Research Progress on the Effector of Fusarium oxysporum f. sp. cubense
WANG Tian, CHEN Dai-Peng, GAO Ya, WANG Yu-Hua, ZHOU Si-Yu, FU Yu-Jia, ZHENG Li*
College of Plant Protection/Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests, Ministry of Education, Hainan University, Haikou 570228, China
Abstract:As an important food crop and trade agricultural products around the world, Banana (Musa spp.) plays a key role in economic and social development. Banana Fusarium wilt is a notorious soil-borne vascular fungal disease caused by Fusarium oxysporum f.sp. cubense (Foc), causing serious harm to the banana industry worldwide. So far, cultivation of resistant varieties is the most effective way to control banana Fusarium wilt. However, there is no significant progress in disease resistance breeding. Previous study indicated that the effector is a highly important category of pathogenic toxic factors, which plays an important role in pathogenic infection, colonization and the interaction with the host plants. This study reviewed the recent research of the effector of the banana Fusarium wilt, discussed the bioinformatic prediction, transcriptome analysis of the effector, and emphatically introduced a significant effector gene family. It will offer important principle guidelines for the study of the interaction mechanism between Fusarium oxysporum and bananas, the cultivation of resistant varieties and the disease control of banana Fusarium wilt.
王田, 陈代朋, 高雅, 王渝华, 周思语, 付羽佳, 郑丽. 香蕉枯萎病菌效应蛋白研究进展[J]. 农业生物技术学报, 2022, 30(8): 1614-1621.
WANG Tian, CHEN Dai-Peng, GAO Ya, WANG Yu-Hua, ZHOU Si-Yu, FU Yu-Jia, ZHENG Li. Research Progress on the Effector of Fusarium oxysporum f. sp. cubense. 农业生物技术学报, 2022, 30(8): 1614-1621.
[1] 高芬, 岳换弟, 秦雪梅, 等. 2018. 植物致病镰刀菌细胞壁降解酶的研究进展[J]. 江苏农业学报, 34(04): 955-960. (Gao F, Yue H D, Qin X M, et al.2018. Research advances on cell wall degrading enzymes produced by pathogenic Fusarium causing plant diseases[J]. Jiangsu Journal of Agricultural Sciences, 34(04): 955-960.) [2] 何艳秋, 颜瑞, 蒙姑, 等. 2020. 香蕉枯萎病菌1号小种分泌蛋白与效应子的预测与分析[J]. 植物病理学报, 50(02): 129-140. (He Y Q, Yan R, Meng G, et al.2020. Genome-scale prediction and analysis of secreted proteins and effectors in Fusarium oxysporum f.sp. cubense race 1[J]. Acta Phytopathologica Sinica, 50(02): 129-140.) [3] 雷忠华. 2018. 基于互作转录组分析的抗病香蕉品系南天蕉与尖孢镰刀菌互作机理研究[D]. 硕士学位论文,华南理工大学, 导师:陈谷. pp. 3-6. (LEI Z H.2018. Dual Rna-sequencing unveils host-pathogen interactions in resistant banana cultivars Nantianjiao upon Fusarium oxysporum race 4 challenge[D]. Thesis of M.S., South China University of Technology, Supervisor: Chen G. pp. 3-6.) [4] 李英, 杜春梅. 2021. 致病性尖孢镰刀菌毒力因子的研究进展[J]. 中国农学通报, 37(12): 92-97. (Li Y, Du C M.2021. Virulence factors of pathogenic Fusarium oxysporum: Research progress[J]. Chinese Agricultural Science Bulletin, 37(12): 92-97.) [5] 刘艳琴, 刘立娜, 陈燕, 等. 2018. 植物病原真菌效应蛋白与植物互作动态分析[J]. 分子植物育种, 16(20): 6678-6687. (Liu Y Q, Liu L N, Chen Y, et al.2018. Dynamic analysis of interaction between plant pathogenic fugus effector protein and plants[J]. Molecular Plant Breeding, 16(20): 6678-6687.) [6] 齐悦, 张悦, 李建嫄, 等. 2020. 利用本氏烟筛选小麦叶锈菌效应蛋白[J]. 农业生物技术学报, 28(01): 150-159. (Qi Y, Zhang Y, Li J J, et al.2020. Effector screening of Puccinia triticina by Nicotiana benthamiana[J]. Journal of Agricultural Biotechnology, 28(01): 150-159.) [7] 秦世雯. 2017. 不同碳源条件下香蕉枯萎病菌2个小种转录组差异分析[D]. 博士学位论文, 华南农业大学, 导师: 王振中, pp. 28-47. (QIN S W.2017. Comparative transcriptomic analysis of Fusarium oxysporum f.sp. cubense race 1 and 4 induced with different carbon sources[D]. Thesis of Ph.D., South China Agricultural University, Supervisor: Wang Z Z, pp. 36-47.) [8] 王丹. 2020. 大丽轮枝菌CFEM类小分子富含半胱氨酸蛋白家族基因功能研究[D]. 博士学位论文,中国农业科学院, 导师: 戴小枫, pp. 9-12. (Wang D.2020. Functional analysis of CFEM domain-containing small secreted cysteine-rich proteins in Verticillium dahiae[D]. Thesis of Ph.D., Chinese Academy of Agricultural Science, Supervisor: Dai X F, pp. 9-12.) [9] 肖义炜, 李春强, 李文彬, 等. 2015. 巴西蕉诱导的香蕉枯萎病菌1号和4号小种致病相关基因表达分析[J]. 热带作物学报, 36(11): 1971-1977. (Xiao Y W, Li C Q, Li W B, et al.2015. Pathogenicity-related gene expression profile of Fusarium oxyporum f.sp. cubense race 1 and race 4 induced by Musa AAA Cavendish subgroup cv. Brazil[J]. Chinese Journal of Tropical Crops, 36(11): 1971-1977.) [10] 杨静. 2016. 香蕉枯萎病菌进化研究和Foc TR4致病相关效应蛋白的鉴定及功能分析[D]. 博士学位论文, 华南农业大学, 导师: 王玉柱, pp. 36-47. (YANG J.2016. Studies on the evolution of Fusarium oxysporum f.sp. cubense strains and identification and functional analysis of pathogenicity related effectors from Foc tr4[D]. Thesis of Ph.D., South China Agricultural University, Supervisor: Wang Y Z, pp. 36-47.) [11] 张楠楠, 刘欣, 孙晶, 等. 2009. 真核细胞非经典蛋白分泌途径[J]. 遗传, 31(01): 29-35. (Zhang N N, Liu X, Sun J, et al.2009. Nonclassical mechanisms of secretory protein in eukaryotic cells[J]. Hereditas, 31(01): 29-35.) [12] 郑雯. 2010. 香蕉与枯萎病病程相关基因的鉴定[D]. 硕士学位论文, 海南大学, 导师: 金志强, pp:3-8. (ZHENG W.2010. Identification of genes related to pathogen of Fusarium oxyporum injected banana[D]. Thesis of M.S., Hainan University, Supervisor: Jin Z Q, pp. 3-8.) [13] Asai S, Ayukawa Y, Gan P, et al.2019. High-quality draft genome sequence of Fusarium oxysporum f. sp. cubense strain 160527, a causal agent of panama disease[J]. Microbiology Resource Announcements, 8(29): e00654-19. [14] Aguayo J, Cerf I, Folscher A B, et al.2020. First report of Fusarium oxysporum f. sp. cubense tropical race 4 (TR4) causing banana wilt in the island of Mayotte[J]. Plant Disease, 105(1): 219. [15] Ausubel, Frederick M.2005. Are innate immune signaling pathways in plants and animals conserved?[J]. Nature Immunology, 6(10): 973-979. [16] Bourras S, Mcnally K E, Müller M C, et al.2016. Avirulence genes in cereal powdery mildews: The gene-for-gene hypothesis 2.0.[J]. Frontiers in Plant Science, 7: 241. [17] Butler D.2013. Fungus threatens top banana[J]. Nature, 504(7479): 195-196. [18] Cécile W.2013. Concluding remarks on the special issue dedicated to bacterial secretion systems: Function and structural biology[J]. Research in Microbiology, 164(6): 683-687. [19] Chen D P, Wang Y, Zhou X, et al.2014. The Sch9 kinase regulates conidium size, stress responses, and pathogenesis in Fusarium graminearum[J]. PLOS ONE, 9(8): e105811. [20] Chen D P, Wu C L, Hao C F, et al.2018. Sexual specific functions of Tub1 beta-tubulins require stage-specific RNA processing and expression in Fusarium graminearum[J]. Environmental Microbiology, 20(11): 4009-4021. [21] Chisholm S T, Coaker G, Day B, et al.2006. Host-microbe interactions: Shaping the evolution of the plant immune response-science direct[J]. Cell, 124(4): 803-814. [22] Cui H, Tsuda K, Parker J E.2015. Effector-triggered immunity: from pathogen perception to robust defense[J]. Annual Review of Plant Biology, 66: 487-511. [23] Dangl J L, Jones J.2001. Plant pathogens and integrated defence responses to infection[J]. Nature, 411(6839): 826-833.018. [24] Darcy A B, Stefania B, Chala J T, et al.2018. Bioinformatic prediction of plant-pathogenicity effector proteins of fungi[J]. Current Opinion in Microbiology, 46: 43-49. [25] Dodds P N, Rathjen J P.2010. Plant immunity: Towards an integrated view of plant-pathogen interactions[J]. Nature Reviews Genetics, 11(8): 539-548. [26] Dubery I A, Sanabria N M, Huang J C.2012. Nonself perception in plant innate immunity[J]. Advances in Experimental Medicine and Biology, 738: 79-107. [27] García-Bastidas F, Ordóñez N, Konkol J, et al.2014. First report of Fusarium oxysporum f. sp. cubense tropical race 4 associated with panama disease of banana outside southeast Asia[J]. Plant Disease, 98(5): 694-694. [28] García-Bastidas F, Quintero-Vargas C, Ayala-Vasquez M, et al.2019. First report of Fusarium wilt tropical race 4 in cavendish bananas caused by Fusarium odoratissimum in Colombia[J]. Plant Disease, 104(3): 994. [29] Gawehns F, Houterman P M, Ichou F A, et al.2014. The Fusarium oxysporum effector Six6 contributes to virulence and suppresses I-2-mediated cell death[J]. Molecular Plant-microbe Interactions, 27(4): 336-348. [30] Guo L, Han L, Yang L, et al.2014. Genome and transcriptome analysis of the fungal pathogen Fusarium oxysporum f. sp. cubense causing banana Vascular wilt disease[J]. PLOS ONE, 9(4): e95543. [31] Houterman P M, Ma L, Van O G, et al.2009. The effector protein Avr2 of the xylem-colonizing fungus Fusarium oxysporum activates the tomato resistance protein I-2 intracellularly[J]. The Plant Journal: for Cell and Molecular Biology, 58(6): 970-8. [32] Jangir P, Mehra N, Sharma K, et al.2021. Secreted in xylem genes: Drivers of host adaptation in Fusarium oxysporum[J]. Frontiers in Plant Science, 12: 628611. [33] Jones J, Dangl J.2006. The plant immune system[J]. Nature, 444(7117): 323-329. [34] Kamoun S.2006. A catalogue of the effector secretome of plant pathogenic oomycetes[J]. Annual Review of Phytopathology, 44(1): 41-60. [35] Kang Q, Zhang D.2020. Principle and potential applications of the non-classical protein secretory pathway in bacteria[J]. Applied Microbiology and Biotechnology, 104(3): 953-965. [36] Lee M C S, Miller E A, Goldberg J, et al.2004. Bi-directional protein transport between the ER and Golgi[J]. Annual Review of Cell and Developmental Biology, 20: 87-123. [37] Li W, Wang X, Li C, et al.2019. Dual species transcript profiling during the interaction between banana (Musa acuminata) and the fungal pathogen Fusarium oxysporum f. sp. cubense[J]. BMC genomics, 20(1): 519. [38] Lilia C. C, Juliane H, Vivian A. R-F, et al.2019. Molecular diagnostics of banana Fusarium wilt targeting secreted-in-xylem genes[J]. Frontiers in Plant Science, 10: 547. [39] Martijn R, H. Charlotte V D D, Michiel M, et al.2004. A small, cysteine‐rich protein secreted by Fusarium oxysporum during colonization of xylem vessels is required for I‐3‐mediated resistance in tomato[J]. Molecular Microbiology, 53(5): 1373-83. [40] Mooney B C, Mantz M, Graciet E, et al.2021. Cutting the line: Manipulation of plant immunity by bacterial type Ⅲ effector proteases[J]. Journal of Experimental Botany, 72(9): 3395-3409. [41] Newman M-A, Sundelin T, Nielsen J T, et al.2013. MAMP (microbe-associated molecular pattern) triggered immunity in plants[J]. Frontiers in Plant Science, 4: 139. [42] Pedro L, Carmen R-R, Concepción H.2018. Role of the phosphatase Ptc1 in stress responses mediated by CWI and HOG pathways in Fusarium oxysporum[J]. Fungal Genetics and Biology, 118: 10-20. [43] Pegg K G, Lindel M C, Wayne T O, et al.2019. The epidemiology of Fusarium wilt of banana[J]. Frontiers in Plant Science 10: 1395. [44] Petersen T N, Brunak S, V H Gunnar, et al.2011. Signalp 4.0: Discriminating signal peptides from transmembrane regions[J]. Nature methods, 8(10): 785-6. [45] Ploetz R C, Kema G H J, MA L.2015. Impact of diseases on export and smallholder production of banana[J]. Annual Review of Phytopathology, 53: 269-288. [46] Ploetz R C.2006. Fusarium wilt of banana is caused by several pathogens referred to as Fusarium oxysporum f. sp. cubense[J]. Phytopathology, 96(6): 653-656. [47] Rajamuthiah R, Mylonakis E.2014. Effector triggered immunity[J]. Virulence, 5(7): 697-702. [48] Shamrai S. N.2014. Plant immune system: Basal immunity[J]. Cytology and Genetics, 48(4): 258-271. [49] Sona J, Kouichi A, Renkichi T, et al.2005. Signaling via the G protein α subunit FGA2 is necessary for pathogenesis in Fusarium oxysporum[J]. Fems Microbiology Letters, (1): 165-172. [50] Sperschneider J, Gardiner D M, Dodds P N, et al.2016. EffectorP: Predicting fungal effector proteins from secretomes using machine learning[J]. The New Phytologist, 210(2): 743-61. [51] Spoel S H, Dong X.2012. How do plants achieve immunity? Defence without specialized immune cells[J]. Nature Reviews Immunology, 12(2): 89-100. [52] Sun J, Zhang J, Fang H, et al.2019.Comparative transcriptome analysis reveals resistance-related genes and pathways in Musa acuminata banana 'Guijiao 9' in response to Fusarium wilt[J]. Plant Physiology and Biochemistry, 141: 83-94. [53] Thangavelu R, Edwin R E, Loganathan M, et al.2021. Draft genome of Fusarium oxysporum f. sp. cubense strain tropical race-4 infecting Cavendish (AAA) group of banana in India[J]. Plant Disease, 105(2): 481-483. [54] Thangavelu R, Muthukathan G, Pushpakanth P, et al.2020. First report of Fusarium oxysporum f.sp. cubense VCG 0125 and VCG 01220 of race 1 infecting Cavendish bananas (Musa sp. AAA) in India[J]. Plant Disease, 105(4): 1215. [55] Vartika G, Siddhesh B. G, Thumballi R. G.2020. FocSge1 in Fusarium oxysporum f. sp. cubense race 1 is essential for full virulence[J]. BMC Microbiology, 20(1): 255. [56] Wang Y, Pruitt R N, Nürnberger T, et al.2022. Evasion of plant immunity by microbial pathogens[J]. Nature Reviews Microbiology, 1-16. [57] Widinugraheni S., Niño-Sánchez J, Does H. C. V D, et al.2018. A SIX1 homolog in Fusarium oxysporum f.sp. cubense tropical race 4 contributes to virulence towards Cavendish banana[J]. PLOS ONE, 13(10): e0205896. [58] Williams A H, Sharma M, Thatcher L F, et al.2016. Comparative genomics and prediction of conditionally dispensable sequences in legume-infecting Fusarium oxysporum formae speciales facilitates identification of candidate effectors[J]. BMC genomics, 17: 191. [59] Zhong W, Mark G, Michael S.2009. RNA-Seq: A revolutionary tool for transcriptomics[J]. Nature Reviews Genetics, 10(1): 57-63. [60] Zipfel C, Felix G.2005. Plants and animals: A different taste for microbes?[J]. Current Opinion in Plant Biology, 8(4): 353-360.