Patterns of genetic variation in Phialocephala fortinii across a broad latitudinal transect in Canada

doi:10.1017/S0953756204000528

Mycological Research

Volume 108, Issue 8, August 2004, Pages 955-964

https://doi.org/10.1017/S0953756204000528 Get rights and content

Dark septate root endophytes (DSE) are an artificial assemblage of fungi that have darkly pigmented, septate hyphae and that are frequent or distinctive intracellular associates of roots of apparently healthy plants. Based on isolates obtained from the roots of Salix spp., the distribution of a common DSE fungus, Phialocephala fortinii was examined along a latitudinal transect in Canada running from the high arctic to the 49° N parallel. Non-sporulating isolates were provisionally identified as P. fortinii through analysis of DNA sequence data of the ITS2 region of rDNA. P. fortinii was isolated frequently from boreal and arctic habitats, but rarely from grassland habitats. Patterns of genetic variation were examined through analysis of amplified fragment length polymorphisms (AFLP). All AFLP profiles were unique with the majority of genetic variation occurring among individuals within the collecting sites at each latitude. Neighbour-joining analysis of genetic distances yielded eight well-supported clusters, three of which included individuals from more than one latitude. Some linkage disequilibrium, possibly due to partial clonality, was detected.

References (62)

H.D. Addy et al.
Distribution and molecular characterization of the root endophyte Phialocephala fortinii along an environmental gradient in the boreal forest of Alberta
Mycological Research
(2000)
G.R. Balali et al.
DNA fingerprinting probe specific to isolates of Rhizoctonia solani AG-3
Mycological Research
(1996)
C.R. Grünig et al.
Characterization of dark septate endophytic fungi (DSE) using inter-simple-sequence-repeat-anchored polymerase chain reaction (ISSR-PCR) amplification
Mycological Research
(2001)
C.R. Grünig et al.
Spatial distribution of dark septate endophytes in a confined forest plot
Mycological Research
(2002)
S. Hambleton et al.
Hymenoscyphus ericae: a new record from western Canada
Mycological Research
(1999)
K.F. LoBuglio et al.
Phylogenetic origins of the asexual mycorrhizal symbiont Cenococcum geophilum Fr. and other mycorrhizal fungi among the ascomycetes
Molecular Phylogenetics and Evolution
(1996)
J. Matthew et al.
DNA probe specific to Rhizoctonia solani anastomosis group 8
Mycological Research
(1995)
T. White et al.
Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics
P. Agapow et al.
AFLP™

W.D. Billings

Arctic and alpine vegetation: plant adaptations to cold summer climates

A.H.D. Brown et al.

Multilocus structure of natural populations of Hordeum spontaneum

Genetics

(1980)

A. Burt et al.

Molecular markers reveal cryptic sex in the human pathogen Coccidioides immitis

Proceedings of the National Academy of Sciences, USA

(1996)

Carleson, T. A. (2002) Molecular diversity of root endophytes in an alpine Bistorta vivipara — Kobresia myosuroides...

R.S. Currah et al.

Vegetative and reproductive morphology of Phialocephala fortinii (Hyphomycetes, Mycelium radicis atrovirens) in culture

Transactions of the Mycological Society of Japan

(1993)

R.S. Currah et al.

Morphology and ecology of Phialocephala fortinii in the roots of Rhododendron brachycarpum

Canadian Journal of Botany

(1993)

J.J. Doyle et al.

A rapid DNA isolation procedure for small quantities of fresh leaf tissue

Phytochemical Bulletin

(1987)

L. Excoffier et al.

Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data

Genetics

(1992)

J. Felsenstein

Confidence limits on phylogenies: an approach using the bootstrap

Evolution

(1985)

A.F. Fernando et al.

A comparative study of the effects of the root endophytes Leptodontidium orchidicola and Phialocephala fortinii (Fungi Imperfecti) on the growth of some subalpine plants in culture

Canadian Journal of Botany

(1996)

C.F. Friese et al.

The interaction of harvester ants and vesicular-arbuscular mycorrhizal fungi in a patchy semi-arid environment: the effects of mound structure on fungal dispersion and establishment

Functional Ecology

(1993)

D.S. Gernandt et al.

Phylogenetics of Helotiales and Rhytismatales based on partial small subunit nuclear ribosomal DNA sequences

Mycologia

(2001)

S.W. Graham et al.

Microstructural changes in noncoding chloroplast DNA: interpretation, evolution, and utility of indels and inversions in basal angiosperm phylogenetic inference

International Journal of Plant Science

(2000)

C.R. Grünig et al.

Genetic variability among strains of Phialocephala fortinii and phylogenetic analysis of the genus Phialocephala based on rDNA ITS sequence analysis

Canadian Journal of Botany

(2002)

Hambleton, S. (1998) Mycorrhizas of the Ericaceae: diversity and systematics of the mycobionts. PhD thesis, University...

S. Hambleton et al.

Fungal endophytes from the roots of alpine and boreal Ericaceae

Canadian Journal of Botany

(1997)

T.C. Harrington et al.

Molecular identification of fungi associated with vascular discoloration of soy bean in the North Central United States

Plant Disease

(2000)

K. Haselwandter et al.

The significance of root-fungus association in two Carex species of high-alpine plant communities

Oecologia

(1982)

S.H. Jabaji-Hare et al.

Investigation of genetic relatedness among anastomosis groups of Rhizoctonia solani using cloned DNA probes

Canadian Journal of Plant Pathology

(1990)

A. Jumpponen

Spatial distribution of discrete RAPD phenotypes of a root endophytic fungus, Phialocephala fortinii, at a primary successional site on a glacier forefront

New Phytologist

(1999)

A. Jumpponen et al.

Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi

New Phytologist

(1998)

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Investigations on host affiliations, seasonal variation and physiological response to drought tolerance of dark septate endophytes (DSE) in extremely arid desert environments can help explain the adaptive mechanisms of these endophytes in desert ecosystems. The colonization and species diversity of DSE and the soil factors in the rhizospheres of five desert shrubs were therefore determined in Anxi extremely arid environment in Northwest China in July, September and December 2020. Subsequently, six DSE strains were selected to test the growth and metabolic response of DSE strains to drought stress in vitro. The sampled plants and seasons significantly influenced the morphology, colonization and species diversity of DSE. Of the 15 DSE species isolated in the roots of these plants, Triangularia allahabadensis was reported in desert ecosystems for the first time. DSE colonization was predominately affected by season and soil factors, while species composition was more corresponded to plant species. The composition of metabolites of DSE strains varied significantly due to levels of drought stress and DSE identity, which indirectly reflected the difference of their traits to respond to drought stress. This study confirmed the establishment of relationship between DSE and roots of xerophytic plants, and proved the drought tolerance of DSE in vitro, providing insight into the application of DSE to assist desert plants to resist drought.
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The best-known root symbionts of forest trees are mycorrhizal fungi. However, dark septate endophytes (DSE) are ubiquitous fungi found systemically in the same roots. Indeed, DSE have been noted to be as abundant in roots as mycorrhiza. Nevertheless, their function in host-fungi continuum is still a mystery. Most of the available studies have focused on nonwoody plants. Since DSE may increase the fitness of their host tree by nutrient uptake, reduce root infections by pathogens, and decrease the detrimental effects of stressful environments (e.g., drought), DSE truly are the key players in forest ecosystems. However, as the studies are still very limited, the DSE-tree interactions in diverse conditions cannot be well explained. In this chapter I summarize the current knowledge on DSE in plant roots, specially emphasizing DSE in forest tree roots, and their affects to host in various conditions.
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Endophytic fungi seem to be ubiquitous as they have been isolated from every plant species examined to date. However, important differences in their diversity and richness were reported among latitudes, ecosystems, sites, hosts, and tissue types (Suryanarayanan et al., 2002; Piercey et al., 2004; Arnold, 2007; Verma et al., 2007; Rodriguez et al., 2009). For example, Arnold and Lutzoni (2007) found that endophytes isolated from tropical forests were more abundant than in temperate forests and that assemblages were composed of a large number of rare species, suggesting that tropical sites are hyperdiverse.
We collected various plant species along an altitudinal gradient ranging from 400 to 2900 m in tropical wet forests of Costa Rica, isolated the associated endophytic fungi, and performed bioinformatic analyses to determine whether changes in altitude are related to changes in their richness and community structure. We showed that the richness of endophytic fungi varied along the altitudinal gradient, being higher in the lowest stratum and decreasing as elevation increases. Each stratum presented a particular composition and diversity of endophytes, although the whole population was characterized by the presence of a few dominant and apparently ubiquitous species, coexisting with a number of less abundant species that presented a more limited host range. These results have important implications for better understanding the role of altitude on the distribution and composition of endophytic fungal populations in tropical forests, but also for maximizing the number and diversity of endophytic isolates in bioprospecting campaigns.
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Low supply of the nutrients nitrogen (N) and phosphorus (P) limit plant growth and spreading, and increase the plant-microbial nutrient competition in subarctic and arctic regions. We investigated the mycorrhizal community structure of a polar shrub willow (Salix polaris) and the microbial turnover in its rhizosphere to explore the adaptation of a mycorrhizal plant in the subarctic tundra. The ectomycorrhizal colonisation ranged from 35 to 64% of the fine root tips and decreased with an increasing soil C/N ratio. In total, 16 ectomycorrhizal morphotypes were found under S. polaris (eight to 13 morphotypes per site, five morphotypes at all four sites). Cenococcum sp. was the most common EM fungus (32% of the ectomycorrhizal fine roots). The abundance of Cenococcum sp. increased with an increasing organic matter content and N/P ratio in the soil. Arbuscular mycorrhizal colonisation of S. polaris was absent or less than 1% of the fine root length. Microbial biomass P accounted for 21–75% of the organic soil P and 6–49% of the total soil P. Microbial biomass P, alkaline and acid phosphatase activities in the rhizosphere increased with increasing soil N concentration. We conclude that a higher N supply decreases the diversity in the mycorrhizal community on polar willows and increases the role of P turnover from the soil microbial biomass for the nutrient supply.
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Patterns of genetic variation in Phialocephala fortinii across a broad latitudinal transect in Canada

Mycological Research

Mycological Research

Mycological Research

Mycological Research

Mycological Research

Molecular Phylogenetics and Evolution

Mycological Research

AFLP™

Arctic and alpine vegetation: plant adaptations to cold summer climates

Multilocus structure of natural populations of Hordeum spontaneum

Genetics

Molecular markers reveal cryptic sex in the human pathogen Coccidioides immitis

Proceedings of the National Academy of Sciences, USA

Vegetative and reproductive morphology of Phialocephala fortinii (Hyphomycetes, Mycelium radicis atrovirens) in culture

Transactions of the Mycological Society of Japan

Morphology and ecology of Phialocephala fortinii in the roots of Rhododendron brachycarpum

Canadian Journal of Botany

A rapid DNA isolation procedure for small quantities of fresh leaf tissue

Phytochemical Bulletin

Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data

Genetics

Confidence limits on phylogenies: an approach using the bootstrap

Evolution

A comparative study of the effects of the root endophytes Leptodontidium orchidicola and Phialocephala fortinii (Fungi Imperfecti) on the growth of some subalpine plants in culture

Canadian Journal of Botany

The interaction of harvester ants and vesicular-arbuscular mycorrhizal fungi in a patchy semi-arid environment: the effects of mound structure on fungal dispersion and establishment

Functional Ecology

Phylogenetics of Helotiales and Rhytismatales based on partial small subunit nuclear ribosomal DNA sequences

Mycologia

Microstructural changes in noncoding chloroplast DNA: interpretation, evolution, and utility of indels and inversions in basal angiosperm phylogenetic inference

International Journal of Plant Science

Genetic variability among strains of Phialocephala fortinii and phylogenetic analysis of the genus Phialocephala based on rDNA ITS sequence analysis

Canadian Journal of Botany

Fungal endophytes from the roots of alpine and boreal Ericaceae

Canadian Journal of Botany

Molecular identification of fungi associated with vascular discoloration of soy bean in the North Central United States

Plant Disease

The significance of root-fungus association in two Carex species of high-alpine plant communities

Oecologia

Investigation of genetic relatedness among anastomosis groups of Rhizoctonia solani using cloned DNA probes

Canadian Journal of Plant Pathology

Spatial distribution of discrete RAPD phenotypes of a root endophytic fungus, Phialocephala fortinii, at a primary successional site on a glacier forefront

New Phytologist

Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi

New Phytologist