全 文 ：植物生态学报 2015, 39 (6): 621–634 doi: 10.17521/cjpe.2015.0060
Chinese Journal of Plant Ecology http://www.plant-ecology.com
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收稿日期Received: 2014-11-14 接受日期Accepted: 2015-05-20
* 通讯作者Author for correspondence (E-mail: chunjie@lzu.edu.cn)
禾草内生真菌作为生防因子的潜力分析
李秀璋 姚 祥 李春杰* 南志标
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, 兰州 730020
摘 要 早熟禾亚科多种禾草可与Neotyphodium内生真菌形成禾草-内生真菌共生体, 这种植物-微生物共生体性状较为稳定,
且在自然界中广泛存在。禾草-内生真菌共生体稳定的互利共生关系不但保证了内生真菌所需的全部营养物质, 而且共生体
产生的次生代谢物又可显著提高宿主禾草对生物胁迫的抗逆性。众多研究表明, 内生真菌的侵染可显著提高宿主禾草对虫
害、病害及伴生植物等多种生物胁迫的抗性。据不完全统计, 禾草内生真菌对蛛形纲、线虫纲、昆虫纲3个纲至少79个种的
害虫表现出较明显的抗性, 对至少22个种的病原真菌表现出明显的抗性。尽管利用内生真菌进行禾草品种选育及其品质改良
的技术日趋成熟, 但是内生真菌在不同宿主禾草之间高效的替代转化技术, 及其在宿主体内遗传的稳定性仍有待于进一步深
入探索。研究者把禾草内生真菌作为生防手段, 在未来的应用过程中不应只考虑其与宿主禾草之间的共生特异性, 而应更全
面地分析禾草-内生真菌-生态环境之间的相互关系, 让内生真菌更好地为人类服务。
关键词 禾草内生真菌, 抗虫, 抗病, 生物防治, 潜力分析
引用格式: 李秀璋, 姚祥, 李春杰, 南志标 (2015). 禾草内生真菌作为生防因子的潜力分析. 植物生态学报, 39, 621–634. doi: 10.17521/cjpe.2015.0060
Potential analysis of grass endophytes Neotyphodium as biocontrol agents
LI Xiu-Zhang, YAO Xiang, LI Chun-Jie*, and NAN Zhi-Biao
State Key Laboratory of Grassland Agro-ecosystems; College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, China
Abstract
Many grasses in the subfamily Pooideae develop symbioses with Neotyphodium fungal endophytes, which exist
widely in nature. The stably symbiotic relationship not only ensures accessible nutrients required by Neotypho-
dium fungal endophytes, but also significantly increases the resistance of host grasses to biological stresses
through the production of secondary metabolites. Previous studies show that infected grasses with endophytic
fungi have prominently enhanced resistance to pests, plant diseases, companion plants and other biological
stresses. Grass endophytic fungi show remarkable resistant to at least 79 species of pests from three classes;
arachnida, nematode and insecta, and to at least 22 species of pathogenic fungi. Although the biotechnological
application of endophytic fungi in grass breeding for variety selection and quality improvement has progressed
well, opportunities remain for further exploring the use of fungal endophytes among different host grasses coupled
with the examination of genetic stability of Neotyphodium in novel host grasses. In the future application of en-
dophytic fungi as a bio-control method, researchers should not only consider specificities of host grasses, but also
need to have comprehensive analysis and knowledge about the mutual relationships among grasses, endophytic
fungi and ecological environments, which will help use endophytic fungi to better serve humanity.
Key words Neotyphodium, pest resistance, disease resistance, biocontrol factor, potential analysis
Citation: Li XZ, Yao X, Li CJ, Nan ZB (2015). Potential analysis of grass endophytes Neotyphodium as biocontrol agents. Chinese
Journal of Plant Ecology, 39, 621–634. doi: 10.17521/cjpe. 2015.0060
自然界中, 几乎所有的陆生植物都可与多种微
生物形成互利共生或内寄生关系 (Easton, 2007;
Brundrett, 2009; Rodriguez et al., 2009)。禾草内生真
菌(grass endophyte)是指在禾草体内度过全部或大
部分生活周期, 而宿主不显示任何外部症状的一大
类真菌(Siegel et al., 1987)。目前, 关于禾草内生真
菌的研究主要集中在广泛分布于冷季型禾草中的
Epichloë属及其无性态Neotyphodium属, 其有性阶
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段属子囊菌门核菌纲肉座菌目麦角菌科(White &
Morgan-Jones, 1987; Schardl et al., 2004)。由于内生
真菌明显的多样性差异, 研究人员预测每种植物至
少存在一种专性寄生真菌, 而Neotyphodium内生真
菌与C3类型禾草形成的共生体分布最为广泛, 研究
价值较高(Faeth, 2002; Schardl et al., 2004; Ren &
Clay, 2009)。Leuchtmann等(2014)对禾草内生真菌进
行了重新命名, 将Neotyphodium属中的内生真菌全
部划归为Epichloë属的无性类群。本文主要对2014
年前相关研究动态进行综述, 为保证引文统一, 仍
按照之前的命名规则进行归纳。
一直以来, 禾草-内生真菌共生体因其在生态
环境中生长的优越性而备受关注(Rudgers et al.,
2004)。在漫长的演化过程中, Neotyphodium属内生
真菌在不同的环境和选择压力下, 与宿主植物协同
进化, 逐渐形成了较为稳定的互惠共生关系(Siegel,
1993; White & Torres, 2010)。从带菌禾草易引致家
畜中毒而受到广泛关注, 到致毒活性物质——生物
碱被发现, 研究人员证实生物碱对宿主禾草的防卫
功能也具有重要的促进作用(Schmidt & Oshorn,
1993; Cross et al., 1995)。内生真菌通过调节和修饰
宿主禾草形态学、生理学及生物化学等特征, 提高
宿主禾草在生物与非生物胁迫下的适应性, 维持共
生关系的稳定性(Malinowski et al., 2000; Clay &
Schardl, 2002; Malinowski & Belesky, 2006; Ras-
mussen et al., 2008)。当前内生真菌提高宿主禾草对
生物因子抗性的研究主要集中在草食动物(Schardl
et al., 2004, 2007; Schardl, 2009)、伴生植物
(Malinowski et al., 1997; Clay & Schardl, 2002)、害虫
(Latch, 1993; Rowan & Latch, 1994; Zhang et al.,
2011)、病原菌(Porras-Alfaro & Bayman, 2011)、线
虫(Kimmons et al., 1990; Bacetty et al., 2009)、螨类
(Li et al., 2007b)、鸟类(Pennell et al., 2010)及鼠类等
(Cunningham, 1958; Conover, 2003)。
在有害生物的综合防治过程中, 尽管化学防治
具有快速、高效、使用方便、抗菌杀虫谱广等优点,
但随着化学农药的长期滥用, 出现了农药残留、环
境污染、生态平衡破坏、病虫抗药性增强等一系列
较严峻的问题(Belovsky & Slade, 1995)。近年来, 随
着生物防治技术的不断发展, 这种不利态势逐渐得
到改观。生物防治即利用一种或一类生物抑制另一
种或一类生物的防治策略, 其最大优点是不造成环
境污染。生物防治中应用较多的是微生物源生防制
剂, 即利用有益微生物自身或其代谢产物进行杀虫
防病的一种技术与方法, 其本质是利用生物种内或
种间竞争实现防治的目的。以绿僵菌(Metarhizium
spp.)、苏云金芽孢杆菌(Bacillus spp.)等为代表的各
种生物制剂在病虫害综合防治中已收得了良好的效
果, 但由于这些微生物制剂的储存、运输及施用条
件较为苛刻, 在实际的施用过程中易受到环境气候
条件的制约(Barrientos-Lozano et al., 2002)。因此,
利用内生真菌与宿主禾草之间良好的共生关系及其
提高禾草抗逆性的巨大贡献, 将禾草内生真菌作为
一种重要的生防因子对禾草品质进行改良, 提高宿
主抗逆性逐渐成为可能(Funk et al., 1993; Kasai et
al., 2004)。在对禾草-内生真菌开展研究的100多年
中, 前人通过大量试验对禾草内生真菌作为生防因
子的潜力进行了较为详细的研究, 本文对前人已有
成果进行了扼要总结, 以期为进一步研究提供理论
支持, 为禾草内生真菌的开发应用提供参考。
1 禾草内生真菌生活史及生物碱
自Li等(2004)从醉马草(Achnatherum inebrians)
中分离并命名内生真菌Neotyphodium gansuense以
来, 禾草内生真菌的研究在我国逐渐展开(南志标
和李春杰, 2004)。目前, 全世界已报道并命名的
Epichloë属内生真菌有14个种, 其中我国有2个种,
这些内生真菌分布在燕麦族、短颖草族、短柄草族、
雀麦族、臭草族、早熟禾族、小麦族7个族至少20
个属的禾本科早熟禾亚科(Poöideae)植物中; Neoty-
phodium属有23个种及5个变种, 其中我国有5个种,
它们分别侵染剪股颖族、燕麦族、雀麦族、臭草族、
早熟禾族、针茅族、小麦族7个族至少19个属的禾本
科植物(Schardl, 2010; Leuchtmann et al., 2014)。
1.1 禾草内生真菌生活史
内生真菌菌丝体通常分布于宿主禾草叶鞘、茎
秆、根状茎的细胞间隙, 偶尔在宿主禾草叶片表面
分布(White et al., 1996; Moy et al., 2000; Dugan et
al., 2002; Tadych et al., 2007)。当禾草开花时, 真菌
沿着花序生长并在其基部形成子座, 最终整个花序
被内生真菌菌丝包裹而停止生长, 称之为香柱病。
其中一些内生真菌仅在宿主部分分蘖上形成子座,
但种子产量基本不受影响或影响较小, 内生真菌可
以随种子垂直传播给下一代, 这种现象被定义为内
李秀璋等: 禾草内生真菌作为生防因子的潜力分析 623

doi: 10.17521/cjpe.2015.0060
生真菌的第2种类型(Clay & Schardl, 2002)。其他内
生真菌在宿主禾草所有或大多数的花序或者分蘖上
形成子座, 严重影响种子发育, 内生真菌的有性孢
子借助昆虫、风和雨水进行水平传播, 这一类被定
义为内生真菌的第1种类型(White, 1988)。一些种类
的禾草内生真菌在整个生活史中都不会出现产生子
座的有性世代, 称之为禾草内生真菌的无性世代类
型或第3种类型(Clay & Schardl, 2002)。第3种类型内
生真菌主要依靠种子进行垂直传播, 但是宿主禾草
叶片中存在的大量可产生分生孢子的菌丝体依然存
在着水平传播的可能(Rodriguez et al., 2009)。
1.2 生物碱
对于生物碱的研究主要集中在以震颤素
(lolitrem B)为代表的吲哚双萜类(lndolditerpene)、以
波胺(peramine)为代表的吡咯并吡嗪类(pyrrolopy-
razine)、以麦角新碱(ergonovine)和麦角酰胺(ergine)
为代表的麦角碱类(ergot alkaloids)、以黑麦草碱
(loine)为代表的饱和吡咯类化合物(pyrrolizidine)等4
大类至少10种生物碱(高嘉卉和南志标, 2007; 徐瑞
等, 2012)。禾草-内生真菌共生体产生的生物碱直接
或间接地参与了宿主在生态过程中的大部分作用,
并扮演着较为重要的角色(Bush et al., 1997; Kuldau
& Bacon, 2008)。与禾草-内生真菌共生体有关的生
物碱因具有抗采食性(Siegel et al., 1990; Bush et al.,
1997; Salminen et al., 2005)、抗虫性(Clay et al.,
1985; Bultman et al., 2004), 以及对哺乳动物
(Hoveland et al., 1983; Stuedemann & Hoveland,
1988; Clay, 1990)和线虫(Elmi et al., 2000)具有的较
高毒力活性而为人所熟知。同时, 生物碱可能会对
腐生微生物(Rudgers & Clay, 2008)及微生物分解者
(Franzluebbers et al., 1999; Franzluebbers & Hill,
2005)的活动起到一定的抑制作用, 这主要是通过
调节宿主禾草营养分配和凋落物的分解过程
(Antunes et al., 2008; Mack & Rudgers, 2008)直接或
间接地影响其他土壤微生物群落来实现的。
2 内生真菌对禾草抗虫性的影响
有效提高宿主抗虫性是内生真菌为宿主禾草带
来的最明显增益特性(Latch, 1993; 南志标和李春
杰, 2004; Popay & Bonos, 2005)。宿主禾草对包括昆
虫、螨虫、线虫在内的多种害虫能产生较为有效的
抗取食作用。禾草-内生真菌共生体对昆虫纲害虫的
抗性明显高于其他类群, 主要包括蚜科、叶甲科、
蝉科、象甲科、蟋蟀科、长蝽科、盲蝽科、夜蛾科、
螟蛾科、金龟子科及拟步甲科在内的至少45种昆虫,
它们主要危害禾草茎基部、叶鞘及其他地上部分,
然而赤拟谷盗(Tribolium castaneum)及金龟甲科部
分 昆 虫 (Prestidge & Gallagher, 1988; Johnson-
Cicalese & White, 1990; Potter et al., 1992; Breen,
1993; Funk et al., 1993)主要危害禾草根部。
近年来研究较多的抗虫宿主禾草主要是多花黑
麦草(Lolium multiflorum)、苇状羊茅(Festuca arun-
dinacea)、草甸羊茅(F. pratensis)、醉马草等。早在
1982年, 就有学者对多花黑麦草-内生真菌共生体
抑制阿根廷茎象甲(Listronotus bonariensis)的取食
活动进行了报道(Prestidge et al., 1982)。Funk等
(1993)研究发现, 相对于不带内生真菌的多花黑麦
草, 内生真菌的侵染可有效地提高宿主对草地螟
(Crambus sp.)的抗性。由于阿根廷茎象甲的取食, 内
生真菌侵染率较高的草地干物质产量高于未被侵染
的近40% (Mortimer & Di Menna, 1983)。通过对草地
贪夜蛾(Spodoptera frugiperda)和赤拟谷盗的饲喂试
验发现, 带菌多花黑麦草明显降低了供试昆虫存活
率及生长速率, 延迟了供试昆虫发育速度(Cheplick
& Clay, 1988)。Li等(2007b)研究发现, 禾草内生真菌
的侵染可有效地提高大田中醉马草对罗格斯石竹蚁
(Tetranychus cinnabarinus)的抗取食性。
研究证实禾草-内生真菌共生体抗虫性与生物
碱关系密切, 尤其是吡咯并吡嗪类(pyrrolopyrazine)
生物碱——波胺(peramine)(Rowan et al., 1986; Ball
et al., 1995), 麦角缬氨酸对饱和吡咯化合物
(pyrrolizidine)中黑麦草碱(loine)的抗虫性具有协同
或增效作用(Siegel et al., 1990; Wilson, 1995)。但是
也有研究发现, 并非所有对害虫具有抗性的共生体
都会产生生物碱类物质。Tanaka等(2005)研究发现,
与多花黑麦草共生的内生真菌中波胺生物合成基因
被阻断。而一直以来, 波胺被认为是内生真菌提高
多花黑麦草对阿根廷象甲抗采食性的关键因子, 这
一研究结果大大降低了生物碱在共生体抗虫作用方
面的重要性。Panaccione等(2006)报道称, 麦角生物
碱并不能降低多花黑麦草的根部寄生线虫——斯克
里布纳短体线虫(Pratylenchus scribneri)的种群数
量。对小地老虎(Agrotis ipsilon)和草地贪夜蛾的饲
喂试验发现, 带内生真菌的多花黑麦草对二者均有
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较高的毒力活性, 同时对其寄生线虫——斯氏线虫
(Steinernema carpocapsae)也会产生抗性, 这种提高
宿主禾草防卫作用与其产生的麦角类生物碱相关性
较高(Kunkel et al., 2004; Richmond et al., 2004)。
与多花黑麦草共生的一些Neotyphodium菌株可
产生对害虫具有毒力活性的一种化合物——Janth-
itrems (Tapper & Lane, 2004)。这种化合物作用范围
较广, 通常导致供试害虫发育迟缓、体重增加、摄
食行为发生改变、生存率降低、死亡率升高等, 同
时, Janthitrems的作用并不局限于某一类害虫或者
害虫的某一个虫态。
分离自草甸羊茅的内生真菌——Neotyphodium
uncinatum, 其次生代谢产物对哺乳类动物无毒, 但
对害虫具有高效毒力活性及其他效应(Blankenship
et al., 2001)。相对于未接种N. uncinatum的多花黑麦
草, 内生真菌的接种可有效地提高宿主对寄生于水
稻叶面的一种须盲蝽(Trigonotylus caelestialium)的
抗性, 须盲蝽生存率明显下降(Shiba et al., 2007)。禾
草-内生真菌共生体对蛛形纲、线虫纲、昆虫纲及其
他无脊椎动物产生抗性的研究近年来逐步增多
(Barratt et al., 2008; Kuldau & Bacon, 2008; Bultman
et al., 2009; Bryant et al., 2010; Clement & Elberson,
2010; Shiba & Sugawara, 2010; Clement et al., 2011;
Shiba et al., 2011; Zhang et al., 2011), 这对内生真菌
的开发利用具有极其重要的积极意义。本文对
Kuldau和Bacon (2008)报道中的虫类进行了重新总
结, 并对其中未涉及近年来国内外报道的相关害虫
种类进行了补充, 详见表1。
3 内生真菌对禾草抗病性的影响
尽管内生真菌提高宿主禾草抗病性是二者协同
作用的结果, 但利用内生真菌对田间病害进行防治
也可能成为一种行之有效的手段。离体条件下禾草
内生真菌对病原真菌的拮抗作用较强, 尽管这些离
体试验无法完全模拟自然条件下二者的互作效应,
但也能在一定程度上间接证实禾草内生真菌作为植
物病原真菌生防因子的巨大潜力 (Christensen &
Latch, 1991; 南志标和李春杰, 2004; Li et al., 2007a;
Tian et al., 2008)。一些田间试验结果证实, 内生真
菌可提高不止一种宿主禾草的抗病性, 部分研究结
果与离体试验结果相一致, 这就在一定程度上大大
推动了对禾草内生真菌开发利用的进程。离体培养
条件下, 禾草内生真菌主要通过释放抗生素或降低
酶活性物质, 实现对某些病原菌的抑制作用(Blank,
1992; Clarke et al., 2006; Tian et al., 2008)。此外, 禾
草内生真菌能够诱导并激活苇状羊茅的防御反应机
制, 增强体内防御酶——苯丙氨酸解氨酶(PAL)的
活性, 从而提高宿主对褐斑病的抗性(王志勇和江
淑平, 2007)。Tian等(2008)报道称, 内生真菌可明显
增强多花黑麦草体内超氧化物歧化酶(SOD)和过氧
化物酶 (POD)的活性 , 提高宿主对细交链孢
(Alternaria alternata)、离蠕孢(Bipolaris sorokinia-
na)、新月弯孢 (Curvularia lunata)和燕麦镰孢
(Fusarium avenaceum) 4种病原真菌的抗性。在田间
锈菌(Puccinia spp.)胁迫条件下, 内生真菌的侵染可
有效地提高多花黑麦草叶片内游离脯氨酸含量, 增
强超氧化物歧化酶与过氧化物酶活性, 降低丙二醛
(MDA)含量、病叶损失率和植株矮化程度, 有效提
高宿主多花黑麦草田间抗锈病能力(马敏芝和南志
标, 2011)。活体材料试验中, 禾草内生真菌诱导宿
主产生抗病性的一些特殊化学物质并未得到最终确
定, 内生真菌提高宿主禾草抗病性的机制仍然有待
于进一步深入研究。内生真菌(Epichloë festucae)对
田间紫羊茅、硬羊茅(F. brevipila)及羊茅(F. ovina)
币斑病(Sclerotinia homeocarpa)产生较强拮抗作用
(Clarke et al., 2006)。然而, 在对苇状羊茅腐霉枯萎
病(Pythium sp.)的研究中发现, 寄生于其体内的内
生真菌(N. coenophialum)不但没有起到积极的保护
作用, 反而促进了病害的流行(Blank, 1992)。在对草
地羊茅德氏霉(Drechslera sp.)叶斑病的研究中也得
到了较为类似的结果, 即未被内生真菌(N. uncina-
tum)侵染的草地羊茅德氏霉叶斑病发病率较低
(Pańka et al., 2004)。
对于同一禾草-内生真菌共生体, 宿主对不同
病害的反应也会有所不同(Pańka et al., 2004)。这可
能与共生体产生的次生代谢物种类有关, 某种特定
的代谢产物可能只对某一种或某一类病害起作用,
但与其他病害的发生无关或者起到促进作用
(Strobel & Daisy, 2003)。带菌禾草产生的倍半萜类、
吲哚类化合物和其他一些尚未被确定具体成分的挥
发性物质可能与香柱菌提高梯牧草(Phleum pra-
tense)抗枝孢菌和柄锈菌等有关, 这一观点在随后
的试验中也得到了证实(Greulich et al., 1999; Yue et
al., 2000)。离体培养下, 禾草内生真菌仍可产生生
李秀璋等: 禾草内生真菌作为生防因子的潜力分析 625

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表1 内生真菌可抑制的昆虫、线虫及螨虫的种类(改自Kuldau & Bacon, 2008)
Table 1 Insect, nematodes and mites deterred by Neotyphodium/Epichloë species (adapted from Kuldau & Bacon, 2008)
内生真菌 Endophyte 宿主植物 Host plant 害虫 Pest
Epichloë glyceriae 苇状羊茅 Festuca arundinacea 禾谷缢管蚜 Rhopalosiphum padi
E. sylvatica 短柄草 Brachypodium sylvaticum 草地贪夜蛾 Spodoptera frugiperda
E. festucae 苇状羊茅 F. arundinacea Endria inimica
东亚飞蝗 Locusta migratoria
黑腹果蝇 Drosophila melanogaster
Exitianus exitiosus
麦长管蚜 Sitobion avenae
紫羊茅 F. rubra Meloidogyne naasi
Metopolophium festucae
Meloidogyne marylandii
Anguina funina
帽状纽带线虫 Hoplolaimus galeatus
双角螺旋线虫 Helicotylenchus digonicus
异毛刺线虫属 Paratrichodorus sp.
E. festuca var. lolii 多花黑麦草 Lolium perenne 黑异爪蔗金龟 Heteronychus arator
E. typhina 苇状羊茅 F. arundinacea Balanococcus poae
Graphania mutans
Persectania ewingii
Neotyphodium coenophialum 苇状羊茅 F. arundinacea 草螟蛾属 Crambus sp.
赤拟谷盗 Tribolium castaneum
Exomala orientalis
玉米跳甲 Chaetocnema pulicaria
禾谷缢管蚜 Rhopalosiphum padi
黑角负泥虫 Oulema melanopus
Adoryphorus coulonii
Graphania mutans
Prosapia bicincta
玉米螟 Ostrinia nubilalis
日本丽金龟 Popillia japonica
乳香平翅根蚜 Aploneura lentisci
斯克里布纳短体线虫 Pratylenchus scribneri
白符跳 Folsomia candida
咖啡短体线虫 Pratylenchus goodeyi
Sphenophorus inaequalis
玉米蚜 Rhopalosiphum maidis
Pogonomyrmex rugosus
N. gansuense 醉马草 Achnatherum inebrians 猬草瘿螨 Abacarus hystrix
亚洲小车蝗 Oedaleus decorus
针毛收获蚁 Messor aciculatus
Pogonomyrmex rugosus
罗格斯石竹蚁 Tetranychus cinnabarinus
N. uncinatum 草甸羊茅 F. pratensis 阿根廷茎象甲 Listronotus bonariensis
玉米跳甲 Chaetocnema pulicaria
黑异爪蔗金龟 Heteronychus arator
褐新西兰肋翅鳃角金龟 Costelytra zealandica

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表1 (续) Table 1 (continued)
内生真菌 Endophyte 宿主植物 Host plant 害虫 Pest
短齿默林线虫 Merlinius brevidens
伤残短体线虫 Pratylenchus pratensis
索氏短体线虫 Pratylenchus thornei
原始毛刺线虫 Trichodorus primitivus
早熟禾缢瘤蚜 Rhopalomyzus poae
N. lolii 多花黑麦草 L. perenne 澳洲日野黑蟋蟀 Teleogryllus commodus
Parapediasia sp.
Meloidogyne naasi
大螟 Sesamia inferens
Cyclocephala lurida
Meloidogyne marylandii
玉米跳甲 Chaetocnema pulicaria
谷物锈螨 Abacarus hystrix
禾谷缢管蚜 Rhopalosiphum padi
黑角负泥虫 Oulema melanopus
Draeculocephala cephala
家蟋蟀 Acheta domesticus
麦无网长管蚜 Metopolophium dirhodum
Graphania mutans
玉米螟 Ostrinia nubilalis
乳香平翅根蚜 Aploneura lentisci
条沙叶蝉Psammotettix striatus
Bitylenchus maximus
Bitylenchus dubius
亚洲玉米螟 Ostrinia furnacalis
Agallia constricta
玉米蚜 Rhopalosiphum maidis
N. starrii 亚利桑那羊茅 F. arizonica 黄地老虎 Agrotis segetum
小地老虎 Agrotis ipsilon
Agrotis infusa
Neotyphodium spp. 布顿大麦草 Hordeum bogdanii 麦双尾蚜 Diuraphis noxia
草甸羊茅 F. pratensis 美洲毛谷杆长蝽 Blissus leucopterus hirtus
苇状羊茅 F. arundinacea Philobota productella
Cyclocephala lurida
玉米跳甲 Chaetocnema pulicaria
Aphodius tasmaniae
黄伪毛蚜 Sipha flava
褐新西兰肋翅鳃角金龟 Costelytra zealandica
麦二叉蚜 Schizaphis graminum
Draeculacephala antica
Sphenophorus minimus
杂拟谷盗 Tribolium confusum
多花黑麦草 L. perenne 阿根廷茎象甲 Listronotus bonariensis
滨海油葫芦 Teleogryllus oceanicus
莓蚜 Sitobion fragariae

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表1 (续) Table 1 (continued)
内生真菌 Endophyte 宿主植物 Host plant 害虫 Pest
长毛草盲蝽 Lygus rugulipennis
玉米跳甲 Chaetocnema pulicaria
Mythimna convecta
Graminella nigrifrons
锯谷盗 Oryzaephilus surinamensis
赤须盲蝽 Trigonotylus caelestialium
Sphenophorus venatus
麦二叉蚜 Schizaphis graminum
乳草长蝽 Oncopeltus fasciatus
Persectania ewingii
Trigonotylus caelestialum
较小拟毛刺线虫 Paratrichodorus minor
Mythimna unipuncta
早熟禾结网毛虫 Parapediasia teterrella
牧草尖隐喙象 Sphenophorus parvulus
粘虫 Mythimna separate
Pseudalectia unipunctata
野大麦 H. brevisubulatum subsp. violaceum 麦双尾蚜 Diuraphis noxia
紫羊茅 F. rubra 美洲毛谷杆长蝽 Blissus leucopterus hirtus

物碱及其他次生代谢产物, 这些化合物对病原菌的
生长均具有较强的抑制作用(Faeth, 2002)。
一些研究发现, 部分内生真菌的侵染可诱导宿
主禾草产生系统抗病性(Kunkel et al., 2004; Roberts
et al., 2008)。相对于未带内生真菌的冰草(Agropyron
cristatum)、紫羊茅及圆柱披碱草(Elymus cylindri-
cus), 侵染内生真菌的宿主叶片上链格孢、枝孢及镰
刀菌病斑数相对较少, 这可能与内生真菌诱导宿主
禾草启动防御机制, 导致相关反应酶量增加、活性
增强有关(Nan & Li, 2000)。在其他一些禾草-内生真
菌共生体抗病性的研究中也得到了较一致的结果
(Kunkel et al., 2004; Tian et al., 2008)。
目前, 禾草内生真菌提高宿主抗病方面研究较
多的病原真菌主要是: 链格孢、壳二孢(Ascochyta
leptospora)、离蠕孢、镰刀菌和德氏霉等(Gwinn &
Gavin, 1992; Yue et al., 2000; 李秀璋等, 2015)。此
外 , 内生真菌的侵染能有效地降低大麦黄萎病
(Barley yellow dwarf virus)的发生, 这可能是由于其
对蚜虫较强的抗取食能力间接降低了蚜虫对黄萎病
毒传播的媒介作用(Mahmood et al., 1993)。
寄生于禾本科羊茅属、黑麦草属、芨芨草属等
冷季型禾草中的Epichloë/Neotyphodium内生真菌至
少对22种病原真菌有拮抗作用, 这为禾草内生真菌
作为潜在生防因子提供了有力的理论依据(南志标
和李春杰, 2004; 李秀璋等, 2015)。
4 内生真菌对禾草竞争作用的影响
在长期的群落演替过程中, 禾草-内生真菌共
生体逐渐显示出较强的适应性及竞争能力, 牢牢地
占据着某一特定的生态位(Clay & Holah, 1999)。在
对雀麦(Bromus benekenill)、多花黑麦草及苇状羊茅
等的研究中发现, 其带菌率随着草地年龄的增加而
呈明显的增加趋势, 带菌禾草大多表现出分蘖数增
多、生物量增加、叶片伸长加快及根系发育改善等
特征 (Malinowski et al., 1999b; Brem & Leucht-
mann, 2002; Clay et al., 2005)。由于带菌多花黑麦草
对白三叶草生长有较强的抑制作用, 因此很难建植
较理想的多花黑麦草-白三叶草混播草地(Sutherland
et al., 1999)。相对于内生真菌侵染率较低的苇状羊
茅草地, 内生真菌能够很好地保证草地持续性并控
制其他杂草的侵入及定植(Clay & Holah, 1999), 这
与苇状羊茅和红三叶(Trifolium pratense)的田间竞
争试验结果相类似(Malinowski et al., 1999a)。通过
对侵染内生真菌、未侵染内生真菌的多花黑麦草与
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百脉根 (Lotus corniculatus)、长叶车前 (Plantago
lanceolata)及3种三叶草的田间竞争试验表明, 内生
真菌能有效地提高宿主禾草在混播草地中的竞争能
力, 明显降低伴生种的生物量(Vázquez-de-Aldana
et al., 2013)。
内生真菌通过诱导宿主禾草的生理生化反应发
生改变或分泌化感物质, 影响其伴生植物生长, 提
高宿主在群落中的竞争能力, 改变群落结构(Clay &
Schardl, 2002; Clay et al., 2005)。黄玺等(2010)研究
发现, 带菌醉马草可抑制其伴生针茅(Stipa capilla-
ta)、硬质早熟禾(Poa sphondylodes)种子的萌发和幼
苗的生长; 同时可有效地抑制针茅和硬质早熟禾的
分蘖数及单株生物量。带内生真菌的披碱草(Elymus
dahuricus)草粉对3种草坪草——多花黑麦草、苇状
羊茅、草地早熟禾(Poa pratensis)种子的萌发及种苗
的生长特性均表现出较明显的化感作用(杨松等,
2010)。
5 禾草内生真菌作为生防因子的前景及展望
一个世纪以前, 研究者就发现内生真菌的侵染
并不会引起宿主禾草发生病害。然而内生真菌作为
潜在生防因子提高宿主禾草抗虫、抗病的报道从20
世纪80年代后期才逐渐增多(Bacon et al., 1986;
Schardl, 2001; Clay & Schardl, 2002; Rudgers et al.,
2004)。
内生真菌主要生长在宿主禾草细胞间隙, 从而
占据着一定的生态位, 这种独特的栖息方式为宿主
禾草抵抗生物与非生物因素的胁迫成为可能(Moy
et al., 2000)。由于Epichloë/Neotyphodium内生真菌的
存在, 宿主禾草细胞间隙的基本生物学特征也因此
而发生改变。内生真菌因其独特的内生方式随宿主
的生长而生长, 因而能免受外界环境变化对其造成
的直接影响。根据内生真菌生长潜力的差异, 不同
内生真菌会随着宿主禾草生长点细胞的分化而在不
同组织细胞间隙中定殖生长。内生真菌的生长特性
因其生殖模式的不同而千差万别, 特别是存在有性
世代的内生真菌, 它不仅具有垂直传播的能力, 同
时还可水平传播 (Schardl, 2001; Clay & Schardl,
2002; Schardl et al., 2004; 贾彤等, 2015)。
未来对禾草内生真菌的应用不应仅局限于对某
些天然共生体的筛选, 而应对现有菌株进行改良并
设法导入目标禾草体内, 创造新的品质优良的禾草
-内生真菌共生体 (Murray et al., 1992; Scott &
Schardl, 1993)。这种方式大多是通过对禾草内生真
菌相关基因进行改造, 并以改造后的内生真菌作为
载体, 间接实现宿主对多种逆境胁迫的优良抗性。
目前这种转化技术大多是利用禾草内生真菌中丰度
较高的杀虫活性基因, 同时对其他毒性基因进行修
饰, 增加或改善宿主禾草营养品质、提高草产量, 使
转化后的禾草具备天然的抗虫活性, 从而实现人们
在农业、草业等领域的应用需求。近年来, 研究人
员利用内生真菌的优良特性已经在多花黑麦草、苇
状羊茅等冷季型禾草的育种试验中取得了成功, 相
继培育出具有抗虫防病, 但对家畜无毒的牧草新品
种(Bouton & Easton, 2005)。也有研究人员利用禾草
内生真菌次生代谢物对鸟类等动物毒力活性较高的
特点, 培育出用于机场绿化的新型草种‘Avanex’,
并在新西兰、美国等地区开始应用①。因此, 这种寄
主替代转换方式不但能间接地提高宿主高产抗逆
性, 还可能比传统的转基因植物具有更高的应用价
值, 且更容易被公众所接受。
随着研究工作的深入, 生物碱在共生体内的合
成途径也逐步变得清晰(Schardl et al., 2013)。研究发
现生物碱在离体条件下对有害生物仍具有较高的毒
力活性 , 不同物种之间生物碱含量差异明显
(Schardl et al., 2013)。目前生物碱的提取和纯化方法
已日趋成熟, 对生物碱进行制剂加工, 进而用作生
物源农药逐步成为可能。当然, 要使生物碱作为生
物源农药进行开发并大面积工厂化生产还面临着诸
多问题, 例如菌株的筛选、加工助剂的选择、大田
施用的稳定性及持久性、对环境的影响等一系列问
题都有待于深入研究。
尽管禾草内生真菌有作为生防因子的巨大潜
力, 且目前也取得了不少成果, 但是将优良内生真
菌菌株导入目标宿主体内, 获得性状良好的新禾草-
内生真菌组合仍存在许多亟需解决的问题, 例如接
种技术的优化、内生真菌在新宿主体内的生存状况、
接种成功后内生真菌的表型及潜在毒性、遗传的稳
定性(魏宇昆和高玉葆, 2008)等。目前, 已经被证明
成功率相对较高的接种方法是创伤法, 即将培养好
的内生真菌菌丝接到受体禾草生长点(Latch et al.,
1985)或愈伤组织中(Johnson et al., 1986)。但即便是

① Pennell CGL, Rolston MP (2012). Novel uses of grass endophyte
technology. In: Nan ZB, Li CJ eds. Proceedings of the 8th International
Symposium on Fungal Endophyte of Grasses. Lanzhou, China. 211–214.
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doi: 10.17521/cjpe.2015.0060
对于经验较丰富的专业技术人员来说, 这种方法仍
然费时费力且成功率极低。其他研究发现, 通过小
花(floret)可向小麦(Triticum aestivum)和大麦(Hor-
deum vulgare)等作物成功接种禾谷镰刀菌(F. gra-
minearum), 这种接种方法经过不断完善, 目前已日
趋成熟 (Engle et al., 2003; Lewandowski et al.,
2006)。尽管禾谷镰刀菌是一种病原真菌, 但是这种
接种策略是否可以作为内生真菌成功地接种目标禾
草, 很值得研究者进一步探索。
一个新的禾草-内生真菌共生体的形成必须保
证宿主的某些基本生物学特征不发生改变, 例如内
生真菌在宿主体外不表现任何外部症状且不引致病
害。因此, 深入研究内生真菌与宿主禾草之间基本
的互作基础对接种成功与否至关重要。有关禾草-
内生真菌互作机制的研究已经在苇状羊茅和多花黑
麦草这两种模式共生禾草中逐步展开, 研究发现其
共生关系涉及多个基因识别位点及互作(Tanaka et
al., 2008; Eaton et al., 2010; Takemoto et al., 2011)。
绝大多数禾草内生真菌主要通过宿主种子垂直传播
到下一代, 因此宿主种子自身的遗传率问题也应受
到重视, 这直接关系到内生真菌的生存环境和带菌
种子稳定遗传的寿命。
研究发现, 禾草内生真菌产生的衍生毒素物质
在其与C3禾草形成的共生体中可能广泛存在(Sch-
ardl et al., 2006), 这是利用内生真菌进行作物育种
过程中不得不考虑的一个潜在威胁。尽管禾草-内生
真菌共生体对人体的毒性作用尚未见报道。抗性优
良的内生真菌菌株与禾本科作物互作有可能产生有
毒的次生代谢产物, 这可能对一些作为人类食物的
新作物-内生真菌共生体的应用带来深远影响。
6 小结
目前, 有关禾草内生真菌作为生物防治手段的
基础理论研究已取得了丰硕的成果。然而, 由于禾
草-内生真菌共生体的多样性及其共生机制的复杂
性, 给内生真菌的应用带来了巨大挑战。大部分有
关内生真菌的研究, 主要集中在其对宿主禾草农艺
性状、物种多样性及对环境的适应性等方面, 但是
从整个生态系统出发研究内生真菌共生体与其他物
种的相互关系依然较少。在运用内生真菌进行有害
生物防治的过程中, 不应只考虑作用双方的相互关
系, 而应全面分析内生真菌在整个生物链或一个小
的生物群落中的作用(周勇等, 2014), 及其是否会对
天敌昆虫、鸟类等其他有益生物造成间接的负面影
响(Omacini et al., 2001; de Sassi et al., 2006), 从而
为开发出安全、低毒、高效的内生真菌生防制剂提
供理论支持。
当今世界多数地区为抗虫防病实现高产而片面
地大量使用化学类农药, 这不但给食品安全问题带
来不可预测的风险, 而且无异于让日趋严重的环境
问题雪上加霜。因此, 各国出台了较严厉的农药使用
法规。那么, 是否可以引入禾草内生真菌提高作物抗
虫防病能力进而逐步替代化学农药呢？利用禾草-内
生真菌共生体在生物防治方面研究的诸多成功经验,
将注意力转移到对禾本科作物的品质改良中, 这有
可能成为未来禾草内生真菌研究的热点之一。是否
可以用禾草内生真菌作为载体改善作物性状、改良
作物品质、提高作物产量, 培育出带有禾草内生真菌
的品质优良的作物品种? 我们拭目以待。
总之, 内生真菌与宿主禾草之间的许多互作机
制仍有待于进一步揭示, 需全面认识禾草内生真菌
的多样性意义, 充分挖掘其在生物防治和其他领域
的巨大潜力, 以期为生物防治策略提供新的借鉴。
基金项目 国家重点基础研究发展规划(“973”计
划) (2014CB138702)、国家自然科学基金(31372-
366)、教育部创新团队发展计划(IRT13019)。
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