Hosts and Distribution of Desert Truffles in Iran, Based on Morphological and Molecular Criteria

Authors
1 Shiraz University
2 Shiraz university
Abstract
Terfezia, Picoa and Tirmania, so called desert truffles, are mycorrhizal fungi mostly endemic to arid and semi-arid areas of the Mediterranean Region, where they are associated with Helianthemum and Carexspecies. The aim of this work was to study the identification, molecular analysis, distribution and hosts of these pezizalean hypogeous fungi in Iran. Among the specimens, Terfezia claveryi, Tirmania pinoyi, T. nivea, Picoa lefebvrei and P. juniperi were identified. Field, laboratory and anatomical studies showed that Helianthemum ledifolium, H. salicifolium, H. lippi and Carex stenophylum have ectomycorrhizal associations with five species in the studied areas. The results of molecular analysis showed that C. stenophylum roots form mycorrhizal associations with T. claveryi. Hyphal mantle was absent from sections of the mycorrhizas. The results of physico-chemical analyses on soil samples from different parts of the Fars Province in Iran showed that the genus Tirmania was more prevalent in soils with high CaCO3 and silt contents than the T. claveryi, P. lefebvrei and P. juniperi. The Canonical Correspondence Analysis (CCA) indicated that soil structure were an important environmental parameter influencing desert truffles distribution.

Keywords


1. Abd-Allah, S. K., Iissa, A. H., Ewaz, J. O. and Al-Bader, S. M. 1989. Taxonomy of Edible Hypogeous Ascomycotina of Iraqi. Int. J. Mycol. Lichenol., 4(1-2): 9-21.
2. Allen, E. B., Chambers, J. C., Connor, K. F., Allen, M. F. and Brown, R. W. 1987. Natural Reestablishment of Mycorrhizae in Disturbed Ecosystems. Arctic Alpine Res., 19: 11–20.
3. Alsheikh, A. 1984. Mycorrhizae of Annual Helianthemum Species Formed with Desert Truffles. Proc. 6th North Amer. Conf. Mycorrhizae, Oregon State University, Corvallis (USA), OR; no.445.
4. Alsheikh, M. and Trappe, J. M. 1983a. Desert Truffles: The Genus Tirmania. Trans. Brit. Mycol. Soc., 81: 83-90.
5. Alsheikh, M. and Trappe, J. M. 1983b. Taxonomy of Phaeangium lefebvrei: A Desert Truffle Eaten by Birds. Can. J. Bot., 61: 1919-1925.
6. Altschuli, S. F., Madden, T. L., Scha Ffer, A. A., Zhang, J. H., Zhang, Z., Miller, W. and Lipman, D. J. 1997. Gapped BLAST and PSI-BLAST: A New Generation of Protein Database Search Programs. Nucl. Aci. Res., 25: 3389–3402.
7. Ammarellou, A. Saremi, H. and Gucin, F. 2007. Evaluation of Morphology, Cytology and Mycorrhizal Relationships of Desert Truffles in Iran. Paki. J. Bio. Sci., 10: 1486-1490.
8. Ammarellou, A., Smith, M. E., Tajick, M. A. and Trappe, J. M. 2011. The Phylogenetic Placement of Picoa, with a First Report on Picoa lefebvrei (Pat.) Maire (= Phaeangium lefebvrei) from Iran. Int. J. Environ. Res., 5(2): 509-514.
9. Awameh, M. S. and Alsheikh, A., 1979. Laboratory and Field Study of Four Kinds of Truffle (Kamah), Terfezia and Tirmania Species, for Cultivation. Mush. Sci., 10: 507–517.
10. Awameh, M. S., Alsheikh, A. and Al-Ghawas, S. 1979. Mycorrhizal Synthesis between Helianthemum ledifolium, H. salicifolium and Four Species of the Genera Terfezia and Tirmania Using Ascospores and Mycelial Cultures Obtained from Ascospore Germination. Proc. 4th North Amer. Conf. Mycorrhizae, Colorado State University, Forth Collins (USA).
11. Awameh, M. S. and Alsheikh, A. 1980. Features and Analysis of Spore Germination in the Brown Kamah Terfezia claveryi. Mycologia, 72: 494-499.
12. Bellgard, S. E. 1991. Mycorrhizal Associations of Plant Species in Hawkesbury Sandstone Vegetation. Aust. J. Bot., 39: 357–364.
13. Bokhary, H. A. 1987. Desert truffle Al-Kamah of the Kingdom of Saudi Arabia. I. Occurrence, Identification and Distribution. Arab Gulf. J. Sc. Res., B5: 245-255.
14. Bokhary, M. A. and Parvez, S. 1988. Desert Truffle Al-Kamah of Kingdom of Saudi Arabia. 2. Additional Contribution. Arab Gulf J. Sci. Res. Agric. Biol. Sci., B6: 103-112.
15. Bokhary, M. A. and Parvez, S. 1992. Soil Mycoflora from Truffle Native Areas of Saudi Arabia. Mycopathologia, 118: 103-107.
16. Calonge, F. D., Garcõ!a, F, Santos, J. C. and Juste, P. 1995. Contribucio!n al Estudio de los Hongos de Valladolid y Provincias Limõ!trofes. III. Algunas Sspecies Hipogeas Interesantes. Boletin de la Sociedad Micologic de Madrid,20: 291-299.
17. Cano, A., Honrubia, M. and Molina-Ninrola, C. 1991. Mycorrhizae in Seminarid Ecosystems: Synthesis of Mycorrhizae between Terfezia claveryi Chat., Picoa juniperi Vit. and Helianthemum almeriense (Cistaceae). In: Proceedings of the Third European Symposium on Mycorrhizas, Sheffield, UK.
18. Chevalier, G., Dupre, C., Riousset, L. and Dexhemier, J. 1984. Synthese Mycorhizienne entre Terfezia leptoderma Tul et Diverses Cistaces. Agronomie, 4:210–211.
19. Daneshpajuh, B. 1991. Two New Species of Hypogeous Ascomycetes in Iran. 10th Iran. Plant Prot.Cong. Kerman. 123.
20. Dexheimer J., Gerard J., Leduc J. P., and Chevalier G. 1985. Etude Ultrastructurale Compare´e des Associations Symbiotiques Mycorhiziennes Helianthemum salicifolium–Terfezia claveryi et Helianthemum salicifolium–Terfezia leptoderma. Can. J. Bot., 63:582–591.
21. Diez, J., Manjon, J. L. and Martin, M. F. 2002. Molecular Phylogeny of the Mycorrhizal Desert Truffles (Terfezia and Tirmania), Host Specificity and Edaphic Tolerance. Mycologia, 94(2): 247–59.
22. El-Kholy, H. 1989. Genetical and Physiological Studies on Truffles. PhD. Thesis, Fac, of Agric, Cairo University, Egypt.
23. Ershad, D. 2009. Fungi of Iran. Ministry of Jihad-e-Agriculture, 531 PP.
24. Esfandiari, E. and Petrak, F. 1950. Pilze aus Iran-Sydowia. Horn, 4: 11-38.
25. Felsenstein, J. 1985. Confidence Limits on Phylogenies: an Approach Using the Bootstrap. Evolution, 39: 783–791.
26. Ferdman, Y., Aviram, S., Roth-Bejerano, N., Trappe, J. M. and Kagan-Zur, V. 2005. Phylogenetic Studies of Terfezia pfeilii and Choiromyces echinulatus (Pezizales) Support New Genera for Southern African Truffles: Kalaharituber and Eremiomyces. Mycol. Res., 109: 237-245.
27. Fernald, M. L. 1980. Grays Manual of Botany. D. Van Nostrand Company, 1585 PP.
28. Fortas, Z. and Chevalier, G. 1992. Effet des Conditions de Culture sur la Mycorhization de l’Helianthemum guttatum par Trois Espèces de Terfez des Genres Terfezia et Tirmania d’Algérie. Can. J. Bot., 70: 2453–2460.
29. Gardes, M., White, T. J., Fortin, J. A., Bruns, T. D. and Taylor, J. W. 1991. Identification of Indigenous and Introduced Symbiotic Fungi in Ectomycorrhizae by Amplification of Nuclear and Mitochondria1 Ribosomal DNA. Can. J. Bot., 69: 180-190.
30. Gay, P. E., Grubb, P. J. and Hudson, H. J. 1982. Seasonal Changes in the Concentrations of Nitrogen, Phosphorus and Potassium, and in the Density of Mycorrhiza, in Biennial and Matrix-forming Perennial Species of Closed Chalkland Turf. J. Ecol., 70: 571–593.
31. Ghahraman, A. 1996. The Families and Genera of the Flora of Iran. Research Institute of Forest Rangelands, Tehran, Iran. PP.1031.
32. Grace, C. and Stribley, D. P. 1991. A Safer Procedure for Routine Staining of Vesicular Arbuscular Mycorrhizal Fungi. Mycol. Res., 95: 1160-1162.
33. Gutierrez, A. 2001. Caracterizacion, Identificacion y Cultivo en Campo de las Trufas de Desierto. Doctoral Thesis, University of Murcia, Murcia.
34. Hall, T. A. 1999. BioEdit: A User-friendly Biological Sequence Alignment Editor and Analysis Program for Windows95/98/NT. Nucleic Acid Symp. Ser., 41: 95–98.
35. Halwagy, R. and Halwagy, M. 1974. Ecological Studies on the Desert of Kuwait. 1. The Physical Environment, J. Univ. Kuwait (Sci.), 1: 75-86.
36. Hansen, K., Lassoe, T. and Pfister, D. H. 2001. Phylogenetics of the Pezizaceae, with Emphasis on Peziza. Mycologia, 93: 958-990.
37. Harley, J. L. and Harley, E. L. 1987. A Check-list of Mycorrhiza in the British Flora. New Phytol., 105: 1-102.
38. Hartnett, D. C., Samunus, R. J., Fischer, L. E. and Hetrick, B. A. D. 1994. Plant Demographic Responses to Mycorrhizal Symbiosis in Tallgrass Prairie. Oecologia, 99: 21–26.
39. Haselwandter, K. and Read, D. J. 1980. Fungal Associations of Roots of Dominant and Sub-dominant Plants in High-alpine Vegetation Systems with Special Reference to Mycorrhiza. Oecologia 45: 57–62.
40. Honrubia M, Cano A. and Molina-Nin˜irola, C. 1992. Hypogeous Fungi from Southern Spanish Semi-arid Lands. Persoonia, 14: 647–653.
41. Hussain, G. and Al-Ruqaie, I. M. 1999. Occurrence, Chemical Composition, and Nutritional Value of Truffles: An Overview. Paki. J. Biol.Sci., 2(2): 510-514.
42. Jamali, S. and Banihashemi, Z. 2010. Two New Species of Hypogeous Ascomycetes, Tirmania nivea and Phaeangium lefebvrei from Iran. Proc.19th Iran. Plant Prot. Cong. Tehran. 67.
43. Koske, R. E., Gemma, J. N. and Flynn, T. 1992. Mycorrhizae in Hawaiian Angiosperms: A Survey with Implications for the Origin of the Native Flora. Ame. J. Bot.,79: 853–862.
44. Kovacs, G. and Jakucs, E. 2001. “Helianthemirhiza hirsuta” Helianthemum ovatum (Viv.) Dun. In: "Description of Ectomycorrhizae", (Eds.): Agerer, R., Danielson, R. M., Egli, S., Ingleby, K., Luoma, D. and Treu, R.. Munich, 5: 49–53.
45. Kovacs, G., Bagi, I., Vagvolgy, Cs., Kottke, I. and Oberwinkler, F. 2002. Studies on the Root Associations of the Truffle Terfezia terfezioides. Acta Microbio. Imm. H., 49(2–3): 207–213.
46. Kumar, S., Tamura, K., Jakobsen, I. B. and Nei, M. 2004. MEGA4: Molecular Evolutionary Genetics Analysis Software. Bioinformatics, 17: 1244-1245.
47. Leduc, J. P., Dexheimer, J. and Chevalier, G. 1986. Etude Ultrastructurale Comparee des Associations de Terfezia leptoderma avec Helianthemum salicifolium, Cistus albidus et Cistus salviaefolius. In Proc. 1st Eur. Symp. Mycorrhizae, Physiological and Genetical Aspects of Mycorrhizae, (Eds): Gianinazzi-Pearson, V. and Gianinazzi, S. INRA, Paris, PP. 291-295.
48. Lovera, M. and Cuencea, G. 1996. Arbuscular Mycorrhizal Infection in Cyperaceae and Gramineae from Natural, Disturbed, and Restored Savannas in La Gran Sabana, Venezuela. Mycorrhiza, 6: 111–118.
49. Maire, R. 1906. Notes Mycologiques. Annal. Mycol., 4: 329-399.
50. Malençon, G. 1973. Champignons Hypoges du Nord de IAfrique. I. Ascomycetes. Persoonia, 7: 261-288.
51. Mejstrik, V. K. 1972. Vesicular-arbuscular Mycorrhizas of the Species of a Molinietum coeruleae L. I. Association: The Ecology. New Phytol., 71: 883–890.
52. Meney, K. A., Dixon, K. W., Scheltema, M. and Pate, J. S. 1993. Occurrence of Vesicular Mycorrhizal Fungi in Dryland Species of Restionaceae and Cyperaceae from South-west Western Australia. Aust. J. Bot., 41: 733–737.
53. Miller, R. M., Smith, C. I., Jastrow, J. D. and Bever, J. D. 1999. Mycorrhizal Status of the Genus Carex (Cypraceae). Am. J. Bot., 86(4): 547–553.
54. Moreno, G., Diez, J. and Manjon, J. L. 2000. Phaeangium lefebvrei and Tirmania nivea, Two Rare Hypogeneous Fungi from Spain. Mycol. Res., 104(3): 378-381.
55. Morte, A. and Honrubia, M. 1994. Metodo para la Micorrizaci_n In vitro de Plantas Micropropagadas de Helianthemum con Terfezia claveryi: Patent P9402430. University of Murcia, Oficina Espanola de Patentes y Marcas.
56. Mostofizadeh, G. R., Jamali, S. and Banihashemi, Z. 2010. Molecular Phylogeny of Three Desert Truffles from Iran Based on Ribosomal Genome. Rostaniha, 11:151-162.
57. Newman, E. L. and Reddell, P. 1987. The Distribution of Mycorrhiza among Families of Vascular Plants. New Phytol. 106: 745-751.
58. Norman, J. E. and Egger, K. N. 1999. Molecular Phylogenetic Analysis of Peziza and Related Genera. Mycologia, 91: 820-829.
59. O’Donnell K., Cigelnik E., Weber N. S. and Trappe, J. M. 1997. Phylogenetic Relationships among Ascomycetous Truffles and True and False Morels Inferred from 18S and 28S Ribosomal DNA Sequence Analysis. Mycologia, 89:48–65.
60. Pacioni, G. and El-Kholy, H. 1994. Tartufi del Deserto Egiziano. Micol. Veget. Medit., 9: 69-84.
61. Patouillard, N. 1894. Les Terfez de la Tunisie. J. de Botanique, 8: 153-156.
62. Pendleton, R. L. and Smith, B. N. 1983. Vesicular-arbuscular Mycorrhizae of Weedy and Colonizer Plant Species at Disturbed Sites in Utah. Oecologia, 59: 296–301.
63. Percudani, R., Trevisi, A., Zambonelli, A. and Ottanello, S. 1999. Molecular Phylogeny of Truffles (Pezizales: Terfeziaceae, Tuberuceae) Derived from Nuclear rDNA Sequence Analysis. Mole. Phylog. Evol., 13: 169-180.
64. Petrak, F. 1949. Beitrage zur Pilzflora Irans–Sydowia. 3: 268-332.
65. Read, D. J., Koucheki, H. K. and Hodgson, J. 1976. Vesicular-arbuscular Mycorrhiza in Natural Vegetation Systems. New Phytol., 77: 641–653.
66. Read, D. J., Kianmehr, H. and Malibari, A. 1977. The Biology of Mycorrhiza in Helianthemum Mill. New Phytol., 78: 305–312.
67. Read, D. J. and Haselwanter, K. 1981. Observation of the Mycorrhizal Status of Some Alpine Plant Communities. New Phytol., 88: 341-352.
68. Riousset, L., Riousset, G., Jalade, M. and Chevalier, G. 1989. Prima Raccolta in Francia di Phaeangium lefebvrei Patouillard 1894. Fungo II: 9-11.
69. Riousset, L., Riousset, G., Jalade, M. and Chevalier, G. 1996. Prima Raccolta in Francia di Picoa lefebvrei (Patouillard) Maire 1906. Il Fungo suppl., 3: 15-17.
70. Roux, C., Sejalon-Delrnas, N., Martins, M., Parguey-Leduc, A., Dargent, R. and Becard, G. 1999. Phylogenetic Relationships between European and Chinese Truffles Based on Parsimony and Distance Analysis of ITS Sequences. FEMS Microbiol. Lett., 180: 147-155.
71. Sbissi, I., Neffati, M., Murat, C., and Gtari, M. 2010. Phylogenetic Affiliation of the Desert Truffles Picoa juniperi and Picoa lefebvrei. Antonie Van Leeuwenhoec. 98(4): 429-436.
72. Singer, R. 1961. Mushrooms and Truffles. XXIII: 272. Leonard Hill Publisher, Ltd., London. PP.189.
73. Tedersoo, L., May, T. M. and Smith, M. E. 2010. Ectomycorrhizal Lifestyle in Fungi: Global Diversity, Distribution, and Evolution of Phylogenetic Lineages. Mycorrhiza, 20: 217-263.
74. Tester, M., Smith, S. E. and Smith, F.A. 1987. The Phenomenon of Nonmycorrhizal Plants. Can. J. Bot., 65: 419-431.
75. Thompson, J. D., Higgins, D. G. and Gibson, T. J. 1994. CLUSTAL W: Improving the Sensitivity of Progressive Multiple Sequence Alignment through Sequence Weighting, Position-specific Gap Penalties and Weight Matrix Choice. Nucl. Aci. Res., 22: 4673–4680.
76. Trappe, J. M. 1971. A Synopsis of the Carbomycetaceae and Terfeziaceae (Tuberales). Trans. Brit. Mycol. Soc., 57: 85-92.
77. Trappe, J. M. 1979. The Orders, Families, and Genera of Hypogeous Ascomycotina (Truffles and Their Relatives). Mycotaxon, IX: 297-340.
78. Urbanelli, S., Sallicandro, P., Devito, E. and Bullini, L. 1998. Identification of Tuber Mycorrhizae Using Multilocus Electrophoresis. Mycologia, 90: 389-395.
79. White, T. J., Bruns, T., Lee, S. and Taylor, J. 1990. Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics. In: "PCR Protocols: A Guide to Methods and Applications", (Eds.): Gelfand, M. A., Sninsky, D. H. and White, T. J.. Academic Press, San Diego, CA, PP. 315-322.
80. Wetzel, P. R. and Van Der Valk, A. G. 1995. Vesicular-arbuscular Mycorrhizae in Prairie Pothole Wetland Vegetation in Iowa and North Dakota. Can. J. Bot., 74: 883–890.