棉花黄萎病菌鸟氨酸脱羧酶抗酶蛋白基因VdOAZ的功能分析
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摘要
【目的】明确棉花黄萎病菌中鸟氨酸脱羧酶抗酶蛋白(OAZ)基因(VdOAZ)的功能。【方法】以大丽轮枝菌野生型菌株V592的基因组DNA和cDNA为模板,对VdOAZ基因全长进行克隆并测序。构建针对VdOAZ基因的敲除载体和互补载体,通过农杆菌介导的遗传转化筛选VdOAZ基因敲除菌株和和互补菌株。以野生型菌株V592为对照,对VdOAZ基因敲除突变体和互补菌株的菌落生长速率、产孢量、微菌核产量及对棉花的致病力进行测定;通过实时荧光定量逆转录聚合酶链式反应测定致病相关的其他基因在VdOAZ基因敲除突变体中的表达量,及亚精胺诱导条件下,V592菌株中VdOAZ基因及致病相关的其他基因的相对表达量。【结果】从棉花黄萎病菌中克隆到VdOAZ基因的全长为1 006 bp,具有2个开放阅读框(Open reading frame,ORF),ORF2编码的蛋白具有OAZ所特有的ODC-AZ保守结构域。与野生型菌株V592和互补菌株相比,VdOAZ基因敲除突变体的菌落生长速率降低、微菌核产量及产孢量明显减少,对棉花的致病力下降,表明VdOAZ基因与大丽轮枝菌分生孢子和微菌核的产生有关,并参与大丽轮枝菌致病。在VdOAZ基因敲除突变体中,VdPKAC1、VMK1、VdNLP1、VdNLP2和VdSge1基因表达量显著上调;V592菌株经亚精胺诱导培养后,VdOAZ基因的表达量显著上调,而上述5个致病相关基因的表达量均明显下调,表明VdOAZ基因对其表达具有负调控作用。【结论】VdOAZ基因响应多胺水平改变,通过调控VdPKAC1、VMK1、VdNLP1、VdNLP2、VdSge1的表达影响大丽轮枝菌孢子产生、微菌核形成和致病过程。
[Objective] To determine the function of ornithine decarboxylase antizyme gene(VdOAZ) in Verticillium dahliae causing cotton wilt disease. [Method] The full length of VdOAZ gene was cloned and sequenced from V. dahliae strain V592 genomic DNA and cDNA. VdOAZ gene deletion plasmid was constructed and transformed into V592 strain by the Agrobacterium tumefaciens-mediated transformation to produce VdOAZ gene deletion strains, and the complementary plasmid was constructed and transformed into a VdOAZ gene deletion strain to produce complemented strains. Colony growth rate on potato dextrose agar medium, microsclerotia production and conidia production and virulence to cotton of VdOAZ gene deletion mutants and complementary strains were measured when compared to V592 strain. Relative expression of other genes involved in virulence in VdOAZ deletion mutants were measured by reverse transcription-quantitative real time PCR(RT-q PCR), and the relative expression of VdOAZ gene and other genes involved in virulence in V592 strain were also determined by RT-q PCR when V592 strain was cultured for 4 hours in the presence of spermidine. [Result] The full length of VdOAZ gene was determined to be 1 006 bp and it has two open reading frames(ORFs), VdOAZ protein encoded by ORF2 contained conserved ODC-AZ domain characterized by OAZ protein. VdOAZ gene deletion mutants displayed decreased colony growth rate, reduced microsclerotia and conidia, and drastic reduction in virulence to cotton compared with the wild type strain V592 and complementary strains, indicating that VdOAZ gene is participated in production of microsclerotia and conidia, and is involved in virulence in V. dahliae. In VdOAZ deletion mutants, transcriptional expression of 5 genes(VdPKAC1, VMK1, VdNLP1,VdNLP2 and VdSge1) in V. dahliae were strongly up-regulated. The transcriptional expression of VdOAZ gene was strongly up-regulated in the presence of spermidine, whereas VdPKAC1, VMK1, VdNLP1, VdNLP2 and VdSge1 were down-regulated,suggesting that VdOAZ gene negatively regulates transcriptional expression of VdPKAC1, VMK1, VdNLP1, VdNLP2 and VdSge1. [Conclusion] In response to changes in polyamine levels, VdOAZ gene regulates the expression of VdPKAC1, VMK1,VdNLP1, VdNLP2 and VdSge1 to participate in the process of conidium production, microsclerotium formation and pathogenesis of V. dahliae.
[Objective] To determine the function of ornithine decarboxylase antizyme gene(VdOAZ) in Verticillium dahliae causing cotton wilt disease. [Method] The full length of VdOAZ gene was cloned and sequenced from V. dahliae strain V592 genomic DNA and cDNA. VdOAZ gene deletion plasmid was constructed and transformed into V592 strain by the Agrobacterium tumefaciens-mediated transformation to produce VdOAZ gene deletion strains, and the complementary plasmid was constructed and transformed into a VdOAZ gene deletion strain to produce complemented strains. Colony growth rate on potato dextrose agar medium, microsclerotia production and conidia production and virulence to cotton of VdOAZ gene deletion mutants and complementary strains were measured when compared to V592 strain. Relative expression of other genes involved in virulence in VdOAZ deletion mutants were measured by reverse transcription-quantitative real time PCR(RT-q PCR), and the relative expression of VdOAZ gene and other genes involved in virulence in V592 strain were also determined by RT-q PCR when V592 strain was cultured for 4 hours in the presence of spermidine. [Result] The full length of VdOAZ gene was determined to be 1 006 bp and it has two open reading frames(ORFs), VdOAZ protein encoded by ORF2 contained conserved ODC-AZ domain characterized by OAZ protein. VdOAZ gene deletion mutants displayed decreased colony growth rate, reduced microsclerotia and conidia, and drastic reduction in virulence to cotton compared with the wild type strain V592 and complementary strains, indicating that VdOAZ gene is participated in production of microsclerotia and conidia, and is involved in virulence in V. dahliae. In VdOAZ deletion mutants, transcriptional expression of 5 genes(VdPKAC1, VMK1, VdNLP1,VdNLP2 and VdSge1) in V. dahliae were strongly up-regulated. The transcriptional expression of VdOAZ gene was strongly up-regulated in the presence of spermidine, whereas VdPKAC1, VMK1, VdNLP1, VdNLP2 and VdSge1 were down-regulated,suggesting that VdOAZ gene negatively regulates transcriptional expression of VdPKAC1, VMK1, VdNLP1, VdNLP2 and VdSge1. [Conclusion] In response to changes in polyamine levels, VdOAZ gene regulates the expression of VdPKAC1, VMK1,VdNLP1, VdNLP2 and VdSge1 to participate in the process of conidium production, microsclerotium formation and pathogenesis of V. dahliae.
引文
[1]刘琳琳,张文文,周易,等.棉花与番茄抗棉花黄萎病不依赖于Ve1[J].中国科学:生命科学,2014,44(8):803-814.https://doi.org/10.1360/052014-90Liu L L,Zhang W W,Zhou Y,et al.Resistance of cotton and tomato to Verticillium dahliae from cotton is independent on Ve1[J].Scientia Sinica Vitae,2014,44(8):803-814.
[2]Schnathorst W C.Life cycle and epidemiology of verticillium.Fungal wilt diseases of plants[M].San Fransisco:Academic Press,1981:81-111.
[3]Hoppenau C E,Tran V,Kusch H,et al.Verticillium dahliae VdTHI4,involved in thiazole biosynthesis,stress response and DNA repair functions,is required for vascular disease induction in tomato[J].Environmental and Experimental Botany,2014,108:14-22.http://dx.doi.org/10.1016/j.envexpbot.2013.12.015
[4]Qi X L,Su X F,Guo H M,et al.VdThit,a thiamine transport protein,is required for pathogenicity of the vascular pathogen Verticillium dahliae[J].Molecular Plant Microbe Interactions,2016,29(7):545-559.http://dx.doi.org/10.1094/MPMI-03-16-0057-R
[5]Maruthachalam K,Klosterman S J,Kang S,et al.Identification of pathogenicity-related genes in the vascular wilt fungus Verticillium dahliae by Agrobacterium tumefaciens-mediated T-DNAinsertional mutagenesis[J].Molecular Biotechnology,2011,49(3):209-221.https://doi.org/10.1007/s12033-011-9392-8
[6]Zhao Y L,Zhou T T,Guo H S.Hyphopodium-specific VdNoxB/VdPls1-dependent ROS-Ca2+signaling is required for plant infection by Verticillium dahliae[J/OL].PLoS Pathogens,2016,12(7):e1005793.https://doi.org/10.1371/journal.ppat.1005793
[7]Li Z F,Liu Y J,Feng Z L,et al.VdCYC8,encoding CYC8 glucose repression mediator protein,is required for microsclerotia formation and full virulence in Verticillium dahliae[J/OL].PLoSONE,2015,10(12):e0144020.https://doi.org/10.1371/journal.pone.0144020
[8]Gao F,Zhou B J,Li G Y,et al.A glutamic acid-rich protein identified in Verticillium dahliae from an insertional mutagenesis affects microsclerotial formation and pathogenicity[J/OL].PLoSONE,2010,5(12):e15319.https://doi.org/10.1371/journal.pone.0015319
[9]Tzima A K,Paplomatas E J,Rauyaree P,et al.VdSNF1,the sucrose nonfermenting protein kinase gene of Verticillium dahliae,is required for virulence and expression of genes involved in cell-wall degradation[J].Molecular Plant Microbe Interactions,2011,24(1):129-142.https://doi.org/10.1094/MPMI-09-09-0217
[10]Zhang Y L,Mao J C,Huang J F,et al.A uracil-DNA glycosylase functions in spore development and pathogenicity of Verticillium dahliae[J].Physiological and Molecular Plant Pathology,2015,92:148-153.http://dx.doi.org/10.1016/j.pmpp.2015.05.001
[11]Jonge R D,Esse H P V,Maruthachalam K,et al.Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing[J].Proceedings of the National Academy of Sciences,2012,109(13):5110-5115.https://doi.org/10.1073/pnas.1119623109
[12]Liu T L,Song T Q,Zhang X,et al.Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis[J].Nature Communications,2014,5(1):4686.https://doi.org/10.1038/ncomms5686
[13]Santhanam P,Esse H P V,Albert I,et al.Evidence for functional diversification within a fungal NEP1-like protein family[J].Molecular Plant Microbe Interactions,2013,26(3):278-286.http://dx.doi.org/10.1094/MPMI-09-12-0222-R
[14]Zhou B J,Jia P S,Gao F,et al.Molecular characterization and functional analysis of a necrosis-and ethylene-inducing,protein-encoding gene family from Verticillium dahliae[J].Molecular Plant Microbe Interactions,2012,25(7):964-975.http://dx.doi.org/10.1094/MPMI-12-11-0319
[15]Gui Y J,Zhang W Q,Zhang D D,et al.A Verticillium dahliae extracellular cutinase modulates plant immune responses[J].Molecular Plant Microbe Interactions,2018,31(2):260-273.https://doi.org/10.1094/MPMI-06-17-0136-R
[16]Rauyaree P,Ospina-Giraldo M D,Kang S,et al.Mutations in VMK1,a mitogen-activated protein kinase gene,affect microsclerotia formation and pathogenicity in Verticillium dahliae[J].Current Genetics,2005,48(2):109-116.http://dx.doi.org/10.1007/s00294-005-0586-0.
[17]Tian L L,Xu J,Zhou L,et al.VdMsb regulates virulence and microsclerotia production in the fungal plant pathogen Verticillium dahliae[J].Gene,2014,550(2):238-244.http://dx.doi.org/10.1016/j.gene.2014.08.035
[18]Wang Y L,Tian L Y,Xiong D G,et al.The mitogen-activated protein kinase gene,VdHog1,regulates osmotic stress response,microsclerotia formation and virulence in Verticillium dahliae[J].Fungal Genetics and Biology,2016,88:13-23.http://dx.doi.org/10.1016/j.fgb.2016.01.011
[19]Qi X Y,Zhou S,Shang X G,et al.VdSho1 regulates growth,oxidant adaptation and virulence in Verticillium dahliae[J].Journal of Phytopathology,2016,164(11-12):1064-1074.https://doi.org/10.1111/jph.12527
[20]Tzima A,Paplomatas E J,Rauyaree P,et al.Roles of the catalytic subunit of c AMP-dependent protein kinase A in virulence and development of the soilborne plant pathogen Verticillium dahliae[J].Fungal Genetics and Biology,2010,47(5):406-415.https://doi.org/10.1016/j.fgb.2010.01.007
[21]Tzima A K,Paplomatas E J,Tsitsigiannis D I,et al.The G proteinβsubunit controls virulence and multiple growth-and development-related traits in Verticillium dahliae[J].Fungal Genetics and Biology,2012,49(4):271-283.https://doi.org/10.1016/j.fgb.2012.02.005
[22]Zhang T,Zhang B S,Hua C L,et al.VdPKS1 is required for melanin formation and virulence in a cotton wilt pathogen Verticillium dahliae[J].Science China Life Sciences,2017,60(8):868-879.https://doi.org/10.1007/s11427-017-9075-3
[23]Santhanam P,Thomma B P H J.Verticillium dahliae Sge1 differentially regulates expression of candidate effector genes[J].Molecular Plant Microbe Interactions,2013,26(2):249-256.http://dx.doi.org/10.1094/MPMI-08-12-0198-R
[24]高云,孟佩,张婷,等.棉花黄萎病菌VdSge1基因的敲除与功能分析[J].棉花学报,2015,27(4):346-353.https://doi.org/10.11963/issn.1002-7807.201504007Gao Y,Meng P,Zhang T,et al.Knockout and functional analysis of VdSge1 in Verticillium dahliae[J].Cotton Science,2015,27(4):346-353.
[25]Luo X M,Mao H Q,Wei Y M,et al.The fungal-specific transcription factor Vdpf influences conidia production,melanized microsclerotia formation and pathogenicity in Verticillium dahliae[J].Molecular Plant Pathology,2016,17(9):1364-1381.https://doi.org/10.1111/mpp.12367
[26]Xiong D G,Wang Y L,Tian L Y,et al.MADS-Box transcription factor VdMcm1 regulates conidiation,microsclerotia formation,pathogenicity,and secondary metabolism of Verticillium dahliae[J].Frontiers in Microbiology,2016,7:1192.https://doi.org/10.3389/fmicb.2016.01192
[27]Xiong D G,Wang Y L,Tang C,et al.VdCrz1 is involved in microsclerotia formation and required for full virulence in Verticillium dahliae[J].Fungal Genetics and Biology,2015,82:201-212.http://dx.doi.org/10.1016/j.fgb.2015.07.011
[28]Zhang W Q,Gui Y J,Short D P G,et al.Verticillium dahliae transcription factor VdFTF1 regulates the expression of multiple secreted virulence factors and is required for full virulence in cotton[J].Molecular Plant Pathology,2018,19(4):841-857.https://doi.org/10.1111/mpp.12569
[29]Wallace H M,Fraser A V,Hughes A.A perspective of polyamine metabolism[J].Biochemical Journal,2003,376(1):1-14.https://doi.org/10.1042/BJ20031327
[30]Casero J R A,Pegg A E.Polyamine catabolism and disease[J].Biochemical Journal,2009,421(3):323-338.https://doi.org/10.1042/BJ20090598
[31]Thomas T,Thomas T J.Polyamine metabolism and cancer[J].Journal of Cellular and Molecular Medicine,2003,2(7):113-126.https://doi.org/10.1111/j.1582-4934.2003.tb00210.x
[32]Schipper R G,Cuijpers V M J I,De Groot L H J M,et al.Intracellular localization of ornithine decarboxylase and its regulatory protein,antizyme-1[J].Journal of Histochemistry and Cytochemistry,2004,52(10):1259-1266.https://doi.org/10.1369/jhc.4C6389.2004
[33]蔡富强,王艳林.鸟氨酸脱羧酶抗酶Ⅰ与多胺代谢[J].生命科学,2011(10):1002-1008.https://doi.org/10.13376/j.cbls/2011.10.016Cai F Q,Wang Y L.Ornithine decarboxylase antizymeⅠand polyamine metabolism[J].Chinese Bulletin of Life Sciences,2011(10):1002-1008.
[34]Wang S,Xing H Y,Hua C L,et al.An improved single-step cloning strategy simplifies the Agrobacterium tumefaciens-mediated transformation(ATMT)-based gene-disruption method for Verticillium dahliae[J].Phytopathology,2016,106(6):645-652.https://doi.org/10.1094/PHYTO-10-15-0280-R
[35]Klimes A,Dobinson K F.A hydrophobin glved in microsclerotial developene,VDH1,is invoment and spore viability in the plant pathogen Verticillium dahliae[J].Fungal Genetics and Biology,2006,43(4):283-294.https://doi.org/10.1016/j.fgb.2005.12.006
[2]Schnathorst W C.Life cycle and epidemiology of verticillium.Fungal wilt diseases of plants[M].San Fransisco:Academic Press,1981:81-111.
[3]Hoppenau C E,Tran V,Kusch H,et al.Verticillium dahliae VdTHI4,involved in thiazole biosynthesis,stress response and DNA repair functions,is required for vascular disease induction in tomato[J].Environmental and Experimental Botany,2014,108:14-22.http://dx.doi.org/10.1016/j.envexpbot.2013.12.015
[4]Qi X L,Su X F,Guo H M,et al.VdThit,a thiamine transport protein,is required for pathogenicity of the vascular pathogen Verticillium dahliae[J].Molecular Plant Microbe Interactions,2016,29(7):545-559.http://dx.doi.org/10.1094/MPMI-03-16-0057-R
[5]Maruthachalam K,Klosterman S J,Kang S,et al.Identification of pathogenicity-related genes in the vascular wilt fungus Verticillium dahliae by Agrobacterium tumefaciens-mediated T-DNAinsertional mutagenesis[J].Molecular Biotechnology,2011,49(3):209-221.https://doi.org/10.1007/s12033-011-9392-8
[6]Zhao Y L,Zhou T T,Guo H S.Hyphopodium-specific VdNoxB/VdPls1-dependent ROS-Ca2+signaling is required for plant infection by Verticillium dahliae[J/OL].PLoS Pathogens,2016,12(7):e1005793.https://doi.org/10.1371/journal.ppat.1005793
[7]Li Z F,Liu Y J,Feng Z L,et al.VdCYC8,encoding CYC8 glucose repression mediator protein,is required for microsclerotia formation and full virulence in Verticillium dahliae[J/OL].PLoSONE,2015,10(12):e0144020.https://doi.org/10.1371/journal.pone.0144020
[8]Gao F,Zhou B J,Li G Y,et al.A glutamic acid-rich protein identified in Verticillium dahliae from an insertional mutagenesis affects microsclerotial formation and pathogenicity[J/OL].PLoSONE,2010,5(12):e15319.https://doi.org/10.1371/journal.pone.0015319
[9]Tzima A K,Paplomatas E J,Rauyaree P,et al.VdSNF1,the sucrose nonfermenting protein kinase gene of Verticillium dahliae,is required for virulence and expression of genes involved in cell-wall degradation[J].Molecular Plant Microbe Interactions,2011,24(1):129-142.https://doi.org/10.1094/MPMI-09-09-0217
[10]Zhang Y L,Mao J C,Huang J F,et al.A uracil-DNA glycosylase functions in spore development and pathogenicity of Verticillium dahliae[J].Physiological and Molecular Plant Pathology,2015,92:148-153.http://dx.doi.org/10.1016/j.pmpp.2015.05.001
[11]Jonge R D,Esse H P V,Maruthachalam K,et al.Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing[J].Proceedings of the National Academy of Sciences,2012,109(13):5110-5115.https://doi.org/10.1073/pnas.1119623109
[12]Liu T L,Song T Q,Zhang X,et al.Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis[J].Nature Communications,2014,5(1):4686.https://doi.org/10.1038/ncomms5686
[13]Santhanam P,Esse H P V,Albert I,et al.Evidence for functional diversification within a fungal NEP1-like protein family[J].Molecular Plant Microbe Interactions,2013,26(3):278-286.http://dx.doi.org/10.1094/MPMI-09-12-0222-R
[14]Zhou B J,Jia P S,Gao F,et al.Molecular characterization and functional analysis of a necrosis-and ethylene-inducing,protein-encoding gene family from Verticillium dahliae[J].Molecular Plant Microbe Interactions,2012,25(7):964-975.http://dx.doi.org/10.1094/MPMI-12-11-0319
[15]Gui Y J,Zhang W Q,Zhang D D,et al.A Verticillium dahliae extracellular cutinase modulates plant immune responses[J].Molecular Plant Microbe Interactions,2018,31(2):260-273.https://doi.org/10.1094/MPMI-06-17-0136-R
[16]Rauyaree P,Ospina-Giraldo M D,Kang S,et al.Mutations in VMK1,a mitogen-activated protein kinase gene,affect microsclerotia formation and pathogenicity in Verticillium dahliae[J].Current Genetics,2005,48(2):109-116.http://dx.doi.org/10.1007/s00294-005-0586-0.
[17]Tian L L,Xu J,Zhou L,et al.VdMsb regulates virulence and microsclerotia production in the fungal plant pathogen Verticillium dahliae[J].Gene,2014,550(2):238-244.http://dx.doi.org/10.1016/j.gene.2014.08.035
[18]Wang Y L,Tian L Y,Xiong D G,et al.The mitogen-activated protein kinase gene,VdHog1,regulates osmotic stress response,microsclerotia formation and virulence in Verticillium dahliae[J].Fungal Genetics and Biology,2016,88:13-23.http://dx.doi.org/10.1016/j.fgb.2016.01.011
[19]Qi X Y,Zhou S,Shang X G,et al.VdSho1 regulates growth,oxidant adaptation and virulence in Verticillium dahliae[J].Journal of Phytopathology,2016,164(11-12):1064-1074.https://doi.org/10.1111/jph.12527
[20]Tzima A,Paplomatas E J,Rauyaree P,et al.Roles of the catalytic subunit of c AMP-dependent protein kinase A in virulence and development of the soilborne plant pathogen Verticillium dahliae[J].Fungal Genetics and Biology,2010,47(5):406-415.https://doi.org/10.1016/j.fgb.2010.01.007
[21]Tzima A K,Paplomatas E J,Tsitsigiannis D I,et al.The G proteinβsubunit controls virulence and multiple growth-and development-related traits in Verticillium dahliae[J].Fungal Genetics and Biology,2012,49(4):271-283.https://doi.org/10.1016/j.fgb.2012.02.005
[22]Zhang T,Zhang B S,Hua C L,et al.VdPKS1 is required for melanin formation and virulence in a cotton wilt pathogen Verticillium dahliae[J].Science China Life Sciences,2017,60(8):868-879.https://doi.org/10.1007/s11427-017-9075-3
[23]Santhanam P,Thomma B P H J.Verticillium dahliae Sge1 differentially regulates expression of candidate effector genes[J].Molecular Plant Microbe Interactions,2013,26(2):249-256.http://dx.doi.org/10.1094/MPMI-08-12-0198-R
[24]高云,孟佩,张婷,等.棉花黄萎病菌VdSge1基因的敲除与功能分析[J].棉花学报,2015,27(4):346-353.https://doi.org/10.11963/issn.1002-7807.201504007Gao Y,Meng P,Zhang T,et al.Knockout and functional analysis of VdSge1 in Verticillium dahliae[J].Cotton Science,2015,27(4):346-353.
[25]Luo X M,Mao H Q,Wei Y M,et al.The fungal-specific transcription factor Vdpf influences conidia production,melanized microsclerotia formation and pathogenicity in Verticillium dahliae[J].Molecular Plant Pathology,2016,17(9):1364-1381.https://doi.org/10.1111/mpp.12367
[26]Xiong D G,Wang Y L,Tian L Y,et al.MADS-Box transcription factor VdMcm1 regulates conidiation,microsclerotia formation,pathogenicity,and secondary metabolism of Verticillium dahliae[J].Frontiers in Microbiology,2016,7:1192.https://doi.org/10.3389/fmicb.2016.01192
[27]Xiong D G,Wang Y L,Tang C,et al.VdCrz1 is involved in microsclerotia formation and required for full virulence in Verticillium dahliae[J].Fungal Genetics and Biology,2015,82:201-212.http://dx.doi.org/10.1016/j.fgb.2015.07.011
[28]Zhang W Q,Gui Y J,Short D P G,et al.Verticillium dahliae transcription factor VdFTF1 regulates the expression of multiple secreted virulence factors and is required for full virulence in cotton[J].Molecular Plant Pathology,2018,19(4):841-857.https://doi.org/10.1111/mpp.12569
[29]Wallace H M,Fraser A V,Hughes A.A perspective of polyamine metabolism[J].Biochemical Journal,2003,376(1):1-14.https://doi.org/10.1042/BJ20031327
[30]Casero J R A,Pegg A E.Polyamine catabolism and disease[J].Biochemical Journal,2009,421(3):323-338.https://doi.org/10.1042/BJ20090598
[31]Thomas T,Thomas T J.Polyamine metabolism and cancer[J].Journal of Cellular and Molecular Medicine,2003,2(7):113-126.https://doi.org/10.1111/j.1582-4934.2003.tb00210.x
[32]Schipper R G,Cuijpers V M J I,De Groot L H J M,et al.Intracellular localization of ornithine decarboxylase and its regulatory protein,antizyme-1[J].Journal of Histochemistry and Cytochemistry,2004,52(10):1259-1266.https://doi.org/10.1369/jhc.4C6389.2004
[33]蔡富强,王艳林.鸟氨酸脱羧酶抗酶Ⅰ与多胺代谢[J].生命科学,2011(10):1002-1008.https://doi.org/10.13376/j.cbls/2011.10.016Cai F Q,Wang Y L.Ornithine decarboxylase antizymeⅠand polyamine metabolism[J].Chinese Bulletin of Life Sciences,2011(10):1002-1008.
[34]Wang S,Xing H Y,Hua C L,et al.An improved single-step cloning strategy simplifies the Agrobacterium tumefaciens-mediated transformation(ATMT)-based gene-disruption method for Verticillium dahliae[J].Phytopathology,2016,106(6):645-652.https://doi.org/10.1094/PHYTO-10-15-0280-R
[35]Klimes A,Dobinson K F.A hydrophobin glved in microsclerotial developene,VDH1,is invoment and spore viability in the plant pathogen Verticillium dahliae[J].Fungal Genetics and Biology,2006,43(4):283-294.https://doi.org/10.1016/j.fgb.2005.12.006