微生物学报

Functional stage	Key mechanism	Molecular mechanism & regulation	References
Mineralization of inorganic phosphorus	Secretion of low molecular weight organic acids (LMWOAs)	Electrostatic/covalent interactions	[26]
Proton (H⁺) release	Acidification: reduces environmental pH	[29]
Siderophore secretion	Chelation: sequesters metal cations	[30]
Enzymatic hydrolysis	Secretion of phosphatases and other hydrolytic enzymes	[27]
Pi uptake	High-affinity phosphate transporters (PTs)	Primarily H⁺:Pi and Na⁺:Pi cotransporters; regulated by Pi levels (upregulated under low Pi conditions)	[32]
Pi storage and transport	Conversion to polyphosphates (poly-P)	Converted to poly-P in hyphal vacuoles; transported within hyphae via a motile tubular vacuole system	[35]
Transport to the Hartig net
Pi release at the symbiotic interface	PT-mediated Pi release	Poly-P hydrolyzed by polyphosphatases; free Pi is released across the hyphal plasma membrane	[36]
Host plant regulation	Upregulation of specific phosphate transporter gene expression	Differential activation of phosphate transporter genes in host plants (e.g., PtPT9 and PtPT12 in Populus tomentosa)	[37]

Functional stage	Key mechanism	Molecular mechanism & regulation	References
Mineralization of inorganic phosphorus	Secretion of low molecular weight organic acids (LMWOAs)	Electrostatic/covalent interactions	[26]
Proton (H⁺) release	Acidification: reduces environmental pH	[29]
Siderophore secretion	Chelation: sequesters metal cations	[30]
Enzymatic hydrolysis	Secretion of phosphatases and other hydrolytic enzymes	[27]
Pi uptake	High-affinity phosphate transporters (PTs)	Primarily H⁺:Pi and Na⁺:Pi cotransporters; regulated by Pi levels (upregulated under low Pi conditions)	[32]
Pi storage and transport	Conversion to polyphosphates (poly-P)	Converted to poly-P in hyphal vacuoles; transported within hyphae via a motile tubular vacuole system	[35]
Transport to the Hartig net
Pi release at the symbiotic interface	PT-mediated Pi release	Poly-P hydrolyzed by polyphosphatases; free Pi is released across the hyphal plasma membrane	[36]
Host plant regulation	Upregulation of specific phosphate transporter gene expression	Differential activation of phosphate transporter genes in host plants (e.g., PtPT9 and PtPT12 in Populus tomentosa)	[37]

Interaction level	Mechanism category	Specific mode	Function	References
Physical-level interactions	Surface attachment and colonization	Bacteria colonize hyphae via adhesins/surfactins	Establishes physical interaction channels	[49-50]
Biofilm formation	Bacteria rely on EPS/TasA/eDNA/ACC signaling to form biofilms→Enhances symbiotic stability	Enhances symbiotic stability	[51-54]
Metabolic-level interactions	Metabolic cross-feeding	ECMF secretes sugar alcohols to induce bacterial community differentiation; auxotrophic fungi-bacteria interactions	Drives nutritional mutualism	[55-59]
Regulation via antimicrobial substances	ECMF secretes mycotoxins/antimicrobial proteins to shape resistant bacterial communities	Optimizes the symbiotic microenvironment	[60-62]
Mediation by volatile organic compounds (VOCs)	Fungal VOCs activate bacterial metabolic pathways	Facilitates community interaction beyond spatial constraints	[63-64]
Functional-level interactions	Nutrient mobilization and synergy	Helper bacteria enhance phosphate dissolution/enzyme activity	Improves nutrient absorption and cycling	[65-66]
Biotic stress defense	Bacteria effectively suppress pathogens, protecting host fungi	Enhances host fungal resistance	[67-69]
Co-evolutionary significance	Community co-adaptation	Highly specific ECMF-bacterial interactions co-drive nutrient cycling and niche differentiation	Maintains ecosystem stability	[42-43]

Interaction level	Mechanism category	Specific mode	Function	References
Physical-level interactions	Surface attachment and colonization	Bacteria colonize hyphae via adhesins/surfactins	Establishes physical interaction channels	[49-50]
Biofilm formation	Bacteria rely on EPS/TasA/eDNA/ACC signaling to form biofilms→Enhances symbiotic stability	Enhances symbiotic stability	[51-54]
Metabolic-level interactions	Metabolic cross-feeding	ECMF secretes sugar alcohols to induce bacterial community differentiation; auxotrophic fungi-bacteria interactions	Drives nutritional mutualism	[55-59]
Regulation via antimicrobial substances	ECMF secretes mycotoxins/antimicrobial proteins to shape resistant bacterial communities	Optimizes the symbiotic microenvironment	[60-62]
Mediation by volatile organic compounds (VOCs)	Fungal VOCs activate bacterial metabolic pathways	Facilitates community interaction beyond spatial constraints	[63-64]
Functional-level interactions	Nutrient mobilization and synergy	Helper bacteria enhance phosphate dissolution/enzyme activity	Improves nutrient absorption and cycling	[65-66]
Biotic stress defense	Bacteria effectively suppress pathogens, protecting host fungi	Enhances host fungal resistance	[67-69]
Co-evolutionary significance	Community co-adaptation	Highly specific ECMF-bacterial interactions co-drive nutrient cycling and niche differentiation	Maintains ecosystem stability	[42-43]

Stage	Key participants	Primary function	Core mechanisms	References
Phosphorus source response	ECMF	Establish a synergistic system	Recruit chemotactic functional bacteria and facilitates biofilm formation	[75]
Synergistic mobilization	ECMF-functional bacteria	Conversion of insoluble phosphorus sources→PO₄^3-	Organic acid synergy enhances dissolution; secretion of phosphatases hydrolyzes organic phosphorus	[76]
Phosphorus transport	Hyphal PT transporters	PO₄^3-→poly-P (vacuolar storage)	Bidirectional vacuolar transport: transported to the Hartig net under sufficient carbon supply; retrieved and stored under carbon limitation	[92-96]
Mycorrhizal uptake	ECMF polyphosphatase (PPX1/VTC)-plant Pht1L phosphate transporter	poly-P→PO₄^3-→organic phosphorus (e.g., ATP/nucleic acids)	Host carbon-phosphorus exchange signals trigger poly-P hydrolysis in the Hartig net and activate Pht1 family genes	[97-100]

Stage	Key participants	Primary function	Core mechanisms	References
Phosphorus source response	ECMF	Establish a synergistic system	Recruit chemotactic functional bacteria and facilitates biofilm formation	[75]
Synergistic mobilization	ECMF-functional bacteria	Conversion of insoluble phosphorus sources→PO₄^3-	Organic acid synergy enhances dissolution; secretion of phosphatases hydrolyzes organic phosphorus	[76]
Phosphorus transport	Hyphal PT transporters	PO₄^3-→poly-P (vacuolar storage)	Bidirectional vacuolar transport: transported to the Hartig net under sufficient carbon supply; retrieved and stored under carbon limitation	[92-96]
Mycorrhizal uptake	ECMF polyphosphatase (PPX1/VTC)-plant Pht1L phosphate transporter	poly-P→PO₄^3-→organic phosphorus (e.g., ATP/nucleic acids)	Host carbon-phosphorus exchange signals trigger poly-P hydrolysis in the Hartig net and activate Pht1 family genes	[97-100]

植物-外生菌根真菌-细菌三方互作体系与磷素循环相关的研究进展

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郑庭裕 , 张美菱 , 贾永 ^*

微生物学报 | 综述 2026,66(1): 1-17

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微生物学报 | 综述 2026, 66(1): 1-17

植物-外生菌根真菌-细菌三方互作体系与磷素循环相关的研究进展

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郑庭裕, 张美菱, 贾永^*

作者信息

南京师范大学生命科学学院，江苏省微生物病原与生态省高校重点实验室，江苏南京

Research advances in the plant-ectomycorrhizal fungus-bacteria tripartite system in relation to phosphorus cycling

Tingyu ZHENG, Meiling ZHANG, Yong JIA^*

Affiliations

Jiangsu Key Laboratory of Microbial Pathogens and Ecology, College of Life Sciences, Nanjing Normal University, Nanjing, Jiangsu, China

出版时间: 2026-01-04 doi: 10.13343/j.cnki.wsxb.20250478

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摘要

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在自然土壤中磷素主要以螯合态无机磷等稳定形式存在，有效磷含量较低。木本植物为应对磷胁迫通常与外生菌根真菌形成菌根共生体系以增强其对磷素的吸收。相关研究表明，外生菌根真菌自身溶解螯合态无机磷的能力有限，但其可通过释放特定的化合物招募土壤中的溶磷相关功能细菌类群聚集在真菌菌丝际，协助解吸螯合态无机磷。然而，目前鲜有关于植物-外生菌根真菌-细菌三者联合体系在磷素循环中作用的综述性分析报道。本文提出了植物-外生菌根真菌-细菌三者联合体系的概念，解析了外生菌根真菌、菌根辅助细菌和宿主植物三者对磷素循环的作用及其生理生化和分子机制，并展望了三者联合体系促进植物磷素吸收的研究前景。

关键词

外生菌根真菌 / 菌根辅助细菌 / 哈蒂氏网 / 三重共生 / 协同进化 / 磷吸收 / 磷转运

Abstract

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In natural soils, phosphorus predominantly exists in stable forms such as chelated inorganic phosphorus, resulting in low levels of available phosphorus. To cope with phosphorus limitation, woody plants typically form symbiotic associations with ectomycorrhizal fungi (ECMF) to enhance phosphorus acquisition. Studies have indicated that ECMF exhibit limited capacity to directly solubilize chelated inorganic phosphorus. However, they can recruit phosphate-solubilizing bacteria in the hyphosphere by releasing specific compounds, thereby facilitating the desorption of chelated inorganic phosphorus. Nevertheless, comprehensive reviews analyzing the role of plant-ECMF-bacteria tripartite systems in phosphorus cycling remain scarce. This article introduces the conceptual framework of plant-ECMF-bacteria tripartite systems, elucidates the physiological, biochemical, and molecular mechanisms underlying phosphorus cycling among ECMF, mycorrhiza helper bacteria, and host plants, and discusses future research directions for optimizing plant phosphorus acquisition through the tripartite systems.

Key words

ectomycorrhizal fungi / mycorrhiza helper bacteria / Hartig net / tripartite symbiosis / coevolution / phosphorus acquisition / phosphorus transport

引用本文

郑庭裕, 张美菱, 贾永. 植物-外生菌根真菌-细菌三方互作体系与磷素循环相关的研究进展. 微生物学报, 2026 , 66 (1) : 1 -17 . DOI: 10.13343/j.cnki.wsxb.20250478

Tingyu ZHENG, Meiling ZHANG, Yong JIA. Research advances in the plant-ectomycorrhizal fungus-bacteria tripartite system in relation to phosphorus cycling[J]. Acta Microbiologica Sinica, 2026 , 66 (1) : 1 -17 . DOI: 10.13343/j.cnki.wsxb.20250478

正文

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在我国大部分地区土壤总磷含量虽很高，但实际上土壤中仅有3%的磷可被植物直接吸收利用，在酸性或碱性土壤中磷酸盐大部分与土壤中的Fe²⁺、Al³⁺、Ca²⁺形成螯合态无机磷，并以磷灰石类矿物形式存在，这种形态的磷在土壤中不易流动，难以满足植物生长需求，严重影响了植物的生长和发育^[1]。研究表明外生菌根真菌(ectomycorrhizal fungi, ECMF)与植物经过近2亿年的共同进化形成了由根外菌丝、菌丝鞘(hyphal mantle)及哈蒂氏网(Hartig net)构成的复杂而精细的外生菌根(ectomycorrhiza, ECM)共生体系，可显著促进植物对土壤中磷素的吸收和利用，是植物微生物组的重要组成部分，也是陆地生态系统的关键参与者，对于维持生态平衡、促进植物健康生长以及实现土壤养分的有效循环具有至关重要的作用^[2-4]。然而，ECMF单独对螯合态无机磷的解吸能力有限，无法完全满足其共生体系对磷的需求。前期研究表明，ECMF可通过释放特定化合物招募土壤中的功能细菌种群，协助其完成对土壤中螯合态无机磷的解吸^[5]。因此自然土壤中存在植物-外生菌根真菌-细菌三者联合体系，可促进植物通过外生菌根体系吸收磷素。

在植物营养学和土壤生态学领域，植物、外生菌根真菌(ECMF)和溶磷细菌之间的相互作用对磷素循环的影响一直是研究热点。根据现有研究结果，本文将分为3个部分层层推进：(1) 植物-外生菌根真菌共生与磷素循环；(2) 外生菌根真菌与溶磷细菌协同促进磷素吸收；(3) 植物-外生菌根真菌-溶磷细菌三者联合体系与植物磷营养。本文主要阐述植物-外生菌根真菌-溶磷细菌三者联合体系在土壤生态系统中促进磷等矿质元素活化和吸收的协同作用，并探讨其存在的生态学意义，以期为解决日益严重的土壤磷素有效性低的问题提供新思路。

1 植物-外生菌根真菌共生与磷素循环

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在长期进化过程中，85%的维管植物与菌根真菌建立了共生关系，显著增强了其对养分和水分的获取能力，其中丛枝菌根(arbuscular mycorrhiza, AM)和外生菌根是最主要的2种菌根类型^[6]。ECMF由腐生祖先的多个谱系趋同进化而来^[7]，但大多数在进化过程中已丧失营腐生的分解能力。外生菌根是ECMF和植物形成的共生体系，其中ECMF通过促进营养吸收和增强对生物与非生物胁迫的抵抗力来改善宿主植物的生长和适应性；作为交换，真菌获得宿主植物通过光合作用产生的碳水化合物用于营养生长和子实体分化，如糖和脂肪酸^[8-9]。

在外生菌根共生系统中ECMF对植物的定殖具有偏好性。这种共生特异性通过对宿主进行匹配与筛选提高了宿主谱系的生态位分化，最终有利于外生菌根真菌谱系的多样化^[10]。Van der Heijden等^[11]利用ECMF与南山毛榉属(Nothofagus)植物专性共生的关系探究ECMF的偏好及其与宿主的协同演化，结果发现24%的ECMF隶属于特定宿主，且宿主的亲缘关系与真菌系统发育之间存在显著相关性。

1.1 植物-外生菌根真菌磷素吸收共生体系的建立

ECM是土壤真菌与植物根系形成的互惠共生体系，广泛分布于森林生态系统中。外生菌根与宿主植物之间的信号识别与传导是建立共生关系的关键步骤，该过程涉及多种分子机制，确保真菌与植物能够相互识别并建立稳定的共生关系^[12]。

植物和ECMF释放的信号分子的互相感知和识别是建立外生菌根共生关系的先决条件。植物根系能分泌许多次级代谢产物作为根际的化感物质，根系分泌物在共生关系建立过程中起重要的信号调节作用，化学作用通常是植物与微生物相互作用的第一步。Plett等^[13]研究表明根系分泌物中存在能被ECMF识别并吸引它们的化合物，这些分泌到根际的信号分子包括黄酮类、脂类和激素类等物质，这些物质在一定程度上也会促进ECMF菌丝生长和孢子萌发等^[9]。2001年，Lagrange等^[14]首次报道了蓝桉(Eucalyptus globulus)根分泌物中的黄酮类化合物芦丁(rutin)对豆马勃属(Pisolithus)真菌菌丝生长具有显著促进作用。植物激素脱落酸(abscisic acid, ABA)是类胡萝卜素途径的产物，Hill等^[15]发现脱落酸有助于增加外生菌根真菌小果豆马勃(Pisolithus microcarpus)的生物量及其对大桉(Eucalyptus grandis)树根的定殖。此外，真菌也会通过释放信号分子与植物进行分子对话。Plett等^[16]研究显示，豆马勃属真菌Pisolithus albus菌丝分泌的10 kDa小分子效应蛋白可以调节宿主桉树根细胞中的多胺生物合成并促进定殖。

在共生建立阶段，菌丝在植物根表面物理接触，部分包裹根尖形成菌丝鞘，部分入侵植物根皮层细胞并形成外生菌根标志性特征——哈蒂氏网，同时由于菌丝的侵染，根系顶端膨大，最后形成ECM典型二叉分枝结构^[4]。哈蒂氏网的形成需要特异酶对植物细胞壁进行重塑，相较于腐生祖先，ECMF的微生物细胞壁降解酶(microbial cell wall degrading enzymes, MCWDEs)得以保留，而植物细胞壁降解酶(plant cell wall degrading enzyme, PCWDEs)出现广泛丢失，为真菌穿透植物细胞壁提供了分子基础，但其作用并非完全降解而是用于促进共生^[17]。已知外生菌根双色蜡蘑(Laccaria bicolor)基因组中只存在一个纤维素降解相关酶GH5，且依附在唯一的纤维素结合域(cellulose-binding module, CBM1)上。LbGH5-CBM1在菌丝鞘和哈蒂氏网显著聚集，而RNA干扰(RNA interference, RNAi)突变体形成ECM的能力较低^[18]，这可能是共生定殖成功的重要因素。此外，位于共生界面的细胞壁中果胶酶LbGH28A也在建立外生菌根共生中起关键作用^[19]。

外生菌根通过菌丝网络扩展植物对磷素等营养的吸收空间，并激活高效的养分转运机制，是陆地生态系统生产力的重要驱动力。值得注意的是，形成共生关系的基础是双方受益^[20]，维持稳定的共生关系依赖于彼此的营养交换，为此在共生中双方不断调节共生关系以保持相对于自身“投资”的最高收益。植物被证明可以通过引入多种ECMF竞争进而获得有益真菌，提高整体的供养量，进一步通过分泌鸟苷酸结合蛋白(guanylate binding proteins, GBPs) (GH81型β-1,3-葡聚糖酶内切葡聚糖酶的一个家族)促进真菌定殖^[21]。此外，经过长期积累ECMF也逐渐塑造了森林生态系统中利于自身竞争的土壤理化性质与微生物群落，用于摄取土壤中N、P等限制性营养^[22-23]。

1.2 植物-外生菌根共生的适应性磷捕获策略

在森林生态系统中磷素是植物生长的主要限制性养分。由于土壤中绝大部分磷以植物无法直接利用的螯合态无机磷和有机磷形式存在，导致正磷酸盐(orthophosphate ions, Pi)等有效磷含量的生物有效性极低。因此，外生菌根(ECM)作为温带和热带森林中普遍存在的共生体系，成为植物获取磷营养的主要途径。研究表明植物通过ECM真菌吸收的磷可占其总磷吸收量的20%-100%^[24-25]，凸显了该共生体系在生态系统磷循环中的关键作用。与许多其他真菌物种一样，ECMF可以释放出低分子量有机酸(low molecular weight organic acids, LMWOAs)溶解螯合态无机磷，有机酸中的负电荷通过静电和共价力附着在矿物阳离子上从而释放出Pi^[26]；有机磷被证明可通过酶解作用矿化^[27]。在已有研究的大约30种ECMF中属于丝膜菌属(Cortinarius)、乳牛肝菌属(Suillus)、桩菇菌属(Paxillus)、豆马勃属(Pisolithus)和乳菇属(Lactarius)的物种被发现能够释放大量的LMWOAs，其中草酸盐是主要酸解物质^[28]。有机酸的分泌并非溶解螯合态无机磷的唯一途径，质子的释放也是真菌活化螯合态无机磷的另一个重要机制，在ECMF菌株中也得到验证^[29]。此外，D’Amico等^[30]研究发现，ECMF可以通过铁载体螯合金属阳离子使磷酸根游离出来，促进对螯合态无机磷的溶解。

长期以来，研究表明外生菌根真菌会产生根外菌丝，这些菌丝被认为在植物克服磷胁迫中起着重要作用，它们可以极大增加菌根植物开发的土壤体积，且根外菌丝通常对正磷酸盐离子具有更高的亲和力，大大增强了对磷的吸收能力^[31]。随后，这部分Pi可通过根部的单向磷运输通道在真菌和根细胞之间交换营养物质。ECMF通过质膜磷酸盐转运蛋白获得游离无机磷酸盐，其含有特异的高亲和力Pi转运蛋白，能够获得土壤中低浓度的Pi，主要有H⁺:Pi和Na⁺:Pi协同转运子^[32]，如美味牛肝菌(Boletus editus)编码的BePT，卷边桩菇(Paxillus involutus)的PiPT1-PiPT3等，它们的表达均受Pi含量的调节，在低Pi条件下强烈上调^[33-34]。当Pi被ECMF菌丝吸收后，大部分则主要以多聚磷酸盐(polyphosphates, poly-P)的形式储存在真菌菌丝内液泡中^[35]，然后运输到菌根的哈蒂氏网(Hartig net)中，真菌Pi在共生界面的转运是通过磷酸盐转运体(phosphate transporter, PT)释放游离的Pi来进行的^[36]。Loth-Pereda等^[37]研究表明，在ECM共生的情况下，来自毛白杨(Populus tomentosa)的磷酸盐转运蛋白基因PtPT9和PtPT12的表达明显上调，ECM磷素的摄取途径在很大程度上由宿主植物通过差异性激活特定共生关系的磷转运基因来控制。综上所述，ECMF通过多种协调机制有效动员和转运土壤中的磷素，以缓解宿主的磷胁迫(表1)。

外生菌根共生是森林生态系统中木本植物根系与土壤真菌之间最为广泛的关联之一。这些共生关联通过养分循环和碳固存为生态系统的可持续性作出了重大贡献。维持成功的长期关系似乎受到共生伙伴之间资源分配的强烈调节，这表明营养物质本身可能起到信号作用。然而，对于双方相互识别的分子机制目前仍知之甚少，需要进一步研究。

2 外生菌根真菌与溶磷细菌协同促进磷素吸收

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细菌和真菌共存于多种环境中，它们相互依存、共同进化。尽管对共生体中微生物相互作用的研究主要集中在对抗和竞争方面，但植物相关的真菌与共生微生物也会进行有益的互动。当真菌定殖于特定的生态位时真菌的菌丝能够以非随机的方式募集功能微生物形成“菌圈” (mycosphere)，从而改善真菌的功能或适应性^[38]。类似于植物根系分泌物在根部微生物群落组装中的作用，多项体外实验提供证据表明富含碳的真菌分泌物可刺激特定细菌的生长，并影响微生物群落结构^[39]。ECMF孢子和外延菌丝体表面还存在大量的功能细菌，即菌根辅助细菌(mycorrhiza helper bacteria, MHB)，这些菌根辅助细菌与ECMF的菌丝生长、营养吸收、次生代谢产物生成、子实体形态变异等密切相关，同时也会影响ECMF和宿主植物之间的相互识别与定殖^[3,40-41]。

2.1 外生菌根真菌与辅助菌的协同进化作用

共生在促进真菌的进化和多样性方面发挥着不可或缺的作用。大多数真菌与其相关微生物组(如细菌)的复杂群落建立共生关系，而这些微生物对真菌的生长、发育、健康及功能起着关键作用^[42]。菌根菌与辅助细菌之间存在协同进化机制，二者相互的选择特异性较强。在自然条件下，ECMF和细菌的相互作用涉及复杂的物理、代谢和功能水平的交互^[43]。随着自然环境的日益变化，ECMF与细菌联合体系仍在不断地进化和更新，但其联合体系的建立及其互作的机制仍然需要进一步研究(表2)。

2.1.1 物理水平的相互作用

物理相互作用通常被认为是细菌和真菌之间最简单的相互作用，主要涉及真菌与细菌在空间位置上的相互关系和直接接触^[44]。在真菌-细菌相互作用中，真菌通常充当细菌的“生物支架”，细菌附着在真菌表面或深入菌丝内部(endohyphal bacteria, EHB)，以实现菌落间的信号传递和代谢响应^[45-46]。

附着是细菌在真菌上定殖的重要前提，该过程可能涉及细菌表面分子(如黏附素)与真菌表面分子的相互作用^[47-48]。Richter等^[49]以枯草芽孢杆菌(Bacillus subtilis)和黑曲霉(Aspergillus niger)作为细菌-真菌相互作用的简单模型，发现枯草芽孢杆菌能够通过增强表面活性素的产生和扩散，促进其在黑曲霉菌丝体上定殖和生长。电镜观察发现：首先，当菌丝扩散至细菌菌落附近时细菌菌落与真菌菌丝周围的液体层发生物理接触；接着，细菌迅速从静止状态转变为运动状态，并在真菌菌丝周围的液态层中游动，直到它们遇到物理障碍或到达交叉点并移动到其他菌丝上；最后，大量细菌定殖在真菌菌丝上^[50]。此外，菌丝体的定殖被认为依赖于细菌的生物膜，生物膜的形成可以增强细菌与真菌的成功附着。细菌-真菌生物膜可以作为两者的混合复合物存在，而真菌(如ECMF)可以为细菌提供大面积的菌丝网络，为其生物膜的建立提供生物支持^[51]。枯草芽孢杆菌可以在黑曲霉菌丝上形成生物膜且具有一定的普适性，枯草芽孢杆菌中生物膜的形成需要胞外多糖(exopolysaccharides, EPS)、TasA淀粉样蛋白纤维和表面疏水素BslA，对这些基因敲除后就不再形成生物膜，也无法再附着在真菌表面^[52]。Miquel Guennoc等^[53]观察到14种细菌产生的生物膜是由细胞外DNA (extracellular DNA, eDNA)构成的细丝网络，eDNA会作为一种凝聚分子将细菌细胞维持在一起，并将生物被膜锚定到双色蜡蘑菌丝的表面。张朝辉等^[54]以双孢蘑菇(Agaricus bisporus)和恶臭假单胞菌(Pseudomonas putida) UW4为对象研究l-氨基环丙烷-l-羧酸(l-aminocyclopropane-l-carboxylic acid, ACC)在生物膜形成过程中的作用，发现ACC是产ACC脱氨酶细菌在真菌菌丝表面形成菌膜的关键信号物质，且使用ACC合成酶抑制剂则UW4不能在双孢蘑菇菌丝表面形成菌膜。

2.1.2 代谢水平的相互作用

在代谢水平上ECMF和细菌通过分泌和感知小分子信号物质进行交互，其中交叉喂养是真菌和细菌之间代谢相互作用的重要方式。研究表明ECMF的存在改变了土壤食物网，增加了细菌的丰富度并改变细菌群落的代谢潜力，产生的独特代谢物既是土壤相互作用的资源又是介质，细菌与真菌共存会改变根内和根-土壤界面的化学环境^[55]。此外，土壤微生物也会促进养分循环和有机质转化，通过各种机制改变土壤生境。

Rangel-Castro等^[56]发现鸡油菌(Cantharellus cibarius)可分泌甘露醇和海藻糖影响假单胞菌属菌群；Timonen等^[57]研究表明根际细菌对真菌产生的甘露醇和果糖偏好导致粘盖牛肝菌(Suillus bovinus)和卷边网褶菌(Paxillus involutus)根际细菌群落存在显著差异，来自粘盖牛肝菌根际的细菌特异性地利用甘露醇，而来自卷边网褶菌根际的细菌似乎更倾向于利用果糖。代谢物有利于营养缺陷型微生物的定殖和生长，还对营养缺陷型的进化频率进行依赖性选择^[58]。多数ECMF无法合成自身生长所需的维生素等物质，在形成菌根前，只能与细菌相互作用，获取所需维生素等生长所需物质。如双色蜡蘑是硫胺素营养缺陷型菌株，需借助荧光假单胞菌(Pseudomonas fluorescens)分泌的硫胺素实现共生体系形成前在土壤中的生存^[59]。ECMF在生长过程中还会产生某些抗菌物质，如霉菌毒素和一些抗菌蛋白，从而影响其周边微生物种群^[60-61]。Shirakawa等^[62]在ECMF与21株细菌体外共培养实验中发现其分泌的抗菌物质对革兰氏阳性细菌敏感，对革兰氏阴性细菌并不敏感，这表明ECMF的抗菌活性将部分革兰氏阳性菌排除在菌根际之外，菌根际特定的土壤细菌群落主要由对ECMF的抗菌活性不敏感的细菌组成。

ECMF子实体内微生物群落的构建受真菌分类、基因型、地理距离和一些非生物因素的影响，大多数微生物生活的空间环境会影响化学物质传输，这时挥发性有机化合物(volatile organic compounds, VOCs)也会在细菌与真菌的互作中发挥作用^[63]。奶酪表皮(cheese rind)是研究挥发性有机化合物对微生物组组装影响的理想模型，Cosetta等^[64]将5种广泛分布的奶酪真菌产生的挥发性物质分别与不同细菌共培养，其中弧菌属(Vibrio)细菌接触到所有真菌产生的挥发物时生长刺激最为显著且最具可重复性；当暴露于真菌VOCs时弧菌属的总丰度会增加，可能与真菌挥发的乙酸、脂肪酸通过乙醛酸途径的激活有关。这些由真菌或细菌分泌产生的代谢产物，在微生物间形成了交叉喂养分配网络，不仅促进生物量生产(生长速率和产量)，也增强微生物群落的分类和功能多样性。

2.1.3 功能水平的相互作用

菌根辅助细菌被招募并定殖于ECMF，进而对真菌的养分吸收、生长发育和生态学功能等过程产生影响。在陆地生态系统中真菌的进化对细菌生态位的发展产生了重大影响，真菌菌丝可能通过相互选择和适应过程影响土壤的细菌群落结构。与周围土壤微生物相比，ECM根际微生物可能表现出更强的溶解营养物质的能力。Uroz等^[65]从橙黄硬皮马勃(Scleroderma citrinum)中分离出的红球菌(Rhodococcus sp.) TMG025 II和萎蔫短小杆菌(Curtobacterium flaccumfaciens) TMG034具有较强的降解β-葡聚糖和溶解螯合态无机磷的能力。Pavić等^[66]发现，从双色蜡蘑子实体内分离出的荧光假单胞菌的溶磷能力和产铁能力均强于菌丝际的荧光假单胞菌。本课题组Zhang等^[5]发现，新苦粉孢牛肝菌(Tylopilus neofelleus)菌丝际细菌具有较强的溶解螯合态无机磷(磷酸三钙)的能力，且部分菌株与宿主真菌共接后显著增强了外生菌根体系对磷素的解吸。

细菌可通过产生抗菌物质抑制病原体和污染性真菌的生长，进而协助宿主真菌在菌根体系中抵御植物病原菌的侵染。Monaco等^[67]研究表明，从双色蜡蘑中分离的荧光假单胞菌菌株全都对病原真菌具有抑制作用，而从土壤中分离出的菌株仅有26%对病原真菌有抑制作用。土副伯克霍尔德氏菌(Paraburkholderia terrae)可以缓解荧光假单胞菌和抗真菌药物(如环己酰亚胺)对宿主真菌离褶伞的拮抗作用^[68]。链霉菌能显著抑制病原真菌松根异担子菌(Heterobasidion annosum)和红褐小蜜环菌(Armillaria obscura)的生长，促进宿主鹅膏菌菌丝生长^[69]。

2.2 外生菌根真菌-细菌共生体的协同磷动员机制

在自然环境中ECMF自身对有机磷以及螯合态无机磷的解吸能力有限，仅依靠外生菌根体系无法满足对磷的大量需求，此时需要招募并利用土壤功能细菌以协助增强磷的获取。Chen等^[70]研究表明，不同外生菌根真菌菌丝际土壤中的细菌群落存在显著差异性，与周围块状土壤中的细菌群落相比，外生菌根真菌会导致土壤细菌群落的多样性和丰度降低。前期本课题组Mei等^[71]发现厚环乳牛肝菌(Suillus grevillea)通过分泌特定的小分子物质吸引拉氏西地西菌(Cededea lapagei)并促使其附着于菌丝表面，二者联合体系使植酸矿化效率提高1.8倍。此类互作可能依赖于真菌分泌的趋化性物质，类似机制在微生物-真菌跨界互作中已有较多文献支持。例如，外生菌根真菌双色蜡蘑(Laccaria bicolor)的菌丝体分泌海藻糖至外部环境，致使菌丝际区域海藻糖浓度升高，进而实现对能有效利用海藻糖的荧光假单胞菌的选择性富集^[56]。除了作为营养物质外，真菌还可以释放其他类型的可溶性化合物诱导细菌趋化，如草酸能在不被消耗的情况下诱导土壤细菌山冈单胞菌(Collimonas)的趋化性^[72]。这在一定程度上表明，ECMF通过释放特定的化合物趋化吸引土壤中的溶磷细菌(phosphate solubilizing bacteria, PSB)以增强磷吸收。

分泌乳酸、乙酸、草酸、琥珀酸、苹果酸、酒石酸、葡萄糖酸和富马酸等低分子量的有机酸，降低土壤的pH，并与铁、镁、铝、钙等离子发生络合反应，释放与之结合的磷酸根离子，形成植物可吸收利用的H₂PO₄^-和HPO₄^2-，是溶磷微生物溶解土壤中难溶性磷的主要作用机制。Zhang等^[5]分离纯化的新苦粉孢牛肝菌(Tylopilus neofelleus)菌丝际细菌上调溶磷相关的葡萄糖脱氢酶基因(gcd、gabY)、磷酸酶基因(acp、pho)，显著增加了乳酸的分泌，进而提高了对螯合态无机磷的解吸效率。此外，菌根真菌和PSB之间的协同相互作用也可以增强植物对有机磷的吸收。植酸是土壤有机磷的主要成分且需要植酸酶分解，而部分菌根真菌不含有编码植酸酶的基因，这就需要定殖在菌丝际中的土壤微生物释放各种酶来降解。Wang等^[73]以蒺藜苜蓿为研究材料募集而来的PSB被认为是菌根磷吸收途径的第二个基因组，它们会刺激磷循环功能提高宿主植物对植酸的利用。

综上所述，ECMF自身虽具有一定的解磷能力，但其不具备高效性和普遍性，不足以满足自身或宿主植物对磷的大量需求。因而，ECMF与PSB协同作用可增强解磷效率，从而增加经外生菌根共生体系转运到植物体内的磷素以维持植物正常的生长发育。

3 植物-外生菌根真菌-细菌三重共生系统与植物磷营养

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在自然界中合作是物种克服资源短缺和提高适应性的重要方式。经报道1 g土壤会包含超过10亿个细菌和200 m长的真菌菌丝^[74]，这些微生物并非孤立存在，而是通过密切的相互作用和协同关系形成了一个复杂的生态系统。ECM是真菌与高等植物的根部形成的共生体系，宿主植物和ECMF的代谢产物通过根皮层细胞间形成的哈蒂氏网进行双向转运^[12]。在土壤中ECMF通过其广泛的菌丝网络吸收土壤中的水分和养分并传递给植物；同时，它们也向土壤中释放有机化合物为细菌等其他微生物提供了养分和栖息地。细菌则通过分解这些有机化合物进一步释放养分，促进土壤养分的循环和转化进而促进植物生长。因此，植物、外生菌根真菌和土壤细菌构成了连续体，可能伴随着多种形式的合作。

3.1 植物-外生菌根真菌-细菌三重共生系统的组成与特性

生命向四面八方伸展“触角”，以发现并利用有用的东西为生活创造新的环境和机会。植物-外生菌根真菌-细菌共生连续体在空间尺度上可看作一种“嵌套模式”，即植物与担子菌门(Basidiomycota)、子囊菌门(Ascomycota)等真菌共生形成外生菌根，继而形成子实体产孢结构，且其根外菌丝和子实体下部的菌索又会与其周围土壤中的细菌等微生物再次建立新的联合功能体，即“菌圈” (mycosphere)^[75]。菌圈具有一定的特异性，有别于普通的土壤细菌，其与真菌之间可能存在特定的互作关系，如菌根辅助细菌(MHB)可协同ECMF发挥各种生态功能。

生物膜的形成是影响菌根辅助细菌(MHB)在菌丝际定殖的首要因素，细菌与真菌间生物膜形成后，部分细菌可以沿真菌菌丝进行迁移，“真菌公路”作为特定细菌在土壤中的运输网络具有重要的作用。Warmink等^[76]研究发现，沉积物副伯克霍尔德菌(Paraburkholderia sediminicola) BS001和离褶伞属(Lyophyllum)菌株Karsten (DSM2979)共培养时细菌可以产生生物膜，并在有生物活性和延伸性的真菌菌丝顶端一起移动，且多数可迁移的细菌菌株均含有hrcR基因[三型分泌系统(type III secretion system, T3SS)存在的指示性标志物]。随后，MHB被招募并定殖于ECMF，进而影响菌根真菌的生长发育，还能提高菌根真菌对植物根部的定殖率，增强菌根系统与宿主植物的营养交换，促进宿主植物生长。Berrios等^[77]的研究显示，ECMF和MHB相互作用可以增加或维持宿主植物的适应性，增加菌根定殖率，有利于植物生长。Wang等^[78]研究发现芽孢杆菌HR10促进宿主真菌刺革菌(Hymenochaete sp.)的生长，调节菌根相关基因的表达，影响真菌的β-1,3-葡聚糖酶活性，并增加了菌根定殖强度，提高了松苗侧根数和根系活性以及松针叶绿素荧光活性，证明了芽孢杆菌HR10通过增强松树的菌根定殖促进养分吸收，诱导松幼苗的光合作用和根系活性增加。MHB和ECMF还可协同增强宿主植物的抗病能力，接种刺革菌和芽孢杆菌HR10后宿主植物的酶和非酶的系统抗氧化活性增加，PR3和PR5基因上调表达的早期启动显著减少由松球壳孢(Sphaeropsis sapinea)引起的松树枝枯病发病率^[79]。综上所述，与ECMF密切相关的细菌作为菌根共生的合作伙伴，形成了植物-外生菌根真菌-细菌三重共生系统深刻影响植物生长和生态系统功能。

3.2 三重共生系统与植物磷的营养相互作用机制

在三重共生系统中ECMF通常通过分泌信号物质从周边招募具有解磷功能的细菌，这些解磷细菌可促进ECMF菌丝的生长，弥补其在解磷功能上的不足，提高对土壤中磷素的解吸效率，形成“交叉喂食”的互利共生模式。

3.2.1 磷元素的信号传递与调控

磷不仅是营养物质，还是一种信号物质。磷充足时菌根真菌的定殖和生长发育程度较低，植物通过自身根系直接获取磷；磷匮乏时植物会优先向菌根真菌提供碳水化合物，菌根真菌则会增加磷的吸收和转运，以满足植物对磷的需求^[80]。ECMF表现出对多种磷源的适应能力，凭借其发达的外延菌丝网络能够到达根际外的磷素养分斑块。与低磷土壤相比，富磷土壤中虽然真菌类群多样性较高，但植物磷吸收效率较低，这表明真菌类群可能在压力环境中定殖根系的特化程度更高^[81]，即低磷土壤条件下的菌根效益大于富磷土壤。ECMF和非菌根真菌与植物的相互作用对比发现，ECMF处理的土壤酶会向更高的营养获取酶(如酸性磷酸酶等)投入，以提高参与P循环等的酶活性，满足ECMF和宿主的养分需求^[82]。

在菌根共生体中，资源交换是互利关系的核心，例如在AM中植物会优先将更多的碳分配给能提供更多磷的真菌以激励养分的供给。关于外生菌根系统的碳营养来源，多项研究共同指向ECMF对植物碳源的结构性依赖。这一结论首先基于对ECMF碳源的直接追踪。Tatry等^[83]通过稳定同位素标记实验证实，与宿主共生的ECMF，其生长所需碳源主要来源于植物提供的糖类。另一方面，对于引发推测的“ECMF保留氧化降解酶活性可获取碳源”的观点^[84]，近年的功能研究已予以澄清。其中，Jörgensen等^[85]通过转录组与酶活分析表明，这些酶活性的主要功能是从土壤有机质中获取NH₄⁺，而非分解有机物以获取碳源。此外，这一碳依赖关系在理论层面也得到了印证。Bogar^[86]基于源-汇动力学构建的模型揭示，植物向真菌输送的碳通量与真菌的呼吸速率、菌丝延伸或生物量增长速率成正比，表明整个资源交换过程是由真菌的生长需求所驱动的。

ECMF对植物营养的贡献也可如此解释：ECMF的菌丝可作为土壤中磷等资源的来源，扩展植物根系单独能接触到的土壤体积，并且释放酶来提高资源的可获取性^[87]，在植物、ECMF和碳源之间形成正反馈回路。在此过程中，ECMF也会分泌富含碳的化合物，如碳水化合物、氨基酸和羧酸盐等，招募MHB并通过提供碳源和能量刺激细菌的生长和代谢。因此，植物-外生菌根真菌-细菌连续体展示了多层次的跨界合作，植物为外生菌根真菌和细菌提供碳源和能源支撑，调节菌丝际中外生菌根真菌与土壤细菌之间的互惠关系，提高各方对环境的适应性。

3.2.2 磷元素的转运过程

磷是植物代谢过程必不可少的物质，在能量转换、信号转导、生物大分子合成、光合和呼吸等过程中发挥着重要作用^[88]。然而，植物吸收磷的主要来源是土壤中的无机磷，土壤中植物可吸收的可溶性无机磷含量非常低，因此如何提高土壤中可溶性磷水平成为改善植物磷营养的主要课题。在植物-外生菌根真菌-细菌三重共生系统中，外生菌根真菌通过形成菌套和哈蒂氏网与植物根系建立共生界面，成为磷吸收的关键媒介^[89]。该系统通过功能分工实现磷的高效获取：ECMF凭借其发达的根外菌丝网络主导远距离磷的获取与跨区域运输，而与其互作的细菌则主要负责局部难溶性磷的活化^[71]。这种协同机制显著提升了系统的整体磷效率，据报道，在低磷土壤中该三重共生体系可使植物的磷吸收效率提高30%-50%^[71]。这存在一个高度协调的级联效应，(1) 植物启动：碳源供应驱动共生；(2) ECMF响应：菌丝网络扩展与磷活化；(3) 细菌协同：菌根际磷的二次活化；(4) 植物反馈：磷吸收与碳分配优化。在外生菌根真菌-细菌通过协同作用将土壤中难溶性无机磷溶解转化为植物和真菌可利用的无机磷形式后，ECMF菌丝通过高亲和力磷酸盐转运蛋白(如PT家族)主动吸收^[90-91]，后续主要涉及菌丝内的磷转运和菌丝-植物根界面的磷转运。在整个磷获取与转运的级联过程中，各阶段参与者、核心功能及机制归纳如表3所示。

在菌丝内部，吸收的无机磷Pi被迅速合成为多聚磷酸盐(polyphosphate, polyP)，该过程依赖多聚磷酸盐激酶(poly phosphate kinase, PPK)，并受菌丝内ATP/ADP比值调控^[92]。与非菌根系统相比，菌根中polyP占比显著提高(Pi/polyP≈1.8)，而非菌根中只有磷酸盐一种形式，表明polyP是ECMF磷储存与长距离运输的主要形式，polyP的快速合成对维持菌丝磷的有效摄取很重要^[93]。研究表明，ECM包含一个运动的管状液泡系统，该系统在多个菌丝隔室之间形成连续体，液泡在菌丝尖端最活跃，它允许polyP独立于细胞质隔室通过菌丝运输，并使真菌能够微调其局部细胞质Pi浓度^[94]。ECMF菌丝的管状液泡网络具有双向运输功能，一方面将polyP从吸收活跃的菌丝尖端(pH较低，促进Pi质子共转运)运向哈蒂氏网；另一方面，当宿主碳供应不足时液泡可回收polyP至菌丝储存^[95-96]。

在菌丝-根界面，polyP需经过水解并跨膜转运后才能被植物吸收。多聚磷酸酶在这一过程中起关键作用^[97]，例如酿酒酵母(Saccharomyces cerevisiae)中的PPX1酶可降解长链polyP为短链Pi，从而维持细胞内磷稳态^[98]。Guan等^[99]进一步研究发现，该酶的活性受细胞内Pi浓度调控，并在液泡中与液泡转运蛋白伴侣(vacuolar transporter chaperone, VTC)复合体协同作用，以平衡polyP的动态积累与降解。ECMF通过PolyP的积累或再动员来调节养分向宿主的运输，而自由生活的ECMF菌丝中磷外排是轻微的，因此有利于外排的条件可能存在于菌丝-根界面，有证据表明寄主植物的碳供应可以触发polyP水解。Torres-Aquino等^[100]建立ECMF荷叶滑锈伞(Hebeloma cylindrosporum)与寄主海岸松(Pinus pinaster)和非寄主玉米(Zea mays)的共生长体系，发现只有寄主植物P. pinaster能够特异性地增强H. cylindrosporum菌丝体中的polyP水解，进一步推测事件发生过程：第一步是松根释放能够引发针对真菌polyP代谢的特异性反应的信号，该信号似乎是ECM植物特有的；第二步是增强胞内多聚磷酸酶的活性导致短链polyP的出现；第三步是增加胞外多聚磷酸酶的活性，作用于短链polyP产生游离Pi，然后在哈蒂氏网中释放。

多聚磷酸盐在菌根-植物共生界面(哈蒂氏网)水解为PO₄^3-，通过植物磷转运蛋白进入植物根系。磷转运蛋白基因是植物与菌根真菌共生过程中所特异驱动的基因，它编码植物菌根吸收途径中磷素利用的关键蛋白，其中Pht1家族是当今菌根互作研究中最重要的磷转运蛋白^[101]。植物根系吸收菌丝释放的磷，同时将光合作用产生的碳水化合物等营养物质转移给真菌，以维持菌根共生关系。最终PO₄^3-在植物体内转化为ATP、核酸、磷脂等有机磷形态，未被吸收的可能进行磷的再固定与循环^[102-103]。

综上所述，植物(尤其是林木)与根际微生物通常形成多重互惠关系。在许多陆地生态系统中磷的有效性被认为极大地限制了陆地上植物的初级生产力。与菌根真菌的共生关系是植物在有效磷含量有限地区的重要营养获取策略，特别是与外生菌根真菌表现出专性共生关系的松科的先锋树种。在此，植物-外生菌根真菌-细菌三重共生系统表现为一系列相互依赖、逐级放大的生理生态过程，通过碳-磷交换、微生物互作和反馈调节显著提升植物对磷的获取效率，具有特殊的生态学意义。

4 总结与展望

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本文系统综述了植物-外生菌根真菌-细菌三者共生体系在植物磷素循环中发挥关键作用。ECMF通过菌丝网络与植物根系形成紧密的共生体。同时，外生菌根真菌能够特异性地吸引土壤中的功能细菌，进而形成更为复杂的三元共生体系。这种共生关系的存在不仅增强了生态系统的稳定性，还促进了磷素等关键养分的有效循环。尽管已有文献报道外生菌根真菌和相关细菌协同作用可促进磷的解吸，但涉及植物的三方联合体系的相互作用及分子机制却鲜有报道。然而，在丛枝菌根真菌方面有类似研究，菌根化辅助细菌德沃斯氏菌(Devosia sp.) ZB163，可通过刺激植物的菌根化和(或)菌根功能，间接为植物提供额外的磷，植物-真菌-细菌三方共生关系能够驱动植物生长和菌根形成^[104]。

尽管现有研究较多聚焦于菌丝际细菌与ECMF的联合溶磷机制(如有机酸分泌、磷酸酶活化等)，近年来越来越多的证据表明，部分细菌可定殖于菌丝内部，并通过胞内互作直接参与养分循环过程。对ECMF-EHB系统的研究最早可追溯至担子菌门真菌双色蜡蘑(Laccaria bicolor) S238N。Bertaux等^[17]通过荧光原位杂交(fluorescence in situ hybridization, FISH)结合16S rRNA基因特异性探针，在其菌丝内检测到类芽孢杆菌(Paenibacillus sp.)的定殖，并证实该细菌位于菌丝胞内而非表面。这一发现提示，EHB可能通过更直接的物理-生化互作影响宿主真菌的代谢，而非仅依赖菌丝表面的间接作用。目前，关于EHB如何参与磷素循环的机制仍有待深入解析。对于黏附在菌丝表面的细菌，其分泌的小分子溶磷酶(如酸性磷酸酶，30-50 kDa)可能通过直接扩散进入土壤环境发挥作用^[71]。然而，对于定殖于菌丝内部的EHB，其分泌的酶需跨越真菌细胞壁/膜屏障，扩散效率受到严重限制，因而可能存在不同于表面菌的酶递送与活化策略。Fröjd等^[105]研究显示，革兰氏阳性放线菌委内瑞拉链霉菌(Streptomyces venezuelae)可通过分泌膜泡(membrane vesicles, MVs, 50-300 nm)运输功能性酶(如几丁质酶、β-葡萄糖苷酶)，这些酶在双层脂膜的保护下可抵抗宿主真菌分泌的蛋白酶降解，并可能通过内吞作用进入菌丝或释放至菌丝际^[106]。类似机制在AMF-细菌共生体系中已被证实：细菌囊泡可携带酸性磷酸酶或植酸酶，并通过脂膜屏障维持酶活性，最终促进磷的矿化与吸收^[107]。

此外，随着分子生物学和基因组学技术的不断发展，未来的研究应进一步探索这一共生体系中微生物间相互作用的具体机制，探究外生真菌刺激植物以实现共生的信号通路，研究体系中具体解磷机制，并分析其中关键基因的表达调控机制，阐明微生物间相互作用的分子基础。综上所述，植物-外生菌根真菌-细菌三者共生体系与磷素循环的研究具有重要的理论和实践意义。未来通过多学科交叉和综合研究，将不断深化对这一复杂共生关系的理解，为农业生产和生态环境保护提供新的思路和方法。

参考文献

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参考文献引证文献

排序方式：

[1]

JIANG

, CROUS

, CARRILLO

, MACDONALD

, ANDERSON

, BOER

, FARRELL

, GHERLENDA

, CASTAÑEDA-GÓMEZ

, HASEGAWA

, JAROSCH

, MILHAM

, OCHOA-HUESO

, PATHARE

, PIHLBLAD

, PIÑEIRO

, POWELL

, POWER

, REICH

, RIEGLER

, et al. Microbial competition for phosphorus limits the CO₂ response of a mature forest[J]. Nature, 2024, 630(8017): 660-665.

[2]

DUAN

, FENG

, LIMPENS

, BONFANTE

, XIE

, ZHANG

. Cross-kingdom nutrient exchange in the plant-arbuscular mycorrhizal fungus-bacterium continuum[J]. Nature Reviews Microbiology, 2024, 22(12): 773-790.

[3]

梅言, 戴传超, 贾永. 外生菌根真菌及其菌根辅助细菌协同解磷的研究进展[J]. 生态学杂志, 2022, 41(8): 1619-1627.

MEI

, DAI

, JIA

. Research progress of synergistic phosphorus solubilization between ectomycorrhizal fungi and ectomycorrhizal helper bacteria[J]. Chinese Journal of Ecology, 2022, 41(8): 1619-1627 (in Chinese).

[4]

SA G, YAO

, DENG

, LIU

, ZHANG

, ZHU

, ZHANG

, MA

, ZHAO

, LIN

, LU

, POLLE

, CHEN

. Amelioration of nitrate uptake under salt stress by ectomycorrhiza with and without a Hartig net[J]. New Phytologist, 2019, 222(4): 1951-1964.

[5]

ZHANG

, ZHANG

, ZHU

, MEI

, XU

, BAI

, SUN

, ZHANG

, DAI

, JIA

. Endofungal bacterial microbiota promotes the absorption of chelated inorganic phosphorus by host pine through the ectomycorrhizal system[J]. Microbiology Spectrum, 2023, 11(4): e0016223.

[6]

GUO

, DENG

, LI

, SCHMID

, HUANG

, WU

, PENG

, YANG

, LIU

. Evolutionary and ecological forces shape nutrient strategies of mycorrhizal woody plants[J]. Ecology Letters, 2024, 27(1): e14330.

[7]

LINDAHL

, KYASCHENKO

, VARENIUS

, CLEMMENSEN

, DAHLBERG

, KARLTUN

, STENDAHL

. A group of ectomycorrhizal fungi restricts organic matter accumulation in boreal forest[J]. Ecology Letters, 2021, 24(7): 1341-1351.

[8]

SHI

, WANG

. Mycorrhizal symbiosis in plant growth and stress adaptation: from genes to ecosystems[J]. Annual Review of Plant Biology, 2023, 74: 569-607.

[9]

冯万艳, 孙学广, 丁贵杰. 外生菌根预共生阶段信号识别机制研究进展[J]. 植物生理学报, 2021, 57(4): 749-758.

FENG

, SUN

, DING

. Advance of ectomycorrhizal signal recognition mechanism in pre-symbiosis[J]. Plant Physiology Journal, 2021, 57(4): 749-758 (in Chinese).

[10]

Van GALEN

, ORLOVICH

, LORD

, NILSEN

, DUTOIT

, LARCOMBE

. Correlated evolution in an ectomycorrhizal host-symbiont system[J]. New Phytologist, 2023, 238(3): 1215-1229.

[11]

Van der HEIJDEN

MGA

, MARTIN

, SELOSSE

, SANDERS

. Mycorrhizal ecology and evolution: the past, the present, and the future[J]. New Phytologist, 2015, 205(4): 1406-1423.

[12]

俞嘉瑞, 袁海生. 外生菌根真菌的共生互作和宿主选择机制研究进展[J]. 菌物学报, 2023, 42(1): 86-100.

, YUAN

. Research progress on symbiotic interaction and host selection mechanisms of ectomycorrhizal fungi[J]. Mycosystema, 2023, 42(1): 86-100 (in Chinese).

[13]

PLETT

, WOJTALEWICZ

, PLETT

, COLLIN

, KOHLER

, JACOB

, MARTIN

. Sesquiterpenes of the ectomycorrhizal fungus Pisolithus microcarpus alter root growth and promote host colonization[J]. Mycorrhiza, 2024, 34(1): 69-84.

[14]

LAGRANGE

, JAY-ALLGMAND

, LAPEYRIE

. Rutin, the phenolglycoside from Eucalyptus root exudates, stimulates Pisolithus hyphal growth at picomolar concentrations[J]. New Phytologist, 2001, 149(2): 349-355.

[15]

HILL

, WONG-BAJRACHARYA

, ANWAR

, COLES

, WANG

, LIPZEN

, NG V, GRIGORIEV

, MARTIN

, ANDERSON

, CAZZONELLI

, JEFFRIES

, PLETT

. Abscisic acid supports colonization of Eucalyptus grandis roots by the mutualistic ectomycorrhizal fungus Pisolithus microcarpus [J]. New Phytologist, 2022, 233(2): 966-982.

[16]

PLETT

, PLETT

, WONG-BAJRACHARYA

, de FREITAS PEREIRA

, COSTA

, KOHLER

, MARTIN

, ANDERSON

. Mycorrhizal effector PaMiSSP10b alters polyamine biosynthesis in Eucalyptus root cells and promotes root colonization[J]. New Phytologist, 2020, 228(2): 712-727.

[17]

BERTAUX

, SCHMID

, PREVOST-BOURE

, CHURIN

, HARTMANN

, GARBAYE

, FREY-KLETT

. In situ identification of intracellular bacteria related to Paenibacillus spp. in the mycelium of the ectomycorrhizal fungus Laccaria bicolor S238N[J]. Applied and Environmental Microbiology, 2003, 69(7): 4243-4248.

[18]

ZHANG

, ANASONTZIS

, LABOUREL

, CHAMPION

, HAON

, KEMPPAINEN

, COMMUN

, DEVEAU

, PARDO

, VENEAULT-FOURREY

, KOHLER

, ROSSO

, HENRISSAT

, BERRIN

, MARTIN

. The ectomycorrhizal basidiomycete Laccaria bicolor releases a secreted β-1,4 endoglucanase that plays a key role in symbiosis development[J]. New Phytologist, 2018, 220(4): 1309-1321.

[19]

ZHANG

, LABOUREL

, HAON

, KEMPPAINEN

, Da SILVA MACHADO

, BROUILLY

, VENEAULT-FOURREY

, KOHLER

, ROSSO

, PARDO

, HENRISSAT

, BERRIN

, MARTIN

. The ectomycorrhizal Basidiomycete Laccaria bicolor releases a GH28 polygalacturonase that plays a key role in symbiosis establishment[J]. New Phytologist, 2022, 233(6): 2534-2547.

[20]

SHI

, ZHAO

, XU

, MA

, ADAMS

, SHI

. Insights into plant-microbe interactions in the rhizosphere to promote sustainable agriculture in the new crops era[J]. New Crops, 2024, 1: 100004.

[21]

WANKE

, van BOERDONK

, MAHDI

, WAWRA

, NEIDERT

, CHANDRASEKAR

, SAAKE

, SAUR

IML

, DERBYSHIRE

, HOLTON

, MENKE

FLH

, BRANDS

, PAULY

, ACOSTA

, ZIPFEL

, ZUCCARO

. A GH81-type β-glucan-binding protein enhances colonization by mutualistic fungi in barley[J]. Current Biology, 2023, 33(23): 5071-5084.e7.

[22]

LUO

, MA

, CADOTTE

, SEIBOLD

, ZOU

, BURGESS

, TAN

, YE

, ZHENG

, CHEN

, LIU

, ZHU

, SHI

, ZHAO

, BI

, HUANG

, LI

, LIU

, LI

, GAO

. Testing the ectomycorrhizal-dominance hypothesis for ecosystem multifunctionality in a subtropical mountain forest[J]. New Phytologist, 2024, 243(6): 2401-2415.

[23]

FERNANDEZ

, SEE CR, KENNEDY

. Decelerated carbon cycling by ectomycorrhizal fungi is controlled by substrate quality and community composition[J]. New Phytologist, 2020, 226(2): 569-582.

[24]

PLASSARD

, DELL

. Phosphorus nutrition of mycorrhizal trees[J]. Tree Physiology, 2010, 30(9): 1129-1139.

[25]

NEHLS

, PLASSARD

. Nitrogen and phosphate metabolism in ectomycorrhizas[J]. New Phytologist, 2018, 220: 1047-1058.

[26]

田江, 梁翠月, 陆星, 陈倩倩. 根系分泌物调控植物适应低磷胁迫的机制[J]. 华南农业大学学报, 2019, 40(5): 175-185.

TIAN

, LIANG

, LU

, CHEN

. Mechanism of root exudates regulating plant responses to phosphorus deficiency[J]. Journal of South China Agricultural University, 2019, 40(5): 175-185 (in Chinese).

[27]

KOUR

, RANA

, KAUR

, YADAV

, KUMAR

, DHALIWAL

, SAXENA

. Biodiversity, current developments and potential biotechnological applications of phosphorus-solubilizing and-mobilizing microbes: a review[J]. Pedosphere, 2021, 31(1): 43-75.

[28]

COURTY

, BUÉE

, DIEDHIOU

, FREY-KLETT

, Le TACON

, RINEAU

, TURPAULT

, UROZ

, GARBAYE

. The role of ectomycorrhizal communities in forest ecosystem processes: new perspectives and emerging concepts[J]. Soil Biology and Biochemistry, 2010, 42(5): 679-698.

[29]

江盈, 邹锋, 黄建, 戴伟红, 左荣花, 田诗义, 熊欢. 六个外生菌根真菌菌株在不同难溶性磷源下的溶磷特性[J]. 菌物学报, 2023, 42(6): 1311-1329.

JIANG

, ZOU

, HUANG

, DAI

, ZUO

, TIAN

, XIONG

. Phosphorus dissolving characteristics of six ectomycorrhizal fungal strains under different insoluble phosphorus sources[J]. Mycosystema, 2023, 42(6): 1311-1329 (in Chinese).

[30]

D’AMICO

, ALMEIDA

, BARBIERI

, CASTELLI

, SGURA

, SINEO

, MARTIN

, BONIFACIO

, WALLANDER

, CELI

. Ectomycorrhizal utilization of different phosphorus sources in a glacier forefront in the Italian Alps[J]. Plant and Soil, 2020, 446(1): 81-95.

[31]

ADELINE

, CARMEN

, EIBENSTEINER

, GABRIELLA

, HEIKE

, ZIMMERMANN

, KEVIN

. The ectomycorrhizal contribution to tree nutrition[J]. Advances in Botanical Research, 2019, 89(1/2): 77-126.

[32]

BECQUER

, GARCIA

, AMENC

, RIVARD

, DORÉ

, TRIVES-SEGURA

, SZPONARSKI

, RUSSET

, BAEZA

, LASSALLE-KAISER

, GAY G, ZIMMERMANN

, PLASSARD

. The Hebeloma cylindrosporum HcPT2 Pi transporter plays a key role in ectomycorrhizal symbiosis[J]. New Phytologist, 2018, 220(4): 1185-1199.

[33]

WANG

, LI

, WU

, ZHAO

. Molecular cloning and functional analysis of a H(+)-dependent phosphate transporter gene from the ectomycorrhizal fungus Boletus edulis in Southwest China[J]. Fungal Biology, 2014, 118(5/6): 453-461.

[34]

PAPAROKIDOU

, LEAKE

, BEERLING

, ROLFE

. Phosphate availability and ectomycorrhizal symbiosis with Pinus sylvestris have independent effects on the Paxillus involutus transcriptome[J]. Mycorrhiza, 2021, 31(1): 69-83.

[35]

KANG

, TWAGIRAYEZU

, XU

, WEN

, SHANG

, SONG

, WANG

, LI

, LIU

, CHEN

, CHENG

, ZHANG

. Arbuscular mycorrhizal fungi regulate lipid and amino acid metabolic pathways to promote the growth of Poncirus trifoliata (L.) Raf[J]. Journal of Fungi, 2024, 10(6): 427.

[36]

MADRID-DELGADO

, OROZCO-MIRANDA

, CRUZ-OSORIO

, HERNÁNDEZ-RODRÍGUEZ

, RODRÍGUEZ-HEREDIA

, ROA-HUERTA

, AVILA-QUEZADA

. Pathways of phosphorus absorption and early signaling between the mycorrhizal fungi and plants[J]. Phyton-International Journal of Experimental Botany, 2021, 90(5): 1321-1338.

[37]

LOTH-PEREDA

, ORSINI

, COURTY

, LOTA

, KOHLER

, DISS

, BLAUDEZ

, CHALOT

, NEHLS

, BUCHER

, MARTIN

. Structure and expression profile of the phosphate Pht1 transporter gene family in mycorrhizal Populus trichocarpa [J]. Plant Physiology, 2011, 156(4): 2141-2154.

[38]

PLETT

, PLETT

. Leveraging genomics to understand the broader role of fungal small secreted proteins in niche colonization and nutrition[J]. ISME Communications, 2022, 2: 49.

[39]

SNELDERS

, ROVENICH

, THOMMA

BPHJ

. Microbiota manipulation through the secretion of effector proteins is fundamental to the wealth of lifestyles in the fungal kingdom[J]. FEMS Microbiology Reviews, 2022, 46(5): fuac022.

[40]

袁志林, 潘雪玉, 靳微. 林木共生菌系统及其作用机制: 以杨树为例[J]. 生态学报, 2019, 39(1): 381-397.

YUAN

, PAN

, JIN

. Tree-associated symbiotic microbes and underlying mechanisms of ecological interactions: a case study of poplar[J]. Acta Ecologica Sinica, 2019, 39(1): 381-397 (in Chinese).

[41]

徐漫, 傅婉秋, 戴传超, 贾永. 外生菌根真菌促生微生物生态功能研究进展[J]. 生态学杂志, 2018, 37(4): 1246-1256.

, FU

, DAI

, JIA

. Ecological function of promoting microorganisms associated with ectomycorrhizal fungi[J]. Chinese Journal of Ecology, 2018, 37(4): 1246-1256 (in Chinese).

[42]

PARTIDA-MARTÍNEZ

. The fungal holobiont: evidence from early diverging fungi[J]. Environmental Microbiology, 2017, 19(8): 2919-2923.

[43]

FREY-KLETT

, GARBAYE

. Mycorrhiza helper bacteria: a promising model for the genomic analysis of fungal-bacterial interactions[J]. New Phytologist, 2005, 168(1): 4-8.

[44]

WANG

, GUO

, FAN

, LIU

, LIN

, SHI

, HE

, YE

, HUANG

, JI

, ZHANG

, WALL

, LIU

, CUI

, LI

. A predator-prey interaction between myxobacteria and fungi mediated by outer membrane vesicles[J]. Journal of Advanced Research, 2025: S2090-1232(25)00771-4.

[45]

LIU

, ZUO

, LI

, FU

, HE

, WANG

, LI

, WAN

, WANG

, ZHU

, SHEN

. Activation of an antifungal pathway in Yersinia pseudotuberculosis by chitin-receptor-mediated fungal recognition[J]. Current Biology, 2025, 35(11): 2672-2683.

[46]

, SHI

, WANG

, ZHOU

, WANG

, XU

, RAZA

, LIU

, SHEN

. Turning antagonists into allies: Bacterial-fungal interactions enhance the efficacy of controlling Fusarium wilt disease[J]. Science Advances, 2025, 11(7): eads5089.

[47]

TIAN

, DING

, KE

, WANG

. Quorum Sensing in Fungal Species[J]. Annual Review of Microbiology, 2021, 75: 449-469.

[48]

LIU

, XU

, CHEN

, XUN

, SHU

, CHEN

, SUN

, WANG

, REN

, SHEN

, ZHANG

. Root colonization by beneficial rhizobacteria[J]. FEMS Microbiology Reviews, 2024, 48(1): fuad066.

[49]

RICHTER

, BLEI

, HU

, SCHWITALLA

, LOZANO-ANDRADE

, XIE

, JARMUSCH

, WIBOWO

, KJELDGAARD

, SURABHI

, XU

, JAUTZUS

, PHIPPEN

CBW

, TYC O, ARENTSHORST

, WANG

, GARBEVA

, LARSEN

, RAM AFJ, van den HONDEL

CAM

, et al. Enhanced surface colonisation and competition during bacterial adaptation to a fungus[J]. Nature Communications, 2024, 15: 4486.

[50]

ZHANG

, KASTMAN

, GUASTO

, WOLFE

. Fungal networks shape dynamics of bacterial dispersal and community assembly in cheese rind microbiomes[J]. Nature Communications, 2018, 9: 336.

[51]

SENEVIRATNE

, ZAVAHIR

, BANDARA

WMMS

, WEERASEKARA

MLMAW

. Fungal-bacterial biofilms: their development for novel biotechnological applications[J]. World Journal of Microbiology and Biotechnology, 2008, 24(6): 739-743.

[52]

KJELDGAARD

, LISTIAN

, RAMASWAMHI

, RICHTER

, KIESEWALTER

, KOVÁCS

ÁT

. Fungal hyphae colonization by Bacillus subtilis relies on biofilm matrix components[J]. Biofilm, 2019, 1: 100007.

[53]

MIQUEL GUENNOC

, ROSE

, LABBÉ

, DEVEAU

. Bacterial biofilm formation on the hyphae of ectomycorrhizal fungi: a widespread ability under controls[J]. FEMS Microbiology Ecology, 2018, 94(7): fiy093.

[54]

张朝辉, 张广, 闻亚美, 杨艳青, 刘亚非, 张会, 王振河, 邱立友. l-氨基环丙烷-l-羧酸在恶臭假单胞菌趋化双孢蘑菇菌丝中的作用[J]. 华北农学报, 2019, 34(6): 209-218.

ZHANG

, ZHANG

, WEN

, YANG

, LIU

, ZHANG

, WANG

, QIU

. The role of l-aminocyclopropane-l-carboxylate in the chemotactic response of Pseudomonas putida to Agaricus bisporus mycelia[J]. Acta Agriculturae Boreali-Sinica, 2019, 34(6): 209-218 (in Chinese).

[55]

BERRIOS

, BOGAR

, VENTURINI

, WILLING

, del

RIO A

, ANSELL

, ZEMAITIS

, VELICKOVIC

, PELLITIER

, YEAM

, HUTCHINSON

, BLOODSWORTH

, LIPTON

, PEAY

. Ectomycorrhizal fungi alter soil food webs and the functional potential of bacterial communities[J]. mSystems, 2024, 9(6): e0036924.

[56]

RANGEL-CASTRO

, DANELL

, PFEFFER

. A ¹³C-NMR study of exudation and storage of carbohydrates and amino acids in the ectomycorrhizal edible mushroom Cantharellus cibarius [J]. Mycologia, 2002, 94(2): 190-199.

[57]

TIMONEN

, JØRGENSEN

, HAAHTELA

, SEN R. Bacterial community structure at defined locations of Pinus sylvestris-Suillus bovinus and Pinus sylvestris-Paxillus involutus mycorrhizospheres in dry pine forest humus and nursery peat[J]. Canadian Journal of Microbiology, 1998, 44(6): 499-513.

[58]

DOUGLAS

. The microbial exometabolome: ecological resource and architect of microbial communities[J]. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences, 2020, 375(1798): 20190250.

[59]

DEVEAU

, BRULÉ

, PALIN

, CHAMPMARTIN

, RUBINI

, GARBAYE

, SARNIGUET

, FREY-KLETT

. Role of fungal trehalose and bacterial thiamine in the improved survival and growth of the ectomycorrhizal fungus Laccaria bicolor S238N and the helper bacterium Pseudomonas fluorescens BBc6R8[J]. Environmental Microbiology Reports, 2010, 2(4): 560-568.

[60]

ZHENG

, LIU

, ZHANG

, WANG

, NG TB. Purification and characterization of an antibacterial protein from dried fruiting bodies of the wild mushroom Clitocybe sinopica [J]. Acta Biochimica Polonica, 2010, 57(1): 43-48.

[61]

ERJAVEC

, RAVNIKAR

, BRZIN

, GREBENC

, BLEJEC

, GOSAK

MŽ

, SABOTIČ

, KOS J, DREO

. Antibacterial activity of wild mushroom extracts on bacterial wilt pathogen Ralstonia solanacearum [J]. Plant Disease, 2016, 100(2): 453-464.

[62]

SHIRAKAWA

, UEHARA

, TANAKA

. Mycorrhizosphere bacterial communities and their sensitivity to antibacterial activity of ectomycorrhizal fungi[J]. Microbes and Environments, 2019, 34(2): 191-198.

[63]

葛伟, 董醇波, 张芝元, 韩燕峰, 梁宗琦. 外生菌根真菌与内生细菌共生互作的研究进展[J]. 微生物学通报, 2021, 48(10): 3810-3822.

, DONG

, ZHANG

, HAN

, LIANG

. Symbiotic interaction between ectomycorrhizal fungi and endobacteria: a review[J]. Microbiology China, 2021, 48(10): 3810-3822 (in Chinese).

[64]

COSETTA

, KFOURY

, ROBBAT

, WOLFE

. Fungal volatiles mediate cheese rind microbiome assembly[J]. Environmental Microbiology, 2020, 22(11): 4745-4760.

[65]

UROZ

, TURPAULT

, van SCHOLL

, PALIN

, FREY-KLETT

. Long term impact of mineral amendment on the distribution of the mineral weathering associated bacterial communities from the beech Scleroderma citrinum ectomycorrhizosphere[J]. Soil Biology and Biochemistry, 2011, 43(11): 2275-2282.

[66]

PAVIĆ

, STANKOVIĆ

, SALJNIKOV

, KRÜGER

, BUSCOT

, TARKKA

, MARJANOVIĆ

. Actinobacteria may influence white truffle (Tuber magnatum Pico) nutrition, ascocarp degradation and interactions with other soil fungi[J]. Fungal Ecology, 2013, 6(6): 527-538.

[67]

MONACO

, NACLERIO

, MELLO

, BUCCI

. Role and potentialities of bacteria associated with Tuber magnatum: a mini-review[J]. Frontiers in Microbiology, 2022, 13: 1017089.

[68]

NAZIR

, TAZETDINOVA

, van ELSAS

. Burkholderia terrae BS001 migrates proficiently with diverse fungal hosts through soil and provides protection from antifungal agents[J]. Frontiers in Microbiology, 2014, 5: 598.

[69]

MAIER

, RIEDLINGER

, FIEDLER

, HAMPP

. Actinomycetales bacteria from a spruce stand: characterization and effects on growth of root symbiotic and plant parasitic soil fungi in dual culture[J]. Mycological Progress, 2004, 3(2): 129-136.

[70]

CHEN

, LI

, CAO

, WU

, KUANG

, YU

. Comparison of bacterial communities in five ectomycorrhizal fungi mycosphere soil[J]. Microorganisms, 2024, 12(7): 1329.

[71]

MEI

, ZHANG

, CAO

, ZHU

, ZHANG

, BAI

, DAI

, JIA

. Endofungal bacteria and ectomycorrhizal fungi synergistically promote the absorption of organic phosphorus in Pinus massoniana [J]. Plant, Cell & Environment, 2024, 47(2): 600-610.

[72]

DEVEAU

, BONITO

, UEHLING

, PAOLETTI

, BECKER

, BINDSCHEDLER

, HACQUARD

, HERVÉ

, LABBÉ

, LASTOVETSKY

, MIESZKIN

, MILLET

, VAJNA

, JUNIER

, BONFANTE

, KROM

, OLSSON

, van ELSAS

, WICK

. Bacterial-fungal interactions: ecology, mechanisms and challenges[J]. FEMS Microbiology Reviews, 2018, 42(3): 335-352.

[73]

WANG

, JIN

, GEORGE

, FENG

, ZHANG

. Arbuscular mycorrhizal fungi enhance plant phosphorus uptake through stimulating hyphosphere soil microbiome functional profiles for phosphorus turnover[J]. New Phytologist, 2023, 238(6): 2578-2593.

[74]

SOKOL

, SLESSAREV

, MARSCHMANN

, NICOLAS

, BLAZEWICZ

, BRODIE

, FIRESTONE

, FOLEY

, HESTRIN

, HUNGATE

, KOCH

, STONE

, SULLIVAN

, ZABLOCKI

, PETT-RIDGE

. Life and death in the soil microbiome: how ecological processes influence biogeochemistry[J]. Nature Reviews Microbiology, 2022, 20(7): 415-430.

[75]

梁宗琦, 韩燕峰, 梁建东, 陈万浩, 张芝元, 董醇波, 邵秋雨, 葛伟, 刘宇星. 从细胞内共生到多尺度共生: 回顾与展望[J]. 菌物学报, 2020, 39(12): 2202-2217.

LIANG

, HAN

, LIANG

, CHEN

, ZHANG

, DONG

, SHAO

, GE

, LIU

. From intracellular symbiosis to multiscale symbiosis: review and prospect[J]. Mycosystema, 2020, 39(12): 2202-2217 (in Chinese).

[76]

WARMINK

, van ELSAS

. Migratory response of soil bacteria to Lyophyllum sp. strain Karsten in soil microcosms[J]. Applied and Environmental Microbiology, 2009, 75(9): 2820-2830.

[77]

BERRIOS

, YEAM

, HOLM

, ROBINSON

, PELLITIER

, CHIN

, HENKEL

, PEAY

. Positive interactions between mycorrhizal fungi and bacteria are widespread and benefit plant growth[J]. Current Biology, 2023, 33(14): 2878-2887.

[78]

WANG

, HOU

, WU

, ZHU

, DAI

, ZHAO

. Mycorrhiza helper bacterium Bacillus pumilus HR10 improves growth and nutritional status of Pinus thunbergii by promoting mycorrhizal proliferation[J]. Tree Physiology, 2022, 42(4): 907-918.

[79]

WANG

, DAI

, KONG

, ZHU

, WU

. Improvement of Sphaeropsis shoot blight disease resistance by applying the ectomycorrhizal fungus Hymenochaete sp. Rl and mycorrhizal helper bacterium Bacillus pumilus HR10 to Pinus thunbergii [J]. Phytopathology, 2022, 112(6): 1226-1234.

[80]

DUAN

, HUO

, TIAN

, YAN

, GEORGE

, HUANG

, FENG

, ZHANG

. The interplay of direct and mycorrhizal pathways for plants to efficiently acquire phosphorus from soil[J]. Frontiers of Agricultural Science & Engineering, 2025, 12(1): 47-56.

[81]

ZAVIŠIĆ

, YANG

, MARHAN

, KANDELER

, POLLE

. Forest soil phosphorus resources and fertilization affect ectomycorrhizal community composition, beech P uptake efficiency, and photosynthesis[J]. Frontiers in Plant Science, 2018, 9: 463.

[82]

ZHOU

, GUBE

, HOLZ

, SONG

, SHAN

, SHI

, KUZYAKOV

, DIPPOLD

, PAUSCH

. Ectomycorrhizal and non-mycorrhizal rhizosphere fungi increase root-derived C input to soil and modify enzyme activities: a ¹⁴C pulse labelling of Picea abies seedlings[J]. Plant, Cell & Environment, 2022, 45(10): 3122-3133.

[83]

TATRY

, KASSIS E

, LAMBILLIOTTE

, CORRATGÉ

, van AARLE

, AMENC

, ALARY

, ZIMMERMANN

, SENTENAC

, PLASSARD

. Two differentially regulated phosphate transporters from the symbiotic fungus Hebeloma cylindrosporum and phosphorus acquisition by ectomycorrhizal Pinus pinaster [J]. The Plant Journal, 2009, 57(6): 1092-1102.

[84]

薛伟, 王庆贵, 闫国永, 邢亚娟. 氮沉降影响土壤磷与ECM和SAP真菌关系研究进展[J]. 环境保护前沿, 2022(6): 1179-1188.

XUE

, WANG

, YAN

, XING

. The effect of nitrogen deposition on the relationship between soil phosphorus and ECM and SAP fungi: a review[J]. Advances in Environmental Protection, 2022(6): 1179-1188 (in Chinese).

[85]

JÖRGENSEN

, CLEMMENSEN

, FRANSSON

, MANZONI

, WALLANDER

, LINDAHL

. A trait spectrum linking nitrogen acquisition and carbon use of ectomycorrhizal fungi[J]. New Phytologist, 2025, 246(6): 2425-2434.

[86]

BOGAR

. Modified source-sink dynamics govern resource exchange in ectomycorrhizal symbiosis[J]. New Phytologist, 2024, 242(4): 1523-1528.

[87]

SUN

, CHENG

, XIAO

, ZENG

, SHEN

, WANG

, CHEN

, ZHANG

. The relationship between ectomycorrhizal fungi, nitrogen deposition, and Pinus massoniana seedling nitrogen transporter gene expression and nitrogen uptake kinetics[J]. Journal of Fungi, 2023, 9(1): 65.

[88]

王保明, 陈永忠, 王湘南, 陈隆升, 彭邵锋, 王瑞, 马力, 杨小胡, 罗键. 植物低磷胁迫响应及其调控机制[J]. 福建农林大学学报(自然科学版), 2015, 44(6): 567-575.

WANG

, CHEN

, WANG

, CHEN

, PENG

, WANG

, MA

, YANG

, LUO

. The response to low phosphorus stress and its regulation mechanism in plants[J]. Journal of Fujian Agriculture and Forestry University:Natural Science Edition, 2015, 44(6): 567-575 (in Chinese).

[89]

曹庆芹, 冯永庆, 刘玉芬, 郭献平, 张国庆, 秦岭. 菌根真菌促进植物磷吸收研究进展[J].生命科学, 2011, 23(4): 407-413.

CAO

, FENG

, LIU

, GUO

, ZHANG

, QIN

. Advance of plant phosphorus uptake improved by mycorrhiza fungi[J]. Chinese Bulletin of Life Sciences, 2011, 23(4): 407-413 (in Chinese).

[90]

KAFLE

, COPE

, RATHS

, KRISHNA YAKHA

, SUBRAMANIAN

, BÜCKING

, GARCIA

. Harnessing soil microbes to improve plant phosphate efficiency in cropping systems[J]. Agronomy, 2019, 9(3): 127.

[91]

TIBBETT

, SANDERS

. Ectomycorrhizal symbiosis can enhance plant nutrition through improved access to discrete organic nutrient patches of high resource quality[J]. Annals of Botany, 2002, 89(6): 783-789.

[92]

GUAN

, JAKOB

. The protein scaffolding functions of polyphosphate[J]. Journal of Molecular Biology, 2024, 436(14): 168504.

[93]

CAIRNEY

JWG

. Ectomycorrhizal fungi: the symbiotic route to the root for phosphorus in forest soils[J]. Plant and Soil, 2011, 344(1): 51-71.

[94]

ASHFORD

, ALLAWAY

. The role of the motile tubular vacuole system in mycorrhizal fungi[J]. Plant and Soil, 2002, 244(1): 177-187.

[95]

GUAN

, CHEN

, LIU

, CHEN

, XING

, DU

, CHENG

, HU

, ZHANG

, MEI

, WAN

, WANG

, ZHANG

, CHENG

, CAI

, CAO

, ZHANG

, YAN

, YIN

, HOTHORN

, LIU

. The cytoplasmic synthesis and coupled membrane translocation of eukaryotic polyphosphate by signal-activated VTC complex[J]. Nature Communications, 2023, 14(1): 718.

[96]

LIU

, WANG

, COMTE-MISEREZ

, ZHANG

, YU

, CHEN

, JESSEN

, MAYER

, WU

, YE

. Cryo-EM structure of the polyphosphate polymerase VTC reveals coupling of polymer synthesis to membrane transit[J]. The EMBO Journal, 2023, 42(10): e113320.

[97]

LICHKO

, KULAKOVSKAYA

, KULAEV

. Inorganic polyphosphates and exopolyphosphatases in different cell compartments of Saccharomyces cerevisiae [J]. Biochemistry (Moscow), 2006, 71(11): 1171-1175.

[98]

LIU

, WANG

, COMTE-MISEREZ

, ZHANG

, YU

, CHEN

, JESSEN

, MAYER

, WU

, YE

. Cryo-EM structure of the polyphosphate polymerase VTC reveals coupling of polymer synthesis to membrane transit[J]. EMBO Journal, 2023, 42(10): e113320.

[99]

GUAN

, CHEN

, LIU

, CHEN

, XING

, DU

, CHENG

, HU

, ZHANG

, MEI

, WAN

, WANG

, ZHANG

, CHENG

, CAI

, CAO

, ZHANG

, YAN

, YIN

, HOTHORN

, et al. The cytoplasmic synthesis and coupled membrane translocation of eukaryotic polyphosphate by signal-activated VTC complex[J]. Nature Communications, 2023, 14: 718.

[100]

TORRES-AQUINO

, BECQUER

, Le GUERNEVÉ

, LOUCHE

, AMENC

, STAUNTON

, QUIQUAMPOIX

, PLASSARD

. The host plant Pinus pinaster exerts specific effects on phosphate efflux and polyphosphate metabolism of the ectomycorrhizal fungus Hebeloma cylindrosporum: a radiotracer, cytological staining and ³¹P NMR spectroscopy study[J]. Plant, Cell & Environment, 2017, 40(2): 190-202.

[101]

NAGY

, DRISSNER

, AMRHEIN

, JAKOBSEN

, BUCHER

. Mycorrhizal phosphate uptake pathway in tomato is phosphorus-repressible and transcriptionally regulated[J]. New Phytologist, 2009, 181(4): 950-959.

[102]

LIM SL, VOON

, GUAN

, YANG

, GARDESTRÖM

, LIM BL. In planta study of photosynthesis and photorespiration using NADPH and NADH/NAD⁺ fluorescent protein sensors[J]. Nature Communications, 2020, 11(1): 3238.

[103]

孙艳, 洪婉婷, 韩阳, 徐梓楷, 程凌云. 植物内部磷循环利用提高磷效率的研究进展[J].植物营养与肥料学报, 2021, 27(12): 2216-2228.

SUN

, HONG

, HAN

, XU

, CHEN

. Targeting internal phosphorus re-utilization to improve plant phosphorus use efficiency[J]. Journal of Plant Nutrition and Fertilizers, 2021, 27(12): 2216-2228 (in Chinese).

[104]

ZHANG

, van der HEIJDEN

MGA

, DODDS

, NGUYEN

, SPOOREN

, VALZANO-HELD

, COSME

, BERENDSEN

. A tripartite bacterial-fungal-plant symbiosis in the mycorrhiza-shaped microbiome drives plant growth and mycorrhization[J]. Microbiome, 2024, 12(1): 13.

[105]

FRÖJD

, FLÄRDH

. Extrusion of extracellular membrane vesicles from hyphal tips of Streptomyces venezuelae coupled to cell-wall stress[J]. Microbiology, 2019, 165(12): 1295-1305.

[106]

MEYER

, NODWELL

. Streptomyces extracellular vesicles are a broad and permissive antimicrobial packaging and delivery system[J]. Journal of Bacteriology, 2024, 206(3): e0032523.

[107]

HOLLAND

, ROTH

. Extracellular vesicles in the arbuscular mycorrhizal symbiosis: current understanding and future perspectives[J]. Molecular Plant-Microbe Interactions, 2023, 36(4): 235-244.

2026年第66卷第1期

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doi: 10.13343/j.cnki.wsxb.20250478

接收时间：2025-06-19
首发时间：2026-01-12
出版时间：2026-01-04

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南京师范大学生命科学学院，江苏省微生物病原与生态省高校重点实验室，江苏南京

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2种不同金属材料的力学参数

科 Family	属数 Number of genus	种数 Number of species	占总种数比例 Percentage of total species (%)	属 Genus	种数 Number of species	占总种数比例 Percentage of total species (%)
鹅膏菌科Amanitaceae	2	11	5.26	鹅膏菌属 Amanita	10	4.78
小菇科 Mycenaceae	2	12	5.74	丝盖伞属 Inocybe	5	2.39
多孔菌科 Polyporaceae	8	14	6.70	蜡蘑属 Laccaria	5	2.39
红菇科 Russulaceae	3	23	11.00	小皮伞属 Marasmius	6	2.87
				小菇属 Mycena	11	5.26
				光柄菇属 Pluteus	5	2.39
				红菇属 Russula	17	8.13
				栓菌属 Trametes	5	2.39

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Functional stage	Key mechanism	Molecular mechanism & regulation	References
Mineralization of inorganic phosphorus	Secretion of low molecular weight organic acids (LMWOAs)	Electrostatic/covalent interactions	[26]
Proton (H⁺) release	Acidification: reduces environmental pH	[29]
Siderophore secretion	Chelation: sequesters metal cations	[30]
Enzymatic hydrolysis	Secretion of phosphatases and other hydrolytic enzymes	[27]
Pi uptake	High-affinity phosphate transporters (PTs)	Primarily H⁺:Pi and Na⁺:Pi cotransporters; regulated by Pi levels (upregulated under low Pi conditions)	[32]
Pi storage and transport	Conversion to polyphosphates (poly-P)	Converted to poly-P in hyphal vacuoles; transported within hyphae via a motile tubular vacuole system	[35]
Transport to the Hartig net
Pi release at the symbiotic interface	PT-mediated Pi release	Poly-P hydrolyzed by polyphosphatases; free Pi is released across the hyphal plasma membrane	[36]
Host plant regulation	Upregulation of specific phosphate transporter gene expression	Differential activation of phosphate transporter genes in host plants (e.g., PtPT9 and PtPT12 in Populus tomentosa)	[37]

Functional stage

Key mechanism

Molecular mechanism & regulation

References

Mineralization of inorganic phosphorus

Secretion of low molecular weight organic acids (LMWOAs)

Electrostatic/covalent interactions

[26]

Proton (H⁺) release

Acidification: reduces environmental pH

[29]

Siderophore secretion

Chelation: sequesters metal cations

[30]

Enzymatic hydrolysis

Secretion of phosphatases and other hydrolytic enzymes

[27]

Pi uptake

High-affinity phosphate transporters (PTs)

Primarily H⁺:Pi and Na⁺:Pi cotransporters; regulated by Pi levels (upregulated under low Pi conditions)

[32]

Pi storage and transport

Conversion to polyphosphates (poly-P)

Converted to poly-P in hyphal vacuoles; transported within hyphae via a motile tubular vacuole system

[35]

Transport to the Hartig net

Pi release at the symbiotic interface

PT-mediated Pi release

Poly-P hydrolyzed by polyphosphatases; free Pi is released across the hyphal plasma membrane

[36]

Host plant regulation

Upregulation of specific phosphate transporter gene expression

Differential activation of phosphate transporter genes in host plants (e.g., PtPT9 and PtPT12 in Populus tomentosa)

[37]

Interaction level	Mechanism category	Specific mode	Function	References
Physical-level interactions	Surface attachment and colonization	Bacteria colonize hyphae via adhesins/surfactins	Establishes physical interaction channels	[49-50]
Biofilm formation	Bacteria rely on EPS/TasA/eDNA/ACC signaling to form biofilms→Enhances symbiotic stability	Enhances symbiotic stability	[51-54]
Metabolic-level interactions	Metabolic cross-feeding	ECMF secretes sugar alcohols to induce bacterial community differentiation; auxotrophic fungi-bacteria interactions	Drives nutritional mutualism	[55-59]
Regulation via antimicrobial substances	ECMF secretes mycotoxins/antimicrobial proteins to shape resistant bacterial communities	Optimizes the symbiotic microenvironment	[60-62]
Mediation by volatile organic compounds (VOCs)	Fungal VOCs activate bacterial metabolic pathways	Facilitates community interaction beyond spatial constraints	[63-64]
Functional-level interactions	Nutrient mobilization and synergy	Helper bacteria enhance phosphate dissolution/enzyme activity	Improves nutrient absorption and cycling	[65-66]
Biotic stress defense	Bacteria effectively suppress pathogens, protecting host fungi	Enhances host fungal resistance	[67-69]
Co-evolutionary significance	Community co-adaptation	Highly specific ECMF-bacterial interactions co-drive nutrient cycling and niche differentiation	Maintains ecosystem stability	[42-43]

Interaction level

Mechanism category

Specific mode

Function

References

Physical-level interactions

Surface attachment and colonization

Bacteria colonize hyphae via adhesins/surfactins

Establishes physical interaction channels

[49-50]

Biofilm formation

Bacteria rely on EPS/TasA/eDNA/ACC signaling to form biofilms→Enhances symbiotic stability

Enhances symbiotic stability

[51-54]

Metabolic-level interactions

Metabolic cross-feeding

ECMF secretes sugar alcohols to induce bacterial community differentiation; auxotrophic fungi-bacteria interactions

Drives nutritional mutualism

[55-59]

Regulation via antimicrobial substances

ECMF secretes mycotoxins/antimicrobial proteins to shape resistant bacterial communities

Optimizes the symbiotic microenvironment

[60-62]

Mediation by volatile organic compounds (VOCs)

Fungal VOCs activate bacterial metabolic pathways

Facilitates community interaction beyond spatial constraints

[63-64]

Functional-level interactions

Nutrient mobilization and synergy

Helper bacteria enhance phosphate dissolution/enzyme activity

Improves nutrient absorption and cycling

[65-66]

Biotic stress defense

Bacteria effectively suppress pathogens, protecting host fungi

Enhances host fungal resistance

[67-69]

Co-evolutionary significance

Community co-adaptation

Highly specific ECMF-bacterial interactions co-drive nutrient cycling and niche differentiation

Maintains ecosystem stability

[42-43]

Stage	Key participants	Primary function	Core mechanisms	References
Phosphorus source response	ECMF	Establish a synergistic system	Recruit chemotactic functional bacteria and facilitates biofilm formation	[75]
Synergistic mobilization	ECMF-functional bacteria	Conversion of insoluble phosphorus sources→PO₄^3-	Organic acid synergy enhances dissolution; secretion of phosphatases hydrolyzes organic phosphorus	[76]
Phosphorus transport	Hyphal PT transporters	PO₄^3-→poly-P (vacuolar storage)	Bidirectional vacuolar transport: transported to the Hartig net under sufficient carbon supply; retrieved and stored under carbon limitation	[92-96]
Mycorrhizal uptake	ECMF polyphosphatase (PPX1/VTC)-plant Pht1L phosphate transporter	poly-P→PO₄^3-→organic phosphorus (e.g., ATP/nucleic acids)	Host carbon-phosphorus exchange signals trigger poly-P hydrolysis in the Hartig net and activate Pht1 family genes	[97-100]

Stage

Key participants

Primary function

Core mechanisms

References

Phosphorus source response

ECMF

Establish a synergistic system

Recruit chemotactic functional bacteria and facilitates biofilm formation

[75]

Synergistic mobilization

ECMF-functional bacteria