小麦赤霉病菌麦角甾醇生物合成途径中关键基因的功能研究
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摘要
麦角甾醇是真菌细胞质膜的组分,在维持真菌细胞膜的流动性、完整性以及膜上的一些蛋白功能的正常行使等方面起到了非常重要的作用。麦角甾醇生物合成途径以乙酰辅酶A为原料,经过20多步的反应形成麦角甾醇。目前已成功开发出多种麦角甾醇生物合成抑制剂(以下简称为SBIs),在临床和农业生产上得到了广泛的应用。目前对于模式生物酿酒酵母中麦角甾醇生物合成途径的的研究报道较多,但是对丝状真菌中该合成途径的研究甚少。因此,研究小麦赤霉病菌中麦角甾醇途径各元件的功能对于进一步阐明SBIs的抗药机制以及发掘该途径上其它潜在的药剂靶标具有重要的理论和现实意义。
本研究通过基因敲除和互补的方法研究了小麦赤霉病菌麦角甾醇生物合成途径上21个ERG基因的生物学功能,并对该菌中麦角甾醇合成途径的调控元件进行了初步探索,结果发现：
1、编码甾醇14-α脱甲基酶(DMI类杀菌剂的作用靶标)的3个同源的cyp51基因都并非小麦赤霉病菌生长和麦角甾醇生物合成所必需。敲除突变体对7种DMI类杀菌剂敏感性水平与野生型菌株相比不一,cyp51A基因敲除突变体对7种DMI类杀菌剂都变敏感；cyp51B基因敲除突变体对7种DMI类杀菌剂的敏感性没有显著变化；cyp51C基因敲除突变体对部分DMI类杀菌剂变敏感。将戊唑醇和三唑酮进行复配对防治小麦赤霉病表现出明显的增效作用。
2、编码甾醇C-14还原酶(胺类杀菌剂的作用靶标)的2个FgERG24基因和编码甾醇C-8异构酶(胺类杀菌剂的作用靶标)的FgERG2基因也都并非小麦赤霉病菌生长和麦角甾醇生物合成必需。FgERG24B基因介导小麦赤霉病菌对胺类杀菌剂的天然抗药性,该基因缺失后突变体对3种胺类杀菌剂的抗药性水平明显降低,FgERG24A和FgERG2基因敲除突变体对胺类杀菌剂的抗药性水平与野生型菌株相当。
3、编码甾醇C-24还原酶的FgERG4基因缺失并不致死,但敲除突变体与野生型菌株相比会发生一系列的表型变化：不能正常合成麦角甾醇、菌丝生长缓慢、分生孢子产量降低、分生孢子畸形且分隔数减少、在麦穗上的致病性显著降低、DON毒素合成量降低、对金属离子和细胞渗透及氧化压力变得敏感和对SBIs抗药性水平上升。
4、麦角甾醇生物合成途径中角鲨烯下游的其它的14个ERG基因有8个敲除可能致死,推测对小麦赤霉病菌的生长非常重要。还有6个ERG基因获得了敲除突变体,但表型测定结果显示与野生型菌株没有明显的差异。
5、根据酿酒酵母、白色念珠菌和烟曲霉中关于麦角甾醇生物合成途径调控元件的相关研究报道,结合小麦赤霉赤霉病菌受DMI类药剂戊唑醇处理6h后的基因组表达谱数据,在小麦赤霉病菌基因组中找到了18个可能的麦角甾醇生物合成调控基因,其中仅有一个基因敲除可能致死,其他的17个基因都获得了敲除突变体。转录调控因子FgSTE12的敲除突变体在菌落形态、产孢等方面与野生型菌株相比没有显著差异,但是在麦穗上的致病力完全丧失；但是并未发现与DMI类杀菌剂的敏感性和cyp51基因或ERG基因的表达量水平相关的调控基因。
本研究结果表明1)小麦赤霉病菌对SBIs的抗药性机制与其他真菌有明显差异：不同的DMI药剂作用于不同的CYP51; FgErg24B调控小麦赤霉病菌对胺类杀菌剂的天然抗药性。2)小麦赤霉病菌麦角甾醇生物合成相关基因FgERG4参与小麦赤霉病菌的致病性、DON毒素合成和产孢等多种重要生理活动；8个敲除可能致死的ERG基因推测为小麦赤霉病菌生长必需的重要基因,它们可能成为潜在的杀菌剂新药靶。
Ergosterol is the major sterol component in fungal membranes and is involved in a variety of cellular functions, including cell fluidity, cell integrity and membrane-bound enzyme function. The important biochemical characteristics of ergosterol make the enzymes involved in its biosynthesis pathway attractive inhibition sites for antifungal agents. In fungi, ergosterol is synthesized from acetyl CoA through a complex pathway. The biosynthetic steps of ergosterol and the related enzymes have been well characterized in Saccharomyces cerevisiae. To date, very little information is available about the ergosterol pathway in filamentous fungi. Thus, it would be interesting to investigate functions of ergosterol biosynthesis genes in the important wheat pathogen Fusarium graminearum, which will be helpful in exploring novel drugs against this fungus.
In this study, we investigated functions of21ERG genes involved in the post-squalene pathway of ergosterol biosynthesis in F. graminearum using a gene deletion and complementation strategy. Results of our study included five major points:
1. Disruption mutants of three paralogous cyp51genes (cyp51A,-B, and-C) encoding sterol14-a demethylases were morphologically indistinguishable from the parent isolate on potato dextrose agar medium, which indicates that none of these genes is essential for mycelial growth. The sensitivity of cyp51A deletion mutants to seven sterol demethylation inhibitor (DMI) fungicides increased significantly compared to the parent strain, while sensitivity of cyp51C deletion mutants increased to some but not all DMIs. No change in DMI sensitivity was observed for cyp51B deletion mutants. The sensitivity of F. graminearum and F. asiaticum isolates increased significantly when subjected in vitro to a mixture of DMI fungicides triadimefon and tebuconazole as compared to the individual components.
2. Disruption mutants of two paralogous FgERG24genes (FgERG24A and FgERG24B) did not show recognizable phenotypic changes in mycelial growth on potato dextrose agar or in virulence on wheat heads. HPLC analysis showed that the amount of ergosterol in FgERG24A or FgERG24B deletion mutants was not significantly different from that in the wild-type strain. These results indicate that neither of the two genes is essential for growth, pathogenicity or ergosterol biosynthesis in F. graminearum. FgERG24B deletion mutants exhibited significantly increased sensitivity to amine fungicides, including tridemorph, fenpropidin and spiroxamine, but not to non-amine fungicides. In contrast, FgERG24A deletion mutants did not show changed sensitivity to any amine tested.
3. FgERG4gene encoding sterol C-24reductase, which catalyzes for the conversion of ergosta-5,7,22,24(28)-tetraenol to ergosterol in the final step of ergosterol biosynthesis. The FgERG4deletion mutant failed to synthesize ergosterol and exhibited a significant decrease in mycelial growth and conidiation, and produced abnormal conidia. In addition, the mutant showed increased sensitivity to metal cations and to various cell stresses. Surprisingly, mycelia of the FgERG4deletion mutant exhibited increased resistance to cell wall degrading enzymes, also to various sterol biosynthesis inhibitors, which is consistent with the over-expression of several ERG genes in the mutant. The FgERG4deletion mutant was impaired dramatically in virulence and produced a significantly low level of DON.
4. Single deletion of other8ERG genes including ERG9, ERG1, ERG7, ERG25, ERG26, ERG27, ERG5B and NCP1B was lethal, which indicated that these8ERG genes could be important to fungal growth in F. graminearum; Other6ERG genes including ERG6A, ERG6B, ERG3A, ERG3B, ERG5A and NCP1A can be deleted, but their deletion mutant showed no recognizable phenotypic changes compared to wild type strain.
5. The regulatory mechanisms of ergosterol biosynthesis in F. graminearum were also investigated, functions of18possible regulatory genes including the sterol uptake control element (upc2) homologs, genes involved in sterol regulatory element binding protein (SREBP) pathway and tebuconazole responsive transcription factors from our DeepSAGE data were characterized. Deletion of only one of these18genes was lethal and other17genes were not required for fungal growth. Transciption factor FgSTE12was required for full virulence. Direct connection between deletion of the17genes and DMI resistance or ERG gene expression level change was not observed.
Results of our study indicate that1) Action and resistant mechanism of F. graminearum to SBIs may be different from yeasts and other filamentous fungi. Different DMI fungicides target different CYP51proteins in F. graminearum and that a mixture of DMI fungicides can result in synergistic effects; FgERG24B controls the intrinsic resistance of F. graminearum to amine fungicides.2) Genes involved in ergosterol biosynthesis including FgERG4and other8deletion lethal ERG genes are important fungal growth determinants in F. graminearum, they could become potential targets for the development of new antifungal compounds.
本研究通过基因敲除和互补的方法研究了小麦赤霉病菌麦角甾醇生物合成途径上21个ERG基因的生物学功能,并对该菌中麦角甾醇合成途径的调控元件进行了初步探索,结果发现：
1、编码甾醇14-α脱甲基酶(DMI类杀菌剂的作用靶标)的3个同源的cyp51基因都并非小麦赤霉病菌生长和麦角甾醇生物合成所必需。敲除突变体对7种DMI类杀菌剂敏感性水平与野生型菌株相比不一,cyp51A基因敲除突变体对7种DMI类杀菌剂都变敏感；cyp51B基因敲除突变体对7种DMI类杀菌剂的敏感性没有显著变化；cyp51C基因敲除突变体对部分DMI类杀菌剂变敏感。将戊唑醇和三唑酮进行复配对防治小麦赤霉病表现出明显的增效作用。
2、编码甾醇C-14还原酶(胺类杀菌剂的作用靶标)的2个FgERG24基因和编码甾醇C-8异构酶(胺类杀菌剂的作用靶标)的FgERG2基因也都并非小麦赤霉病菌生长和麦角甾醇生物合成必需。FgERG24B基因介导小麦赤霉病菌对胺类杀菌剂的天然抗药性,该基因缺失后突变体对3种胺类杀菌剂的抗药性水平明显降低,FgERG24A和FgERG2基因敲除突变体对胺类杀菌剂的抗药性水平与野生型菌株相当。
3、编码甾醇C-24还原酶的FgERG4基因缺失并不致死,但敲除突变体与野生型菌株相比会发生一系列的表型变化：不能正常合成麦角甾醇、菌丝生长缓慢、分生孢子产量降低、分生孢子畸形且分隔数减少、在麦穗上的致病性显著降低、DON毒素合成量降低、对金属离子和细胞渗透及氧化压力变得敏感和对SBIs抗药性水平上升。
4、麦角甾醇生物合成途径中角鲨烯下游的其它的14个ERG基因有8个敲除可能致死,推测对小麦赤霉病菌的生长非常重要。还有6个ERG基因获得了敲除突变体,但表型测定结果显示与野生型菌株没有明显的差异。
5、根据酿酒酵母、白色念珠菌和烟曲霉中关于麦角甾醇生物合成途径调控元件的相关研究报道,结合小麦赤霉赤霉病菌受DMI类药剂戊唑醇处理6h后的基因组表达谱数据,在小麦赤霉病菌基因组中找到了18个可能的麦角甾醇生物合成调控基因,其中仅有一个基因敲除可能致死,其他的17个基因都获得了敲除突变体。转录调控因子FgSTE12的敲除突变体在菌落形态、产孢等方面与野生型菌株相比没有显著差异,但是在麦穗上的致病力完全丧失；但是并未发现与DMI类杀菌剂的敏感性和cyp51基因或ERG基因的表达量水平相关的调控基因。
本研究结果表明1)小麦赤霉病菌对SBIs的抗药性机制与其他真菌有明显差异：不同的DMI药剂作用于不同的CYP51; FgErg24B调控小麦赤霉病菌对胺类杀菌剂的天然抗药性。2)小麦赤霉病菌麦角甾醇生物合成相关基因FgERG4参与小麦赤霉病菌的致病性、DON毒素合成和产孢等多种重要生理活动；8个敲除可能致死的ERG基因推测为小麦赤霉病菌生长必需的重要基因,它们可能成为潜在的杀菌剂新药靶。
Ergosterol is the major sterol component in fungal membranes and is involved in a variety of cellular functions, including cell fluidity, cell integrity and membrane-bound enzyme function. The important biochemical characteristics of ergosterol make the enzymes involved in its biosynthesis pathway attractive inhibition sites for antifungal agents. In fungi, ergosterol is synthesized from acetyl CoA through a complex pathway. The biosynthetic steps of ergosterol and the related enzymes have been well characterized in Saccharomyces cerevisiae. To date, very little information is available about the ergosterol pathway in filamentous fungi. Thus, it would be interesting to investigate functions of ergosterol biosynthesis genes in the important wheat pathogen Fusarium graminearum, which will be helpful in exploring novel drugs against this fungus.
In this study, we investigated functions of21ERG genes involved in the post-squalene pathway of ergosterol biosynthesis in F. graminearum using a gene deletion and complementation strategy. Results of our study included five major points:
1. Disruption mutants of three paralogous cyp51genes (cyp51A,-B, and-C) encoding sterol14-a demethylases were morphologically indistinguishable from the parent isolate on potato dextrose agar medium, which indicates that none of these genes is essential for mycelial growth. The sensitivity of cyp51A deletion mutants to seven sterol demethylation inhibitor (DMI) fungicides increased significantly compared to the parent strain, while sensitivity of cyp51C deletion mutants increased to some but not all DMIs. No change in DMI sensitivity was observed for cyp51B deletion mutants. The sensitivity of F. graminearum and F. asiaticum isolates increased significantly when subjected in vitro to a mixture of DMI fungicides triadimefon and tebuconazole as compared to the individual components.
2. Disruption mutants of two paralogous FgERG24genes (FgERG24A and FgERG24B) did not show recognizable phenotypic changes in mycelial growth on potato dextrose agar or in virulence on wheat heads. HPLC analysis showed that the amount of ergosterol in FgERG24A or FgERG24B deletion mutants was not significantly different from that in the wild-type strain. These results indicate that neither of the two genes is essential for growth, pathogenicity or ergosterol biosynthesis in F. graminearum. FgERG24B deletion mutants exhibited significantly increased sensitivity to amine fungicides, including tridemorph, fenpropidin and spiroxamine, but not to non-amine fungicides. In contrast, FgERG24A deletion mutants did not show changed sensitivity to any amine tested.
3. FgERG4gene encoding sterol C-24reductase, which catalyzes for the conversion of ergosta-5,7,22,24(28)-tetraenol to ergosterol in the final step of ergosterol biosynthesis. The FgERG4deletion mutant failed to synthesize ergosterol and exhibited a significant decrease in mycelial growth and conidiation, and produced abnormal conidia. In addition, the mutant showed increased sensitivity to metal cations and to various cell stresses. Surprisingly, mycelia of the FgERG4deletion mutant exhibited increased resistance to cell wall degrading enzymes, also to various sterol biosynthesis inhibitors, which is consistent with the over-expression of several ERG genes in the mutant. The FgERG4deletion mutant was impaired dramatically in virulence and produced a significantly low level of DON.
4. Single deletion of other8ERG genes including ERG9, ERG1, ERG7, ERG25, ERG26, ERG27, ERG5B and NCP1B was lethal, which indicated that these8ERG genes could be important to fungal growth in F. graminearum; Other6ERG genes including ERG6A, ERG6B, ERG3A, ERG3B, ERG5A and NCP1A can be deleted, but their deletion mutant showed no recognizable phenotypic changes compared to wild type strain.
5. The regulatory mechanisms of ergosterol biosynthesis in F. graminearum were also investigated, functions of18possible regulatory genes including the sterol uptake control element (upc2) homologs, genes involved in sterol regulatory element binding protein (SREBP) pathway and tebuconazole responsive transcription factors from our DeepSAGE data were characterized. Deletion of only one of these18genes was lethal and other17genes were not required for fungal growth. Transciption factor FgSTE12was required for full virulence. Direct connection between deletion of the17genes and DMI resistance or ERG gene expression level change was not observed.
Results of our study indicate that1) Action and resistant mechanism of F. graminearum to SBIs may be different from yeasts and other filamentous fungi. Different DMI fungicides target different CYP51proteins in F. graminearum and that a mixture of DMI fungicides can result in synergistic effects; FgERG24B controls the intrinsic resistance of F. graminearum to amine fungicides.2) Genes involved in ergosterol biosynthesis including FgERG4and other8deletion lethal ERG genes are important fungal growth determinants in F. graminearum, they could become potential targets for the development of new antifungal compounds.
引文
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