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菌物学报, 2021, 40(6): 1299-1316 doi: 10.13346/j.mycosystema.210077

综述

杜鹃花科植物菌根的研究进展

张艳华, 孙立夫,*

绍兴文理学院生命科学学院 浙江 绍兴 312000

Research advances on the mycorrhizas of Ericaceae plants

ZHANG Yan-Hua, SUN Li-Fu,*

School of Life Sciences, Shaoxing University, Shaoxing, Zhejiang 312000, China

责任编辑: 王敏

收稿日期: 2021-02-5   接受日期: 2021-03-22   网络出版日期: 2021-06-22

基金资助: 国家自然科学基金.  31170469
浙江省自然科学基金.  LY19C030002

Corresponding authors: *E-mail: sunlifu@usx.edu.cn

Received: 2021-02-5   Accepted: 2021-03-22   Online: 2021-06-22

Fund supported: National Natural Science Foundation of China.  31170469
Natural Science Foundation of Zhejiang Province.  LY19C030002

摘要

杜鹃花科Ericaceae植物可与土壤真菌形成杜鹃花类菌根ericoid mycorrhizas（ERM）共生体,且广泛分布于全球不同的陆地生态系统,特别是在贫瘠、酸性等严酷的环境中占优势。杜鹃花科植物菌根类型多样,绝大多数宿主具有ERM,还有少量宿主具有其他类型的菌根结构,且常与暗隔内生菌（dark septate endophyte,DSE）并存;ERM的宿主植物除已知的杜鹃花科外,岩梅科Diapensiaceae植物也具有ERM结构;ERM真菌以子囊菌和担子菌为主,主要来自柔膜菌目Helotiales和蜡壳耳目Sebacinales;与杜鹃花科宿主形成ERM的真菌也常与壳斗科Fagaceae、松科Pinaceae等宿主植物形成外生菌根（ectomycorrhiza,ECM）结构;ERM对宿主植物在营养吸收、忍耐贫瘠环境、抵抗重金属污染等能力方面都有积极的促进作用,对环境变化的响应是多样的,生境和季节的变化对ERMF群落的组成和分布有着显著影响,资源比率变化可能改变ERM宿主与其他菌根或非菌根植物之间的竞争关系。本文回顾了近40多年来国内外有关ERM的研究进展,还对ERM研究的前景进行了展望,以期在理论和实践中对杜鹃花科及其菌根的研究能取得更丰硕的成果。

关键词： 杜鹃花科植物 ; 杜鹃花类菌根 ; 菌根真菌 ; 多样性

Abstract

Ericaceae plants and soil fungi often form ericoid mycorrhiza (ERM) symbiosis. ERM fungi are distributed widely over different global continental ecosystems, especially dominate in harsh environment with poor and acid soil. The mycorrhizal types of Ericaceae were diverse; apart from ERM, a few other types of mycorrhizae can be found in some ericaceous hosts, and often coexist with dark septate endophyte (DSE). Besides the well-known Ericaceae, ERM structure was also discovered in Diapensiaceae plants. ERM fungi mainly belonged to Ascomycetes and Basidiomycetes, and mostly Helotiales and Sebacinales. ERM fungi often formed ectomycorrhizal (ECM) structures on other hosts such as Fagaceae and Pinaceae. ERM not only helped their hosts on absorbing nutrients, increasing tolerant capacity in poor nutrient habitats, but also enhancing the resistance to heavy metal contamination. The community composition and distribution of ERM fungi showed significant variation with habitats and seasons. The variation of resource ratio might change the competitive relationship between ERM host and other mycorrhizal or non-mycorrhizal plants. In this paper, the advances of researches on ERM and their hosts over the past 40 years were reviewed. Prospect about ERM study was also previewed.

Keywords： Ericaceae ; ericoid mycorrhiza ; mycorrhizal fungi ; diversity

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本文引用格式

张艳华, 孙立夫. 杜鹃花科植物菌根的研究进展. 菌物学报[J], 2021, 40(6): 1299-1316 doi:10.13346/j.mycosystema.210077

ZHANG Yan-Hua, SUN Li-Fu. Research advances on the mycorrhizas of Ericaceae plants. Mycosystema[J], 2021, 40(6): 1299-1316 doi:10.13346/j.mycosystema.210077

植物作为生产者是陆地生态系统的主体,可以与土壤真菌形成高度进化的互利共生体,即菌根（mycorrhiza）,植物物种的生态位分化和扩展与菌根的共生有关（Gerz et al. 2018 ）,形成菌根的真菌主要包括接合菌纲、子囊菌纲、担子菌纲及部分卵菌纲的成员,而宿主植物则包括了绝大多数的维管植物（Brundrett 1991）。目前已知至少有7种不同类型的菌根共生体,即丛枝菌根（arbuscular mycorrhizas,AM）、外生菌根（ectomycorrhizas,ECM）、内外生菌根（ectendomycorrhizas,EEM）、兰科菌根（orchid mycorrhizas,OM）、欧石南类菌根或杜鹃花类菌根（ericoid mycorrhizas,ERM）、浆果鹃类菌根（arbutoid mycorrhizas,ARM）和水晶兰类菌根（monotropoid mycorrhiza,MM）。与研究较多的AM和ECM相比,ERM的研究相对不多。而作为ERM主要宿主的杜鹃花科Ericaceae植物,种类多样,资源丰富,广泛分布于全球陆地生态系统,其中很多种类都可以作为先锋植物,定居在从酸性的沙土到湿润的粗腐殖质的基质上,都得益于它们有共生的菌根真菌（Perotto et al. 2002 ）。杜鹃花科植物最主要的菌根类型是ERM,其菌根真菌简称为ERMF。本文对近40多年来,国内外有关杜鹃花科植物菌根的类型、真菌、宿主、功能等方面所展现出来的多样性进行了总结,为深入认识、了解进而利用这一类型的菌根提供参考。

1 杜鹃花科植物菌根类型的多样性

杜鹃花科有数千个物种且分布广泛,是否都能形成ERM的菌根结构呢?Gorman & Starrett（2003）用同一种公认的ERMF接种10个不同属的杜鹃花科植物,除了吊钟花属Enkianthus植物未被侵染以及草莓树属Arbutus unedo侵染后形成了AM外,其他8个属的植物都能被侵染并形成ERM结构,证明了Read（1996）认为的杜鹃花科植物大多数能形成ERM结构的论断,同时也认为杜鹃花科植物根部的菌根类型并不是单一的ERM,还可以形成AM、MM（Jansa & Vosatka 2000;Kamal & Varma 2008）、ECM（Read 1996）和被称为伪菌根或假菌根（pseudomycorrhizal）的暗隔内生菌（dark septate endophyte,DSE）（Currah et al. 1993a ;Cázareset al. 2005 ;Chaurasia et al. 2005 ;Tian et al. 2011 ）。不同结构类型的菌根也可能共存于同一个植物的根系中,比较典型的情况是ERM和DSE常常同时出现（Cázareset al. 2005 ;Schulz 2006;Chambers et al. 2008 ;Tian et al. 2011 ;Vohník & Albrechtová 2011）;也偶尔发现部分杜鹃花科植物根中AM和DSE并存的现象（Chaurasia et al. 2005 ;宁楚涵等 2018）。这些研究表明杜鹃花科植物的菌根类型具有一定的复杂性和多样性。菌根结构的形成不仅与宿主植物种类有关,也与真菌种类有关,同一种杜鹃花属Rhododendron植物与不同的真菌形成不同的菌根（Currahet al. 1993a ;Vohníket al. 2005 ）。总体而言,ERM是杜鹃花科植物最主要且最常见的菌根类型。

不同宿主植物根中发现的ERM结构非常一致（Jansa & Vosatka 2000）,正如Read 1996和Peterson et al.（2004） 概括的那样,杜鹃花科植物都具有特别纤细的毛根（hair roots）,是由1层膨大的表皮细胞、1-2层皮层细胞和纤细的中柱组成,通常每一毛根末梢区域的直径都小于100µm,在表皮细胞中常有菌丝卷（或称菌丝圈、菌丝节,coil）（Read 1996）,在皮层细胞中也发现了子囊菌和担子菌的菌丝,但是它们的分布不同,子囊菌是在活的菌根细胞中占优势,而担子菌则主要出现在死的皮层细胞中（Duddridge & Read 1982）,当然在Rhododendron菌根活细胞中也发现了担子菌的隔片（Allen et al. 2003 ）。但未见有入侵中柱细胞的报道。

2 ERM宿主植物的多样性

Smith & Read（2008）认为ERM的宿主包括杜鹃花目Ericales杜鹃花科的多个亚科的植物,如杜鹃花亚科Ericoideae、岩须亚科Cassiopoideae、越橘亚科Vaccinioideae、澳石楠亚科Styphelioideae,且将原来Ericales的尖苞树科（或称掌脉石南科或澳石南科）Epacridaceae和岩高兰科Empetraceae的植物种类降级为族,这与此前发表的文献中有关ERM及其宿主植物提到的植物分类系统有了较大差异。为了尊重被引用文献和避免混淆,对需要引用的Epacridaceae和Empetraceae进行说明时前面都加上“原”字。在北半球,特别是在杜鹃花科的帚石南属Calluna、欧石南属Erica、杜鹃花属Rhododendron、越橘属（或乌饭树属）Vaccinium等植物中,ERM是普遍存在的（Jansa & Vosatka 2000）;在南半球原Epacridaceae中的澳石南属Epacris、贝叶石南属Leucopogon、松石南属Astroloma、瑞香石南属Brachyloma和垂钉石南属Styphelia等植物的根中ERM也很常见（McLean & Lawrie 1996）。日本学者Okuda et al.（2011） 对岩梅目Diapensiales岩梅科Diapensiaceae的Schizocodon soldanelloides var. magnus菌根的结构和功能进行鉴定后认为也是ERM。Ericales和Diapensiales同属于五桠果亚纲Dilleniidae,具有很近的亲缘关系,因此,能够形成ERM的宿主植物范围比原来想象的要大。

3 ERM真菌的多样性

从目前的研究成果来看,能够形成ERM共生体的真菌主要是来自子囊菌纲和担子菌纲的成员,也有少量的接合菌纲（Chambers et al. 2008 ）和无性型真菌的成员（Berch et al. 2002 ;Allen et al. 2003 ;Bougoure & Cairney 2005b）。这些真菌和宿主植物形成的共生关系,既有兼性的又有专性的。如在北半球的地中海森林中,从Erica arborea获得的优势菌根真菌（Bergeroet al. 2000 ）与在南半球澳大利亚的Astroloma pinifolium中获得的内生菌（McLean et al. 1998 ）极为相似,并且从两个半球不同宿主植物根中获得的内生菌,很多都可以在对方的根中形成ERM结构（Read 1996;Steinke et al. 1996 ;Liu et al. 1998 ;McLeanet al. 1998 ;Perotto et al. 2002 ）,这表明能够共生于两个半球的不同植物类群间的真菌可能有很近的亲缘关系。从杜鹃花科植物根部分离最多而且也是最容易培养并形成ERM结构的主要是子囊菌纲中柔膜菌目Helotiales的Rhizoscyphus ericae和树粉苞属Oidiodendron等真菌（Usuki et al. 2003 ;Kamal & Varma 2008;Grelet et al. 2010 ）。这两大类群在Diapensiaceae（Okuda et al. 2011 ）和原Epacridaceae（Chambers et al. 2000 ）植物根中也均有报道。Gorman & Starrett（2003）用R.ericae接种到杜鹃花科的10属15种宿主植物根上,其中8属13种植物都被侵染并形成ERM,说明这种真菌在杜鹃花科植物中具有广泛的宿主选择范围,属于兼性互利共生的典范。但是,McLeanet al.（1999） 却认为从原Epacridaceae分离出的一些菌株并非杜鹃花科内ERMF的相同物种,不同植物物种中可能有专性的共生真菌种类。

真菌Rhizoscyphus ericae与之前发表的Hymenoscyphus ericae（Cairney & Burke 1998）和Pezoloma ericae（Midgleyet al. 2017 ）是同物异名（本文统一用R.ericae）,是一种广谱型ERMF。研究发现R.ericae不仅有无性型的Scytalidium vaccinii（Egger & Sigler 1993）,而且R.ericae也不是一个单一真菌种类,而是一个聚集体（aggregate）,其含有4个在遗传学上关系密切的分支,即Meliniomyces variabilis、M.vraolstadiae、M.bicolor和Cadophora finlandica,其中发现M.vraolstadiae至今只能形成ECM而不能形成ERM,其他3种真菌均可以在不同宿主根中形成ECM和ERM（Greletet al. 2010 ）。这表明R.ericae作为公认的ERM共生体中常见的真菌,它们形成何种菌根结构取决于宿主与真菌之间的相互识别和选择。

形成ERM的Oidiodendron spp.中以O.maius最为典型和常见,其宿主的选择范围也很广（Douglas et al. 1989 ;Berch et al. 2002 ;Piercey et al. 2002 ;Rice & Currah 2005;Vohníket al. 2005 ;Zhang et al. 2009 ）。本属的其他种,如O.griseum（Couture et al. 1983 ;Dalpé 1986;Xiao & Berch 1992）、O.rhodogenum和O.cerealis（Dalpé 1986）、O.periconiodes（Currah et al. 1993b ）和O.chlamydosporicum、O.citrinum、O.flavum和O.scytaloides（Dalpé 1991）等,在杜鹃花科植物根中也能形成ERM,但是不同植物的ERM中共生的Oidiodendron spp.的种类有一定差异,如从Rhododendron植物中分离出的多为O.maius,而从Vaccinium根系中分离出其他的Oidiodendron spp.菌株则较多。而且本属中也有无性型真菌Stephanosporium cerealis（Monreal et al. 1999 ）,与O.cerealis（Xiao 1994）属于同物异名。

除了子囊菌纲的Oidiodendron maius和Rhizoscyphus ericae聚集体的成员外,担子菌纲的蜡壳耳目Sebacinales也是Ericacea宿主根中普遍存在的真菌类群（Bonfante-Fasolo 1980;Allen et al. 2003 ;Selosse et al. 2007 ;Setaro & Kron 2011）,在ERM解剖结构研究中认为,珊瑚菌属Clavaria的某些菌种也许是ERMF（Petersonet al. 1980 ）,此后,在Vaccinium sp.上发现C.oronoensis,证明了担子菌也能形成ERM（Straker 1996）。生长在北极生态系统的Cassiope tetragona（Ericaceae）宿主中占优势的是担子菌,不仅有Clavaria,还有Cortinarius和Mycena等属的真菌（Lorberauet al. 2017 ）,而且很多都是原来公认的腐生菌或ECM真菌,但是却能形成典型的ERM结构而非ECM结构。

另外,皮盘菌科Dermatcaceae部分真菌以及几种未知名真菌（Xiao 1994;Usuki et al. 2003 ;Bougoure & Cairney 2005a,2005b;Grelet et al. 2009 ）和被称为variable white taxon（VWT）的真菌（Hambleton & Currah 1997;Piercey et al. 2002 ）,以及属于Helotiales的DSE真菌,如瓶霉属Phialophoraspp.（Hambleton & Currah 1997;Grüniget al. 2008 ）、Phialocephala fortinii（Vohníket al. 2003 ）在多种杜鹃花宿主的ERM根中也经常出现。

与同一宿主植物共生的ERMF也是多样的,Wurzburgeret al.（2011） 从生长于温带森林Rhododendron maximum的ERM中分离出来71种真菌,包括常见的Rhizoscyphus ericae和Oidiodendron maius,来自Helotiales、刺盾炱目Chaetothyriales和Sebacinales的真菌,以及一些已知的ECM真菌和腐生菌。Zhanget al.（2016） 通过高通量测序获得在中国亚热带森林中Vaccinium carlesii的根部真菌组成,也证明在有ERM结构的宿主毛根中还有大量的其他类型真菌的存在,ERMF只占其中的一部分。Allenet al.（2003） 就在白珠树属Gaultheria shallon的同一个ERM结构中发现了担子菌的蜡壳耳属Sebacina spp.、砖隔腔菌Capronia sp.和R.ericae,平均每根有3.8个遗传上不同的真菌分类单元。还有研究表明,ERM的相邻细胞能够与不同真菌形成菌根结构（Monreal et al. 1999 ;Perotto et al. 2002 ）。对来自中国四川和云南的杜鹃花属Rhododendron decorum菌根真菌的研究发现有25个公认的ERMF种类（Sun et al. 2012 ）。这些研究说明ERMF的多样性水平较高,但是这些内生真菌的种类和分布是否存在宿主特异性和生境特异性还有待进一步验证（Walker et al. 2011 ）。

尽管用分子生物学手段已经把ERMF的分类鉴定精确到目,甚至更精细的分类等级,但是有很多真菌仍然因为缺少明显的子实体或分离培养困难,而难以鉴定到物种水平（Perotto et al. 2002 ;Allen et al. 2003 ;Hamímet al. 2017 ）,这也是ERMF研究进展缓慢的重要原因。

4 ERM真菌形成菌根类型的多样性

在开放的自然生态系统中,杜鹃花科植物常与松科Pinaceae、桦木科Betulaceae、壳斗科Fagaceae、杨柳科Salicaceae、禾本科Poaceae等的植物种类伴生。而且有证据表明,一些公认的ERMF也可与其他植物的根共生,形成不同类型的菌根（Cairney & Meharg 2003）。

在北半球的地中海,从相邻的Fagaceae植物（ECM）栎属Quercus ilex和杜鹃花科植物（ERM）Erica arborea分离出相同的真菌（Bergero et al. 2000 ;Cairney & Meharg 2003）;同样地,在北温带森林中,相邻的Pinaceae植物（ECM）Pinus sylvestris和杜鹃花科植物（ERM）Vaccinium vitis-idaea,杜鹃花科植物Vaccinium myrtillu与Pinaceae植物Pinus sylvestris和Piceirhiza bicolorata之间也都分离出相似的真菌菌株,且发现其中38%以上形成ECM的Pinus根尖被典型ERMF——Rhizoscyphus ericae聚集体所侵染（Grelet et al. 2009 ,2010）。因此,在北半球能形成ERM和ECM的不同伴生物种可能存在较为普遍的基因型相似的共生真菌。同样,在南半球干旱的澳大利亚东部的硬叶林中,从伞形科Apiaceae、火把树科（或南蔷薇科）Cunoniaceae、莎草科Cyperaceae、茅藳菜科Droseraceae、豆科Fabaceae的含羞草亚科Mimosoideae、点柱花科Lomandraceae、桃金娘科Myrtaceae、海桐花科Pittosporaceae、山龙眼科Proteaceae和花柱草科Stylidiaceae的10个科17种植物根中分离出来的真菌涉及子囊菌、担子菌和接合菌多个类群（Chamberset al. 2008 ）,发现其中能够在Epacris sp.形成ERM的真菌是澳大利亚东北部硬叶林中非杜鹃花植物根中常见的栖息者。在欧洲、澳洲和南极半岛,苔藓植物——地钱常与杜鹃花科植物伴生,而杜鹃花科植物根部常见的ERMF——R.ericae及其亲缘关系较近的真菌也是一些叶状地钱的内生菌（Duckett & Read 1995;Chambers et al. 1999 ）,与从温带杜鹃花科植物中获得的真菌功能相同（Cairney et al. 2000 ;Whittaker & Cairney 2001）。

在具有相同菌根真菌存在的条件下,菌根共生体（ERM或ECM）的形态结构是在宿主植物控制下发生的（Grelet et al. 2009 ）,如在实验条件下Helotiales的Phialophora finlandia与不同宿主植物分别形成了ERM、ECM或EEM结构（Perotto et al. 2002 ）;在无菌条件下,一个Rhizoscyphus ericae聚集体菌株,与Vaccinium myrtillus和Pinus sylvestris可以同时形成ERM和ECM结构（Villarreal-Ruiz et al. 2004 ）;在荷兰和丹麦欧石南荒地,从Poaceae的Deschampsia flexuosa的根中分离出来Helotiales的真菌,可以侵染并提高Calluna vulgaris幼苗吸收氮的能力（Zijlstra et al. 2005 ;Chambers et al. 2008 ）。因此,Bergero & Girlanda（2002）推断在地中海缺少杜鹃花宿主的成熟Quercus ilex森林土壤中,能够形成ERM的真菌仍然能够坚持和保持形成菌根的能力,为在干扰后的Q.ilex纯林中杜鹃花科植物Erica arborea幼苗的定居储备了必要的真菌资源。根据真菌与不同宿主形成不同类型菌根能力的情况来看,非杜鹃花科植物种类在阔叶林土壤中能够起着ERM真菌库的作用（Chambers et al. 2008 ）。

虽然有很多研究认为ERM植物和其他类型菌根在植物根部或者土壤中的真菌种类相似,但是并不等于就一定能发生交叉侵染。从Picea stichensis（ECM）根部分离得来的Oidiodendron maius菌株在杜鹃花宿主上未能形成ERM（Douglas et al. 1989 ）,该真菌甚至会表现出很强的腐生性（Piercey et al. 2002 ;Brundrett 2006）;分别来自ECM和ERM的Rhizoscyphus ericae野生菌株,只能分别与乔木种类形成ECM共生体,或与杜鹃花植物形成典型的ERM结构（Vrålstadet al. 2001 ）,交叉侵染都未能在对方的宿主根中形成应有的菌根结构（Bergero et al. 2000 ;Piercey et al. 2002 ;Brundrett 2006）。这些相反的结果表明,尽管在ERMF和菌根结构的研究中取得了一定的进展,但是,仍有很多问题还待于进一步的研究。

5 ERM功能的多样性

van der Heijden & Horton（2009）在对60个案例的研究中发现,菌根真菌网络对不同种类的幼苗生长有促进作用、负作用和没影响的分别占48%、25%和27%,说明幼苗与菌根共生获利占主流。这些现象在ERM共生体中也有相应的报道,正面影响的实例很多,如Rhizoscyphus ericae的有性型和无性型及Oidiodendron griseum对Calluna vulgaris的幼苗生长有促进作用（Read 1996）;在Vaccinium corymbosum上接种Cadophora菌株能形成典型的ERM并促进宿主的生长（Bizabani & Dames 2015）;拟隐孢壳属Cryptosporiopsis和瓶头霉属Phialocephala菌株接种在Rhododendron formosanum中,形成ERM菌根结构后其幼苗均比对照健壮（Lin et al. 2011 ）;一些ERMF在Rhododendron fortunei的幼苗生长（Yu et al. 2008 ,Wei et al. 2016 ）和在其他Rhododendron spp.植物生长过程中也表现出同样的促进作用（Jansa & Vosatka 2000）;在不同营养条件下,ERM菌根的存在提高了Calluna vulgaris与Poaceae的Nardus stricta的竞争力（Genney et al. 2000 ）。

5.1 ERM促进营养吸收

ERM的功能往往通过其组成的菌根真菌来实现,ERMF能产生多种水解酶和氧化酶,有降解多种有机物如纤维素、木质素等和加速必要营养素释放的能力（Cairney & Meharg 2003）。真菌种类不同,所分泌酶的类型也就不同,Phialocephala属的菌株能分泌过氧化物酶和酪氨酸酶,而Cryptosporiopsis属菌株除了分泌出这两种酶外,还可以分泌漆酶和纤维素酶（Lin et al. 2011 ）。Oidiodendron maius和O.scytaloides能够降解单宁酸,分泌多酚氧化酶（Thormann et al. 2002 ）。ERMF分泌的酶类不仅能帮助有机物降解,而且还能够提高对必要营养素,特别是氮和磷的直接吸收（Lin et al. 2011 ）,如ERMF分泌的蛋白酶和几丁质酶帮助宿主植物获得蛋白质和几丁质中的氮,磷酸酯酶则使宿主从磷酸单脂和磷酸二酯中获得磷（Bajwa et al. 1985 ;Leake & Read 1989;Myers & Leake 1996;Kerley & Read 1997）;ERMF也可以促进宿主植物从氨基酸和核酸中吸收氮（Bending & Read 1996,1997;Cairney & Burke 1998;Nielsena et al. 2009 ）,生长在大西洋西北部贫瘠的温带常绿森林中的Vaccinium membranaceum,其ERMF是磷的主要供应者（van der Wal et al. 2006 ）。比较生理学研究指出,对于Rhizoscyphus ericae及其类似的菌株、甚至更远缘的相关内生真菌,不管分类地位和原生境如何,它们从有机源获得氮和磷的能力几乎相同（Chen et al. 1999 ;Whittaker & Cairney 2001）。在自然生态系统中,植物对氮和磷的需求分别多达80%和90%来自菌根真菌（van der Heijden et al. 2008 ）,进而菌根真菌也能在抵御干旱和土壤病原体等胁迫方面提供帮助（Auge 2001;Sikes et al. 2009 ;Vohníket al. 2009 ）。如由于土壤有机物通常分解缓慢,ERMF利用复杂的有机氮的机制有益于宿主植物在寒温带气候区的生长（Straker 1996）。这些研究都充分说明了与ERMF共生的宿主植物具有很强的营养吸收能力,在逆境中具有生存和竞争优势。

将AM、ECM与ERM菌根的营养吸收能力进行比较发现,具有ECM（Picea abies）和ERM（Vaccinium myrtillus）的宿主从所有有机和无机氮源中获得了相似量的氮,而AM（Deschampsia flexuosa）宿主除了NH4+-N外,所吸收的所有氮源都显著低于NO3--N（Persson et al. 2003 ）;在对加利福尼亚沿海森林酸性、贫瘠和高有机质的土壤中,生长的ERM宿主（Rhododendron macrophyllum和Vaccinium ovatum）和AM宿主（Cupressus goveniana ssp. pigmaea）比较也发现,ERM宿主没有显示出对有机氮和无机氮的偏好,而AM宿主获得的无机氮明显高于有机氮（Rains & Bledsoe 2007）。这些研究表明AM宿主对无机氮吸收的偏好,在吸收有机氮方面的能力没有ERM和ECM宿主的能力强（Read & Perez-Moreno 2003）。

5.2 ERM抵抗重金属污染的能力

通常认为微生物比植物对金属毒性的耐受力更高（Hartley et al. 1997 ）,因此,具有ERM的共生体能提高宿主在重金属污染的土壤环境中的适合度（Meharg & Cairney 2000;Sharples et al. 2000a ,2000b;Chambers et al. 2008 ）。有关ERM在抗重金属污染方面的研究以Calluna vulgaris的成果最多,在Zn和Cu（Bradleyet al. 1981 ;Meharg & Cairney 2000）、Cu和Ni（Monniet al. 2000a ,2000b）、As和Cu（Cairney & Meharg 2003）、Pb和Cu污染（Marrs & Bannister 1978）的土壤中都表现出很强的抵抗力和进化适应的能力。另外,ERM宿主自然定居的土壤通常呈酸性,这就意味着有害金属如Al,氧化还原作用活跃的金属Fe和Mn等在这样的环境下更加活跃（Cairney & Meharg 2003）。这些研究都说明具有ERM结构的杜鹃花科宿主植物能忍耐的金属离子的范围非常广。

从生长于重金属污染土壤Calluna vulgaris的毛根中能分离出来的ERMF主要是Rhizoscyphus ericae和Oidiodendron maius。Sharples（2000b,2000c）认为R.ericae及其宿主C.vulgaris在抵抗重金属污染方面是平行进化的;将从Cd、Zn、Al污染（Vallino et al. 2011 ）和Cr、Ni污染（Martino et al. 2002 ）的土壤中都分离出O.maius的耐受菌株,且都比未污染地分离出来的O.maius菌株易于培养。经过污染地驯化的真菌菌株可能会在宿主植物适应环境污染方面发挥更大的作用,具有显著的生态价值和潜在的商业价值。

真菌怎样抵抗重金属毒害来保护自己呢?研究认为ERM中的真菌如Rhizoscyphus ericae对金属阳离子有很强的亲和力（Bradley et al. 1981 ）,真菌通过降低吸收或增加金属离子的流出来避免和限制重金属进入细胞质,如金属离子可以被吸收到菌丝表面以及在宿主和真菌的交界处（Bradleyet al. 1982 ）,被固定在真菌的细胞壁上（Leyval et al. 1997 ）,或被分隔在液泡或其他细胞器中（Pócsi 2011）;菌丝的细胞外分泌物对金属离子有耐受性（Perotto et al. 2002 ）,可与重金属结合并产生沉淀,或形成螯合物等方式（Colpaertet al. 2011 ）来降低重金属毒性。对于ERMF在重金属污染土壤中的存活、降解机制以及在污染地的治理方面的研究还需要进行更多的实践和总结。

6 ERM及其组成真菌对环境变化响应的多样性

6.1 ERMF群落组成随生境条件而变化

杜鹃花科植物能广泛地分布于全世界范围内的多种生境中,包括北半球的粗腐殖质的欧石南荒地、地中海木本林地、热带云雾森林和澳大利亚干旱沙化平原,被认为与ERM的存在有关（Cairney & Meharg 2003）。菌根真菌与植物兼性共生者很多,可能也是杜鹃花广泛分布的重要原因,如北美洲的加拿大和欧洲的意大利北部的不同杜鹃花植物根中都发现了高丰富度的Oidiodendron spp.（Hambleton & Currah 1997;Monreal et al. 1999 ）;Zhanget al.（2009） 调查的中国亚热带的黄山等4个不同山体Rhododendron fortunei时发现,Oidiodendron maius在宿主根中普遍存在,但是其分离出来的频率差距很大;Hamímet al.（2017） 发现在摩洛哥和法国5个样点的6种杜鹃花科宿主根中Helotiales最常见,但是毛根内生真菌分离频率因地区和宿主种类的不同而有很大差异;同样地,在欧洲,Calluna vulgaris在英格兰西南的矿质和自然欧石南荒地生境中主要被Rhizoscyphus erica侵染（Sharples et al. 2000a ）,在意大利北部的欧石南荒地则主要是被O.maius侵染（Perotto et al. 1996 ,2002）。说明ERMF种类及其丰富度可能与特殊的立地条件有关。土地利用方式的改变也会影响到ERM真菌在宿主根部真菌群落中的相对丰度,如Zhanget al.（2016,2017）在我国亚热带森林中对Vaccinium carlesii和Rhododendron ovatum的研究均发现,相同种类宿主根中的ERMF生长在人工林下的比生长在天然林下或次生林下的要少得多。DSE真菌也有对环境选择的类似情况（Zhanget al. 2009 ）,Vohník & Albrechtová（2011）对6种Rhododendronspp.研究发现,频率最高的ERM出现在欧洲南部与中部,而DSE的最高频率则在芬兰北部的亚北极区与喀尔巴阡山脉的亚高山区出现,认为纬度和海拔高度改变了ERM共生体的结构和组成;但是,Sunet al.（2012） 在中国云南和四川的15个样点采集分析的Rhododendron decorum毛根发现,其ERMF群落组成受到宿主遗传组成的影响比地理因素的影响更大,在诸多地理因素中仅与纬度相关,而非ERMF群落则与纬度、经度、海拔高度和年平均降雨量等多个因素有关。

ERMF群落组成在不同的生境中有明显的差异,优势真菌种类随着环境的不同而有变化,这些差异是由哪些因素影响造成的,还需要进行更深入的研究。

6.2 ERMF群落的季节性变化

杜鹃花毛根受到ERMF侵染不仅有水平分布和垂直分布的变化,还呈现出季节性的变化（Chambers et al. 2008 ）,如在澳大利亚西南季节性变化明显的地中海式气候区,在较冷湿条件下,毛根和内生菌的活力优势最为明显（Hutton et al. 1994 ）;Cairney & Ashford（2002）研究了毛根的季节变化发现,毛根长度在夏季土壤变干时都快速下降到很低的水平,在秋季再次出现,在湿润的冬季变为菌根,到了春季每株植物的侵染率都达到最高的水平,说明毛根及其菌根的形成和侵染率的高低与温度和湿度等气候因子存在着一定的相关性。原Epacridaceae的Woollsia pungens中菌根侵染水平差异与水分无关,但是却与温度呈现负相关。而Lorberauet al.（2017） 在人工控制条件下发现,温度升高对Cassiope tetragona宿主根部真菌群落的影响却较微弱。Read（1996）指出不同水分区域导致毛根发育的特点不同,然而更广泛的调查并没有发现任何侵染强度和纬度、海拔、土壤或气候因子之间的关系,北半球研究的大多数宿主种类存在着全年侵染的情况（Read & Kerley 1995）。Calluna vulgaris根中菌根侵染的季节变化非常显著,而且菌根侵染的空间变化都相当大（Johansson 2000）。研究指出,除非是在非常干旱的条件下,否则ERM可以全年起作用。

从对ERMF季节性变化的研究可以看出,高温和干旱可能会影响到具有ERM宿主的毛根发育,进而会对ERMF群落的组成和结构产生一定的影响。在欧洲和澳洲的研究认为湿、冷对毛根的发育和ERMF的侵染有促进作用。

6.3 ERM植物与其他物种的竞争关系随着资源比率的变化而变化

欧石南荒地的土壤通常养分水平低,并伴有pH值低、金属阳离子高、排水不良或持水很差、极端温度频繁出现等多种组合（Cairney & Meharg 2003）。以前由杜鹃花科的Calluna vulgaris和Erica tetralix矮灌木占优势的荷兰欧石南荒地,在近几十年中已经快速地被多年生草本植物Deschampsia flexuosa和Molinia caerulea所取代（van der Eerden et al. 1991 ;Aerts 1993;Bobbink & Heil 1993;Berendse 1994）。高水平的氮沉积极大地促进了土壤有机质的积累和从杜鹃花科植物向草本植物占优势的群落方向演替（Berendse & Aerts 1984;Berendse & Elberse 1990;Hofland -Zijlstra & Berendse 2010）。类似的情况也出现在英国的部分地区（Barker et al. 2004 ）。虽然氮沉积会导致欧石南荒地植被的演替,但是低水平的磷供给可能会阻止或减缓这一过程（Nielsena et al. 2009 ）。与荷兰相比,中等水平的氮沉积在丹麦同样类型的欧石南荒地中并没有引起Calluna占优势的植被发生变化（Kristensen & Henriksen 1998）。说明可能是资源比率的变化引起不同菌根类型植物竞争关系发生变化导致。从菌根功能的研究可以看出,具有ERM的杜鹃花科植物在氮贫瘠土壤占优势,但是无机氮输入可能更有利于那些AM或无菌根的宿主。欧石南荒地的植被受到氮沉积影响发生的演替是否会影响到地下菌根真菌群落的变化还需要进一步研究,但是能在杜鹃花科根部形成ERM的真菌也往往具有可以与其他植物物种形成其他菌根类型的特性（Ishida & Nordin 2010）,再加上构成ERM的真菌具有一定的腐生生活能力,因此,地上部分植被的演替并不一定会在短时间内影响到地下部分真菌群落结构的变化。

7 ERM研究的展望

尽管有关于ERM的研究取得了一定的进展,但是在理论基础和实践体系的建立方面还有很多有待于进一步探索的问题。

（1）杜鹃花科植物种类及资源十分丰富,据《中国植物志》记载,本科有约103属,3 350种（杨汉碧等 2006）,将原Empetraceae和Epacridaceae归属于杜鹃花科（Smith & Read 2008）,种类则更多,这些植物广泛分布于全球不同气候区的生态系统中,生境类型多样。各地区研究ERM起步时间和水平的差异较大,欧洲、北美和澳洲的研究成果居多,而亚洲的研究成果相对较少。今后对于不同生长环境和不同种类杜鹃花的ERMF资源的调查、分类和鉴定还有很多工作要做。

He et al.（2010） 概括了过去60年我国在菌根研究领域中的成就,总结了AM、ECM和OM的研究成果,而ERM的研究成果还很少。中国是杜鹃花的起源和分布中心,约有15属,757种（杨汉碧等 2006）,目前Zhanget al.（2009） 对Rhododendron fortunei,郑钰等（2010）对Rhododendron argyrophyllum和R.floribundum,Tian et al.（2011） 和Sun et al.（2012） 对Rhododendron decorum,Zhanget al.（2017,2019）对Rhododendron ovatum和R. simsii等的内生菌多样性进行了研究,还有很多ERM宿主及其共生真菌有待研究。特有的生态环境和特有种是孕育ERM的重要基础和前提,中国是世界ERM研究不可或缺的组成部分,缩短与欧美研究差距将是一项长期而艰巨的工作。

（2）杜鹃花科宿主和内生真菌的种类之间是否存在共生特异性?目前存在两种观点,从Rhododendron的不同栽培品种和Vaccinium myrtillus都分离出来Oidiodendron sp.,且从Vaccinium宿主中分离的比从Rhododendron分离的种类更多（Jansa & Vosatka 2000）,Zhanget al.（2016,2019）用高通量测序也发现Rhododendron宿主其根部真菌多样性比Vaccinium少,共生真菌可能存在一定的宿主偏好,但是,从Cassiope tetragona、Empetrum nigrum和Vaccinium vitis-idaea等3种植物分离的根部真菌,侵染实验室培养的Vaccinium uliginosum时却没有发现宿主特异性的证据（Walker et al. 2011 ）。更多的研究和实践可能在不久的将来能客观地回答这一问题,特别是我国特有杜鹃花种类仅生长在特定的区域内,对其宿主和真菌特异性的研究,可能是未来成功引种的重要基础。

（3）在有杜鹃花科植物的自然生态系统演替过程中,杜鹃花科宿主和共生真菌是否能够协同进化和迁移?从厄瓜多尔、巴拿马和北美的Vaccinioideae的58个宿主个体中Sebacinales的研究认为,两个新热带区和北美的温带区Vaccinioideae-Sebacinales群落的植物-真菌发生了共同迁移（Setaro & Kron 2011）。在我国29个植被类型中有4个其关键种属于杜鹃花科（Enright & Cao 2010）,这些宿主不断受到自然和人为的干扰,它们的地上植物-地下真菌群落之间有着怎样的联系,植被-真菌群落的演替未来向什么方向发展也将是生态学家关注的问题。

（4）在能够形成ERM的真菌种类中有哪些对杜鹃花科的生长和适应起着促进作用?这些有益的内生菌是否能够被成功地分离、培养、纯化和成功回接?人工培养和释放的内生菌株对目标宿主的侵染效果如何?能否形成ERM结构?共存的ERM与DSE是有益的相互补充还是发生拮抗作用?Vohník（2020）全面总结了ERM共生体的实验研究方法,可以在此基础上进一步对共生真菌进行分离、培养和纯化,对未知的ERMF种类进行鉴定,弄清共生真菌群落的物种组成和结构特点,为进一步了解其功能作用奠定基础。

（5）在能够分离、培养、鉴定和纯化的基础上,对于不同菌种在营养吸收、忍耐瘠薄、对各类污染的抗性及机理的研究,合适菌剂的研发,利用菌根技术引种优良的高山杜鹃,研究其在新生境中的成活、生长、开花等生物学特性与菌根之间的关系,都将是未来ERM研究很重要的发展方向。

（6）自然生态系统是一个开放的动态系统,研究根系ERMF群落与土壤中存在的其他生物群落类型之间的关系,ERMF对土壤环境因子如氮、磷、硫等元素的加入、对全球CO2和温度升高、对干旱和洪涝的响应,以及ERMF群落将在不同气候、土壤、植被区域存在着怎样的动态规律等,都需要进行大量的调查和分析。

随着国内外学者对ERM关注度的提高,相信未来有关杜鹃花及其菌根的研究会逐步深入,必将进一步推动杜鹃花资源的保护和利用,为杜鹃花在自然生态系统、城市园林绿化以及果树栽培等方面发挥更大作用奠定坚实的基础。

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Climate change may alter mycorrhizal communities, which impact ecosystem characteristics such as carbon sequestration processes. These impacts occur at a greater magnitude in Arctic ecosystems, where the climate is warming faster than in lower latitudes. Cassiope tetragona (L.) D. Don is an Arctic plant species in the Ericaceae family with a circumpolar range. C. tetragona has been reported to form ericoid mycorrhizal (ErM) as well as ectomycorrhizal (ECM) symbioses. In this study, the fungal taxa present within roots of C. tetragona plants collected from Svalbard were investigated using DNA metabarcoding. In light of ongoing climate change in the Arctic, the effects of artificial warming by open-top chambers (OTCs) on the fungal root community of C. tetragona were evaluated. We detected only a weak effect of warming by OTCs on the root-associated fungal communities that was masked by the spatial variation between sampling sites. The root fungal community of C. tetragona was dominated by fungal groups in the Basidiomycota traditionally classified as either saprotrophic or ECM symbionts, including the orders Sebacinales and Agaricales and the genera Clavaria, Cortinarius, and Mycena. Only a minor proportion of the operational taxonomic units (OTUs) could be annotated as ErM-forming fungi. This indicates that C. tetragona may be forming mycorrhizal symbioses with typically ECM-forming fungi, although no characteristic ECM root tips were observed. Previous studies have indicated that some saprophytic fungi may also be involved in biotrophic associations, but whether the saprotrophic fungi in the roots of C. tetragona are involved in biotrophic associations remains unclear. The need for more experimental and microscopy-based studies to reveal the nature of the fungal associations in C. tetragona roots is emphasized.

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The prominent ericoid mycorrhizal fungus, Pezoloma ericae, has not been found in Australia to date. In the present study, internal transcribed spacer (ITS) data from the Biomes of Australia Soil Environments (BASE) was searched for evidence of P. ericae and other known ericoid mycorrhizal and root-associated taxa. ITS sequences with high identity to P. ericae, Meliniomyces bicolor, Meliniomyces variabilis, Cairneyella sp. 2, Cadophora finlandica and Woollsia mycorrhizal fungus VI were identified and their distribution in Australia visualised. This is the first evidence that P. ericae, M. bicolor and M. variabilis very likely occur on the Australian continent and provides a set of locations from which to seek isolates for further characterisation. The presence of P. ericae in South America, South Africa, and now Australia suggests a broad and ancient Gondwanan distribution for this well-studied species.

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