Huanglongbing chlorosis by downregulating host DDX3 gene. International Journal of Molecular Sciences, 21 (21):7996.