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Biology of the ectomycorrhizal genus, Rhizopogon
I. Host associations, host-specificity and pure culture syntheses
RANDY MOLINA,
JAMES M. TRAPPE,
RANDY MOLINA
U.S. Department of Agriculture, Forest Service, Pacific Northwest Research Station, Forestry Sciences Laboratory, 3200 Jefferson Way, Corvallis, OR 97331, USA
Search for more papers by this authorJAMES M. TRAPPE
Department of Forest Science, Oregon State University, Corvallis, OR 97331, USA
Search for more papers by this author
RANDY MOLINA,
JAMES M. TRAPPE,
RANDY MOLINA
U.S. Department of Agriculture, Forest Service, Pacific Northwest Research Station, Forestry Sciences Laboratory, 3200 Jefferson Way, Corvallis, OR 97331, USA
Search for more papers by this authorJAMES M. TRAPPE
Department of Forest Science, Oregon State University, Corvallis, OR 97331, USA
Search for more papers by this authorSUMMARY
Twenty nine isolates of Rhizopogon from 20 spp. differed markedly in their ability to form ectomycorrhizas with Douglas fir, western hemlock and lodgepole pine in pure-culture syntheses, Within the four sections of Rhizopogon there were similarities in ectomycorrhizal appearance and range of potential hosts. Intermediate and overlapping ectomycorrhiza! characters were evident in closely related species complexes. Although the host-specificity of many species, based on field observations of sporocarps, often correlated with their host range in the syntheses, some fungi formed well-developed ectomycorrhiza on hosts with which they appear not to be associated in the field. The specificity of host associations is suggested as a major contributor to the speciation and diversification of Rhtzopogon in the Pacific Northwest of the USA and Canada.
REFERENCES
- Adams AJS. 1951 A forest nursery for Pinus radiata at Mt. Burr in the southeast of South Australia. Australian Forestry 15: 47–56.
10.1080/00049158.1951.10675797 Google Scholar
- Agerer R. 1990 Studies on ectomycorrhizae. XXIV. Ectomycorrhizae of Chroogomphus kelveticus and C. rutilus (Gomphidiaceae, Bastdiomycetes) and their relationship to those of Suillus and Rhizopogon. Nova Hedwigia 50: 1–63.
- Agerer R. 1991 Studies on ectomycorrhizae. XXXIV. Mycorrhizae of Gomphidius glutinosus and of G. roseus with some remarks on Gomphidiaceae (Basidiomycetes). Nova Hedwigia 53: 127–170.
- Alvarez IF, Linderman RG. 1983 Effects of ethylene and fungicide dips during cold storage on root regeneration and survival of estern conifers and their mycorrhizal fungi. Canadian Journal of Forest Research 13: 962–971.
- Alvarez IF, Parlade J, Trappe JM, Castellano MA. 1993 Hypogeous mycorrhizal fungi of Spain. Mycotaxon 47: 201–217.
- Baxter DV. 1928 Mycorrhiza and Scotch pine in the University of Michigan forest nursery. Michigan Academy of Arts, Science Si Letters Papers 9, 509–516.
- Birch TTC. 1937 A synopsis of forest fungi of significance in New Zealand. Nail Zealand Journal of Forestry 4: 109–125.
- Borchers SL, Perry DA. 1990 Growth and ertomycorrhiza formation of Douglas-fir seedlings grown in soils collected at different distances from pioneering hardwoods in southwestern Oregon clearcuts. Canadian Journal of Forest Research 20: 712–721.
- Bowen GD. 1968 Phosphate uptake by mycorrhizas and uninfected roots of Pinus radial a in relation to root distribution. Transactions of the 9th Congress of Soil Science 2: 219–228.
- Bowen GD, Theodorou C. 1979 Interactions between bacteria and ectomycorrhizal fungi. Soil Biology and Biochemistry 11: 119–126.
- Brownlee CJ, Duddridge A, Malibari A, Read DJ. 1983 The structure and function of mycelial systems of ectomycorrhizal roots with special reference to their role in forming inter-plat connections and providing pathways for assimilate and water transport. Plant and Soil 71: 433–443.
- Bnuis TD, Fogei RD, White TJ, Palmer JD. 1989 Accelerated evolution of a false truffle from a mushroom ancestor. Nature 339: 140–142.
- Castellano MA. 1985 Basidiospores of Rhizopogon vinicolor and Rhizopogon colossus as ectomycorrhizal inoculum. In: R. Molina ed. 6th North American conference on mycorrhiza.Corvallis: Forest Research Laboratory, Oregon State University, 211.
- Castellano MA. 1987 Ectomycorrhizal inoculum production and utilization in the Pacific Northwestern U.S. - A glimpse at the past, a look to the future. In: DM Sylvia, LL Hung, JH Graham, eds. 7th North American conference on mycorrhizae. Gainesville : Institute of Food and AgTicuituraJ Sciences, University of Florida, 290–291.
- Castellano MA, Molina R. 1989 Mycoirhizae. In: TD Landis, RW Tinus, SE McDonald, JP Barnen, eds. The container tree nursery manual, vol. 5, Agricultural handbook 614, Washington , DC : U.S . Department of Agriculture. Forest Sen-ice, 101–167.
- Castellano MA, Trappe JM. 1988 Ectomycorrhizal formation and plantation performance of Douglas-fir nursery stock inoculated with Rhizopogon spores. Canadian Journal of Forest Research 15: 613–617.
- Castellano MA, Trappe JM, Molina R. 1985 Inoculation of container-grown Douglas-fir seedlings with basidiospores of Rhizopogon vinicolor and R. colossus: effects of fertility and spore application rate, Canadian Journal of Forest Research 15: 10–13.
- Cázares E, Garcia J, Castillo J, Trappe JM. 1992 Hypogeous fungi from northern Mexico. Mycologia 84: 341–359.
- Chilvers GA. 1973 Host range of some eucalypt mycorrhizal fungi. Australian Journal of Botany 21: 103–111.
- Chu-Chou M. 1979 Mycorrhizal fungi of Pinus radiata in New Zealand. Soil Biology and Biochemistry 11: 557–562.
- Chu-Chou M. 1985 Effect of different myeorrhizal fungi on Finns radiata seedling growth. In: R. Molina 6th North American conference on mycorrhiza. Corvallis : Forest Research Laboratory, Oregon State University, 208.
- Chu-Chou M, Grace LJ. 1981 Mycorrhizal fungi of Pseudotsuga menziesii in the north island of New Zealand. Soil Biology and Biochemistry 13: 247–249.
- Chu-Chou M, Grace LJ. 1983a. Characterization and identification of mycorrhizas of Douglas-fir in New Zealand, European Journal of Forest Pathology 13: 251–260.
- Chu-Chou M, Grace LJ. 1983b. Characterization and identification of mycorrhizas of radiata pine in New Zealand. Australian Forestry Research 13: 121–132.
- Chu-Chou M, Grace LJ. 1983c. Hypogeous fungi associated with some forest trees in New Zealand. New Zealand Journal of Botany 21, 183–190.
- Chu-Chou M, Grace LJ. 1985 Comparative efficiency of the mycorrhizal fungi Laccaria laccata, Hebelomo crustuliniforme, and Rhizopogon species on growth of radiata pine seedlings. Naw Zealand Journal of Botany 23: 417–424.
- Cline ML, Reid PP. 1982 Seed source and mycorrhizal fungus effects on growth of containerized Pinus cuntorta and Pinus ponderosa seedlings. Forest Science 28: 237–250.
- Coker WC, Couch JN. 1928 The gasteromycetes of the Eastern United States and Canada. Chapel Hill : University of North Carolina Press.
- Croghan CG. 1984 Survey for mycorrhizal fungi in lake states tree nurseries. Mycologia 76: 951–953.
- Donald DGM. 1975 Mycorrhizai inoculation for pines. South African Forestry Journal 92: 27–29.
10.1080/00382167.1975.9629357 Google Scholar
- Dosskey M. Boersma L, Linderman RG. 1990 Role for photosynthate demand by ectomycorrhizas in the response of Douglas-fir seedings to drying soil, New Phytologist 117: 327–334.
- Duddridge JA. 1986a. Specificity and recognition in mycorrhizal associations. In: V Gianinazzi-Pearson, S Gianinazzi, eds. Mycorrhizae: Physiology and Genetics. Paris : INRA, 45–58.
- Duddridge JA. 1986b. The development and ultrastructure of ectomycorrhizas. III. Compatible and incompatible interactions between Suillus grevillei (Klotzsch) Sing, and 11 species of ectomycorrhizal hosts in vitro in the absence of exogenous carbohydrate. New Phytotogist 103: 457–464.
- Duddridge JA. 1986c. The development and infrastructure of ectomycorrhizas. IV. Compatible and incompatible interactions between Suillus grevillei (Klotzsch) Sing, and a number of ectomycorrhizal hosts in vitro in the presence of exogenous carbohydrate. New Phvtologist 103: 465–471.
- Duddridge JA, Read DJ. 1984 Modification of the host-fungus interface in mycorrhizas synthesized between Suillus bovinus (FT.) O. Kuntz and Pinus sylvestris L. New Phvtologist 96: 583–588.
- Duddridge JA, Malibari A, Read DJ. 1980 Structure and function of mycorrhizai rhizomorphs with special reference to their role in water transport. Nature 287: 834–836.
- Ekwebelam SA, Odeyinde MA. 1985 Field response of Pinus species inoculated with ectomycorrhizal fungi in Nigeria. In: R Molina, ed. 6th North American conference on mycorrhiza. Corvallis : Forest Research Laboratory, Oregon State University, 220.
- Finlay RD, Eh H. Odham G, Söderström B. 1988 Mycelial uptake, translocation and assimilation of nitrogen from 15N-labelled ammonium by Pinus sylvestris plants infected with four different eetomycorrhizal fungi. New Phytologist 110: 59–66.
- Fogel R. 1980 Additions to the hypogeous mycofiora of the Canary Islands and Madeira. Contributions of the University of Michigan Herbarium 14: 75–82.
- Fontana A, Centrella E. 1967 Ectomicorrize prodotte da fungi ipogel. Allionia 13: 149–176.
- Ford VL, Torbert JL, Burger JA, Miller OK. 1985 Comparative effects of four mycorrhizal fungi on loblolly pine seedlings growing in a greenhouse in a Piedmont soil. Plant and Soil 83: 215–221.
- Gross G, Runge A, Winterhoff W. 1980 Bauchpilze (Gasteromycetes S. L.) in der Bundesrepublik Deutschland und Westberlin. Zeitschrift für Mykologie Beihefte 2: 1–220.
- Harrley JL, Smith SE. 1983 Mycorrhizal symbiosis. London : Academic Press.
- Harrison KA, Smith AH. 1968 Some new species and distribution records of Rhisopogon in North America. Canadian Journal of Botany 46: 881–889.
- Henderson GS, Stone EL. 1970 Growth of mycorrhizal monterey pine supplied with phosphorus fixed on perlite. In: CT Youngberg, DB Davey, eds. Tree growth and forest soils. Corvallis : Oregon State University Press, 171–180.
- Hodgson TJ. 1979 Basidiospore inoculation of soil: The effect of application timing on Pinus elliottii seedling development. South African Forestry Journal 108: 10–15.
10.1080/00382167.1979.9630486 Google Scholar
- Hosford DR. 1972 Rhizopogon of the northwestern United States. Ph.D. thesis. University of Washington, Seattle .
- Hosford DR, Trappe JM. 1980 Taxonomic studies on the genus Rhizopogon. II. Notes and new records of species from Mexico and Caribbean countries. Boletin de la Sociedad Mexicana de Miculogia 14: 3–5.
- Hyppel A. 1968 Antagonistic effects of some soil fungi on Fomes annosus in laboratory experiments. Studio Forestalia Suecica 64: 1–18.
- Ivory MH, Munga FM. 1983 Growth and survival of container-grown Pinus caribaea infected with various ectomycorrhizal fungi. Plant and Soil 71: 339–344.
- Jansen AE, de Vries FW. 1989 Mycorrhizas on Douglas fit in the Netherlands. Agriculture, Ecosystems and Environment 28: 197–200.
- Johansen DA. 1940 Plant microtechnique. New York : McGraw-Hill Book Co., Inc.
- Jones MD, Browning MHR, Hutchinson TC. 1986 The influence of mycorrhizai associations on paper birch and jack pine seedlings when exposed to elevated copper, nickel or aluminium. Water, Air, and Soil Pollution 31: 441–448.
- Kessel SL. 1927 Soil organisms. The dependence of certain pine species on a biological soil factor. Empire Forestry Journal 6: 70–74.
- Kropp BR, Trappe JM. 1982 Ectomycorrhizal fungi of Tsuga heterophylla. Mycologia 74: 479–488.
- Lamb RJ. 1979 Factors responsible for the distribution of mycorrhizai fungi of Pinus in Eastern Australia. Australian Forestry Research 9: 25–34.
- Lamb RJ, Richards BN. 1971 Effect of mycorrhizai fungi on the growth and nutnent status of slash and radiara pine seedlings. Australian Forestry 35: 1–7.
- Lamb RJ, Richards BN. 1974a. Inoculation of pines with mycorrhizal fungi in natural soils. I. Effects of density and time of application of inoculum and phosphorus amendments on mycorrhizai infection. Soil Biology and Biochemistry 6: 167–171.
- Lamb, RJ, Richards BN. 1974b. Inoculation of pines with mycorrhizal fungi in natural soils. 11. Effects of density and time of application of inoculum and phosphorus amendment on seedling yield. Soil Biology and Biochemistry 6: 73–177.
- Lamb, RJ, Richards BN. 1974c. Survival potential of sexual and asexual spoTes of ectomycorrhizal fungi. Transactions of the British Mycological Society 62: 181–191.
- Lamb RJ, Richards BN. 1978 Inoculation of pines with mycorrhizal fungi in natural soils. III. Effects of soil fumigation on rate of infection and response to inoculum density. Soil Biology and Biochemistry 10: 273–276.
- Levisohn I. 1956 Growth stimulation of forest Iree seedlings by the activity of free living mycorrhizal mycelia. Forestry 29: 53–59.
10.1093/forestry/29.1.53 Google Scholar
- Levisohn I. 1965 Nutritional problems in forest nurseries - mycorrhizal investigations. Great Britain Forestry Commonwealth Bulletin 37: 228–235.
- Massicotte HB, Molina, R. Luoma, DL, Smith JE. 1994 Biology of the ectomycorrhizal genus, Rhizopogon. II. Patterns of host-fungus specificity following spore inoculation of diverse hosts grown in mono- and dual cultures. Neic Phytologist 126, 677–690.
- Malajczuk N, Molina R, Trappe JM. 1982 Ectomycorrhizal formation in Eucalyptus. I. Pure culture synthesis, host specificity and mycorrhizal compatibility with Pinus radiata. New Phytologist 91: 467–482.
- Marx DH. 1980 Ectomycorrhizal fungus inoculations: a tool for improving forestation practices. In: P Mikola, ed. Tropical mycorrhiza research. Oxford : Clarendon Press, 11–71.
- Melin E, Nilsson H, Hacskaylo E. 1958 Translocation of cations to seedlings of Pinus virginiana through mycorrhizal mycelium. Botanical Gazette. 119: 243–246.
- Miller SL. 1986 Hypogeous fungi from the southeastern United States. I. The genus Rhizopogon. Mycotaxon 27: 193–218.
- Miller SL, Koo, CD, Molina R. 1992 Early colonization of red alder and Douglas-fir by ectomycorrhizal fungi and Ftankia in soils from the Oregon Coast Range. Mycorrhiza 2: 53–61.
10.1007/BF00203250 Google Scholar
- Mohan V, Natarajan K, Ingleby K 1993 Anatomical studies on ectomycorrhizas. III. The ectomycorrhizas produced by Rhizopagon lutealus and Scleroderma citrinum on Pinus patula. Mycorrhiza 3: 51–56.
- Molina R. 1979 Pure culture synthesis and host specificity of red alder mycorrhizae. Canadian Journal of Botany 57: 1223–1228.
- Molina R. 1980a. Ectomycorrhial inoculation of containerized western conifer seedlings. Research Note PNW-357, Pacific Northwest Forest and Range Experiment Station, U.S. Department of Agriculture, Forest Service.
- Molina R. 1980b. Ectomycorrhizal specificity in the genus Alnua. Canadian Journal of Botany 59: 325–334.
- Molina R, Massicotte H, Trappe JM. 1992 Specificity phenomena in mycorrhizal symbioses: community-ecological consequences and practical implications. In: MF Alien, ed. Mycorrhizal functioning: an integrative plant-fungal process. New York : Chapman and Hall, 357–423.
- Molina R, Trappe JM. 1982a. Lack of mycorrhizal specificity by the ericaceous hosts Arbutus menziesii and Arctostaphylos uvaursi. New Phytologist 90: 495–509.
- Molina R, Trappe JM. 1982b. Patterns of ectomycorrhizal host specificity and potential among Pacific Northwest conifers and fungi. Forest Science 28: 423–458.
- Momoh ZO. 1976 Synthesis of mycorrhiza on Pinus oocarpa. Annals of Applied Biology 82: 221–226.
- Odeyinde MA, Ekwebelam SA. 1947 In search of a suitable pine mycorrhiza fungus in the high forest zones of Nigeria. Nigerian Journal of Forestry 4: 93–97.
- Parke JL, Linderman RG, Black CH. 1983 The role of ectomycorrhizas in drought tolerance of Douglas-fir seedlings. New Phytologist 95: 83–95.
- Parladé J, Alvarez IF. 1993 Coinoculation of aseptically grown Douglas fir with pairs of ectomycorrhizal fungi. Mycorrhiza 3: 93–96.
- Pilz P, Perry DA. 1983 Impact of clearcutting and slash burning on ectomycDrrhizal associations of Douglas-fir seedlings. Canadian Journal of Forestry Research 14: 94–100.
- Purnell H. 1957 Notes on fungi found in Victorian plantations. III. The mycorrhizal fungi. Plantation Technical Papers, Forests Commission of Victoria 3: 9–13.
- Rammeloo J. 1971 Note preliminaires sur 1'emploi de cultures de mycelium dans I'etude taxonomique du genre Rhisopogon (Gastéromycetes). Biotogiuh jaarboek 39: 112–121.
- Raytter MC. 1938 The use of soil or humus inocula in nurseries and plantations. Empire Forestry Journal 17: 236–243.
- Read DJ. 1984 The structure and function of vegetative mycelium of mycorrhizal roots. In: DH Jennings, ADM Rayner, eds. Ecology and physiology of the fungal mycelium. Cambridge : Cambridge University Press, 215–240.
- Read DJ, Boyd R. 1986 Water relations of mycorrhizal fungi and their host plants. In: PG Ayres, L Boddy, eds. Water, futtgi, and plants. Cambridge : Cambridge University Press, 287–303.
- Read DJ, Finlay RD. 1985 Mycorrhizas and inter-plant transfer of nutrients. I. Ectomycorrbizas. In: R. Molina ed. 6th North American conference on mycorrhiza. Corvaliis : Forest Research Laboratory, Oregon State University, 319.
- Read DJ, Francis R, Finlay RD. 1985 Mycorrhizal mycelia and nutrient cycling in plant communities. In: AH Fitter, D Atkinson, DA Read, MB Usher, eds. Ecological interactions in soil. Palo Alto : Blackwell Scientific Publications, 193–217.
- Sands R, Theodorou C. 1978 Water uptake by mycorrhiza) roots of radiata pine seedlings. Australian Journal of Plant Physiology 5: 301–309.
- Sasek V, Musilek V. 1967 Cultivation and antibiotic activity of mycorrhizal basidiomycetes. Folia Microbiologica 12: 515–523.
- Skinner MF, Bowen GD. 1974a. The penetration of soil by mycelial strands of ectomycorrhizal fungi. Soil Biology and Biochemistry 6: 57–61.
- Skinner MF, Bowen GD. 1974. The uptake and translocation of phosphate by mycelial strands of pine mycarrhizas. Soil Biology and Biochemistry 6: 53–56.
- Smith AH. 1964 Rhizopogon, a curious genus of false truffle. Michigan Botanist 3: 13–19.
- Smith AH. 1966 New and noteworthy higher fungi from Michigan. Michigan Botanist 5: 18–25.
- Smith AH. 1968 Further studies on Rhisopogon. I. J. Elisha Mitchell Science Society 84: 274–280.
- Smith AH. 1971. Taxonomy of ectomycorrhiza-lorming fungi. In: E Hacskaylo, ed. Mycorrhizae. Washington , DC : U.S. Department of Agriculture. Forest Service, Miscellaneous Publication 1189, 1–8.
- Smith AH, Zeller SM. 1966 A preliminary account of the North American species of Rhizopogon. Memoirs of the New York Botanical Garden 14: 1–178.
- Theodorou C. 1967 Inoculation with pure cultures of mycorrhizal fungi of radiata pine growing in partially sterilized soil. Australian Forestry 31, 303–309.
10.1080/00049158.1967.10675452 Google Scholar
- Theodorou C. 1971 Introduction of mycorrhizal fungi into soil by spore inoculation of seed. Australian Forestry 35: 17–22.
10.1080/00049158.1971.10675531 Google Scholar
- Theodorou C. 1978 Soil moisture and the mycorrhizal association of Pinus radiata D. Don. Soil Biology and Biochemistry 10: 33–37.
- Theodorou C. 1980 The sequence of mycorrhizal infection of Pinus radiata D. Don. following inoculation with Rkizopogon luteotus Fr. and Nordh. Australian Forestry Research 10: 381–387.
- Theodorou C. 1984 Mycorrhizal inoculation of pine nurseries by spraying basidiospores onto soil prior to sowing. Australian Forestry 47: 76–78.
10.1080/00049158.1984.10675981 Google Scholar
- Theodorou C, Benson AD. 1983 Operational mycorrhizal inoculation of nursery beds with seed-borne fungal spores. Australian Forestry 46: 43–47.
10.1080/00049158.1983.10674376 Google Scholar
- Theodorou C, Bowen GD. 1970 Mycorrhtzal responses of radiata pine in experiments with different fungi. Australian Forestry 34: 183–191.
10.1080/00049158.1970.10675525 Google Scholar
- Theodorou C, Bowen GD. 1973 Inoculation of seeds and soil with basidiospores of mycorrbizal fungi. Soil Biology and Biochemistry 5: 765–771.
10.1016/0038-0717(73)90021-7 Google Scholar
- Theodorou C, Bowen GD. 1987 Germination of basidiospores of mycorrhizal fungi in the rhizosphere of Pimis radiata, D. Don. New Phytologist 106: 217–223.
- Theodorou C, Skinner MF. 1976 Effects of fungicides on seed inocula of basidiospores of mycorrhizal fungi. Australian Forestry Research 7: 53–58.
- Thoen D. 1974 Premieres indications sur les mycorrhizes et les champignons mycorrhiziques des plantations d'exotiques du Hant-Shaba (Republique du Zaire). Bulletin de Recherche Agronomique Gembloux 9: 215–227.
- Totten HR. 1923 Development of the fruit-body of a new parasitic Rhisopogon. J Elisha Mitchell Science Society 39: 101–107.
- Trappe JM. 1962 Fungus associates of ectotrophic mycorrhizae. Botanical Review 28: 538–606.
- Trappe JM. 1967 Pure culture synthesis of Douglas-fir mycorrhizae with species of Hebeloma, Suillum, Rhizopogon, and Astraeus. Forest Science 13: 121–130.
- Trappe JM. 1975 A revision of the genus Alpova with notes on Rhizopogon and the Melanogastraceae. Beiheft Nova Hedwigia 51: 279–309.
- Trappe JM. 1979 Selection of fungi for ectomycorrhizal inoculation in nurseries. Annual Review of Phytopathology 15: 203–222.
- Trappe JM, Guzman G. 1971 Notes on some hypogeous fungi from Mexico. Myculogia 63: 317–332.
- Volkart CM. 1964 Formacion de micorrizas en pinos centro- americanos bajo condiciones controladas. Turriaiba 14: 203–205.
- Young HE. 1937 Rhisopogon luteolus, a mycorrhizai fungus of Pinus. Forestry 11: 30–31.
10.1093/oxfordjournals.forestry.a062667 Google Scholar
- Zak B. 1971 Characterization and classification of mycorrhizae of Douglas-fir. II. Pseudotsuga menziesij + Rhizopogon vinicolor. Canadian Journal of Botany 49: 1079–1084.
- Zak B. 1973 Classification of ectomycorrhizae. In: GC Marks, TT Kozlowski, eds. Ectomycorrhizae, their ecology and physiology. New York : Academic Press, 43–78.
10.1016/B978-0-12-472850-9.50008-6 Google Scholar
- Zeller SM, Dodge CW. 1918 Rhizopogon in North America. Annals of the Missouri Botanical Garden 5: 1–36.
