Cenococcum geophilum

Last updated

Cenococcum geophilum
Cenococcum geophilum.jpg
Cenococcum geophilum ectomycorrhiza
Scientific classification
Kingdom:
Fungi
Division:
Ascomycota
Class:
Dothideomycetes
Order:
Mytilinidiales
Family:
Gloniaceae
Genus:
Cenococcum
Species:
C. geophilum
Binomial name
Cenococcum geophilum
Fr. (1829)

Cenococcum geophilum Fr., synonym Cenococcum graniforme (Sow.) Ferd. and Winge, is an Ascomycete fungal species and is the only member in the genus Cenococcum. It is one of the most common ectomycorrhizal fungal species encountered in forest ecosystems. The geographic distribution of the species is notably cosmopolitan; it is found in ecosystems with a wide range of environmental conditions, and in many cases in high relative frequency. [1] Because of its wide distribution and abundance in forest soils, it is one of the most well-studied ectomycorrhizal fungal species. While the species has long been known to be sterile and not produce asexual or sexual spores, cryptic sexual stages may exist. [2] The hyphae produced by C. geophilum are characterized by their thick (1.5-8 um), straight and jet black appearance with little branching. They usually form monopodial (unbranched) ectomycorrhizas. The mantles of C. geophilum ectomycorrhizas are usually thick with few to many emanating hyphae.

Contents

Taxonomy

Originally described in 1800 from its sclerotia by James Sowerby, the species was named Lycoperdon graniforme Sow. Later, Elias Fries introduced the genus Cenococcum and the sole species was called Cenococcum geophilum Fr. These names were later combined to form Cenococcum graniforme (Sow) Ferd. and Winge in the monographic study of the species by Ferdinandsen and Winge in 1925. [3] Hatch identified hyphae that formed ectomycorrhizas with “jet-black” mantles calling it Mycelium radicus-nigrostrigosum Hatch. Finally, Linhell linked the fungi forming the ectomycorrhizas to the fungus producing the sclerotia earlier described. The officially accepted name for the species is Cenococcum geophilum Fr. [4] Molecular analyses have revealed that C. geophilum is not closely related to other Ascomycete ectomycorrhizal fungi (mostly in the Pezizales) and is actually a member of the Dothideomycetes. [5] Cenococcum geophilum is the only known ectomycorrhizal member of the Dothideomycetes. Spatafora et al. (2012) placed C. geophilum in the Gloniaceae as a close relative to members of the Genus Glonium. [2]

Ecology

Abundance and distribution

It is not unusual to find Cenococcum geophilum mycelium and ectomycorrhizas in high relative frequency in soil where ectomycorrhizal tree hosts are present. Unlike many ectomycorrhizal fungi, Cenococcum geophilum readily colonizes the fine roots of most ectomycorrhizal hosts. It may be found in all forest successional stages. [6] Unlike most ectomycorrhizal fungal species, Cenococcum geophilum appears to have no distinct vertical distribution in the organic horizons of soil [7] though it appears to prefer organic horizons to mineral soil. [8] [9] Cenococcum geophilum also appears to have an even horizontal spatial distribution pattern at the microscale [10] and site level. [11] This unusual distributional pattern may be the result of wide niche breadth of Cenococcum geophilum and/or genetic variation within the species. [6] A factor that may contribute to this wide niche breadth is the species ability to tolerate a wide range of stressors. Cenococcum geophilum isolates have been shown to tolerate freezing, [12] salinity, [13] and heavy metal [14] stressors, but is probably best known for its ability to tolerate water stress. [15] [16] [17] Hasselquist et al. (2005) found evidence that suggests that increased colonization of fine roots of Douglas fir seedlings by C. geophilum may alleviate water stress of the host plant during periods of low water availability. [18] Melanin biosynthesis, which is quite high in C. geophilum, gives its hyphae the “jet-black” appearance, and has been linked with stress tolerance in fungi. [19] It may thus be a key functional trait reducing water stress in C. geophilum. [20] Other potential traits that C. geophilum may employ for water stress tolerance include the production and accumulation of compatible osmolytes [21] [22] and the production of heat shock proteins. [23] Nitrogen fertilization appears to have negative effects on the abundance of C. geophilum, [24] which may be the result of host trees allocating less carbon to ectomycorrhizal symbiosis when nitrogen in the soil becomes non-limiting to the plant growth.

Enzyme production and nutrient acquisition

Along with other species of ectomycorrhizal fungi, C. geophilum produces extracellular enzymes that are able to hydrolyze substrates found in the soil to access and acquire nutrients important to itself and its host plant. The ectomycorrhizas of C. geophilum have been shown to hydrolyze 14C labeled substrate common in plant litters, including hemicellulose and cellulose. [25] Cenococcum geophilum ectomycorrhizas have also been shown to produce high levels of laccase, glucoronidase, and xylodase and phosphatase enzymes. [26]

Carbon sequestration

In the light of climate change there is growing interest in understanding carbon sequestration in mycorrhizal fungal tissues. There is considerable evidence suggesting that C. geophilum mycelium, ectomycorrhizas and sclerotia are highly resistant to decay and have potential to sequester a great deal of carbon in their tissues. Fernandez et al. (2013) found that C. geophilum ectomycorrhizas persisted considerably longer in the soil than those of other ectomycorrhizal fungi. [27] This resistance to decay is likely related to the heavy melanization of the cell wall found in C. geophilum hyphae which cannot be degraded with hydrolyzing enzymes and requires the implementation of oxidative enzymes, much like lignin in plant litters. [28] Cenococcum geophilum produces resting structures called sclerotia. These structures have been found to remain viable in the soil for years. Remarkably, these structures are known to persist relatively undecomposed in the soil for thousands of years. [29]

Genetic diversity and cryptic speciation

Once regarded as a single species, observed variation in morphology, growth rates and response to growth conditions among C. geophilum isolates led researchers to speculate on possibility of cryptic speciation. Advances in molecular techniques have allowed researchers to test this hypothesis by examining the genetic variation in C. geophilum strains at various spatial scales. LoBuglio et al. 1991 examined the degree of variation in the ribosomal DNA across 71 isolates of C. geophilum of varying geographic origin (distinct to similar) and found a great deal of genetic variation across the isolates. [30] A high degree of genetic variation of C. geophilum has been repeatedly observed at the stand level. [31] [32] Douhan & Rizzo (2005) found phylogenetically distinct lineages of C. geophilum at the scale of the soil sample supporting the hypothesis that there is cryptic sympatric speciation occurring in C. geophilum. [33]

Related Research Articles

<span class="mw-page-title-main">Mycorrhiza</span> Fungus-plant symbiotic association

A mycorrhiza is a symbiotic association between a fungus and a plant. The term mycorrhiza refers to the role of the fungus in the plant's rhizosphere, its root system. Mycorrhizae play important roles in plant nutrition, soil biology, and soil chemistry.

<span class="mw-page-title-main">Russulaceae</span> Family of fungi in the order Russulales

The Russulaceae are a diverse family of fungi in the order Russulales, with roughly 1,900 known species and a worldwide distribution. They comprise the brittlegills and the milk-caps, well-known mushroom-forming fungi that include some edible species. These gilled mushrooms are characterised by the brittle flesh of their fruitbodies.

<span class="mw-page-title-main">Arbuscular mycorrhiza</span> Symbiotic penetrative association between a fungus and the roots of a vascular plant

An arbuscular mycorrhiza (AM) is a type of mycorrhiza in which the symbiont fungus penetrates the cortical cells of the roots of a vascular plant forming arbuscules. Arbuscular mycorrhiza is a type of endomycorrhiza along with ericoid mycorrhiza and orchid mycorrhiza .They are characterized by the formation of unique tree-like structures, the arbuscules. In addition, globular storage structures called vesicles are often encountered.

<span class="mw-page-title-main">Root hair</span> Part of plant root

Root hair, or absorbent hairs, are outgrowths of epidermal cells, specialized cells at the tip of a plant root. They are lateral extensions of a single cell and are only rarely branched. They are found in the region of maturation, of the root. Root hair cells improve plant water absorption by increasing root surface area to volume ratio which allows the root hair cell to take in more water. The large vacuole inside root hair cells makes this intake much more efficient. Root hairs are also important for nutrient uptake as they are main interface between plants and mycorrhizal fungi.

<i>Laccaria bicolor</i> Species of fungus

Laccaria bicolor is a small tan-colored mushroom with lilac gills. It is edible but not choice, and grows in mixed birch and pine woods. It is found in the temperate zones of the globe, in late summer and autumn. L. bicolor is an ectomycorrhizal fungus used as a soil inoculant in agriculture and horticulture.

<span class="mw-page-title-main">Ericoid mycorrhiza</span> Species of fungus

The ericoid mycorrhiza is a mutualistic relationship formed between members of the plant family Ericaceae and several lineages of mycorrhizal fungi. This symbiosis represents an important adaptation to acidic and nutrient poor soils that species in the Ericaceae typically inhabit, including boreal forests, bogs, and heathlands. Molecular clock estimates suggest that the symbiosis originated approximately 140 million years ago.

<i>Rhizopogon</i> Genus of fungi

Rhizopogon is a genus of ectomycorrhizal basidiomycetes in the family Rhizopogonaceae. Species form hypogeous sporocarps commonly referred to as "false truffles". The general morphological characters of Rhizopogon sporocarps are a simplex or duplex peridium surrounding a loculate gleba that lacks a columnella. Basidiospores are produced upon basidia that are borne within the fungal hymenium that coats the interior surface of gleba locules. The peridium is often adorned with thick mycelial cords, also known as rhizomorphs, that attach the sporocarp to the surrounding substrate. The scientific name Rhizopogon is Greek for 'root' (Rhiz-) 'beard' (-pogon) and this name was given in reference to the rhizomorphs found on sporocarps of many species.

<i>Suillus brevipes</i> Species of edible fungus in the family Suillaceae found throughout North America

Suillus brevipes is a species of fungus in the family Suillaceae. First described by American mycologists in the late 19th century, it is commonly known as the stubby-stalk or the short-stemmed slippery Jack. The fruit bodies (mushrooms) produced by the fungus are characterized by a chocolate to reddish-brown cap covered with a sticky layer of slime, and a short whitish stipe that has neither a partial veil nor prominent, colored glandular dots. The cap can reach a diameter of about 10 cm, while the stipe is up to 6 cm long and 2 cm thick. Like other bolete mushrooms, S. brevipes produces spores in a vertically arranged layer of spongy tubes with openings that form a layer of small yellowish pores on the underside of the cap.

<span class="mw-page-title-main">Hartig net</span> Network of inward-growing hyphae

The Hartig net is the network of inward-growing hyphae, that extends into the plant host root, penetrating between plant cells in the root epidermis and cortex in ectomycorrhizal symbiosis. This network is the internal component of fungal morphology in ectomycorrhizal symbiotic structures formed with host plant roots, in addition to a hyphal mantle or sheath on the root surface, and extramatrical mycelium extending from the mantle into the surrounding soil. The Hartig net is the site of mutualistic resource exchange between the fungus and the host plant. Essential nutrients for plant growth are acquired from the soil by exploration and foraging of the extramatrical mycelium, then transported through the hyphal network across the mantle and into the Hartig net, where they are released by the fungi into the root apoplastic space for uptake by the plant. The hyphae in the Hartig net acquire sugars from the plant root, which are transported to the external mycelium to provide a carbon source to sustain fungal growth.

<i>Suillus collinitus</i> Species of fungus

Suillus collinitus is a pored mushroom of the genus Suillus in the family Suillaceae. It is an edible mushroom found in European pine forests. The mushroom has a reddish to chestnut-brown cap that reaches up to 11 cm (4.3 in) in diameter, and a yellow stem measuring up to 7 cm (2.8 in) tall by 1 to 2 cm thick. On the underside of the cap are small angular pores, initially bright yellow before turning greenish-brown with age. A characteristic feature that helps to distinguish it from similar Suillus species, such as S. granulatus, is the pinkish mycelia at the base of the stem.

The mycorrhizosphere is the region around a mycorrhizal fungus in which nutrients released from the fungus increase the microbial population and its activities. The roots of most terrestrial plants, including most crop plants and almost all woody plants, are colonized by mycorrhiza-forming symbiotic fungi. In this relationship, the plant roots are infected by a fungus, but the rest of the fungal mycelium continues to grow through the soil, digesting and absorbing nutrients and water and sharing these with its plant host. The fungus in turn benefits by receiving photosynthetic sugars from its host. The mycorrhizosphere consists of roots, hyphae of the directly connected mycorrhizal fungi, associated microorganisms, and the soil in their direct influence.

<span class="mw-page-title-main">Mycorrhizal network</span> Underground fungal networks that connect individual plants together

A mycorrhizal network is an underground network found in forests and other plant communities, created by the hyphae of mycorrhizal fungi joining with plant roots. This network connects individual plants together. Mycorrhizal relationships are most commonly mutualistic, with both partners benefiting, but can be commensal or parasitic, and a single partnership may change between any of the three types of symbiosis at different times.

<span class="mw-page-title-main">Mycorrhizal fungi and soil carbon storage</span>

Soil carbon storage is an important function of terrestrial ecosystems. Soil contains more carbon than plants and the atmosphere combined. Understanding what maintains the soil carbon pool is important to understand the current distribution of carbon on Earth, and how it will respond to environmental change. While much research has been done on how plants, free-living microbial decomposers, and soil minerals affect this pool of carbon, it is recently coming to light that mycorrhizal fungi—symbiotic fungi that associate with roots of almost all living plants—may play an important role in maintaining this pool as well. Measurements of plant carbon allocation to mycorrhizal fungi have been estimated to be 5 to 20% of total plant carbon uptake, and in some ecosystems the biomass of mycorrhizal fungi can be comparable to the biomass of fine roots. Recent research has shown that mycorrhizal fungi hold 50 to 70 percent of the total carbon stored in leaf litter and soil on forested islands in Sweden. Turnover of mycorrhizal biomass into the soil carbon pool is thought to be rapid and has been shown in some ecosystems to be the dominant pathway by which living carbon enters the soil carbon pool.

<span class="mw-page-title-main">Ectomycorrhiza</span> Non-penetrative symbiotic association between a fungus and the roots of a vascular plant

An ectomycorrhiza is a form of symbiotic relationship that occurs between a fungal symbiont, or mycobiont, and the roots of various plant species. The mycobiont is often from the phyla Basidiomycota and Ascomycota, and more rarely from the Zygomycota. Ectomycorrhizas form on the roots of around 2% of plant species, usually woody plants, including species from the birch, dipterocarp, myrtle, beech, willow, pine and rose families. Research on ectomycorrhizas is increasingly important in areas such as ecosystem management and restoration, forestry and agriculture.

<i>Rhizophagus irregularis</i> Species of arbuscular mycorrhizal fungus used as a soil inoculant in agriculture and horticulture

Rhizophagus irregularis is an arbuscular mycorrhizal fungus used as a soil inoculant in agriculture and horticulture. Rhizophagus irregularis is also commonly used in scientific studies of the effects of arbuscular mycorrhizal fungi on plant and soil improvement. Until 2001, the species was known and widely marketed as Glomus intraradices, but molecular analysis of ribosomal DNA led to the reclassification of all arbuscular fungi from Zygomycota phylum to the Glomeromycota phylum.

<span class="mw-page-title-main">Ectomycorrhizal extramatrical mycelium</span>

Ectomycorrhizal extramatrical mycelium is the collection of filamentous fungal hyphae emanating from ectomycorrhizas. It may be composed of fine, hydrophilic hypha which branches frequently to explore and exploit the soil matrix or may aggregate to form rhizomorphs; highly differentiated, hydrophobic, enduring, transport structures.

Dark septate endophytes (DSE) are a group of endophytic fungi characterized by their morphology of melanized, septate, hyphae. This group is likely paraphyletic, and contain conidial as well as sterile fungi that colonize roots intracellularly or intercellularly. Very little is known about the number of fungal taxa within this group, but all are in the Ascomycota. They are found in over 600 plant species and across 114 families of angiosperms and gymnosperms and co-occur with other types of mycorrhizal fungi. They have a wide global distribution and can be more abundant in stressed environments. Much of their taxonomy, physiology, and ecology are unknown.

Orchid mycorrhizae are endomycorrhizal fungi which develop symbiotic relationships with the roots and seeds of plants of the family Orchidaceae. Nearly all orchids are myco-heterotrophic at some point in their life cycle. Orchid mycorrhizae are critically important during orchid germination, as an orchid seed has virtually no energy reserve and obtains its carbon from the fungal symbiont.

<span class="mw-page-title-main">Mycorrhiza helper bacteria</span> Group of organisms

Mycorrhiza helper bacteria (MHB) are a group of organisms that form symbiotic associations with both ectomycorrhiza and arbuscular mycorrhiza. MHBs are diverse and belong to a wide variety of bacterial phyla including both Gram-negative and Gram-positive bacteria. Some of the most common MHBs observed in studies belong to the phylas Pseudomonas and Streptomyces. MHBs have been seen to have extremely specific interactions with their fungal hosts at times, but this specificity is lost with plants. MHBs enhance mycorrhizal function, growth, nutrient uptake to the fungus and plant, improve soil conductance, aid against certain pathogens, and help promote defense mechanisms. These bacteria are naturally present in the soil, and form these complex interactions with fungi as plant root development starts to take shape. The mechanisms through which these interactions take shape are not well-understood and needs further study.

<i>Rhizopogon salebrosus</i> Species of fungus

Rhizopogon salebrosus is a mushroom species within the Rhizopogon sub-genus Amylopogon. R.salebrosus is a monotropoid mycorrhiza that is of vital importance to the ecology of conifer forests, especially in the Pacific Northwest region of North America. Although it is native to North America, R. salebrosus has been found in Europe and its range is generally limited to mountainous regions with sufficient precipitation. The mycoheterotrophic plant, Pterospora andromedea is often found in an obligate association with R. salebrosus in western parts of the U.S. Eastern populations of P. andromedea are typically symbiotic with another Rhizopogon sub species, R. kretzerae.

References

  1. ↑ Trappe, J. M. (1962). Cenococcum graniforme--its distribution, ecology, mycorrhiza formation, and inherent variation (Doctoral dissertation).
  2. 1 2 Spatafora, J. W., Owensby, C. A., Douhan, G. W., Boehm, E. W., & Schoch, C. L. (2012). Phylogenetic placement of the ectomycorrhizal genus Cenococcum in Gloniaceae (Dothideomycetes). Mycologia, 104(3), 758-765.
  3. ↑ Ferdinandsen, C., & Winge, Ö. (1925). Cenococcum Fr. A monographic study. Kongelige Veterinaer-og Landbohoiskoles Aarsskrift, 332-382.
  4. ↑ LoBuglio, K. F. (1999). Cenococcum. In Ectomycorrhizal Fungi Key Genera in Profile (pp. 287-309). Springer Berlin Heidelberg.
  5. ↑ LoBuglio, K. F., Berbee, M. L., & Taylor, J. W. (1996). Phylogenetic Origins of the Asexual Mycorrhizal Symbiont Cenococcum geophilum Fr. and Other Mycorrhizal Fungi among the Ascomycetes. Molecular Phylogenetics and Evolution, 6(2), 287-294.
  6. 1 2 Visser, S. (1995). Ectomycorrhizal fungal succession in jack pine stands following wildfire. New Phytologist, 129(3), 389-401.
  7. ↑ Dickie, I. A., Xu, B., & Koide, R. T. (2002). Vertical niche differentiation of ectomycorrhizal hyphae in soil as shown by T‐RFLP analysis. New Phytologist, 156(3), 527-535.
  8. ↑ Goodman, D. M., & Trofymow, J. A. (1998). Distribution of ectomycorrhizas in micro-habitats in mature and old-growth stands of Douglas-fir on southeastern Vancouver Island. Soil Biology and Biochemistry, 30(14), 2127-2138.
  9. ↑ Rosling, A., Landeweert, R., Lindahl, B. D., Larsson, K. H., Kuyper, T. W., Taylor, A. F. S., & Finlay, R. D. (2003). Vertical distribution of ectomycorrhizal fungal taxa in a podzol soil profile. New Phytologist, 159(3), 775-783.
  10. ↑ Scattolin, L., Montecchio, L., Mosca, E., & Agerer, R. (2008). Vertical distribution of the ectomycorrhizal community in the top soil of Norway spruce stands. European journal of forest research, 127(5), 347-357.
  11. ↑ Pickles, B. J., Genney, D. R., Potts, J. M., Lennon, J. J., Anderson, I. C., & Alexander, I. J. (2010). Spatial and temporal ecology of Scots pine ectomycorrhizas. New Phytologist, 186(3), 755-768.
  12. ↑ Corbery, Y., & Le Tacon, F. (1997). Storage of ectomycorrhizal fungi by freezing. In Annales des sciences forestières (Vol. 54, No. 2, pp. 211-217). EDP Sciences.
  13. ↑ Saleh‐Rastin, N. (1976). Salt tolerance of the mycorrhizal fungus Cenococcum graniforme (Sow.) Ferd. European Journal of Forest Pathology, 6(3), 184-187.
  14. ↑ Gonçalves, S. C., Martins-Loução, M. A., & Freitas, H. (2009). Evidence of adaptive tolerance to nickel in isolates of Cenococcum geophilum from serpentine soils. Mycorrhiza, 19(4), 221-230.
  15. ↑ Pigott, C. D. (1982). Survival of mycorrhiza formed by Cenococcum geophilum Fr. in dry soils. New Phytologist, 92(4), 513-517.
  16. ↑ Jany, J. L., Martin, F., & Garbaye, J. (2003). Respiration activity of ectomycorrhizas from Cenococcum geophilum and Lactarius sp. in relation to soil water potential in five beech forests. Plant and soil, 255(2), 487-494.
  17. ↑ Coleman, M. D., Bledsoe, C. S., & Lopushinsky, W. (1989). Pure culture response of ectomycorrhizal fungi to imposed water stress. Canadian Journal of Botany, 67(1), 29-39.
  18. ↑ Hasselquist, N., Germino, M. J., McGonigle, T., & Smith, W. K. (2005). Variability of Cenococcum colonization and its ecophysiological significance for young conifers at alpine–treeline. New Phytologist, 165(3), 867-873.
  19. ↑ Butler, M. J., & Day, A. W. (1998). Fungal melanins: a review. Canadian Journal of Microbiology, 44(12), 1115-1136.
  20. ↑ Fernandez, C. W., & Koide, R. T. (2013). The function of melanin in the ectomycorrhizal fungus Cenococcum geophilum under water stress. Fungal Ecology, 6(6), 479-486.
  21. ↑ Jennings, D. H., & Burke, R. M. (1990). Compatible solutes–the mycological dimension and their role as physiological buffering agents. New Phytologist,116(2), 277-283.
  22. ↑ Bois, G., Bertrand, A., Piché, Y., Fung, M., & Khasa, D. P. (2006). Growth, compatible solute and salt accumulation of five mycorrhizal fungal species grown over a range of NaCl concentrations. Mycorrhiza, 16(2), 99-109.
  23. ↑ Kerner, R., Delgado-Eckert, E., Del Castillo, E., Müller-Starck, G., Peter, M., Kuster, B., ... & Pritsch, K. (2012). Comprehensive proteome analysis in Cenococcum geophilum Fr. as a tool to discover drought-related proteins.Journal of proteomics, 75(12), 3707-3719.
  24. ↑ Kernaghan, G., Widden, P., Bergeron, Y., Légaré, S., & Paré, D. (2003). Biotic and abiotic factors affecting ectomycorrhizal diversity in boreal mixed‐woods.Oikos, 102(3), 497-504.
  25. ↑ Durall, D. M., Todd, A. W., & Trappe, J. M. (1994). Decomposition of 14C‐labelled substrates by ectomycorrhizal fungi in association with Douglas fir. New Phytologist, 127(4), 725-729.
  26. ↑ Courty, P. E., Pritsch, K., Schloter, M., Hartmann, A., & Garbaye, J. (2005). Activity profiling of ectomycorrhiza communities in two forest soils using multiple enzymatic tests. New Phytologist, 167(1), 309-319.
  27. ↑ Fernandez, C. W., McCormack, M. L., Hill, J. M., Pritchard, S. G., & Koide, R. T. (2013). On the persistence of Cenococcum geophilum ectomycorrhizas and its implications for forest carbon and nutrient cycles. Soil Biology and Biochemistry, 65, 141-143.
  28. ↑ Butler, M. J., & Day, A. W. (1998). Destruction of fungal melanins by ligninases of Phanerochaete chrysosporium and other white rot fungi. International journal of plant sciences, 159(6), 989-995.
  29. ↑ Watanabe, M., Sato, H., Matsuzaki, H., Kobayashi, T., Sakagami, N., Maejima, Y., ... & Hiradate, S. (2007). 14C ages and δ13C of sclerotium grains found in forest soils. Soil Science and Plant Nutrition, 53(2), 125-131.
  30. ↑ LoBuglio, K. F., Rogers, S. O., & Wang, C. J. K. (1991). Variation in ribosomal DNA among isolates of the mycorrhizal fungus Cenococcum geophilum. Canadian Journal of Botany, 69(11), 2331-2343.
  31. ↑ Jany, J. L., Garbaye, J., & Martin, F. (2002). Cenococcum geophilum populations show a high degree of genetic diversity in beech forests. New Phytologist, 154(3), 651-659.
  32. ↑ Wu, B., Nara, K., & Hogetsu, T. (2005). Genetic structure of Cenococcum geophilum populations in primary successional volcanic deserts on Mount Fuji as revealed by microsatellite markers. New Phytologist, 165(1), 285-293.
  33. ↑ Douhan, G. W., & Rizzo, D. M. (2005). Phylogenetic divergence in a local population of the ectomycorrhizal fungus Cenococcum geophilum. New Phytologist, 166(1), 263-271.
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.