稻瘟病菌V-ATPase c’亚基Movmall和六个SNARE蛋白的功能分析
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摘要
稻瘟病菌引起的水稻稻瘟病对世界的水稻产量危害极大。由于稻瘟病菌及其宿主水稻的基因组已测序完成,同时结合不断涌现的新技术,稻瘟病菌-水稻互作系统已成为病原菌-宿主植物病害研究的模式系统。定位于质膜或细胞器上的膜蛋白参与生物体的众多重要的功能。对于膜蛋白的进一步研究,可以完善稻瘟病菌致病机制的阐释。本文主要对Monyv1等六个SNARE蛋白和V-ATPase c'亚基在稻瘟病菌病害循环中的作用进行了系统的分析。
液泡的许多功能依赖于液泡ATP酶(V-ATPase)的活性,从而使液泡有一个酸性的腔内环境,并提供驱动大量离子和代谢物穿梭于液泡膜的动力。亚细胞定位和Quinacrine染色表明在稻瘟病菌侵染发育过程中,V-ATPase的V1V0部分被完全组装而且液泡腔呈酸性。V-ATPase c'亚基Movma11功能的缺失干扰了液泡的酸性反应,并引起贫乏菌落表型、抑制的无性及有性繁殖、选择性的碳源利用,和提高的钙及重金属的敏感性等类似于酵母V-ATPase突变体的Vma-表型；但未表现出pH碱性环境条件致死。MoVMA11缺失突变体形成的气生菌丝纠缠于一起,形成异常粗厚的纤维状结构。结果还指出MoVMA11参与细胞壁完整性和附着胞形成的调控。ΔMovma11突变体菌丝尖端在洋葱细胞表面形成大量未黑色素化的膨大结构,以及稀少的不具穿透能力的缩小的附着胞。另外,MoVMA11缺失突变体还丧失了对完整和损伤宿主叶片的侵染能力。和其它真菌VMA基因的功能分析一致,我们的研究数据指出MoVMA11参与众多细胞功能的调控。
作为膜融合过程重要元件的SNARE蛋白,在真核生物的生长发育过程中发挥着关键的作用。我们敲除并分析了稻瘟病菌SNARE基因家族中的MoNYV1, MoTOM, MoSNC, MoSSO2, MoTLG2和MoSYN8等六个成员基因。MoNYV1和MoTOM基因缺失突变体在生长发育及致病性等方面和野生菌株无明显的差异。MoSNC等其它四个基因参与稻瘟病菌的菌丝生长、分生孢子和附着胞形成等过程,其中MoTLG2和MoSYN8还参与致病过程的调控。AMotlg2突变体分生孢子形态、附着胞大小及侵染菌丝发育能力都较Guy11减小。我们同时发现,MoSYN8还和细胞壁完整性相关,外源糖类高渗环境能很大程度上恢复该基因缺失突变体的生长。ΔMosyn8突变体附着胞还表现出与黑色素层相关的细胞壁孔隙变小,膨压上升等表型。此外,由于MoSYN8缺失后附着胞穿透能力的严重下降,ΔMosyn8突变体的宿主致病性显著降低。植物叶片的擦伤或高浓度山梨醇的添加能轻微互补MoSYN8缺失突变体的致病能力。
综上所述,V-ATPase是稻瘟病菌侵染相关发育和致病性所必需的；同时,MoSNC, MoSSO2, MoTLG2和MoSYN8这四个膜融合相关SNARE基因在稻瘟病菌生长、分生孢子及附着胞发育过程中具有重要的调控作用。
Rice blast, caused by Magnaporthe oryzae, is one of the most serious rice diseases that cause substantial cultured crop losses worldwide. Genomic sequence availability and genetic tractability of both M. oryzae and rice, combined with multiple analytical tools, make them a model plant pathosystem for fungus-plant interaction research. Membrane associated proteins contribute to the growth and development of organisms. Further research in membrane associated proteins will provide novel insights into the molecular mechanism of pathogenicity for M. oryzae. In this study, V-ATPase c' subunit Movma11and six SNARE proteins were identified and characterized in this model phytopathogenic fungus.
Many functions of vacuole depend on the activity of vacuolar ATPase to maintain an acidic lumen and create the driving forces for massive fluxes of ions and metabolites through vacuolar membrane. Subcellular colocalization and quinacrine staining suggested that the V1Vo domains of V-ATPase were fully assembled and the vacuoles were kept acidic during infection-related developments in M. oryzae. Targeted gene disruption of MoVMA11gene, encoding the putative c'subunit of V-ATPase, impaired vacuolar acidification and mimicked the phenotypes of yeast V-ATPase mutants in the poor colony morphology, abolished asexual and sexual reproductions, selective carbon source utilization, and increased calcium and heavy metals sensitivities, however, not typical pH conditional lethality. Strikingly, aerial hyphae of MoVMA11null mutant intertwined with each other to form extremely thick filamentous structures. The results also implicated MoVMA11involving in cell wall integrity and appressorium formation. Abundant non-melanized swollen structures and rare, small appressoria without penetration ability were produced at the hyphal tips of ΔMovma11mutant on onion epidermal cells. Finally, MoVMA11null mutant lost pathogenicity on both intact and wounded host leaves. Our data indicated that MoVMA11, like other fungal VMA genes, is associated with numerous cellular functions.
Soluble N-ethylmaleimide-sensitive factor attached protein receptor (SNARE) proteins are implicated in many eukaryotic cellular processes during growth and development. In this report, we characterized six members of the SNARE repertoire in M. oryzae, which we designated MoNYV1, MoTOM, MoSNC, MoSSO2, MoTLG2and MoSYN8. Functional analyses revealed that MoNYV1and MoTOM null mutants were indistinguishable from wild-type strain in phenotypes, while MoTOM, MoSNC, MoSSO2, MoTLG2and MoSYN8were involved in mycelial growth, conidiogenesis, and appressorial morphogenesis. Compared with Guy11, ΔMotlg2mutant showed reduced sizes of conidia and appressoria, as well as invasive growth ability. Our findings also indicated a role for MoSYN8in the maintenance of cell wall integrity, and carbohydrate osmotic solutions, to a large extent, complemented the growth defect of ΔMosyn8mutant. Appressoria of ΔMosyn8mutant exhibited higher turgor pressure and decreased cell wall porosity, which was closely related to the melanin layer. In addition, discruption of MoSYN8severely impaired appressorial penetration ability and pathogenicity of M. oryzae, but the pathogenicity defect could be slightly restored when leaves were abraded or supplemented with1M sorbitol.
In summary, our results demonstrate that MoSNC, MoSSO2, MoTLG2and MoSYN8play an important role in mycelial growth, conidial and appressorial development, and highlight the significance of V-ATPase function for infection-related morphogenesis and pathogenesis in M. oryzae.
液泡的许多功能依赖于液泡ATP酶(V-ATPase)的活性,从而使液泡有一个酸性的腔内环境,并提供驱动大量离子和代谢物穿梭于液泡膜的动力。亚细胞定位和Quinacrine染色表明在稻瘟病菌侵染发育过程中,V-ATPase的V1V0部分被完全组装而且液泡腔呈酸性。V-ATPase c'亚基Movma11功能的缺失干扰了液泡的酸性反应,并引起贫乏菌落表型、抑制的无性及有性繁殖、选择性的碳源利用,和提高的钙及重金属的敏感性等类似于酵母V-ATPase突变体的Vma-表型；但未表现出pH碱性环境条件致死。MoVMA11缺失突变体形成的气生菌丝纠缠于一起,形成异常粗厚的纤维状结构。结果还指出MoVMA11参与细胞壁完整性和附着胞形成的调控。ΔMovma11突变体菌丝尖端在洋葱细胞表面形成大量未黑色素化的膨大结构,以及稀少的不具穿透能力的缩小的附着胞。另外,MoVMA11缺失突变体还丧失了对完整和损伤宿主叶片的侵染能力。和其它真菌VMA基因的功能分析一致,我们的研究数据指出MoVMA11参与众多细胞功能的调控。
作为膜融合过程重要元件的SNARE蛋白,在真核生物的生长发育过程中发挥着关键的作用。我们敲除并分析了稻瘟病菌SNARE基因家族中的MoNYV1, MoTOM, MoSNC, MoSSO2, MoTLG2和MoSYN8等六个成员基因。MoNYV1和MoTOM基因缺失突变体在生长发育及致病性等方面和野生菌株无明显的差异。MoSNC等其它四个基因参与稻瘟病菌的菌丝生长、分生孢子和附着胞形成等过程,其中MoTLG2和MoSYN8还参与致病过程的调控。AMotlg2突变体分生孢子形态、附着胞大小及侵染菌丝发育能力都较Guy11减小。我们同时发现,MoSYN8还和细胞壁完整性相关,外源糖类高渗环境能很大程度上恢复该基因缺失突变体的生长。ΔMosyn8突变体附着胞还表现出与黑色素层相关的细胞壁孔隙变小,膨压上升等表型。此外,由于MoSYN8缺失后附着胞穿透能力的严重下降,ΔMosyn8突变体的宿主致病性显著降低。植物叶片的擦伤或高浓度山梨醇的添加能轻微互补MoSYN8缺失突变体的致病能力。
综上所述,V-ATPase是稻瘟病菌侵染相关发育和致病性所必需的；同时,MoSNC, MoSSO2, MoTLG2和MoSYN8这四个膜融合相关SNARE基因在稻瘟病菌生长、分生孢子及附着胞发育过程中具有重要的调控作用。
Rice blast, caused by Magnaporthe oryzae, is one of the most serious rice diseases that cause substantial cultured crop losses worldwide. Genomic sequence availability and genetic tractability of both M. oryzae and rice, combined with multiple analytical tools, make them a model plant pathosystem for fungus-plant interaction research. Membrane associated proteins contribute to the growth and development of organisms. Further research in membrane associated proteins will provide novel insights into the molecular mechanism of pathogenicity for M. oryzae. In this study, V-ATPase c' subunit Movma11and six SNARE proteins were identified and characterized in this model phytopathogenic fungus.
Many functions of vacuole depend on the activity of vacuolar ATPase to maintain an acidic lumen and create the driving forces for massive fluxes of ions and metabolites through vacuolar membrane. Subcellular colocalization and quinacrine staining suggested that the V1Vo domains of V-ATPase were fully assembled and the vacuoles were kept acidic during infection-related developments in M. oryzae. Targeted gene disruption of MoVMA11gene, encoding the putative c'subunit of V-ATPase, impaired vacuolar acidification and mimicked the phenotypes of yeast V-ATPase mutants in the poor colony morphology, abolished asexual and sexual reproductions, selective carbon source utilization, and increased calcium and heavy metals sensitivities, however, not typical pH conditional lethality. Strikingly, aerial hyphae of MoVMA11null mutant intertwined with each other to form extremely thick filamentous structures. The results also implicated MoVMA11involving in cell wall integrity and appressorium formation. Abundant non-melanized swollen structures and rare, small appressoria without penetration ability were produced at the hyphal tips of ΔMovma11mutant on onion epidermal cells. Finally, MoVMA11null mutant lost pathogenicity on both intact and wounded host leaves. Our data indicated that MoVMA11, like other fungal VMA genes, is associated with numerous cellular functions.
Soluble N-ethylmaleimide-sensitive factor attached protein receptor (SNARE) proteins are implicated in many eukaryotic cellular processes during growth and development. In this report, we characterized six members of the SNARE repertoire in M. oryzae, which we designated MoNYV1, MoTOM, MoSNC, MoSSO2, MoTLG2and MoSYN8. Functional analyses revealed that MoNYV1and MoTOM null mutants were indistinguishable from wild-type strain in phenotypes, while MoTOM, MoSNC, MoSSO2, MoTLG2and MoSYN8were involved in mycelial growth, conidiogenesis, and appressorial morphogenesis. Compared with Guy11, ΔMotlg2mutant showed reduced sizes of conidia and appressoria, as well as invasive growth ability. Our findings also indicated a role for MoSYN8in the maintenance of cell wall integrity, and carbohydrate osmotic solutions, to a large extent, complemented the growth defect of ΔMosyn8mutant. Appressoria of ΔMosyn8mutant exhibited higher turgor pressure and decreased cell wall porosity, which was closely related to the melanin layer. In addition, discruption of MoSYN8severely impaired appressorial penetration ability and pathogenicity of M. oryzae, but the pathogenicity defect could be slightly restored when leaves were abraded or supplemented with1M sorbitol.
In summary, our results demonstrate that MoSNC, MoSSO2, MoTLG2and MoSYN8play an important role in mycelial growth, conidial and appressorial development, and highlight the significance of V-ATPase function for infection-related morphogenesis and pathogenesis in M. oryzae.
引文
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