Rhizopogon

Rhizopogon
Rhizopogon rubescens
Scientific classification Edit this classification
Domain: Eukaryota
Kingdom: Fungi
Division: Basidiomycota
Class: Agaricomycetes
Order: Boletales
Family: Rhizopogonaceae
Genus: Rhizopogon
Fr. (1817)
Type species
Rhizopogon luteolus
Fr. & Nordholm (1817)

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.

Rhizopogon species are primarily found in ectomycorrhizal association with trees in the family Pinaceae and are especially common symbionts of pine, fir, and Douglas fir trees. Through their ectomycorrhizal relationships Rhizopogon are thought to play an important role in the ecology of coniferous forests. Recent micromorphological and molecular phylogenetic study has established that Rhizopogon is a member of the Boletales, closely related to Suillus.[1]

Taxonomy and diversity

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An image of Rhizopogon luteolus (=obtextus) showing rhizomorphs with attached substrate.
A sporocarp of Rhizopogon luteolus (=obtextus) showing rhizomorphs with adhering substrate

Historical classification

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The genus Rhizopogon occurs throughout the natural and introduced ranges of family Pinaceae trees. Though this range covers much of the northern temperate zones, the diversity of Rhizopogon species is well characterized only in North America and Europe. There are currently over 150 recognized species of Rhizopogon. The morphology of Rhizopogon species is highly cryptic and characters vary greatly throughout sporocarp maturity. This has led to the description of multiple species from various developmental stages of a single fungus.

The genus Rhizopogon was first described from Europe by Elias Magnus Fries in 1817.[2] The North American monograph was produced by Alexander H. Smith in 1966[3] with second author credits given posthumously to Sanford Myron Zeller due to his contributions to the study of the genus. A European monograph of Rhizopogon has also been published.[4] In the recent past, molecular phylogenetic methods have allowed the revision of the taxonomic concepts of the genus Rhizopogon[5]

Modern classification

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Modern taxonomic concepts of the genus Rhizopogon recognize five subgenera of Rhizopogon.[5] These are subgenus Rhizopogon, subgenus Versicolores, subgenus Villosuli, subgenus Amylopogon, and subgenus Roseoli.

Ecology

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An image of Rhizopogon roseolus showing a close up of gleba locules.
A sporocarp of Rhizopogon roseolus in cross section showing a close up of the gleba locules

Mammalian diet and spore dispersal

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Rhizopogon species have been established as a common component in the diet of many small mammals [6][7] as well as deer[8] in Western North America. The viability of Rhizopogon spores is maintained [9][10] and may even be increased after mammalian gut passage,[9] making mammals an important dispersal vector for Rhizopogon.

Disturbance ecology

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Rhizopogon species are common members of the fungal communities that colonize the roots of trees during seedling establishment and persist into old growth stands.[11][12] Rhizopogon spores are long lived in soil and the spores of some species can persist for at least four years with an increase in viability over time.[13] Rhizopogon seems to be especially common upon the roots of establishing tree seedlings following disturbance such as fire[14] or logging.[15] Rhizopogon are also abundant colonizers of pot cultivated[14][16][17][18] and field cultivated [14] conifer seedlings growing in soil from conifer stands that lacked observations of Rhizopogon upon the roots of mature trees. These finding suggest that Rhizopogon species are an important factor in the recovery of conifer forests following disturbance.

Invasive facilitator

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Rhizopogon species have been shown to have a global distribution in the Homogenocene.[19][3][20] The enzymes exuded from some species within the subgenus Amylopogon is essential in activating seed germination in some species of Monotropoideae,[21] such as Pterspora andromedeae. This makes Rhizopogon an obligatory host to species like P. andromedeae. The exoenzymatic activity also confers higher competitive advantages to host species,[22][23] mainly within the genus Pinus, by helping to break down nutrients within the soil. The presence of Rhizopogon in soil facilitates Pinus as an invasive species.[24] This exoenzymatic activity is nitrogen limited.[22] In the case of subgenus Amylopogon parasitized by P. andromedeae the nitrogen cost of exoenzymatic production is in part paid for by bacteria within the family Burkholderiaceae that is hosted by P. andromedeae[25]

Species

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Ethnomycology

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Forestry

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The first intentional use of Rhizopogon species in forestry occurred in the early part of the 20th century when Rhizopogon luteolus was deliberately introduced into Pinus radiata plantations in Western Australia after it was observed to improve tree growth.[26] Since that time, Rhizopogon species have been widely studied as a component of managed forests. Rhizopogon species have been noted as common members of the ectomycorrhizal community colonizing tree roots of pine and Douglas-fir timber plantations.[27] Naturally occurring Rhizopogon roseolus (=rubescens) spores have been shown to out-compete the spores of other ectomycorrhizal fungi in pine plantations even when competing spores were directly inoculated onto seedlings.[23] The survival rate and performance of pine[28] and Douglas-fir[29] plantation seedlings are increased after inoculation with Rhizopogon species.

Gastronomy

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Though this genera is considered edible, most members are not held in high culinary esteem.[30] A notable exception is Rhizopogon roseolus (=rubescens) which is considered a delicacy in Japan where it is traditionally known as shōro.[31] Techniques for the commercial cultivation of this fungus in pine plantations have been developed and applied with successful results in Japan and New Zealand.[31]

References

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  1. ^ Manfred Binder & David S. Hibbett (2006). "Molecular systematics and biological diversification of Boletales". Mycologia. 98 (6): 971–981. doi:10.3852/mycologia.98.6.971. PMID 17486973.
  2. ^ Fries, Elias Magnus (1817). Symbolae Gasteromycorum. Lundae: Ex officina Berlingiana.
  3. ^ a b Smith AH, Zeller SM (1966). "A Preliminary Account of the North American Species of Rhizopogon". Memoirs of the New York Botanical Garden. 14 (2): 1–178.
  4. ^ Martín, MP (1996). The Genus Rhizopogon in Europe. Barcelona, Spain: BCG. pp. 173 p. ISBN 8992161700.
  5. ^ a b Grubisha LC, Trappe JM, Molina R, Spatafora JW (2002). "Biology of the ectomycorrhizal genus Rhizopogon. VI. Re-examination of infrageneric relationships inferred from phylogenetic analyses of ITS sequences". Mycologia. 94 (4): 607–619. doi:10.2307/3761712. JSTOR 3761712. PMID 21156534.
  6. ^ Maser C, Maser Z (1988). "Interactions among squirrels, mycorrhizal fungi, and coniferous forests in Oregon". Western North American Naturalist. 48 (3): 358–369.
  7. ^ Izzo AD, Meyer M, Trappe JM, North M, Bruns TD (2005). "Hypogeous ectomycorrhizal fungal species on roots and in small mammal diet in a mixed conifer forest". Forest Science. 51 (3): 243–254. doi:10.1093/forestscience/51.3.243.
  8. ^ Ashkannehhad S, Horton TR (2006). "Ectomycorrhizal ecology under primary succession on coastal sand dunes: interactions involving Pinus contorta, suilloid fungi and deer". New Phytologist. 169 (2): 345–354. doi:10.1111/j.1469-8137.2005.01593.x. PMID 16411937.
  9. ^ a b Colgan III W, Claridge AW (2002). "Mycorrhizal effectiveness of Rhizopogon spores recovered from faecal pellets of small forest-dwelling mammals". Mycological Research. 106 (3): 314–320. doi:10.1017/S0953756202005634.
  10. ^ Kotter M, Farentinos RC (1984). "Formations of Ponderosa pine ectomycorrhizae after inoculation with feces of tassel-eared squirrels". Mycologia. 76 (2): 758–760. doi:10.2307/3793237. JSTOR 3793237.
  11. ^ Twieg BD, Durall DM, Simard SW (2007). "Ectomycorrhizal fungal succession in mixed temperate forests". New Phytologist. 176 (2): 437–447. doi:10.1111/j.1469-8137.2007.02173.x. PMID 17888121.
  12. ^ Molina, R; Trappe, JM; Grubisha, LC; Spatafora, JW (1999). "Rhizopogon". In Cairney, JWG; Chambers, SM (eds.). Ectomycorrhizal Fungi Key Genera in Profile. Heidelberg: Springer Berlin. pp. 129–161. doi:10.1007/978-3-662-06827-4_5. ISBN 978-3-642-08490-4.
  13. ^ Bruns, TD; Peay KG; Boynton PJ; Grubisha LC; Hynson NA; Nguyen NH; Rosenstock NP (2009). "Inoculum potential of Rhizopogon spores increases with time over the first 4 yr of a 99-yr spore burial experiment". New Phytologist. 181 (2): 463–470. doi:10.1111/j.1469-8137.2008.02652.x. PMID 9121040.
  14. ^ a b c Baar J.; Horton T.R.; Kretzer A.M.; Bruns T.D. (1999). "Mycorrhizal colonization of Pinus muricata from resistant propagules after a stand-replacing wildfire". New Phytologist. 143 (2): 409–418. doi:10.1046/j.1469-8137.1999.00452.x.
  15. ^ Luoma DL, Stockdale CA, Molina R, Eberhart JL (2006). "The spatial influence of Pseudotsuga menziesii retention trees on ectomycorrhiza diversity". Canadian Journal of Forest Research. 36 (10): 2561–2573. doi:10.1139/x06-143.
  16. ^ Taylor DL, Bruns TD (1999). "Community structure of ectomycorrhizal fungi in a Pinus muricata forest: minimal overlap between the mature forest and resistant propagule communities". Molecular Ecology. 8 (11): 1837–1850. Bibcode:1999MolEc...8.1837T. doi:10.1046/j.1365-294x.1999.00773.x. PMID 10620228. S2CID 1687794.
  17. ^ Kjøller R, Bruns TD (2003). "Rhizopogon spore bank communities within and among California pine forests". Mycologia. 95 (4): 603–613. doi:10.2307/3761936. JSTOR 3761936. PMID 21148969.
  18. ^ Murata M, Kinoshita A, Nara K (2013). "Revisiting the host effect on ectomycorrhizal fungal communities: implications from host–fungal associations in relict Pseudotsuga japonica forests". Mycorrhiza. 23 (8): 641–653. Bibcode:2013Mycor..23..641M. doi:10.1007/s00572-013-0504-0. PMID 23702643. S2CID 2303003.
  19. ^ Pietras, Marcin (2019-06-07). "First record of North American fungus Rhizopogon pseudoroseolus in Australia and prediction of its occurrence based on climatic niche and symbiotic partner preferences". Mycorrhiza. 29 (4): 397–401. Bibcode:2019Mycor..29..397P. doi:10.1007/s00572-019-00899-x. ISSN 0940-6360. PMID 31175441.
  20. ^ Zhao, Pei-shan; Guo, Mi-shan; Gao, Guang-lei; Zhang, Ying; Ding, Guo-dong; Ren, Yue; Akhtar, Mobeen (March 2020). "Community structure and functional group of root-associated Fungi of Pinus sylvestris var. mongolica across stand ages in the Mu Us Desert". Ecology and Evolution. 10 (6): 3032–3042. Bibcode:2020EcoEv..10.3032Z. doi:10.1002/ece3.6119. ISSN 2045-7758. PMC 7083681. PMID 32211174.
  21. ^ Bruns, Thomas D.; Read, David J. (2000-11-27). "In vitro germination of nonphotosynthetic, myco-heterotrophic plants stimulated by fungi isolated from the adult plants". New Phytologist. 148 (2): 335–342. doi:10.1046/j.1469-8137.2000.00766.x. ISSN 0028-646X.
  22. ^ a b Ning, Chen; Xiang, Wenhua; Mueller, Gregory M.; Egerton-Warburton, Louise M.; Yan, Wende; Liu, Shuguang (2019-11-16). "Differences in ectomycorrhizal community assembly between native and exotic pines are reflected in their enzymatic functional capacities". Plant and Soil. 446 (1–2): 179–193. doi:10.1007/s11104-019-04355-9. ISSN 0032-079X. S2CID 208042202.
  23. ^ a b Karkouri KE, Martin F, Mousain D (2002). "Dominance of the mycorrhizal fungus Rhizopogon rubescens in a plantation of Pinus pinea seedlings inoculated with Suillus collinitus". Annals of Forest Science. 59 (2): 197–204. Bibcode:2002AnFSc..59..197E. doi:10.1051/forest:2002006.
  24. ^ Wood, Jamie R.; Dickie, Ian A.; Moeller, Holly V.; Peltzer, Duane A.; Bonner, Karen I.; Rattray, Gaye; Wilmshurst, Janet M. (2014-12-15). "Novel interactions between non-native mammals and fungi facilitate establishment of invasive pines". Journal of Ecology. 103 (1): 121–129. doi:10.1111/1365-2745.12345. ISSN 0022-0477.
  25. ^ Gans, Maya (2019). "Invariant Communities of Endophytic Nitrogen-fixing Bacteria Associated with a Non-photosynthetic Plant". ProQuest Dissertations Publishing.
  26. ^ Kessel SL (1927). "Soil organisms. The dependence of certain pine species on a biological soil factor". Empire Forestry Journal. 6: 70–74.
  27. ^ Molina R, Trappe JM (1994). "Biology of the ectomycorrhizal genus, Rhizopogon I. Host associations, host-specificity and pure culture syntheses". New Phytologist. 126 (4): 653–675. doi:10.1111/j.1469-8137.1994.tb02961.x.
  28. ^ Steinfield D, Amaranthus M, Cazares E (2003). "Survival of Ponderosa pine (Pinus ponderosa Dougl. ex Laws) seedlings outplanted with Rhizopogon mycorrhizae inoculated with spores at the nursery". Journal of Arboriculture. 29 (4): 4197–208.
  29. ^ Castellano MA, Trappe JM (1985). "Ectomycorrhizal formation and plantation performance of Douglas-fir nursery stock inoculated with Rhizopogon spores". Canadian Journal of Forest Research. 15 (4): 613–617. doi:10.1139/x85-100.
  30. ^ Trappe, M; Evans; Trappe, J (2007). Field guide to North American Truffles. Berkeley, CA: Ten Speed Press. pp. 136 p. ISBN 978-1580088626.
  31. ^ a b Yun W, Hall IR (2004). "Edible ectomycorrhizal mushrooms: challenges and achievements". Canadian Journal of Botany. 82 (8): 1063–1073. doi:10.1139/b04-051.
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