Ectendomycorrhizal Associations – Characteristics and Functions
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Mycorrhiza (2001) 11:167–177 DOI 10.1007/s005720100110 REVIEW Trevor E. J-C. Yu · Keith N. Egger R. Larry Peterson Ectendomycorrhizal associations – characteristics and functions Accepted: 12 May 2001 / Published online: 4 August 2001 © Springer-Verlag 2001 Abstract Mycorrhizal symbioses are widespread mutu- Introduction alistic associations of many plant hosts found in many habitats. One type of putative mycorrhizal association, Fungi are a major biotic component of the soil and thus ectendomycorrhiza, is confined to Pinus and Larix spp. plant roots interact with various fungus species through- and is common in conifer nurseries and in disturbed hab- out their development. Some interactions are deleterious itats. This association is characterized by the unique and others beneficial. Many fungus species form combination of a fungal mantle, Hartig net, and intracel- mutualistic symbioses, mycorrhizas, with the majority of lular hyphae, the latter forming soon after Hartig net de- plant species (Smith and Read 1997) and develop vari- velopment. Many reports of the occurrence of ectendo- ous categories of mycorrhizas based on the identity of mycorrhizas from field-collected specimens are likely er- the fungal partner and the structural modifications of the roneous and instead may represent senescent ectomycor- symbionts during the formation of the association rhizas. The fungus species involved in the formation of (Peterson and Farquhar 1994). Most research has fo- ectendomycorrhizas were initially called E-strain fungi cused on two categories of mycorrhizas, arbuscular my- and their identification was based on characteristics of corrhizas (AM) and ectomycorrhizas (ECM), because hyphae and chlamydospores. With the discovery of these are very widespread and are associated with many teleomorphs for some of these fungi, they were found to commercially important plant species (Smith and Read be ascomycetes. More recently, molecular methods have 1997). One category of mycorrhizas, first called “ecten- been used to clarify their systematics and phylogeny and dotrophic mycorrhizas” by Melin (1923) and now usual- it is apparent that most of the isolates belong to two spe- ly referred to as ectendomycorrhizas (Egger and Fortin cies, Wilcoxina mikolae and Wilcoxina rehmii. Two spe- 1988), is of restricted occurrence and has received little cies of dematiaceous fungi and a member of the Peziz- attention. The definition of an ectendomycorrhiza in- ales, Sphaerosporella brunnea, also have been reported cludes the fungal taxa and host species involved in the to form ectendomycorrhizas. These fungi can form ec- symbiosis and the resulting structural features of the as- tendomycorrhizas with their hosts over a broad pH range sociation. The fungal taxa usually involved are two spe- and may utilize many substrates as a carbon source. Ec- cies of Wilcoxina (W. mikolae, W. rehmii), Sphaerospor- tendomycorrhizas may be important in the revegetation ella brunnea and, to a lesser extent, Phialophora finlan- of disturbed sites and in the establishment of conifer dia and Chloridium paucisporum. The hosts are primari- seedlings in post-fire situations. ly Pinus and Larix species. Structurally, ectendomycor- rhizas are characterized by a thin mantle (sometimes ab- Keywords Chlamydospore · E-strain · Pinaceae · sent), Hartig net, and various degrees of intracellular hy- Sphaerosporella · Wilcoxina phal penetration into epidermal and cortical cells. These anatomical features led Egger and Fortin (1988) to sug- gest that ectendomycorrhizas should be considered a T.E.J-C. Yu · R.L. Peterson (✉) variant of ECM. Department of Botany, University of Guelph, Guelph, Ontario, The early literature on ectendomycorrhizas was re- N1G 2W1 Canada e-mail: [email protected] viewed by Mikola (1965) and Laiho (1965). More re- Fax: +1-519-7671991 cently, Mikola (1988) reviewed some aspects of the fun- gi involved, the distribution and ecology, as well as the K.N. Egger College of Science and Management, confusion in terminology in early papers on mycorrhizas. University of Northern British Columbia, Prince George, He suggested that the term “pseudomycorrhiza” be British Columbia, V2N 4Z9 Canada dropped because it is not meaningful from a functional 168 point of view and that the term ectendomycorrhiza be re- Since these studies, additional reports of ectendomycor- stricted to those associations in which intracellular hy- rhizas in Pinus roots collected from the field, or from phal penetration occurs almost simultaneously with Hartig seedlings grown in soil collected from forest sites, net formation. Although this restriction on the use of the have been published (Table 1). Several of these (Danielson term ectendomycorrhiza is important in distinguishing 1982; Ursic and Peterson 1997; Ursic et al. 1997; these associations from senescent ECMs, it remains to be Massicotte et al. 1999) identified the fungus involved as determined whether there is nutrient exchange between E-strain, while others (v. Hofsten 1969; Wilcox 1971; Scan- intracellular hyphae and root cells, typical of a biotro- nerini 1972; Pachlewski et al. 1991–1992) did not mention phic association. If not, intracellular hyphae may repres- the fungus involved. McGee et al. (1999) reported structural ent a “latent pathogen” stage becoming active in nutrient features similar to those of ectendomycorrhizas in roots of absorption only after the onset of root senescence. Al- one adult specimen of the recently discovered Wollemi pine though arbutoid and monotropoid mycorrhizal associa- (Wollemia nobilis, Araucariaceae) in Australia. Because the tions have some features in common with ectendomycor- fungus involved was not determined, the occurrence was rhizas, and have been referred to as ectendomycorrhizas very restricted and most members of the Araucariaceae by Zak (1974, 1976), they are not considered here be- have AM associations, this finding is difficult to evaluate. cause the fungus species involved are those typical of The reports of ectendomycorrhizas in field collections of ectomycorrhizas (Zak 1974, 1976). Intracellular hyphae the angiosperm species Uapaca kirkiana (Högberg 1982) are confined to the epidermis and, in the case of mono- and the dipterocarp species Shorea parvifolia (Louis 1988) tropoid mycorrhizas, very specialized fungal structures are based solely on the presence of intracellular hyphae; (“pegs”) are formed within epidermal cells; these be- these may be hyphae of senescing ectomycorrhizas. come surrounded by an elaborate host-derived cell wall Several cases of ectendomycorrhizas synthesized under (Smith and Read 1997). laboratory conditions have been reported (Table 1) since The objectives of this review are to bring together and the reviews of Mikola (1965) and Laiho (1965). The critique information related to the occurrence, structure, strength of these reports in most cases lies in the use of and functions of ectendomycorrhizas, to discuss the cur- known fungus species and the determination of anatomi- rent knowledge of the taxonomy of the fungi involved in cal features of mycorrhizal roots. In the paper by Wilcox the association, and to propose areas of research required et al. (1974), fungus isolates (identified as BDG-58 and to elucidate the role(s) of these mycorrhizas in natural BDD-22) obtained from Pinus resinosa roots were used. and other ecosystems. BDD-22 was identified as Chloridium paucisporum Wang & Wilcox and the anamorph of BDG-58 was later identi- fied as Complexipes sp. (LoBuglio and Wilcox 1988), of Occurrence of ectendomycorrhizas which the teleomorph is Wilcoxina (Yang and Korf 1985). Ectendomycorrhizas have been synthesized with Pinus Laiho (1965) summarized the gymnosperm and angio- resinosa (red pine) using various identified fungus spe- sperm tree species reported to form ectendomycorrhizas. cies, including Wilcoxina mikolae var. mikolae (Yang and Many of the early reports, however, are questionable be- Wilcox 1984, as Tricharina mikolae; Piché et al. 1986; see cause field-collected roots with any type of intracellular our Fig. 1), Phialophora finlandia (Wang and Wilcox hypha development were often categorized as ectendo- 1985; Wilcox and Wang 1987a, b), and Chloridium pauci- trophic. It was not until the pioneering work of Mikola sporum (Wang and Wilcox 1985; Wilcox and Wang (1965) and Laiho (1965) that the unique characteristics 1987b). Ectendomycorrhizas of Pinus contorta inoculated of the fungi involved in this association were recognized with Sphaerosporella brunnea (Egger and Paden 1986; and the term E-strain applied to the isolates obtained. Iwanyzki 1992) and Pinus banksiana inoculated with two Mikola (1965) grouped all isolates showing similar gross varieties of Wilcoxina mikolae and Wilcoxina rehmii morphological characteristics of mycelium in culture in- (Scales and Peterson 1991a) have been reported (Table 1). to a single species of E-strain fungus. The dimorphic S. brunnea colonized short roots of Pinus contorta and mycelium consisted of pigmented, coarse aerial hyphae formed a thin mantle (Figs. 2, 3). of variable thickness (straight and septate), and hyaline A group of dematiaceous soil fungi also has been de- submerged hyphae, septate (winding and branching). scribed in association with roots of many plant species Chlamydospore-like swellings often occurred. from a variety of habitats (Jumponnen and Trappe 1998). Ectendomycorrhizas described by Mikola (1965) and Melin (1922) first described these fungi from the roots of Laiho (1965) from the field