Mycobiology

The Korean Society of Mycology (한국균학회)
권호 표지
DOI QR코드

DOI QR Code

A New Report on Edible Tropical Bolete, Phlebopus spongiosus in Thailand and Its Fruiting Body Formation without the Need for a Host Plant

  • Received : 2020.04.06
  • Accepted : 2020.06.15
  • Published : 2020.08.31
Download PDF
⟨ Previous Next ⟩

Abstract

Phlebopus spongiosus is a well-known edible ectomycorrhizal mushroom indigenous to southern Vietnam. The mushroom specimens collected from northern Thailand in this study were identified as P. spongiosus. This identification was based on morphological characteristics and the multi-gene phylogenetic analyses. Pure cultures were isolated and the relevant suitable mycelial growth conditions were investigated. The results indicated that the fungal mycelia grew well on L-modified Melin-Norkans, and Murashige and Skoog agar all of which were adjusted to a pH of 5.0 at 30 ℃. Sclerotia-like structures were observed on cultures. The ability of this mushroom to produce fruiting bodies in the absence of a host plant was determined by employing a bag cultivation method. Fungal mycelia completely covered the cultivation substrate after 90-95 days following inoculation of mushroom spawn. Under the mushroom house conditions, the highest amount of primordial formation was observed after 10-15 days at a casing with soil:vermiculite (1:1, v/v). The primordia developed into a mature stage within one week. Moreover, identification of the cultivated fruiting bodies was confirmed by both morphological and molecular methods. This is the first record of P. spongiosus found in Thailand and its ability to form fruiting bodies without a host plant.

Keywords

References

  1. Singer R. The Agaricales in modern taxonomy. Koenigstein (Germany): Koeltz Scientific Books; 1986.
  2. Binder M, Bresinsky A. Derivation of polymorphic lineage of gasteromycetes from boletoid ancestors. Mycologia. 2002;94:85-98. https://doi.org/10.2307/3761848
  3. Wilson AW, Binder M, Hibbett DS. Diversity and evolution of ectomycorrhizal host associations in the Sclerodermatineae (Boletales, Basidiomycota). New Phytol. 2012;194:1079-1095. https://doi.org/10.1111/j.1469-8137.2012.04109.x
  4. Singer R, Araujo I, Ivory MH. The ectotrophically mycorrhizal fungi of the neotropical lowlands, especially central Amazonia. Beih Nova Hedwig. 1983;77:1-352.
  5. Watling R, Li TH. Australian boletes: a preliminary survey. Edinburgh (UK): Royal Botanic Garden; 1999.
  6. Heinemann P, Rammeloo J. Observations sur le genre Phlebopus (Boletineae). Mycotaxon. 1982;15:384-404.
  7. Li TH, Watling R. New taxa and combinations of Australian boletes. Edinburgh J Bot. 1999;56:143-148. https://doi.org/10.1017/S0960428600002419
  8. Sanmee R, Lumyong R, Dell B, et al. In vitro cultivation and fruit body formation of the black bolete, Phlebopus portentosus, a popular edible ectomycorrhizal fungus in Thailand. Mycoscience. 2010;51:15-22. https://doi.org/10.1007/S10267-009-0010-6
  9. Ji K-P, Cao Y, Zhang C-X, et al. Cultivation of Phlebopus portentosus in southern China. Mycol Progress. 2011;10:293-300. https://doi.org/10.1007/s11557-010-0700-7
  10. Pham NDH, Takahashi H, Fukiharu T, et al. Phlebopus spongiosus sp. nov. (Boletales, Boletinellaceae) with a sponge-like tissue. Mycotaxon. 2012a;119:27-34. https://doi.org/10.5248/119.27
  11. Baroni TJ, Cifuentes J, Santana BO, et al. A new species of Phlebopus (Boletales, Basidiomycota) from Mexico. North Amer Fungi. 2010;10:1-13.
  12. Pegler DN. A preliminary agaric flora of East Africa. Kew Bulletin Additional Series VI. Edinburgh (UK): Royal Botanic Garden Kew; 1977.
  13. Pegler DN. Agaric flora of Sri Lanka. Kew Bulletin Additional Series XII. Edinburgh (UK): Royal Botanic Garden Kew; 1986.
  14. Halling RE. A synopsis of Colombian boletes. Mycotaxon. 1989;34:93-113.
  15. Palacio M, Gutierrez Y, Franco-Molano AE, et al. Nuevos registros de macrohongos (Basidiomycota) para Colombia procedentes de unbosque seco tropical. Actualidades Biologicas. 2014;37:319-339.
  16. Kumla J, Hobbie EA, Suwannarach N, et al. The ectomycorrhizal status of a tropical black bolete, Phlebopus portentosus, assessed using mycorrhizal synthesis and isotopic analysis. Mycorrhiza. 2016;26:333-343. https://doi.org/10.1007/s00572-015-0672-1
  17. Calaca FJS, Magnago AC, Alvarenga RLM, et al. Phlebopus beniensis (Boletinellaceae, Boletales) in the Brazilian Cerrado biome. Rodriguesia. 2018;69:939-944. https://doi.org/10.1590/2175-786020186924x6
  18. Bougher NL, et al. Diversity of ectomycorrhizal fungi associated with eucalypts in Australia. In: Brundrett MC, Dell B, Malajczuk N, editors. Mycorrhizal for plantation forestry in Asia. Canberra (Australia): Australian Centre for International Agricultural Research; 1995. p. 8-15.
  19. Watling R. The relationships and possible distributional patterns of boletes in south-east Asia. Mycol Res. 2001;105:1440-1448. https://doi.org/10.1017/S0953756201004877
  20. Watling R. The sclerodermatoid fungi. Mycoscience. 2006;47:18-24. https://doi.org/10.1007/S10267-005-0267-3
  21. Mortimer PE, Karunarathna SC, Li Q, et al. Prized edible Asian mushrooms: ecology, conservation and sustainability. Fungal Divers. 2012;56:31-47. https://doi.org/10.1007/s13225-012-0196-3
  22. Thoen D, Ducousso M. Mycorrhizal habit and sclerogenesis of Phlebopus sudanicus (Gyrodontaceae) in Senegal. Agric Ecosyst Environ. 1990;28:519-523. https://doi.org/10.1016/0167-8809(90)90091-Q
  23. Pham NDH, Yamada A, Shimizu K, et al. A sheathing mycorrhiza between the tropical bolete Phlebopus spongiosus and Citrus maxima. Mycoscience. 2012b;53:347-353. https://doi.org/10.1007/s10267-011-0177-5
  24. Williams DJ. Mealybugs of southern Asia. Kuala Lumpur (Malaysia): The Natural History Museum, London, and Southdene; 2004.
  25. Zhang CX, He MX, Cao Y, et al. Fungus-insect gall of Phlebopus portentosus. Mycologia. 2015;107:12-20. https://doi.org/10.3852/13-267
  26. Thongklang N, Hyde DK, Bussaban B, et al. Culture condition, inoculum production and host response of a wild mushroom, Phlebopus portentosus strain CMUHH121-005. Maejo Int J Sci Technol. 2010;5:413-425.
  27. Kumla J, Danell E, Lumyong S. Improvement of yield for a tropical black bolete, Phlebopus portentosus, cultivation in northern Thailand. Mycoscience. 2015;56:114-117. https://doi.org/10.1016/j.myc.2014.04.005
  28. Le TTN, Tran CH, Phan MH, et al. Mycelial cultivation of Phlepobus spongiosus, an edible ectomycorrhizal mushroom in southern Vietnam. J Sci Ho Chi Minh City Open University. 2017;7:14-21.
  29. Zhang C, He M, Liu J, et al. Brief introduction to a unique edible bolete-Phlebopus portentosus in southern China. J Agri Sci Tech B. 2017;7:386-394.
  30. Chandrasrikul A, Suwanarit P, Sangwanit U, et al. Mushroom (Basidiomycetes) in Thailand. Bangkok (Thailand): Office of Natural Resources and Environmental Policy and Planning; 2011.
  31. Kornerup A, Wanscher JH. Methuen Handbook of Colour. 3rd ed. London (UK): Methuen; 1978.
  32. Vilgalys R, Hester M. Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol. 1990;172:4238-4246. https://doi.org/10.1128/jb.172.8.4238-4246.1990
  33. Rehner SA, Buckley EP. A Beauveria phylogeny inferred from nuclear ITS and EF1-alpha sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia. 2005;97:84-98. https://doi.org/10.1080/15572536.2006.11832842
  34. Matheny PB. Improving phylogenetic inference of mushrooms with RPB1 and RPB2 nucleotide sequences (Inocybe; Agaricales). Mol Phylogenet Evol. 2005;35:1-20. https://doi.org/10.1016/j.ympev.2004.11.014
  35. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792-1797. https://doi.org/10.1093/nar/gkh340
  36. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22:2688-2690. https://doi.org/10.1093/bioinformatics/btl446
  37. Ronquist F, Teslenko M, Van der Mark P, et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61:539-542. https://doi.org/10.1093/sysbio/sys029
  38. Darriba D, Taboada GL, Doallo R, et al. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 2012;9:772.
  39. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 1985;39:783-791. https://doi.org/10.2307/2408678
  40. Hillis DM, Bull JJ. An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol. 1993;42:182-192. https://doi.org/10.1093/sysbio/42.2.182
  41. Alfaro ME, Zoller S, Lutzoni F. Bayes or bootstrap? A simulation study comparing the performance of Bayesian Markov Chain Monte Carlo sampling and bootstrapping in assessing phylogenetic confidence. Mol Biol Evol. 2003;20:255-266. https://doi.org/10.1093/molbev/msg028
  42. Xu M, Zhu J, Kang H, et al. Optimum conditions for pure culture of major ectomycorrhizal fungi obtained from Pinus sylvestris var. mongolica plantations in southeastern Keerqin sandy lands. China. J Forest Res. 2008;19:113-118. https://doi.org/10.1007/s11676-008-0019-2
  43. Vaario L-M, Gill WM, Tanaka M, et al. Aseptic ectomycorrhizal synthesis between Abies firma and Cenococcum geophilum in artificial cuture. Mycoscience. 2000;41:395-399. https://doi.org/10.1007/BF02463953
  44. Brundrett MC, Bougher N, Dell B, et al. Working with mycorrhizas in forestry and agriculture. Canberra (Australia): Australian Centre for International Agricultural Research; 1996.
  45. Langer I, Krpata D, Peintner U, et al. Media formulation influences in vitro ectomycorrhizal synthesis on the European aspen Populus tremula L. Mycorrhiza. 2008;18:297-307. https://doi.org/10.1007/s00572-008-0182-5
  46. Danell E. Cantharellus. In: Cairney JWG, Chambers SM, editors. Ectomycorrhizal fungi: key genera in profile. Berlin (Germany): Springer-Verlag; 1985. p. 253-267.
  47. Ohta A, Fujiwara N. Fruit-body production of an ectomycorrhizal fungus in genus Boletus in pure culture. Mycoscience. 2003;44:295-300. https://doi.org/10.1007/S10267-003-0120-5
  48. Binder M, Hibbett DS. Molecular systematics and biological diversification of Boletales. Mycologia. 2006;98:971-981. https://doi.org/10.3852/mycologia.98.6.971
  49. Wu G, Feng B, Xu J, et al. Molecular phylogenetic analyses redefine seven major clades and reveal 22 new generic clades in the fungal family Boletaceae. Fungal Divers. 2014;69:93-115. https://doi.org/10.1007/s13225-014-0283-8
  50. Wu G, Li YC, Zhu XT, et al. One hundred noteworthy boletes from China. Fungal Divers. 2016;81:25-188. https://doi.org/10.1007/s13225-016-0375-8
  51. Boedijn KB. Some mycological notes. Sydowia. 1951;5:211-229.
  52. Bruns TD, Bidartondo MI, Taylor DL. Host specificity in ectomycorrhizal communities: what do the exceptions tell us? Integr Comp Biol. 2002;42:352-359. https://doi.org/10.1093/icb/42.2.352
  53. Martin F, Diez J, Dell B, et al. Phylogeography of the ectomycorrhizal Pisolithus species as inferred from nuclear ribosomal DNA ITS sequences. New Phytol. 2002;153:345-357. https://doi.org/10.1046/j.0028-646X.2001.00313.x
  54. Hirose D, Shirouzu T, Tokumasu S. Host range and potential distribution of ectomycorrhizal basidiomycete Suillus pictus in Japan. Fungal Ecol. 2010;3:255-260. https://doi.org/10.1016/j.funeco.2009.11.001
  55. Bahram M, Polme S, Koljalg U, et al. A single European aspen (Populus tremula) tree individual may potentially harbour dozens of Cenococcum geophilum ITS genotypes and hundreds of species of ectomycorrhizal fungi. FEMS Microbiol Ecol. 2011;75:313-320. https://doi.org/10.1111/j.1574-6941.2010.01000.x
  56. Zang M. Taxonomy, mycogeography and ectomycorrhizal association with the Boletales from China. I. Family Strobilomycetaceae. Mycosystema. 1997;16:264-269.
  57. Phosri C, Martin MP, Sihanonth P, et al. Molecular study of the genus Astraeus. Mycol Res. 2007;111:275-286. https://doi.org/10.1016/j.mycres.2007.01.004
  58. Phosri C, Watling R, Suwannasai N, et al. A new representative of star-shaped fungi: Astraeus sirindhorniae sp. nov. from Thailand. PLoS One. 2014;9:e71160. https://doi.org/10.1371/journal.pone.0071160
  59. Rossi MJ, Oliveira VL. Growth of the ectomycorrhizal fungus Pisolithus microcarpus in different nutritional conditions. Braz J Microbiol. 2011;42:624-632. https://doi.org/10.1590/S1517-83822011000200027
  60. Islam F, Ohga S. Effects of media formulation on the growth and morphology of ectomycorrhizae and their association with host plant. ISRN Agronomy. 2013;2013:1-12. https://doi.org/10.1155/2013/317903
  61. Kumla J, Danell E, Bussaban B, et al. Suitable growth conditions and nutrition factors on in vitro culture of Phlebopus portentosus (Boletales). Chiang Mai J Sci. 2011;38:156-159.
  62. Cotter HVT, Miller O. Sclerotia of Boletinellus meruloides in nature. Mycologia. 1985;77:927-931. https://doi.org/10.2307/3793304
  63. Daza A, Manjon JL, Camacho M, et al. Effect of carbon and nitrogen sources, pH and temperature on in vitro culture of several isolates of Amanita caesarea (Scop.:Fr.) Pers. Mycorrhiza. 2006;16:133-136. https://doi.org/10.1007/s00572-005-0025-6
  64. Saensuk T, Suntararak S. Mycelia cultivation 4 edible mushroom from Khao Kra-Dong volcano forest park, Thailand. NU J Sci Tech. 2018;2:38-45.
  65. Lazarevic J, Stojicic D, Keca N. Effects of temperature, pH and carbon and nitrogen sources on growth of in vitro cultures of ectomycorrhizal isolates from Pinus heldreichii forest. Forest Syst. 2016;25:e048.
  66. Yamanaka K, Namba K, Tajiri A. Fruit body formation of Boletus reticulatus in pure culture. Mycoscience. 2000;41:189-191. https://doi.org/10.1007/BF02464330
  67. Lumyong S, Sanmee R, Lumyong P. Is large scale cultivation of boletes possible? Opera Mycol. 2007;1:34-37.
  68. Kumla J, Bussaban B, Suwannarach N, et al. Basidiome formation of an edible wild, putatively ectomycorrhizal fungus, Phlebopus portentosus without host plant. Mycologia. 2012;104:597-603. https://doi.org/10.3852/11-074
  69. Kikuchi K, Matsushita N, Suzuki K. Fruit body formation of Tylopilus castaneiceps in pure culture. Mycoscience. 2009;50:313-316. https://doi.org/10.1007/S10267-009-0481-5
  70. Martos ET, Zied DC, Junqueira PPG, et al. Casing layer and effect of primordia induction in the production of Agaricus subrufescens mushroom. Agric Nat Resour. 2017;51:231-234.
  71. Salmones D, Gaitan-Hernandez R, Mata G. Cultivation of Mexican wild strains of Agaricus bisporus, the button mushroom, under different growth conditions in vitro and determination of their productivity. Biotechnol Agron Soc Environ. 2018;22:45-53.
  72. Carrasco J, Tello ML, Perez M, et al. Biotechnological requirements for the commercial cultivation of macrofungi: substrate and casing layer. In: Singh B, Lallawmsanga PA, editros. Biology of macrofungi. fungal biology. Cham (Switzerland): Springer; 2018. p. 159-175.

Cited by

  1. Secondary metabolites of Phlebopus species from Northern Thailand vol.19, pp.12, 2020, https://doi.org/10.1007/s11557-020-01643-y