丛枝菌根共生体磷信号转运受体的发现及其分子机制的研究
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摘要
丛枝菌根是球囊菌门的从枝菌根真菌与高等维管束植物根系建立的互惠共生体,丛枝菌根是自然界中分布最为广泛的共生体,80%以上的陆生维管束植物能与菌根真菌形成植物内共生体。丛枝菌根真菌为宿主植物提供无机矿质营养,主要是磷素与氮素,促进植物的生长和矿质营养的吸收利用。反过来,植物通过光合作用为AM真菌提供碳源,使其菌丝正常生长发育并完全成生适史。AM真菌介导的磷吸收途径第一步是靠真菌细胞膜上Pi转运蛋白将土壤中的无机磷酸盐转运到根外菌丝中,在真菌与植物的共生界面又依靠AM特异性的植物Pi转运蛋白将质外体空间的游离态磷酸盐转运到皮层细胞。然而到目前为止,这些代谢途径中的许多科学问题还没有完全被理解,甚至对有些问题尚不清楚。Pi作为营养物质被AM菌根途径吸收转运,同时Pi又作为一种信号来调控AM共生体系的建立与发育,Pi信号调控AM共生体系的分子机理还是不明确。
在本文中,以AM真菌Gigaspora margarita和紫云英(Astragalua sinicus)为材料,通过分子生物学,生物化学,反向遗传学,细胞生物学以及生理学等方法详细深入探讨了AM共生体系中磷转运基因的功能及其作用的分子机制。
1.发现了G margarita (BEG34)中存在一个高亲和力磷转运系统,分离出该系统关键调控基因GigmPT,属于高亲和力无机磷酸盐转运基因。GigmPT是MFS超家族转运体,编码一个膜整合蛋白,由12个疏水的跨膜结构域组成,包括6个N端的跨膜区与6个C端的跨膜区,第六个和第七个跨膜区之间存在一个大中央亲水环,氨基酸N端和c端均在细胞质侧。在AM真菌中调控一个类似酵母PHO调控系统的途径。从A. sinicus中分离到类似的AM特异性AsPT1与AsPT4磷转运蛋白,调控AM共生界面磷转运。
2.分离到的这些磷转运基因在共生时期诱导表达,尤其是在丛枝细胞中大量表达,同时受Pi抑制表达。宿主根组织碳源能够激发GigmPT基因的表达,GigmPT基因的活性同样影响着AM共生体的碳转运。
3.反向遗传学研究结果表明GigmPT是AM共生体系的必需基因,GigmPT的功能直接影响AM真菌G margarita菌丝以及丛枝的生长与发育,维持真菌在植物体内持续生长是必不可少的。该基因失活后阻断共生Pi转运,且在丛枝细胞积累大量多聚磷酸盐。
4.利用生物化学方法研究该基因发现其还具有受体功能,即是一个转运受体,调控PKA信号途径；利用SCAM与突变分析找到了转运受体GigmPT的磷酸盐结合位点,并发现该转运体利用同一个位点进行转运与信号识别。转运受体GigmPT的信号激活需要发生特异的构象变化。
5.研究还发现在AM共生体中存在第二类AM特异性磷转运基因AsPT1,与第一类AsPT4基因一起非冗余性调节AM共生体系,尤其调节丛枝的发育。还发现AsPT4对AM途径磷转运起主要作用,而AsPT1不是共生磷转运必须基因,可能编码一个非转运型转运受体,调控丛枝界面Pi与营养代谢平衡。研究还发现AsPT4在非公生时期植物根尖以及分生组织中表达,在共生时期却只在含丛枝的细胞中表达,该基因调节侧根生长发育。
6.通过本文研究,得出一个重要的假说：在AM共生体系中存在一类磷素营养转运受体,同时调控PHO与PKA途径,对AM共生体的磷代谢与营养平衡起至关重要的作用。推测在AM共生体中这是一个普遍规律,绝大多数营养转运子(包括C,N和P等)可能都获得了受体功能,起着信号转导功能,调节AM真菌在植物体内正常生长发育。还提出了传统的化学信号受体最早是由营养转运体进化而来的模型。
The majority vascular plants are able to form symbiotic associations with arbuscular mycorrhizal fungi. The symbiosis, termed arbuscular mycorrhiza is a reciprocal symbiosis, improving plant uptake of phosphate. The more than80%of land plants form AM interactions, in which plants supply associatedAM fungi with carbohydrates, essential for fungalsurvival and growth. In exchange, AMfungi provide their host plants with mineral nutrients, phosphorus (P), nitrogen(N)and other benefits. The first step of the fungus-mediated uptake is carried out by fungal membrane Pi transporters (PT) that transfer Pi from the soil into the extraradical hyphae, then the AM-specific Pi transporters transport the phosphate from the apoplastic space to plant cell.,So far, however, the Pi metabolic pathway of AM fungi are still not fully understood. Pi as a signal to permit continued development of theAM symbiosis, however, the mechanisms involved in signaling are poorly understood.
To characterize the detailfunctions of Pi transporters in AM symbiosis, we combined cellular localization, heterologous functional expression in yeast with expression/subcellular localization studies and reverse genetics approaches in planta.
l.Here we report the cloning and the functional analysis of a gene encoding a phosphate transporter (GigmPT) from the arbuscular mycorrhizal fungus Gigaspora margarita during mycorrhizal association with Astragalua sinicus roots. The kinetic analysis of GigmPT reveals that it belongs to high affinity phosphate transporter family. The GigmPT polypeptide belongs to the major facilitator superfamily (MFS). Homology modeling reveals that GigmPT exhibits twelve transmembrane helices divided into two halves connected by a large hydrophilic loop in the middle.
2.GigmPT, a fungal Pi transporter highlyinduced during AM symbiosis. GigmPT is expressed in arbuscules and intercellular hyphae. These analyses show that GigmPT expression is regulated in response to external Pi concentrations. Phosphate concentrations, typical of those found in the soil solution, result in expression of GigmPT. Carbon availability triggers fungal phosphate uptake andtransport in AM symbiosis.
3.We show that GigmPTis essential for the acquisition of Pidelivered by the AM fungus. However, more significantly, GigmPT function is critical for AM symbiosis. Loss of GigmPT function leadsto premature death of the arbuscules; the fungus is unable toproliferate within the root, and symbiosis is terminated. Thus, Pitransport is also a requirementfor the AM symbiosis.
4. The GigmPTphosphate transceptor transports phosphate and mediatesrapid phosphate activation of the protein kinase A (PKA) pathway.Using Substituted CysteineAccessibility Method (SCAM) we identified A146in TMDIV and V357in TMD VIII as residues exposed with their side chaininto the phosphate-binding site of GigmPT. Our results provide to the best of our knowledge the first insightinto the molecular mechanism of a phosphate transceptor.
5. There also exists a second AM-specific Pi-transporter AsPT1indispensable for the development of AM symbiosis indicots. Knockdown of AsPTl by RNA interferenceled to degenerating or dead arbuscule phenotypesidentical to that of;AsPT4silencing lines. Nonredundant regulation of A. sinicusAM. symbiosis byAsPT1and AsPT4. AsPT4but not AsPTl is necessary and sufficient to mediatesymbiotic Pi transfer.
6.These results substantiatethe hypothesis that phosphate transporteracts as the main provider of phosphate to the cell, but alsomediates rapid activation of thePKApathway. The nutrientsensers haveevolved from nutrient transporters andthus provide further support for the proposed evolutionaryscheme from nutrient transporters to chemicalsignal receptors.
在本文中,以AM真菌Gigaspora margarita和紫云英(Astragalua sinicus)为材料,通过分子生物学,生物化学,反向遗传学,细胞生物学以及生理学等方法详细深入探讨了AM共生体系中磷转运基因的功能及其作用的分子机制。
1.发现了G margarita (BEG34)中存在一个高亲和力磷转运系统,分离出该系统关键调控基因GigmPT,属于高亲和力无机磷酸盐转运基因。GigmPT是MFS超家族转运体,编码一个膜整合蛋白,由12个疏水的跨膜结构域组成,包括6个N端的跨膜区与6个C端的跨膜区,第六个和第七个跨膜区之间存在一个大中央亲水环,氨基酸N端和c端均在细胞质侧。在AM真菌中调控一个类似酵母PHO调控系统的途径。从A. sinicus中分离到类似的AM特异性AsPT1与AsPT4磷转运蛋白,调控AM共生界面磷转运。
2.分离到的这些磷转运基因在共生时期诱导表达,尤其是在丛枝细胞中大量表达,同时受Pi抑制表达。宿主根组织碳源能够激发GigmPT基因的表达,GigmPT基因的活性同样影响着AM共生体的碳转运。
3.反向遗传学研究结果表明GigmPT是AM共生体系的必需基因,GigmPT的功能直接影响AM真菌G margarita菌丝以及丛枝的生长与发育,维持真菌在植物体内持续生长是必不可少的。该基因失活后阻断共生Pi转运,且在丛枝细胞积累大量多聚磷酸盐。
4.利用生物化学方法研究该基因发现其还具有受体功能,即是一个转运受体,调控PKA信号途径；利用SCAM与突变分析找到了转运受体GigmPT的磷酸盐结合位点,并发现该转运体利用同一个位点进行转运与信号识别。转运受体GigmPT的信号激活需要发生特异的构象变化。
5.研究还发现在AM共生体中存在第二类AM特异性磷转运基因AsPT1,与第一类AsPT4基因一起非冗余性调节AM共生体系,尤其调节丛枝的发育。还发现AsPT4对AM途径磷转运起主要作用,而AsPT1不是共生磷转运必须基因,可能编码一个非转运型转运受体,调控丛枝界面Pi与营养代谢平衡。研究还发现AsPT4在非公生时期植物根尖以及分生组织中表达,在共生时期却只在含丛枝的细胞中表达,该基因调节侧根生长发育。
6.通过本文研究,得出一个重要的假说：在AM共生体系中存在一类磷素营养转运受体,同时调控PHO与PKA途径,对AM共生体的磷代谢与营养平衡起至关重要的作用。推测在AM共生体中这是一个普遍规律,绝大多数营养转运子(包括C,N和P等)可能都获得了受体功能,起着信号转导功能,调节AM真菌在植物体内正常生长发育。还提出了传统的化学信号受体最早是由营养转运体进化而来的模型。
The majority vascular plants are able to form symbiotic associations with arbuscular mycorrhizal fungi. The symbiosis, termed arbuscular mycorrhiza is a reciprocal symbiosis, improving plant uptake of phosphate. The more than80%of land plants form AM interactions, in which plants supply associatedAM fungi with carbohydrates, essential for fungalsurvival and growth. In exchange, AMfungi provide their host plants with mineral nutrients, phosphorus (P), nitrogen(N)and other benefits. The first step of the fungus-mediated uptake is carried out by fungal membrane Pi transporters (PT) that transfer Pi from the soil into the extraradical hyphae, then the AM-specific Pi transporters transport the phosphate from the apoplastic space to plant cell.,So far, however, the Pi metabolic pathway of AM fungi are still not fully understood. Pi as a signal to permit continued development of theAM symbiosis, however, the mechanisms involved in signaling are poorly understood.
To characterize the detailfunctions of Pi transporters in AM symbiosis, we combined cellular localization, heterologous functional expression in yeast with expression/subcellular localization studies and reverse genetics approaches in planta.
l.Here we report the cloning and the functional analysis of a gene encoding a phosphate transporter (GigmPT) from the arbuscular mycorrhizal fungus Gigaspora margarita during mycorrhizal association with Astragalua sinicus roots. The kinetic analysis of GigmPT reveals that it belongs to high affinity phosphate transporter family. The GigmPT polypeptide belongs to the major facilitator superfamily (MFS). Homology modeling reveals that GigmPT exhibits twelve transmembrane helices divided into two halves connected by a large hydrophilic loop in the middle.
2.GigmPT, a fungal Pi transporter highlyinduced during AM symbiosis. GigmPT is expressed in arbuscules and intercellular hyphae. These analyses show that GigmPT expression is regulated in response to external Pi concentrations. Phosphate concentrations, typical of those found in the soil solution, result in expression of GigmPT. Carbon availability triggers fungal phosphate uptake andtransport in AM symbiosis.
3.We show that GigmPTis essential for the acquisition of Pidelivered by the AM fungus. However, more significantly, GigmPT function is critical for AM symbiosis. Loss of GigmPT function leadsto premature death of the arbuscules; the fungus is unable toproliferate within the root, and symbiosis is terminated. Thus, Pitransport is also a requirementfor the AM symbiosis.
4. The GigmPTphosphate transceptor transports phosphate and mediatesrapid phosphate activation of the protein kinase A (PKA) pathway.Using Substituted CysteineAccessibility Method (SCAM) we identified A146in TMDIV and V357in TMD VIII as residues exposed with their side chaininto the phosphate-binding site of GigmPT. Our results provide to the best of our knowledge the first insightinto the molecular mechanism of a phosphate transceptor.
5. There also exists a second AM-specific Pi-transporter AsPT1indispensable for the development of AM symbiosis indicots. Knockdown of AsPTl by RNA interferenceled to degenerating or dead arbuscule phenotypesidentical to that of;AsPT4silencing lines. Nonredundant regulation of A. sinicusAM. symbiosis byAsPT1and AsPT4. AsPT4but not AsPTl is necessary and sufficient to mediatesymbiotic Pi transfer.
6.These results substantiatethe hypothesis that phosphate transporteracts as the main provider of phosphate to the cell, but alsomediates rapid activation of thePKApathway. The nutrientsensers haveevolved from nutrient transporters andthus provide further support for the proposed evolutionaryscheme from nutrient transporters to chemicalsignal receptors.
引文
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