全 文 ：丛枝菌根结构与功能研究进展*
田摇 蜜1 摇 陈应龙2 摇 李摇 敏1 摇 刘润进1**
( 1青岛农业大学菌根生物技术研究所, 山东青岛 266109; 2School of Earth and Environment / UWA Institute of Agriculture, Uni鄄
versity of Western Australia, WA 6009, Perth, Australia)
摘摇 要摇 丛枝菌根(arbuscular mycorrhiza, AM)是陆地生态系统中分布最广泛、最重要的互惠
共生体之一,对提高植物抗逆性、修复污染生境、保持生态系统稳定与可持续生产力的作用显
著. AM结构特征是判断菌根形成的主要指标,与其功能密切相关. 本文总结了 AM 丛枝结
构、泡囊结构、菌丝结构和侵入点结构等发育特征;分析了 A型丛枝结构、P型丛枝结构、泡囊
结构和根外菌丝结构与促进寄主植物养分吸收和生长、提高植物抗旱性、耐涝性、耐盐性、抗
高温、拮抗病原物、提高植物抗病性、抗重金属毒性、分解有毒有机物、修复污染与退化土壤等
功能的关系,及其所发挥的重要作用;探讨了影响 AM结构与功能的因子,以及基于 AM 不同
结构所发挥功能的作用机制.旨在为系统研究 AM 真菌发育特征、AM 真菌效能机制,以及评
价和筛选 AM真菌高效菌种提供依据.
关键词摇 丛枝菌根摇 丛枝菌根真菌摇 侵染摇 寄主植物
文章编号摇 1001-9332(2013)08-2369-08摇 中图分类号摇 Q949摇 文献标识码摇 A
Structure and function of arbuscular mycorrhiza: A review. TIAN Mi1, CHEN Ying鄄long2, LI
Min1, LIU Run鄄jin1 ( 1 Institute of Mycorrhizal Biotechnology, Qingdao Agricultural University,
Qingdao 266109, Shandong, China; 2School of Earth and Environment / UWA Institute of Agricul鄄
ture, University of Western Australia, WA 6009, Perth, Australia) . 鄄Chin. J. Appl. Ecol. ,2013,24
(8): 2369-2376.
Abstract: Arbuscular mycorrhiza (AM) is one of the most widely distributed and the most impor鄄
tant mutualistic symbionts in terrestrial ecosystems, playing a significant role in enhancing plant re鄄
sistance to stresses, remediating polluted environments, and maintaining ecosystem stabilization and
sustainable productivity. The structural characteristics of AM are the main indicators determining
the mycorrhizal formation in root system, and have close relations to the mycorrhizal functions. This
paper summarized the structural characteristics of arbuscules, vesicles, mycelia and invasion points
of AM, and analyzed the relationships between the Arum (A) type arbuscules, Paris (P) type ar鄄
buscules, vesicles, and external mycelia and their functions in improving plant nutrient acquisition
and growth, enhancing plant resistance to drought, waterlogging, salinity, high temperature, disea鄄
ses, heavy metals toxicity, and promoting toxic organic substances decomposition and polluted and
degraded soil remediation. The factors affecting the AM structure and functions as well as the action
mechanisms of mycorrhizal functions were also discussed. This review would provide a basis for the
systemic study of AM structural characteristics and functional mechanisms and for evaluating and
screening efficient AM fungal species.
Key words: arbuscular mycorrhiza (AM); arbuscular mycorrhizal fungi; colonization; host plant.
*国家自然科学基金项目(31272210)和山东省科技发展计划项目
(2012GNC11010)资助.
**通讯作者. E鄄mail: liurj@ qau. cdu. cn
2012鄄10鄄29 收稿,2013鄄06鄄22 接受.
摇 摇 丛枝菌根(AM)真菌在侵染植物根系形成共生
体过程中,通过参与植物生理生化代谢与基因调控,
改善植物营养、提高植物抗逆性、改善生态环境安全
性、保持和增强生态系统可持续生产力. 众所周知,
任何有生命的有机体和无生命的无机体的结构往往
决定了其所具备的功能. 基于“结构决定功能冶的理
念和思路,尤其是前人研究结果所给出的有关迹象
或证据[1-2],作者提出 AM 结构特征与其功能密切
相关的科学假设. 越来越多的试验结果表明,AM真
应 用 生 态 学 报摇 2013 年 8 月摇 第 24 卷摇 第 8 期摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇
Chinese Journal of Applied Ecology, Aug. 2013,24(8): 2369-2376
菌所具有的促进植物吸收养分、增强植物对干旱、水
涝、高温、高盐、重金属毒害和土传病害等抗逆性、促
进植物生长、分解有毒有机物、修复和改良污染土壤
等功能与其菌根结构发育特征密切相关[3-5] . 那么,
AM不同结构特征是否具备与以往认识所不同的功
能? AM各结构,特别是菌根侵染率与其功能之间
到底是什么关系? 影响 AM结构发育和功能的关键
因素有哪些? 深入系统地探讨这些问题,对于建立
高效的菌种评价体系和指导高效菌种的筛选与应用
具有一定的理论和实际意义.
1摇 丛枝菌根结构特征
AM 真菌侵染植物根系,首先形成附着泡和侵
入点结构,随后侵染菌丝进入根内,扩展成胞间菌丝
和胞内菌丝.其中一部分根内菌丝与根外(表)真菌
结构相连,另一部分顶端膨大形成泡囊( vesicles)
或 /和菌丝二分叉式生长形成丛枝结构.研究表明,
AM 真菌可形成不同形态结构的丛枝,其中,Arum
(A)型和 Paris(P)型最为典型[6] . Szymon 等[7]对 15
种药用植物观察发现,大多数植物 AM形成 A型,少
数形成 P型,部分是中间型.
AM 真菌可以从幼嫩根系任何部位侵染,多数
情况下是从根系成熟区侵入,也可以从根尖(即根
冠、分生区或 /和伸长区)侵入,形成丛枝、泡囊、根
内菌丝等典型的菌根结构.分支级次越高的根尖,菌
根侵染率也越高[8] . 舒玉芳等[9]观察到 AM 真菌侵
染的桑树根尖,单条根系侵染率在 0 ~ 100% ,82%
的根尖形成了 AM,包括典型的泡囊、丛枝和根内孢
子等 AM 结构. 该结果支持了早期的研究结论[8] .
AM真菌侵染根尖的特性, 表明该真菌的生态位与
土传病原物相同,这就为拮抗病原物创造了得天独
厚的条件[10] .更为重要的是,由根内伸展至根外于
土壤中形成的巨大菌丝网络,以及由此形成的菌根
网路为其发挥生理生态功能(如水分养分吸收等)
奠定了坚实的生物学和生态学基础.
2摇 丛枝菌根结构与功能的相关性
2郾 1摇 AM真菌可以改善植物的营养状况
研究表明,AM 真菌可以改善植物对养分的吸
收[11-12] .例如,AM真菌促进了黄花蒿(Artemisia an鄄
nu)根系对养分的吸收, 增加了各器官中 N、P、K含
量[13] .摩西球囊霉(Glomus mosseae)对木薯(Mani鄄
hot esculenta)的侵染率较高,菌根的形成增加了茎
内 P含量和植株的生长[14] .接种 AM 真菌处理的番
茄叶片中的可溶性糖、可溶性蛋白、硝酸还原酶活性
均比不接种处理有所增加,菌根侵染率与植株茎、根
干质量及可溶性糖含量之间呈极显著正相关[15] .
AM真菌与根系共生后,能显著促进根系对土壤矿
质营养元素特别是 P 的吸收,甚至在土壤温度降
低、植物生长和 P吸收受抑的情况下,AM 真菌仍能
增加植物体内 P含量[16] . 14C跟踪研究发现,碳水化
合物在 AM共生结构界面上的转移(从根系细胞到
AM菌丝体)对 AM 吸收 P 及 P 在植物体内的运输
有促进作用[17] .
2郾 2摇 AM真菌可以提高植物的抗旱性
AM 真菌可以促进植物水分吸收,提高水分利
用率,特别是干旱条件下能增强植物的抗旱能
力[18-19] .接种 AM 真菌提高了叶片相对水分含量、
木质部压力势、叶片气孔导度和光合速率,降低了永
久凋萎点,从而提高其水分利用效率[20] . 在接种处
理与对照植株体内磷含量和生长量无差异条件下,
随着土壤的持续干旱,AM 真菌的侵染能提高土壤鄄
根系水分导度[21] .狗牙根(Cynodon dactylon)单接种
聚丛球囊霉(G. aggregatum)或摩西球囊霉比两者
的混合菌种有更高的侵染率和更好的抗旱性[22] .
AM真菌的菌丝可以直接吸收水分[23-24] . 因此,AM
真菌改善植物水分状况与菌根发育数量有关. 干旱
条件下, 随着菌根侵染率的提高, 连翘(Forsythia
suspensa)幼苗叶绿素和脯氨酸含量增加, SOD 活性
增强, 而丙二醛含量和膜透性降低, 苗木枯死率下
降[25] .通过研究根内活性菌丝数量发现,具有磷酸
酶活性的菌丝对于促进植物生长和提高抗旱性的作
用最强[26] .因此,大多数研究者通过测定菌根侵染
率或 /和根内外菌丝数量等来评价 AM真菌的功能.
2郾 3摇 AM真菌可以改善植物的耐涝性
有迹象表明,AM 真菌通过自身特有的方式可
改善植物的耐涝性. 具有繁殖功能的泡囊结构自身
抗逆性强,当土壤水分含量过高时,AM 真菌增加了
细叶百脉根(Lotus tenuis)泡囊结构数量[27],在一定
水涝逆境下泡囊结构仍可保存一定活力,当洪水退
去后,存活下来的泡囊便又可生长发育,形成新的菌
根结构,促进养分吸收,补偿植物涝灾时受到的损
害.关于菌根结构与提高植物抗涝性的关系值得进
一步试验.
2郾 4摇 AM真菌可以增强植物耐盐性
AM 真菌可降低植物盐害程度,保护植物的正
常生长[28-29] .摩西球囊霉能降低大豆叶片 Na 含量,
显著提高叶片 K+含量和 K / Na 比值,且随着盐浓度
0732 应摇 用摇 生摇 态摇 学摇 报摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 24 卷
升高而增大,从而增强了其抗盐性[30] . Giri 等[31]研
究表明,金合欢(Acacia farnesiana)接种 AM真菌后,
其地上部 K / Na 比值增加,从而提高了金合欢的抗
盐性.高盐下(1. 0% ),接种 AM 真菌能促进番茄植
株生长,增加叶片和根系的可溶性糖含量、叶片可溶
性蛋白含量及根系脯氨酸含量,增强植株的耐盐能
力[32] .盐胁迫下,菌丝对玉米植株 P 的贡献率由
45. 3%降为 42. 6% ,菌丝吸收的水分可缓解盐胁迫
下的生理干旱[33] . Jahromi等[34]研究发现,不同盐浓
度下,根内球囊霉(Glomus intraradices)菌株能促进
植物生长,可以作为耐盐 AM真菌.在今后筛选高效
菌种过程中,应重视 AM真菌侵染发育,尤其是根外
菌丝数量.
2郾 5摇 AM真菌可以提高植物抗高温能力
AM 真菌能保护植物免受高温伤害. 李思龙
等[35]研究表明,接种 AM 真菌能降低高温对牡丹
(Paeonia suffruticosa)幼苗造成的伤害,接种后的根
系活力显著增强,脯氨酸和可溶性糖含量明显增加,
植株对高温逆境的忍耐力和适应性提高,植物细胞
的保水能力增强,从而提高其对高温的抗性.高温下
接种 AM真菌的玉米的光合效率、水分利用率升高;
AM真菌共生通过改善光和性能以及水的状态来保
护玉米抵御高温胁迫[36] . 10:00—12:00 高温阶段接
种 AM真菌后,彩叶草(Coleus blumei)叶片的净光合
速率明显高于对照,且摩西球囊霉与地表球囊霉
(Glomus versiforme)混合接种的侵染率高于单一菌
种[37] .
2郾 6摇 AM真菌可以增强植物抗病性
AM真菌可以不同程度地抑制土传病原细菌、
真菌和线虫的生长、繁殖和危害,提高植物的抗病
性[38-40];但由于寄主鄄AM菌种及病原物组合不同以
及生长环境的变化,AM 发育特征对植物抗病性会
产生不同的影响[41] . AM 表面着生和延伸着大量的
根上菌丝与根外菌丝组成的庞大菌丝网络系统,对
病原物入侵构成机械屏障,而且 AM 真菌通过与病
原真菌在侵染中进行活力竞争,提高植物抗病
性[42] . AM真菌丛枝结构的发育和植物抗病性有关,
AM丛枝着生数量(% )与植物抗病性呈正相关关
系[43] .唐明和陈辉[44]调查了 24 个杨树种和无性系
的溃疡病自然发病情况,结果表明, 7—8 年生杨树
外生菌根的侵染率与病情指数呈负相关. Thyges鄄
en[45]认为, 根内球囊霉降低发病率的效果比近明
球囊霉(Glomus claroideum)更显著,并且与其菌根
发育数量相关.本课题组在调查设施黄瓜根结线虫
危害时也观察到,黄瓜栽培品种“津优 35 号冶同一
根系内存在 P型和 A+P 混合型两种类型的 AM 形
态,而且还发现一条没有线虫侵染危害的根系丛枝
结构为 P型(未发表数据).初步推测 P 型丛枝结构
可能具有独特的生理代谢功能,尤其是在防御性酶
基因表达和酶活性方面值得深入研究.
2郾 7摇 AM真菌可以促进植物生长
研究表明,菌根侵染率与植物生长呈正相
关[15] .例如,玉米接种摩西球囊霉 30、45、60 和 75 d
后,植株高度与侵染率呈正相关[46]; 大须芒草(An鄄
dropogon gerardii)的 AM 真菌侵染率与总干质量等
呈正相关.也有少量试验结果例外,可能与植物种类
以及 AM真菌种类等因素有关[47-48] .
2郾 8摇 AM真菌可以改善植物耐重金属毒害
AM 真菌自身对重金属具有较强的耐性,为其
提高植物耐重金属毒害奠定了生物学基础. 根内球
囊霉能显著提高铅胁迫下玉米的生物量[49] .重金属
污染下,AM发育降低了植物体内尤其是地上部的
重金属浓度,有利于植物生长. 摩西球囊霉减少 Cd
向玉米植株地上部运输,将更多 Cd 固持于菌根
中[50] .因此,菌根发育越多,固持的重金属数量就越
多,使植物不受重金属毒害[51] . AM真菌还能通过菌
丝对重金属的过滤、菌丝固持等降低重金属对植物
组织造成的伤害[52-53] .从垃圾焚烧厂的植物根围土
壤中提取的土壤球囊霉素相关蛋白与 AM真菌侵染
率呈正相关[54]的研究结果,间接证明了 AM 发育与
提高植物耐重金属毒害的效应是正相关关系. AM
真菌生物量越多,所具备的吸附重金属能力和容量
就可能越大, 可见,它们之间存在一定正相关关系
的生物学基础,这有待进一步直接给予试验证明.
2郾 9摇 AM真菌可以分解有毒有机物,修复污染与退
化土壤
业已证实,AM 真菌能在不同程度上分解石油、
有机磷 (氯)农药、多环芳烃 ( PAHs)等有毒有机
物[55] . 接种 AM 真菌能促进土壤中 PAHs 的降
解[56] .接种苏格兰球囊霉(Glomus caledonium)促进
对土壤中苯并[a]芘的降解,接种处理比不接种最
大可提高 34%的 B[a]P 降解[57] . 石油污染土壤中
缩球囊霉(Glomus constinctum)对三叶草(Trifolium
subterraneum)根系的侵染率达到 83% ,显著促进三
叶草生长[58] . 对矿区脆弱地带的新疆杨(Populus
bolleana)和白蜡(Fraxinus chinensis)幼苗混合接种
摩西球囊霉和幼套球囊霉(Glomus etunicatum)后,
其侵染率在 80%以上,接种后根围孢子数量较多,
17328 期摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 田摇 蜜等: 丛枝菌根结构与功能研究进展摇 摇 摇 摇 摇
对矿区环境修复和生态恢复起到了重要作用[59] .接
种 AM真菌显著提高球囊霉素相关土壤蛋白含量和
土壤水稳性大团聚体数量;接种处理提高了土壤的
平均质量直径和几何平均直径,降低了土壤分形维
数[60] .而球囊霉素与孢子密度和总定殖率呈极显著
正相关[61] .因此,AM真菌所具有的促进植物吸收养
分、生长、改良退化土壤、提高土壤质量与健康状况
等功能必然与其菌根结构发育特征密切相关[62] .
综上所述,不同生态条件、不同农艺措施下,各
类 AM真菌特别是高效菌种的菌根发育特征及其数
量与其功能的关系,值得系统深入研究.
3摇 影响丛枝菌根结构发育及其功能的因素
丛枝结构发育特征是由寄主植物和 AM真菌共
同决定的[6] .亚麻(Linum usitatissimum)上 6 种不同
AM真菌均形成 A 型;而野生番茄上根内球囊霉等
形成 A 型,副冠球囊霉(G. coronatum)等则形成 P
型[63] . Gigaspora rosea 等在日本常春藤 ( Hedera
rhombea)上形成 P 型,在茅莓(Rubus parvifolius)上
形成 A型;分子生物学测定表明,球囊霉科的幼套
球囊霉和近明球囊霉多分布于茅莓(Rubus parvifoli鄄
us)和蔷薇(Rose multiflora)根内形成 A 型;而巨孢
囊霉科的巨盾孢囊霉( Scutellospora erythropa)多分
布于日本常春藤根内形成 P型[64] .
一些生态因子也影响到 AM结构发育及其与植
物抗逆性的关系.如土壤类型影响 AM 真菌侵染及
生理效应.棕壤中玉米根侵染率最高,为 71. 1% ,低
磷草甸土次之,高磷草甸土最差.各类黄潮土中 AM
真菌侵染率以两合土最高,盐碱土最低[65] . 不同土
壤类型、土壤质地显著影响菌根侵染率、菌根侵染强
度和丛枝丰度[66-67] . 土壤含水量[68]、磷含量和 pH
值与菌根形成的关系最为密切,速效磷含量过高往
往抑制菌根形成[69-70] .这也必然影响到 AM 结构与
功能的关系.另外,季节、接种试验中接种物类型、数
量和采样测定时间[69,71],以及测定侵染率的不同方
法[72]均影响到 AM 侵染率,也必须给予足够的
重视.
从单纯的数理分析角度来看,表面上 AM 结构
发育特征或数量与其功能存在相关性.其实,这恰恰
是这两者之间具备本质的密切关联性、因果机制性
和相互依存性的反映.
4摇 基于丛枝菌根结构所发挥功能的作用机制
作为 AM 的主要功能结构,丛枝是 AM 真菌与
植物之间进行养分交换与拮抗病原物诱导植物抗病
性的核心构造.因此,丛枝结构特征与数量会直接影
响到 AM真菌的生理生态效应.根据试验结果推理
认为,P型中假如菌丝和菌丝圈作用不同,那么二者
比率不同就会导致功能的强弱产生差异[73] .由于 A
型和 P型发育特点各异———P 型 AM 发育较 A 型
慢[63],二者吸收养分与促进植物生长效应,以及防
御基因表达和介导的防御反应亦可能不同[6,74] . 虽
然已观察到丛枝结构与抑制植物病原物的侵染和扩
展有关,但遗憾的是,相关的观察并没有区分这些丛
枝是属于哪些类型的丛枝结构.
土壤中 AM网络通过菌丝将不同植物根系连成
一体,进行养分、能量物质和信息的传递与交换,促
进各种植物高效利用有限的信息和资源. AM 菌丝
体能够提高土壤团聚体的水稳定性,改善土壤结
构[75] . AM真菌的根外菌丝可穿过土壤颗粒间极细
小的孔隙,由于根外菌丝与土壤颗粒密切接触,其分
泌的有机小分子物质可以作为土壤颗粒的黏着吸附
剂,促进土壤颗粒形成团聚体,提高其水稳性,使土
壤保持较好的水渗透速率、耕作条件和通气状况,从
而抵抗风和水的侵蚀[76] . Wang 等[77]观察到 Glomus
caledonium提高了重金属污染土壤中磷酸酶和脲酶
活性,改善了土壤质量. 可见,AM 真菌调控土壤酶
活性也是其提高植物抗逆性的机制之一.
AM真菌的菌丝内聚磷酸盐可能参与改善植物
耐毒性机制. Cd2+胁迫作用下,聚磷酸盐含量降低而
菌丝密度随着该盐的升高而升高,表明聚磷酸盐在
减弱重金属毒性方面发挥了重要作用[78] . 此外,庞
大的菌丝网络可以作为屏障,阻止金属向根部运输,
从而减轻重金属毒害[79] .接种 AM真菌提高蜈蚣草
(Nephrolepis cordiffolia)根部吸收和积累砷,抑制砷
向地上部分运输[80] . 铬和锌污染下,接种 AM 真菌
增加了紫花苜蓿(Medicago sativa)根内重金属积累,
减少地上部的积累,间接地减轻了重金属对地上部
的毒害作用[81-82] .
5摇 研究展望
菌根真菌接种试验及野外菌根调查都涉及到菌
根结构观察与侵染率等测定,这可以明确菌根发育
状况,更重要的是可为结果分析、确定菌根结构及数
量与其功能的关系提供数理依据.然而,多数试验缺
乏针对菌根结构及数量与其功能进行直接的数理相
关分析,因此不能全面认识 AM结构与功能的关系.
因此,今后工作中,可采用生物化学、组织化学、激光
2732 应摇 用摇 生摇 态摇 学摇 报摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 24 卷
共聚焦显微镜技术、分子原位杂交等技术与方法,深
入系统开展以下几项工作:
1)进一步加大野外自然调查研究力度、深度和
广度,注重菌根形态结构的观察,善于探索和发现新
的菌根结构特征,同时对菌根侵染率、根内和根外菌
丝发育数量、丛枝着生数量、泡囊数、孢子数量等进
行定量精确测定,为后续室内试验研究提供依据和
技术基础;
2)有计划的顺序开展逐步深入的室内接种效
应试验,通过将这些菌根发育数量与其生理效应
(功能)作相关和回归分析,为诠释菌根真菌的生理
生态功能机制奠定基础;
3)于上述基础上,进一步开展一些专门研究菌
根结构与功能的试验,例如,在 AM真菌介导植物拮
抗病原物的机制研究中,应着重研究不同类型丛枝
结构可能具备的不同生理功能;一种植物根内 A
型 / P型比率不同的生物学意义及其与 AM 真菌功
能的关系;通过测定 A型、P型或 /和 A+P混合型丛
枝结构状况、吸收养分与促进生长发育的效应,特别
是抑制根结线虫的生理与分子基础研究,应结合数
理分析,探讨其抑制根结线虫的作用机制.这将有助
于深化了解丛枝结构的生理功能及其作用机制,大
大推动菌根结构与功能关系的研究和进展.
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作者简介摇 田摇 蜜,女,1989 年生,硕士研究生.主要从事蔬
菜栽培生理与菌根学研究. E鄄mail: tmfling@ 126. com
责任编辑摇 李凤琴
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