农业生态系统中AM真菌、禾草内生真菌及病原菌互作

李 芳，张 峰，高 萍，段廷玉

(草地农业生态系统国家重点实验室，兰州大学草地农业科技学院，甘肃 兰州 730020)



农业生态系统中AM真菌、禾草内生真菌及病原菌互作

李 芳，张 峰，高 萍，段廷玉

(草地农业生态系统国家重点实验室，兰州大学草地农业科技学院，甘肃 兰州 730020)

摘要：丛枝菌根真菌(Arbuscular Mycorrhizal Fungi，AMF)、禾草内生真菌和植物病原菌广泛存在于农业生态系统中。AMF和禾草内生真菌均能与宿主植物形成共生体，促进宿主植物对养分、水分的吸收，提高植物对病害、干旱等生物和非生物逆境的抗性。植物病原菌引致的植物病害可降低植物产量和品质，造成生产上的重大损失。AMF可降低植物发病率和病情指数，其机理包括AMF与病原菌竞争侵染位点，养分和空间、消耗病原菌的能量、提高菌根植物对水分和养分的利用效率、调节病程相关蛋白。禾草内生真菌可通过分泌抑菌活性物质、诱导植物体产生抗性反应及减少病害介体的传播，提高植物地上生物量和抗病性。AMF和禾草内生真菌与其它微生物的互作因植物、真菌而异，有相互促进的效应，也有相互抑制的效应。研究和明确农业生态系统中三类微生物的互作机理，进而利用禾草内生真菌和AMF提高抗逆性及产量、防治病害，对于促进和维持农业生态系统可持续发展具有重要的意义。

关键词：丛枝菌根真菌；禾草内生真菌；植物病原菌；互作

微生物是农业生态系统中的重要成员，有着不可替代的作用。作为生态系统中的重要分解者，参与C、N、P、S等养分循环[1]，或与植物建立共生关系，如丛枝菌根(Arbuscular Mycorrhiza，AM)真菌和禾草内生真菌(Epichlo⊇)，两类共生微生物均可提高植物对N、P、K等养分[2-4]、水分[5-6]的吸收和利用效率，提高植物对病[7-8]、虫[8-9]等生物逆境以及干旱[8,10]、盐碱[11-13]、低温[14-15]和重金属[16-17]等非生物逆境的抗性，从而促进植物的生长，提高植物在农业生态系统中的竞争力，进而维持农业生态系统的稳定性和可持续性[18]。

同时，微生物亦可作为消费者，如，病原菌(病原真菌、细菌、病毒和线虫等)可引致植物病害，降低植物产量，改变植被组成[19]，导致家畜中毒，造成重大经济损失。以天然草地为例， 2013年，我国天然草地鲜草总产量105 581.21万t，折合干草约32 542.92万t，以病害造成干草损失5%[19]计算，可造成干草产量损失1 627.15万t，以每公斤干草0.2元计算，造成经济损失32.54亿元。

微生物与植物在长期协同进化过程中形成了共生、共栖和寄生等多种复杂关系，如何利用农业生态系统中的微生物与植物、微生物与微生物之间的关系，降低病害的发生和危害，提高农业生态系统的生产力和可持续性是目前国际上研究的热点[18]。

本文就近年来国内外有关AM真菌、禾草内生真菌与病原菌的互作进行综述，以期为利用AM真菌和禾草内生真菌来防治植物病害，提高和维持农业生态系统生产力和可持续发展，为开展AM真菌、禾草内生真菌和病原菌三者之间的互作研究提供理论依据。

1AM真菌与病原菌

AM真菌属球囊菌门，可与约90%的维管植物形成共生体[20]，广泛存在于农业生态系统中。AM真菌与病原菌的互作关系较为复杂，有研究表明,AM真菌对植物具有一定的保护作用[21]、可减轻病害[22]，还有研究发现AM真菌与植物抗病性无关[23]，但也有AM真菌能加重植物病害的报道[24]。就目前的研究而言，有关抗病的报道居多[25-31]。

1.1AM真菌与病原真菌的互作

1968年Safir[32]首次报道了摩西球囊霉(Glomusmosseae)能减少洋葱红根腐菌(Pyrenochaetaterestris)对洋葱根系的侵染并能减轻红腐病(Red root)的危害，提高植物抗病性。此后，关于二者相互作用的关系被大量报道，但大部分研究仅限于球囊霉属的几个种，如摩西球囊霉、幼套球囊霉(Glomusetunicatum)、根内球囊霉(Glomusintraradices)、地表球囊霉(Glomusversiforme)等。该属AM真菌均可以不同程度地降低立枯丝核菌(Rhizoctoniasolani)、尖孢镰刀菌(Fusairumoxysporum)、黄萎病原菌(Verticilliumdahliae)等引起的植物病害，发病率和病情指数下降[33-36]。随着近年来栽培草地面积的不断扩大，根腐病逐渐成为限制牧草生产的主要病害，仅在紫花苜蓿(Medicagosativa)上，就有镰刀菌(Fusariumspp.)、丝核菌(Rhizoctoniaspp.)、腐霉(Pythiumspp.)和疫霉(Phytophthoraspp.)等病原菌可引致根腐病[37]，但之前AM真菌与病原真菌互作的研究多见于农作物和蔬菜等(表1)，在牧草上的研究相对较少，以后应加大在此方面的研究。

1.2AM真菌与病原菌互作机理

AM真菌可以促进植物对养分、水分的吸收和利用，从而提高植物的生长，这是其提高植物抗病性最主要的功能，但亦存在其它抗病机制，主要包括：1)菌根表面本身分布着大量菌丝体，对病原物构成天然的机械屏障，再加上AM真菌的侵染增强细胞壁木质化程度，增加细胞壁富含羟基脯氨酸糖蛋白(Hydroxyproline-rich Glycoprotein)，使植物根尖表皮增厚，从而阻止病原物的侵入[44]；2)AM真菌能显著改变植物根围的微生物区系，刺激对土传病原物(Soil-borne Pathogens)有拮抗作用的微生物活性，使促进植物生长的细菌[如荧光假单胞菌(Pseudomonasfluorescens)、芽孢杆菌(Bacillus)和其它拮抗菌木霉属(Trichodermaspp.)、链霉菌(Streptomycesspp.)]数量增加[45]。这些有益菌的协同作用有利于降低植物土传病害的危害[46]；3)AM真菌能诱导植物合成茉莉酸等物质[47]产生或激活几丁质酶[48]、β-1，3葡聚糖酶[49]、苯丙氨酸裂解酶[50]等保护酶，从而明显增强了植物抗病性；4)AM真菌可以和病原菌竞争侵染位点[29-30,51-53]、养分和空间[54]。在苗床上聚生球囊霉(G.fasciculatum)接种显著限制了腐霉菌(Pythiumaphanidermatum)在沉香(Aquilariaagallocha)根系组织中的侵染，这正是由于丛枝菌根真菌先侵染根系位点所致[55]；5)AM真菌侵染感病寄主植物时，可以消耗病原菌的光合产物[52]，从而使病原菌的致病能力下降；6)AM真菌根外菌丝体相互交错形成庞大的菌丝网，促进植物对水分和养分，特别是磷酸盐和硝酸盐的吸收利用[25,27]，通过对营养物质和水分的吸收，补偿了因病原菌侵染造成的根系生物量的损失，从而间接减轻病原微生物引起的危害，提高宿主植物的抗病能力[45]；7)AM真菌可以诱导病程相关蛋白，提高宿主对病原物的抵抗力[56]。研究发现，当病原菌侵染菌根化寄主植物时，AM真菌能诱导PAL5基因和几丁质酶基因Chib1等[57]，或通过调控各种抗病基因的表达量及特异性表达来增强宿主植物的抗病性[58]。此外，Gallou等[59]通过实时定量PCR分析发现，菌根化马铃薯(Solanumtuberosum)叶片的疫霉菌(P.infestans)病情指数和病害症状之所以减轻，可能和菌根化马铃薯中与植株系统抗性相关的PR1和PR2基因的诱导表达有关。

表1　AM真菌与病原真菌的互作效应

续表1

AM真菌Arbuscularmycorrhizalfungi病原真菌Pathogenicfungi病害名称Disease寄主植物Host互作结果Interactioneffect试验条件Experimentalconditions参考文献Reference幼套球囊霉G.etunicatum、根内球囊霉G.intraradices立枯丝核菌R.solani菌核病Sclerotina甘薯Ipomoeabatatas病情指数下降Reduceddiseaseindex盆栽Pot[42]巨孢囊霉G.rosea、摩西球囊霉G.mosseae、地表球囊霉G.versiforme尖镰孢菌F.oxysporum枯萎病Fusariumwilt西瓜Citrulluslanatus抑制病原菌的生长和侵染32.7%~53.7%和27.7%~35.1%Restrainpathogenicgrowthandinfection32.7%~53.7%and27.7%~35.1%,respectively大田Field[43]

2禾草内生真菌与病原菌的互作

本文所指内生真菌为寄生在植株体内完成全部或大部分生活周期，而植物体不显示外部症状的一类真菌，无性阶段为Neotyphodium属，有性阶段为香柱菌属(Epichlo⊇)真菌[60],目前众多学者一致认为将Neotyphodium属真菌并入Epichlo⊇属，其菌丝体存在于植物的所有地上部分：茎杆、叶鞘、叶片、花序及种子，但未发现存在于根系中[8]。全世界已发现43种，我国已报道7种Epichlo⊇内生真菌[61-62]。

2.1禾草内生真菌与病原真菌的互作

从1983年Shimanuki和Sato[63]发现含有内生真菌(Epichlo⊇typhina)的梯牧草(Phleumpratense)对引致叶斑病的病原真菌(Cladosporiumphlei)有抗性开始，相继有很多试验均证明禾草内生真菌能够提高植物的抗病性。田沛[64]发现,内生真菌对细交链孢、离蠕孢、燕麦链孢、新月弯孢、小孢壳二孢等10种病原真菌均有抗病性。高羊茅(Festucaarundinacea)、黑麦草(Loliumperenne)、羊草(Leymuschinensis)等植物的内生真菌也能不同程度地降低寄主植物发病率、病情指数、病斑数和植株矮化程度，提高防御性保护酶活性、病叶损失率，增强抗病性，促进植物生长。在PDA培养基上，进行内生真菌和病原真菌竞争试验，发现内生真菌对病原真菌的生长表现出明显的抑制作用[65-68](表2)。

目前，美国和新西兰已经利用禾草内生真菌培育出了对害虫、干旱等具有抗性的品种，并被大量推广、应用[69]，但专门针对抗病性的品种，尚未有报道。

2.2禾草内生真菌提高植物抗病性的机理

禾草内生真菌与AMF一样，可促进植物生长，提高植物抗逆性，这应是该菌提高植物抗病性的机理之一。关于禾草内生真菌的抗病机制，存在以下几种可能：1)禾草内生真菌与病原菌之间存在空间、养分和水分的竞争[8,70-74]。一方面，禾草内生真菌菌丝体在植物叶片、叶鞘等部位的存在，形成菌丝防护网，占据了一定的空间和生态位，从而抵抗病原菌的侵入和定殖[8]；另一方面，禾草内生真菌从寄主植物获得营养,使病害真菌侵染时可获得的水分、养分减少，从而降低植株发病程度[70]；2)禾草内生真菌能够分泌抑制病原菌生长的活性物质，从而降低病原真菌的繁殖和进一步扩展[71-73]。此外，禾草内生真菌共生体产生的化学物质可以作为杀菌剂抑制或杀死一些引起病害的病原真菌、细菌、病毒和原生动物[74]；3)当病原真菌入侵时，禾草内生真菌能快速诱导宿主植物产生几丁质酶、β-1, 3-葡聚糖酶和过氧化物酶、病程相关蛋白、以及抗病相关物质的生成，提高感染内生真菌的禾草中酚类物质和木质素的含量等[75-76]；4)减少病害介体的传播。有些病害会通过昆虫介体传播，而禾草内生真菌能够产生毒素，阻抑带有病毒和真菌的昆虫采食[77-78]，从而阻止了介体昆虫传播病毒，减轻了病毒病的发生。Mahmood等[79]发现E+高羊茅的大麦黄矮病毒(BYDVs)发病率低主要是由于其内生真菌阻抑了大麦黄矮病毒介体的蚜虫的采食率；5)禾草内生真菌可以改变植物的营养，促进植物生长，从而强化寄主植物的能力，间接增加植物对病害的抗性[80]；6)禾草内生真菌能诱导寄主植物本身产生系统抗性反应，从而抑制病原菌的入侵，而植物本身的基因并未发生改变，仍然可以保持天然性状[81]。

表2　禾草内生真菌与病原真菌的互作结果

3AM真菌与禾草内生真菌的互作

农业生态系统中存在着丰富的微生物类群，因此在植物组织中，这些微生物也必然存在复杂的双共生，甚至三共生的相互作用。Porras-Alfaro等[82]利用免培(Culture Independent)环境PCR方法，通过真菌特异性引物扩增发现，植株体内存在丰富多样的真菌类群，包括菌根真菌和内生真菌，因此,植物同时形成两种共生现象在农业生态系统中十分普遍，研究菌根真菌、内生真菌与植物的双共生可以真实反映植物的微生态系统[75-84]。

禾草内生真菌和土壤中的AM真菌可以相互影响。研究发现,禾草内生真菌和AM真菌存在相互竞争的关系，且带内生真菌的禾草植物AM真菌侵染率会降低[85-87]，而Novas等[88]却发现,禾草内生真菌可以增加AM真菌的侵染率，而且在一定浓度内生真菌浸提液作用下可以增加AM真菌菌丝长度。Liu等[89]报道禾草内生真菌降低AM真菌侵染率的同时，AM真菌反过来又减少了内生真菌的菌丝密度和寄主植物叶片中生物碱的含量(生物碱是禾草内生真菌提高宿主抗性的主要原因)；Vicari等[84]和Barker[90]的研究发现，带内生真菌Epichlo⊇festucae的黑麦草被摩西球囊霉(G.mosseae)和聚生球囊霉(G.fasciculatum)侵染后抗虫性降低。也有研究发现，内生真菌Epichlo⊇elymi可以促进摩西球囊霉侵染，抑制近明球囊霉(G.claroideum)的侵染[91]，即摩西球囊霉和内生真菌E.elymi共同作用于寄主植物时，对植物的生长效应是叠加的。研究表明，在无胁迫条件下，禾草内生真菌和菌根真菌均可显著增加野大麦(Hordeumbrevisubulatum)的地上生物量和总生物量，而菌根真菌可显著增加野大麦的地下生物量，禾草内生真菌的存在可显著抑制丛枝菌根真菌的侵染，抑制率为41.67%；高磷、低磷和无磷水平下，禾草内生真菌处理显著提高了野大麦的株高和分蘖，两种共生体共存时，地上、地下生物量显著大于其它水平的处理。在无磷条件下，有AM真菌处理的地下生物量显著高于其它处理。在低磷水平下，禾草内生真菌的处理和AM真菌的处理对野大麦氮、磷累积有显著的促进作用[92-93]。

综上所述，关于AM真菌与禾草内生真菌的互作，目前主要有两种观点：一种观点认为，禾草内生真菌与AM真菌互作对植物体具有正效应，禾草内生真菌感染的牧草能提高丛枝菌根真菌的侵染率[88]。另一种观点则认为，菌根真菌和禾草内生真菌有相互抑制效应：内生真菌的存在显著减少菌根真菌的侵染[85-87]，而AM真菌侵染可以减少禾草内生真菌菌丝密度和寄主植物叶片中生物碱含量，二者的互作结果可能与土壤营养水平、内生真菌菌株类型和AM真菌类型等因素有关[89]。探究二者互作的内在机制，明确植物是如何同时与不同的微生物建立共生关系，并从中找到平衡点将对未来的实际应用有指导意义。

4问题与展望

目前，国内外有关AM真菌、禾草内生真菌和植物病原菌两者之间互作关系的研究已取得一定的成果，且在生产上开始应用，如美国、澳大利亚、日本等国家，已开始利用AM真菌菌剂，提高作物生产；美国和新西兰已培育出含内生真菌的黑麦草品种，且已投放市场[68]。而关于这3类微生物共同作用关系的研究尚未见报道。

随着社会的不断发展，人民生活水平逐渐提高，对食品安全的要求也不断增长。但在城市化和工业化不断推进的今天，生态环境在不断恶化，食品安全也存在较多隐患，而且大面积种植同一品种植物，可能导致植物病害的爆发和流行，因此必须密切关注植物病害的监测和防控。农业生态系统中蕴藏着丰富的植物、微生物资源。鉴于AM真菌与禾草内生真菌对于植物病原菌的显著防效，有必要研究农业生态系统中这3类重要微生物的互作机理，并在此基础上，利用禾草内生真菌和AM真菌提高植物抗逆性及产量、防治植物病害、促进农业生态系统可持续发展。

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(责任编辑张瑾)

Progress of research on the interactions of arbuscular mycorrhizal fungi,grass endophyte and plant pathogens in agro-ecosystem

Li Fang, Zhang Feng, Gao Ping, Duan Ting-yu

(State Key Laboratory of Grassland Agro-ecosystems, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, China)

Abstract:Arbuscular myucorrhizal fungi (AMF), grass endophyte and plant pathogens are widely distributed in agro-ecosystems. Both AMF and grass endophyte could establish symbiosis with plants which could improve plant nutrient uptake, water absorption and enhance plant stress resistance, such as disease and drought stress. AMF could reduce plant disease incidence and disease index by a series of mechanisms including competing invading sites, nutrition and space with plant pathogens, consuming plant pathogens energy, improving plant water and nutrition efficiency and adjusting plant disease related proteins. Grass endophyte also could decrease plant disease incidence and the possible mechanism including excreting antimicrobial metabolites, inducing plant resistance and inhibiting medium of disease spread. The interactions of AMF and grass endophyte depended on plants and fungi which are mutual or antagonism. Research and utilization of AMF and grass endophyte are very important for improving and maintaining agro-ecosystem productivity and sustainability.

Key words:arbuscular mycorrhizal fungi; grass endophyte; plant pathogen; interaction

Corresponding author:Duan Ting-yuE-mail:duanty@lzu.edu.cn

中图分类号：S181.6;S432.4+4

文献标识码：A

文章编号：1001-0629(2016)2-0219-11

通信作者：段廷玉(1976-)，男，甘肃靖远人，副教授，博士，研究方向为菌根生态学。E-mail:duanty@lzu.edu.cn

基金项目：甘肃省自然科学基金项目(1208RJZA270)；国家自然科学基金项目(31100368/C0309)；教育部博士点基金新青年教师项目(20110211120032)

*收稿日期：2015-03-18接受日期：2015-07-24

DOI:10.11829/j.issn.1001-0629.2015-0151

李芳，张峰，高萍，段廷玉.农业生态系统中AM真菌、禾草内生真菌及病原菌互作.草业科学,2016,33(2)：219-229.

Li F,Zhang F,Gao P,Duan T Y.Progress of research on the interactions of arbuscular mycorrhizal fungi, grass endophyte and plant pathogens in agro-ecosystem.Pratacultural Science，2016,33(2)：219-229.

第一作者：李芳(1990-)，女，青海西宁人，在读硕士生，研究方向为菌根生态学。E-mail:lif2013@lzu.edu.cn