Mycobiology

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

DOI QR Code

Taxonomic Revision of the Genus Lactifluus (Russulales, Basidiomycota) of South Korea

  • Lee, Hyun (School of Biological Sciences and Institute of Microbiology, Seoul National University) ;
  • Wissitrassameewong, Komsit (National Biobank of Thailand (NBT), National Science and Technology Development Agency (NSTDA)) ;
  • Park, Myung Soo (School of Biological Sciences and Institute of Microbiology, Seoul National University) ;
  • Fong, Jonathan J. (Science Unit, Lingnan University) ;
  • Verbeken, Annemieke (Ghent University, Department of Biology, Research Group Mycology) ;
  • Kim, Changmu (Biological and Genetic Resources Utilization Division, National Institute of Biological Resources) ;
  • Lim, Young Woon (School of Biological Sciences and Institute of Microbiology, Seoul National University)
  • Received : 2021.02.25
  • Accepted : 2021.06.11
  • Published : 2021.08.31
Download PDF
⟨ Previous Next ⟩

Abstract

Lactifluus (Pers.) Roussel is an ectomycorrhizal genus that was recently recognized to be distinct from the genus Lactarius. To date, 226 Lactifluus species have been reported worldwide. Misidentification of Lactifluus species is common because of intraspecific morphological variation, cryptic diversity, and the limited number of taxonomic keys available. Molecular data are indispensable for species delimitation; a multilocus phylogenetic analysis showed that most Asian Lactifluus species are not conspecific with morphologically similar species present on other continents. In particular, Korea has misused European and North American Lactifluus names. In this study, we evaluated the taxonomy of Lactifluus in Korea using both morphological and multilocus molecular (ITS, nrLSU, rpb1, and rpb2) data. We examined 199 Lactifluus specimens collected between 1980 and 2016, and a total of 24 species across the four Lactifluus subgenera were identified. All Korean species are distinct and clearly separated from European and North American species. Five taxa corresponded to previously described species from Asia and the remaining 19 taxa are confirmed as new species. Herein, we provide keys to the Korean Lactifluus species within their subgenera, molecular phylogenies, a summary of diversity, and detailed description of the new species.

Keywords

Acknowledgement

The authors thank Dr. Soon Ja Seok, Prof. Jong Kyu Lee, and Dr. Sang Kuk Han for providing specimens. We also greatly appreciate Dr. Xiang-Hua Wang to improve our manuscript through detailed comments.

References

  1. Buyck B, Hofstetter V, Eberhardt U, et al. Walking the thin line between Russula and Lactarius: the dilemma of Russula subsect. Ochricompactae. Fungal Divers. 2008;28:15-40.
  2. Buyck B, Hofstetter V, Verbeken A, et al. Proposal 1919: To conserve Lactarius nom. Cons. (Basidiomycota) with avconserved type. Taxon. 2010;59(1):295-296. https://doi.org/10.1002/tax.591031
  3. McNeill J, Turland NJ, Monro AM, et al. XVIII International Botanical Congress: Preliminary mail vote and report of Congress action on nomenclature proposals. Taxon. 2011;60(5):1507-1520. https://doi.org/10.1002/tax.605034
  4. Verbeken A, Nuytinck J. Not every milkcap is a Lactarius. Scr Bot Bel. 2013;51:162-168.
  5. De Crop E, Nuytinck J, Van de Putte K, et al. A multi-gene phylogeny of Lactifluus (Basidiomycota, Russulales) translated into a new infrageneric classification of the genus. Persoonia. 2017;38:58-80. https://doi.org/10.3767/003158517X693255
  6. De Crop E, Delgat L, Nuytinck J, et al. A short story of nearly everything in Lactifluus (Russulaceae). Fungal Syst Evol. 2021;7(1):133-164. https://doi.org/10.3114/fuse.2021.07.07
  7. Verbeken A, Walleyn R. Monograph of Lactarius in tropical Africa. Fungus Flora of Tropical Africa. National Botanic Garden, Belgium. 2010;2.
  8. Le HT, Verbeken A, Nuytinck J, et al. Lactarius in Northern Thailand: 3. Lactarius Subgenus Lactoriopsis. Mycotaxon. 2007;102:281-291.
  9. Stubbe D, Nuytinck J, Verbeken A. Critical assessment of the Lactarius gerardii species complex (Russulales). Fungal Biol. 2010;114(2-3):271-283. https://doi.org/10.1016/j.funbio.2010.01.008
  10. Van de Putte K, Nuytinck J, Stubbe D, et al. Lactarius volemus sensu lato (Russulales) from northern Thailand: morphological and phylogenetic species concepts explored. Fungal Divers. 2010;45(1):99-130. https://doi.org/10.1007/s13225-010-0070-0
  11. Wang XH, Stubbe D, Verbeken A. Lactifluus parvigerardii sp. nov., a new link towards the pleurotoid habit in Lactifluus subgen. Gerardii (Russulaceae, Russulales). Cryptogam Mycol. 2012; 33(2):181-190. https://doi.org/10.7872/crym.v33.iss2.2012.181
  12. Wang X-H, Buyck B, Verbeken A, et al. Revisiting the morphology and phylogeny of Lactifluus with three new lineages from southern China. Mycologia. 2015;107(5):941-958. https://doi.org/10.3852/13-393
  13. Henkel TW, Aime MC, Miller SL. Systematics of pleurotoid Russulaceae from Guyana and Japan, with notes on their ectomycorrhizal status. Mycologia. 2000;92(6):1119-1132. https://doi.org/10.2307/3761479
  14. Miller SL, Aime MC, Henkel TW. Russulaceae of the Pakaraima Mountains of Guyana. I. New species of pleurotoid Lactarius. Mycologia. 2002;94(3): 545-553. https://doi.org/10.2307/3761789
  15. Smith ME, Henkel TW, Aime MC, et al. Ectomycorrhizal fungal diversity and community structure on three co-occurring leguminous canopy tree species in a Neotropical rainforest. New Phytol. 2011;192(3):699-712. https://doi.org/10.1111/j.1469-8137.2011.03844.x
  16. Sa MCA, Baseia IG, Wartchow F. Lactifluus dunensis, a new species from Rio Grande do Norte. Brazil. Mycosphere. 2013;4(2):261-265. https://doi.org/10.5943/mycosphere/4/2/9
  17. Sa MCA, Wartchow F. Lactifluus aurantiorugosus (Russulaceae), a new species from Southern Brazil. Darwiniana, Nueva Serie. 2013;1(1):54-60.
  18. Crous PW, Wingfield MJ, Burgess TI, et al. Fungal Planet description sheets: 625-715. Persoonia. 2017;39(715):270-467.
  19. Sa MCA, Delgat L, Verbeken A, et al. A new species of Lactifluus (Russulales, Agaricomycetes) from the Brazilian caatinga semiarid region. N Z J Botan. 2019;57(3):169-110. https://doi.org/10.1080/0028825X.2019.1587474
  20. Delgat L, Dierickx G, De Wilde S, et al. Looks can be deceiving: the deceptive milkcaps (Lactifluus, Russulaceae) exhibit low morphological variance but harbour high genetic diversity. IMA Fungus. 2019;10(1):14. https://doi.org/10.1186/s43008-019-0017-3
  21. Bok JD, Shin GC. Taxonomic Studies on the Genus Lactarius of Korea (I). Kor J Mycol. 1985; 13(4):249-262.
  22. Lee YS, Lim YW, Kim JJ, et al. 2015. National list of species of Korea: Basidiomycota. National Institute of Biological Resources, Korea. 364 pp.
  23. Hyde KD, Norphanphoun C, Abreu VP, et al. Fungal divers notes 603-708: taxonomic and phylogenetic notes on genera and species. Fungal Divers. 2017;87(1):1-235. https://doi.org/10.1007/s13225-017-0391-3
  24. Lee H, Park JY, Wisitrassameewong K, et al. First report of eight milkcap species belonging to Lactarius and Lactifluus in Korea. Mycobiology. 2018;46(1):1-12. https://doi.org/10.1080/12298093.2018.1454012
  25. Van de Putte K, Nuytinck J, Das K, et al. Exposing hidden diversity by concordant genealogies and morphology - a study of the Lactifluus volemus (Russulales) species complex in Sikkim Himalaya (India). Fungal Divers. 2012;55(1):171-194. https://doi.org/10.1007/s13225-012-0162-0
  26. Van de Putte K, Nuytinck J, De Crop E, et al. Lactifluus volemus in Europe: three species in one-Revealed by a multilocus genealogical approach, Bayesian species delimitation and morphology. Fungal Biol. 2016;120(1):1-25. https://doi.org/10.1016/j.funbio.2015.08.015
  27. Boa E. 2004. Wild Edible Fungi. A Global Overview of Their Use and Importance to People. Non-Wood Forest Products 17. FAO, Rome.
  28. Colak A, Faiz O, Sesli E. Nutritional composition of some wild edible mushrooms. Turk J Biochem. 2009;34(1):25-31.
  29. Garibay-Orijel R, Cifuentes J, Estrada-Toress A, et al. People using macro-fungal diversity in Oaxaca. Mexico. Fungal Divers. 2006;21:41-67.
  30. Garibay-Orijel R, Caballero J, Estrada-Toress A, et al. Understanding cultural significance, the edible mushrooms case. J Ethnobiol Ethnomed. 2007;3:4. https://doi.org/10.1186/1746-4269-3-4
  31. Christensen M, Bhattarai S, Devkota S, et al. Collection and use of wild edible fungi in Nepal. Econ Bot. 2008;62(1):12-23. https://doi.org/10.1007/s12231-007-9000-9
  32. Dell B, Sanmee R, Lumyong P, et al. 2005. Ectomycorrhizal fungi in dry and wet dipterocarp forests in northern Thailand - diversity and use as food. Asia Pacific Association of Forestry Research Institutions (APAFRI). 8th Round-Table Conference on Dipterocarps. Ho Chi Minh, Vietnam
  33. Wang XH, Liu P, Yu F. 2004. Color atlas of wild commercial mushrooms in Yunnan (in Chinese). Yunnan Science and Technology Press, Yunnan.
  34. Daniewski WM, Gumulka M, Przesmycka D, et al. Sesquiterpenes of Lactarius origin, antifeedant structure-activity relationships. Phytochemistry. 1995;38(5):1161-1168. https://doi.org/10.1016/0031-9422(94)00781-N
  35. Mooibroek H, Cornish K. Alternative sources of natural rubber. Appl Microbiol Biotechnol. 2000; 53(4):355-365. https://doi.org/10.1007/s002530051627
  36. Tanaka Y. Structural characterization of natural polyisoprenes: solve the mystery of natural rubber based on structural study. Rubber Chemistry and Technology. 2001;74(3):355-375. https://doi.org/10.5254/1.3547643
  37. Eberhardt U. Molecular kinship analyses of the agaricoid Russulaceae: correspondence with mycorrhizal anatomy and sporocarp features in the genus Russula. Mycol Prog. 2002;1(2):201-223. https://doi.org/10.1007/s11557-006-0019-6
  38. Miller SL, Buyck B. Molecular phylogeny of the genus Russula in Europe with a comparison of modern infrageneric classifications. Mycol Res. 2002;106(3):259-276. https://doi.org/10.1017/S0953756202005610
  39. Matheny PB, Liu YJ, Ammirati JF, et al. Using RPB1 sequences to improve phylogenetic inference among mushrooms (Inocybe, Agaricales). Am J Bot. 2002;89(4):688-698. https://doi.org/10.3732/ajb.89.4.688
  40. Matheny PB. Improving phylogenetic inference of mushrooms with RPB1 and RPB2 nucleotide sequences (Inocybe; Agaricales). Mol Phylogenet Evol. 2005;35(1):1-20. https://doi.org/10.1016/j.ympev.2004.11.014
  41. Stubbe D, Le HT, Wang XH, et al. The Australasian species of Lactarius subgenus Gerardii (Russulales). Fungal Divers. 2012;52(1):141-167. https://doi.org/10.1007/s13225-011-0111-3
  42. De Crop E, Nuytinck J, Van de Putte K, et al. Lactifluus piperatus (Russulales, Basidiomycota) and allied species in Western Europe and a preliminary overview of the group worldwide. Mycol Prog. 2014;13(3):493-511. https://doi.org/10.1007/s11557-013-0931-5
  43. Hesler LR, Smith AH. 1979. North American species of Lactarius. University of Michigan Press, Ann Arbor, 841. pp.
  44. Heilmann-Clausen J, Verbeken A, Vesterholt J. The Genus Lactarius: Fungi of Northern Europe. Svampetryk, Mundelstrup, DK. 1998;2
  45. Pegler DN, Fiard JP. Taxonomy and ecology of Lactarius (Agaricales) in the Lesser Antilles. Kew Bull . 1979;33(4):601-628. https://doi.org/10.2307/4109804
  46. Singer R, Araujo I, Ivory MH. The ectotropically mycorrhizal fungi of the neotropical lowlands, especially Central Amazonia. (Litter decomposition and ectomycorrhiza in Amazonian forests 2.) Beihefte zur. Nova Hedwigia. 1983;77:1-352. https://doi.org/10.1127/0029-5035/2003/0077-0001
  47. Lee H, Wissitrassameewong K, Park MS, et al. Taxonomic revision of the genus Lactarius (Russulales, Basidiomycota) in Korea. Fungal Divers. 2019;95(1):275-335. https://doi.org/10.1007/s13225-019-00425-6
  48. Kornerup A, Wanscher JH. 1978. Methuen Handbook of colour., 3rd ed. Eyre Methuen Ltd., London.
  49. Rogers SO, Bendich AJ. 1994. Extraction of total cellular DNA from plants, algae and fungi. In: Gelvin SB, Schilperoort RA (eds), Plant molecular biology manual. Kluwer Academic Publisher, Boston. pp 183-190.
  50. Rozen S, Skaletsky HJ. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol. 2000;132:365-386.
  51. Tamura K, Stecher G, Peterson D, et al. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30(12):2725-2729. https://doi.org/10.1093/molbev/mst197
  52. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013; 30(4):772-780. https://doi.org/10.1093/molbev/mst010
  53. Miller MA, Pfeiffer W, Schwartz T. 2010. Creating the CIPRES Science Gateway for Inference of Large Phylogenetic Trees. SC10 Workshop on Gateway Computing Environments (GCE10).
  54. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30(9):1312-1313. https://doi.org/10.1093/bioinformatics/btu033
  55. Darriba D, Taboada GL, Doallo R, et al. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 2012;9(8):772.
  56. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19(12):1572-1574. https://doi.org/10.1093/bioinformatics/btg180
  57. Rambaut A, Suchard M, Xie W, et al. 2014. Tracer v. 1.6. Institute of Evolutionary Biology. Edinburgh. Available from: http://tree.bio.ed.ac.uk/software/tracer/.
  58. Bon M. Un nouveau lactaire de la section Plinthogali (Burl. Sing. - Lactarius Brunneo-Violascens Bon n. sp. Documents Mycologiques (in French. 1971;1(2):45-48.
  59. Stubbe D, Verbeken A, Wang XH. New combinations in Lactifluus. 2. Lf. subgenus Gerardii. Mycotaxon. 2012;119(1):483-485. https://doi.org/10.5248/119.483
  60. Das K, Sharma JR, Verbeken A. New species of Lactarius from Kumaon Himalaya. India. Mycotaxon. 2003;88:333-342.
  61. Lee YW. Higher fungi of Dagelet Island (forest experiment station). Korean Journal of Botany. 1959;2:22-24.
  62. Ko PY, Lee HB, Lee SH, et al. New records of fungi growing on Jejudo. Korean Journal of Mycology. 2015;43(3):142-148. https://doi.org/10.4489/KJM.2015.43.3.142
  63. Verbeken A. New Taxa of Lactarius (Russulaceae) in Tropical Africa. Bull Jard Bot Natl Belg. 1996; 65(1/2):197-213. https://doi.org/10.2307/3668185
  64. Verbeken A, Stubbe D, Nuytinck J. Two new Lactarius species from Cameroon. Cryptogamie Mycologie. 2008;29:137-143.
  65. Miller SL, Aime MC, Henkel TW. Russulaceae of the Pakaraima Mountains of Guyana 2. New species of Russula and Lactifluus. Mycotaxon. 2013;121(1):233-253. https://doi.org/10.5248/121.233
  66. Morozova OV, Popov ES, Kovalenko AE. Studies on mycobiota of Vietnam II. Two Species of Lactifluus (Russulaceae) with Pleurotoid Basidiomata. Mikol Fitopatol. 2013;47(2):92-102.
  67. Latha KPD, Raj KNA, Farook VA, et al. Three new species of Russulaceae from India based on morphology and molecular phylogeny. Phytotaxa. 2016;246(1):61-77. https://doi.org/10.11646/phytotaxa.246.1.5
  68. De Crop E, Hampe F, Wisitrassameewong K, et al. Novel diversity in Lactifluus section Gerardii from Asia: five new species with pleurotoid or small agaricoid basidiocarps. Mycologia. 2018;110(5): 962-984. https://doi.org/10.1080/00275514.2018.1508979
  69. Singer R. Tropical Russulaceae. II. Lactarius section Panuoidei. Nova Hedwigia. 1984;40(1-4): 435-447.
  70. Murata M, Kanetani S, Nara K. Ectomycorrhizal fungal communities in endangered Pinus amamiana forests. PloS One. 2017;12(12):e0189957. https://doi.org/10.1371/journal.pone.0189957
  71. Murata M, Kinoshita A, Nara K. Revisiting the host effect on ectomycorrhizal fungal communities: implications from host-fungal associations in relict Pseudotsuga japonica forests. Mycorrhiza. 2013; 23(8):641-653. https://doi.org/10.1007/s00572-013-0504-0
  72. Sakamoto Y, Yokoyama J, Maki M. Mycorrhizal diversity of the orchid Cephalanthera longibracteata in Japan. Mycoscience. 2015;56(2):183-189. https://doi.org/10.1016/j.myc.2014.06.002