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Following Citations: 7 7832 Correction Proc. Natl. Acad. Sci. USA 91 (1994) Evolution. In the article "Ancient and recent patterns of geographic speciation in the oyster mushroom Pleurotus revealed by phylogenetic analysis of ribosomal DNA se- quences" by Rytas Vilgalys and Bao Lin Sun, which ap- peared in number 10, May 10, 1994, ofProc. Natl. Acad. Sci. USA (91, 4599-4603), several references were incorrectly numbered or omitted in the paper. The citation referred to by the numbered reference on the last line ofthe first column on p. 4599 [". .. broadly distributed over one or more conti- nents (4)."] should be replaced with the following citation: 4. Vilgalys, R., Smith, A., Sun, B. L. & Miller, 0. K., Jr. (1993) Can. J. Bot. 71, 113-128. The citations referred to in Table 1 (numbered 7-13) should be replaced with the following citations: 7. Vilgalys, R., Smith, A., Sun, B. L. & Miller, 0. K., Jr. (1993) Can. J. Bot. 71, 113-128. 8. Pegler, D. N. (1977) Kew Bull. 31, 501-510. 9. Pegler, D. N. (1986) Agaric Flora ofSri Lanka (Her Majesty's Stationary Office, London). 10. Moore, R. T. (1985) Trans. Brit. Mycol. Soc. 85, 354-358. 11. Miller, 0. K., Jr. (1969) Mycologia 61, 887-893. 12. Hilber, 0. (1982) Bibl. Mycol. 87, 1-448. 13. GuzmAn, G., Bandala, V. M. & Montoya, L. (1991) Mycol. Res. 95, 1264-1269. The citations referred to in the first sentence under Discus- sion on p. 4601 [".... to delimit intersterility groups in Pleurotus (4, 7-10, 15, 27-30)."] should be replaced with the following citations: 4. Anderson, N. A., Wang, S. S. & Schwandt, J. W. (1973) Mycologia 65, 28-35. 7. Bresinsky, A., Fischer, M., Meixner, B. & Paulus, W. (1987) Mycologia 79, 234-245. 8. Cailleux, R., Diop, A. & Joly, P. (1981) Bull. Soc. Mycol. France 97, 97-124. 9. Eger, G. (1978) in The Biology and Cultivation of Edible Mushrooms, eds. Chang, S. T. & Hayes, W. A. (Academic, New York), pp. 497-519. 10. Eger, G., Li, S. F. & Leal, L. H. (1979) Mycologia 71, 577-588. 15. Hilber, 0. (1982) Bibl. Mycol. 87, 1-448. 27. Ohira, I. & Matsumoto, T. (1980) Rep. Tottori Mycol. Inst. 18, 129-132. 28. Ohira, I. (1977) Rep. Tottori Mycol. Inst. 15, 29-37. 29. Ohira, I. (1990) Rep. Tottori Mycol. Inst. 28, 143-150. 30. Petersen, R. H. & Hughes, K. W. (1992) Sydowia 45, 139-152. Downloaded by guest on September 23, 2021 Proc. Nati. Acad. Sci. USA Vol. 91, pp. 4599-4603, May 1994 Evolution Ancient and recent patterns of geographic speciation in the oyster mushroom Pleurotus revealed by phylogenetic analysis of ribosomal DNA sequences (biogeogaphy/specis concept/vcarau) RYTAS VILGALYS AND BAO LIN SUN Department of Botany, Duke University, Durham, NC 27708-0338 Communicated by John C. Avise, February 7, 1994 (receivedfor review December 9, 1993) ABSTRACT Evidence from molecular systematic studies Saprobic basidiomycetes such as Pleurotus present an ex- suggests that many mushroom species may be quite ancient. cellent system for analysis of speciation in fungi. Many Gene phylogenies were developed to examine the relationship species may be grown and fruited in pure culture, permitting between reproductive isolation, genetic divergence, and bioge- analysis of their mating relationships and other features. ography in oyster mushrooms (Plurotus). Sequence data were Phylogenetic analyses using molecular sequence data partic- obtained for two regions ofDNA from populations belonging to ularly show much promise for resolving phylogenetic rela- eight intersterility groups (biological species). Phylogenetic tionships and understanding speciation for many problematic analysis ofsequences from the 5' portion ofthe nuclear encoded species complexes in basidiomycetes (4-6). large subunit rDNA demonstrates an ancient origin for four In this study we analyzed (i) mating compatibility relation- intersterility groups of broad geographic distribution (world- ships among collections from different parts ofthe world that wide), with a more recent radiation of several intersterility reveal at least eight intersterility groups in Pleurotus and (ii) groups that are restricted to the Northern Hemisphere. An gene phylogenies for two different regions of the nuclear expanded analysis using sequence data from the more variable rDNA locus representing 38 individuals.* Molecular phylo- rDNA internal transcribed spacer region also reveals a phylo- genetic analysis reveals two groups of species in Pleurotus, genetically based pattern of genetic divergence associated with with one ancient group of broad worldwide distribution and allopatric speciation among populations from different conti- a second group of species evolving much more recently nents in the Northern Hemisphere. The ability of rDNA within the Northern Hemisphere. These results demonstrate sequences to resolve phylogenetic relationships among geo- the utility ofrDNA phylogenies for understanding patterns of graphically isolated populations within intersterility groups evolution and speciation in basidiomycete fungi within a illustrates the importance of biogeography for understanding biogeographical context. speciation in Pleurotus. Patterns of geographic distribution among intersterilit groups suggest that several species line- ages evolved quite early, with recently evolved groups re- MATERIALS AND METHODS stricted to the Northern Hemisphere and older lineages occur- Cultures and Mating Compatibility Studies. The fungal ring throughout the world. Based on phylogenetic evidence, strains used in this study are listed in Table 1 along with other analysis of historical biogeography using area cladograms data on their geographic origin and intersterility group. All shows that multiple dispersal and vicariance events are respon- strains were grown and stored on YPSS/2 agar (14). Tester sible for patterns of speciation observed. strains for determining mating compatibility relationships representing five intersterility groups were available from Speciation in many mushroom groups is often associated with previous studies (4, 15). Spore prints were obtained from tremendous levels of genetic divergence that suggest an additional strains by fruiting them on sterilized rye grain ancient origin for some species (1). Within many mushroom substrate in the laboratory. Patterns of mating compatibility species, clear patterns of morphological and genetic diver- among single-spore isolates originating from the same parent gence among geographically distinct populations also suggest (intrastock crosses) were used to determine mating system. an allopatric mode for speciation (2). The combined study of Interstock pairings among single-basidiospore isolates from phylogeny and biogeography provides a framework for un- different parent strains were used to determine the limits of derstanding the relationship among different components of additional intersterility groups. Formation of clamp connec- evolution at the species level, including geographic variation, tions in positive matings was used as the primary criterion for genetic isolation mechanisms, and morphological evolution mating compatibility (15). (3). The recent development of rigorous molecular phyloge- DNA Amplification and Sequencing. Cultures of each iso- netic approaches has made it possible to reexamine many late were grown in liquid YPSS/2 medium, and DNA mini- classic questions regarding the importance of biogeography preparations were prepared using CTAB extraction buffer as a primary factor involved in speciation. described by Zolan and Pukkila (16). PCR amplification was The oyster mushroom Pleurotus ostreatus and its related performed using reagents and primers described in Vilgalys species are among the more conspicuous fungi causing wood and Hester (17) and White et al. (19). Primers 5.8SR and LR7 decay in terrestrial ecosystems worldwide and are widely were used to amplify a 1.7- to 1.8-kb fragment of rDNA collected and cultivated as edible fungi. Mating compatibility including the internal transcribed spacer 2 (ITS-2) region and studies have demonstrated the existence of discrete interste- RNA region, and rility groups (biological species) in Pleurotus, many of which the 5' halfofthe large subunit (LSU) coding are broadly distributed over one or more continents (4). Abbreviations: indel, insertion/deletion; ITS, internal transcribed spacer; LSU, large subunit; CI, consistency index; RI, retention The publication costs ofthis article were defrayed in part by page charge index. payment. This article must therefore be hereby marked "advertisement" *The sequences reported in this paper have been deposited in the in accordance with 18 U.S.C. §1734 solely to indicate this fact. GenBank data base (accession nos. U04058-U04160). 4599 4600 Evolution: Vilgalys and Sun Proc. Natl. Acad. Sci. USA 91 (1994) Table 1. Pleurotus strains studied, with information concerning their intersterility groups, geographic origin, and other data Intersterility group Strain,* geographic origin, other culturest Comments I 261, Virginia; 403, Arizona; 850, California; 330, Includes P. ostreatus (with several varieties), presently known Czechoslovakia; 331, Czechoslovakia; 334, Germany; only from North America and northern Eurasia. Deciduous 1743, Japan (= TMI 30054); 1742, Japan (= TMI 30055) hardwood logs are the preferred substrates for this group. II 263, Virginia; 352, North Carolina; 700, British Columbia; Known in Europe as Pleurotus pulmonarius, widely distributed 479, Germany; 480, Germany; 481, Sweden; 1745, Japan across Eurasia and North America. Depending on where (= TMI 30632); 1748, Japan (= TMI 30058) they
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