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Department of Plant & Microbial Biology, University of California at Berkeley, 111 Koshland Hall, No. 3102, Berkeley, California 94720-3102
Rogier P. J. de Kok
Centre for Plant Biodiversity Research, Australian National Herbarium, CSIRO Plant Industry, G.P.O. Box 1600, Canberra, Australian Capital Territory 2601, Australia
Thomas D. Bruns
Department of Plant and Microbial Biology, University of California at Berkeley, 111 Koshland Hall, No. 3102, Berkeley, California 94720-3102
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ABSTRACT |
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The position and composition of Macrolepiota within the Agaricaceae and its phylogenetic relationships with other members of the family were investigated, using both molecular (ITS and LSU rDNA sequences) and morphological characters. The molecular data separate the genus into two clades. The first clade comprises M. procera, M. mastoidea, M. clelandii and allies and is a sister group of Leucoagaricus and Leucocoprinus. The second, more diverse, clade, with M. rachodes and allies, M. globosa, Chlorophyllum molybdites, Leucoagaricus hortensis and Endoptychum agaricoides, is a sister group of Agaricus. The separation of the two clades is supported by morphological characters, such as the structure of the pileus covering, the stipitipellis and the shape of the germ pore and the spore apex. The two clades are regarded as genera for which the names Macrolepiota and Chlorophyllum are proposed. Macrolepiota nympharum does not belong to either clade but is assigned to the genus Leucoagaricus, close to L. leucothites. Endoptychum depressum is transferred to the genus Agaricus as A. inapertus.
Key words: Agaricaceae, Chlorophyllum, Endoptychum, ITS and LSU rDNA, phylogeny
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, Johnson 1999, Moncalvo et al 2000, 2002). The molecular data support Singer's morphological concept of the family (1986), although tribus Cystodermatae was excluded and the family Lycoperdaceae was included (Kirk et al 2001, Moncalvo et al 2002). A separate family for the white-spored taxa, Lepiotaceae Over., as advocated by some authors, was ruled out by the molecular data. However, relationships within the family Agaricaceae remained largely unresolved, due to the small sample of this diverse family, conservatively estimated to comprise more than 900 species (Kirk et al 2001).
In the studies of Johnson (1999) and Johnson and Vilgalys (1998), Macrolepiota comprising five species, is polyphyletic but taxonomic conclusions were not drawn. Morphologically, Macrolepiota has been recognized by these characters: big and fleshy basidiocarps; hymenidermal or trichodermal universal veil that splits up into coarse-to-fine squamules on the pileus; an often complicated, double annulus, and white-to-pink, thick-walled spores with a germ pore that are dextrinoid, metachromatic in Cresyl blue and congophilous. The lamella trama is trabecular (Buller 1924, Heinemann 1989, Clémençon 1997), a character shared with Leucoagaricus Singer, Leucocoprinus Pat., and Chlorophyllum Mass.
Several genera are very similar to Macrolepiota. Chlorophyllum differs only in the distinctly green or ochre spores; these colors obscure the staining reactions of the spores. The genus Chlorolepiota Sathe & Deshpande (1979) hypothetically occupies an intermediate position between Chlorophyllum and Macrolepiota because the spore print is primrose yellow and the spores are provided with a germ pore but are not truncate; clamp connections are said to be absent. Volvolepiota Singer also closely resembles Macrolepiota; a volva is present, the pileus covering is trichodermal, clamp connections are present (in the context of the stipe) and the spores have a germ pore (Heinemann and De Meijer 1996).
The position of Leucoagaricus hortensis (Murrill) Pegler is anomalous and has been the subject of recent discussion (Akers and Sundberg 1997, Johnson 1999). This species was placed in the genus Leucoagaricus by Pegler (1983) because the spores lack a germ pore; yet clamp connections are present, a character state that does not occur elsewhere in the genus Leucoagaricus. The structure of the veil resembles that found in Macrolepiota rachodes (Vittad.) Singer.
The secotioid genus Endoptychum was considered a member of the Agaricaceae by some authors (e.g., Moser 1983). Singer (1986), on the other hand, regarded it as a Gasteromycete and as such an ancestor of the Agaricales.
Two competing infrageneric classifications of the genus Macrolepiota have been proposed: i) a division into two sections based on the presence or absence of clamp connections in which section Macrolepiota has clamp connections and section Macrosporae (Singer) Bon is lacking clamp connections in the trama (Singer 1986, Candusso and Lanzoni 1990, Ballero and Contu 1991, though the last authors treated Macrolepiota and Lepiota as belonging to one genus); ii) a classification with three sections, Macrolepiota, Macrosporae and Laevistipedes (Pázmány) Bon (Bon 1993), based on diverse macroscopical and microscopical characters, such as the shape of the spore and the germ pore, the structure of the annulus and the covering of the stipe. According to Singer's (1986) classification, M. rachodes and M. procera belong to the same section, though according to the molecular analyses of Johnson (1999), and our own, these taxa belong to different lineages.
Several toxic species are known within Macrolepiota and Chlorophyllum, and a natural question is whether these species form one clade, setting them apart from the edible species, sharing characters that facilitate recognition and medical treatment. Chlorophyllum molybdites (G. Meyer : Fr.) Mass. causes gastro-intestinal problems and is a particular threat to children, because it frequents lawns and other man-made habitats in tropical, subtropical areas and other places with humid summers. It is very common in urban and suburban areas in the eastern and southern parts of the United States. An extensive list of references to this species and its toxicity can be found in Reid and Eicker (1991). The toxic component of this species is unknown (Lehmann and Khazan 1992). Endoptychum agaricoides Czern. caused hemolytic anemia in a dog, which had eaten a mature basidiocarp (DE Desjardin pers obs). Macrolepiota neomastoidea (Hongo) Hongo and M. venenata Bon are reportedly toxic (in the case of the former, by Yokoyama and Yamaji 1981; in the case of the latter, by Bon et al 1979, Mazzolai 1989), whereas many other species, especially M. rachodes and M. procera, are considered excellent edibles. Some species are commercially grown or sold in cultivation kits. Arora (1986) suspected that Leucoagaricus hortensis (as Lepiota humei) might be very toxic, but this species is sold on the market in Bolivia (E Boa pers obs; identification by senior author).
Some Macrolepiota species are widespread, and reported from all over the world, others, such as M. excoriata (Schaeff. : Fr) Wasser, and M. phaeodisca Bellù, are restricted in their area of distribution (Courtecuisse and Duhem 1994, Nauta and Vellinga 1995; resp. Candusso and Lanzoni 1990). Many species occur in man-made habitats, such as gardens, lawns, compost-heaps; others occur in grasslands or open places in woods. There are striking disparities in the number of species in different areas. These differences are genuine and are not artifacts of the extent to which they have been studied or of taxonomic perspective. Western Europe is rich, with 11 to 19 species recorded, depending on the author. In North America, on the other hand, only two species generally are recorded, although the true number might be seven (senior author pers obs). Despite the fact that many species form big, conspicuous basidiocarps, several species are still undescribed. It is important to note that European names often have been applied prematurely to similar-looking species in other parts of the world, complicating clear understanding of this group. For example, the name M. procera has been misapplied to a North American entity (designated M. spec. nov. 5 in this study) and to the Australian M. clelandii Grgur. (Grgurinovic 1997).
This study has three themes. First, it focuses on phylogeny of Macrolepiota as inferred from ribosomal DNA data and how this phylogeny relates to the classification, based on morphology; second, on the placement of the taxa within the family Agaricaceae; and third, on the relationship of the secotioid genus Endoptychum Czern. to the Agaricaceae. In the course of the study several new taxa were discovered; they will be described separately. Many collections from a large area (including representatives from Africa, and Australia) were examined, and ITS and LSU sequences, and morphological characters were used. The choice deliberately was made to use a high number of taxa and samples instead of data from other genes from a small sample (e.g., Greybeal 1998).
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MATERIAL AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) or to putative species in this group were used for molecular screening, along with an additional seven sequences, which were accessed through Genbank. These 99 collections represent at least 24 taxa or monophyletic species complexes, and one sample of each (i.e., 24 in total) was arbitrarily chosen from each set of sequences with up to five differences in base pairs and used in these analyses; in a few cases the ITS sequence was taken from a different specimen than the LSU-sequence. Material of 28 species representing the genera Agaricus, Allopsalliota, Endoptychum, Lepiota, Leucoagaricus, Leucocoprinus, and Micropsalliota was used for comparison (see Table I for collections and species analyzed).
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) for the ITS region, and primers LR0R, LR3R, LR7, and LR16 for LSU (see http://www.biology.duke.edu/fungi/mycolab/primers.htm). Sequencing of both strands was performed with an ABI model 377 sequencer (Applied Biosystems, Foster City, CA, U.S.A.) using a Thermo SequenaseTM Dye terminator Cycle Sequencing Pre-Mix Kit (Amersham Pharmacia Biotech, Piscataway, NJ, U.S.A.) or a BigDyeTM Terminator Cycle Sequencing Ready Reaction Kit (Applied Biosystems Co.); the primers ITS1 or ITS5, ITS2, ITS3, and ITS4 were used for the ITS region, and primers LR0R, LR3R, LR7, and LR16 for the LSU-region. Raw data were processed with DNA Sequencing Analysis v.2.1.2 and Sequence Navigator v.1.0.1 (also of Applied Biosystems). The sequences thus obtained were aligned in ClustalW (Thompson et al 1994), with these settings: opening gap penalty 10, end gap penalty 10, extending gap and separation gap penalty both 0.05. Visual alignment was the next step. The alignments have been deposited in TreeBASE under number S782. Sequences have been deposited in Genbank, and the accession numbers are given in Table I. Morphological data – Nine morphological character states were scored for all taxa and added to the databases (Table II).
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). One hundred heuristic searches were conducted with random sequence addition and tree bisection-reconnection (TBR) branch-swapping algorithms, collapsing zero-length branches and saving all minimal-length trees (MulTrees) on different datasets (ITS data, LSU sequences, and ITS and LSU combined). Three members of tribus Lepioteae, L. brunneoincarnata, L. cristata and L. rufipes, were chosen as outgroup. Noninformative characters and part of the ITS1 region (190 base pairs) that was not unambiguously alignable were excluded from the analyses. Gaps were treated as missing data. To measure relative support for the resulting clades, 500 bootstrap replications (Felsenstein 1985) were performed with the same parameters as for the parsimony analyses.
To test alternative phylogenetic relationships, the Kishino-Hasegawa maximum-likelihood ratio test (Kishino and Hasegawa 1989) was performed, as implemented in PAUP* with default settings, under the model developed by Hasegawa et al (1985). The hypotheses tested are enumerated in Table III under results.
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RESULTS |
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Four lineages were recovered (Fig. 1): (i) Lineage 1, composed of Agaricus, Micropsalliota, and Endoptychum depressum. (ii) Lineage 2 included M. rachodes and allies, M. neomastoidea, Chlorophyllum molybdites, M. globosa, Endoptychum agaricoides and Leucoagaricus hortensis. This lineage shows relatively long branches. Lineages 1 and 2 are sister groups of each other. (iii) Lineage 3 to which Leucoagaricus and Leucocoprinus species belonged. (iv) Lineage 4 comprising M. procera, M. mastoidea, M. excoriata, and allies; the branches within this lineage in general are short.
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The topological constraint enforcing Macrolepiota sensu Singer (1986), i.e., without Chlorophyllum molybdites and M. globosa, without Leucoagaricus hortensis, and without Endoptychum agaricoides, does not yield a less likely tree (Table III). But, enforcing Leucoagaricus hortensis with Lineage 3 has to be rejected (P < 0.05). Significantly less likely than the best tree are the options in which Endoptychum agaricoides is excluded from Lineage 2, Macrolepiota nympharum is included in Macrolepiota, or E. depressum and E. agaricoides form a monophyletic group. A position of Macrolepiota (lineages 2 and 4 together) together with Lineage 3 (Leucocoprinus and Leucoagaricus), is significantly worse than the option of a monophyletic group of lineages 1, 2 and 4, which is the most likely topology recovered.
Analyses of LSU dataset – The aligned dataset shows a total of 934 characters, of which 82 are parsimony informative. One hundred most-parsimonious trees, occurring in four islands, were recovered (l = 225). Only a few distinct lineages were recognized in all four: Agaricus and Endoptychum depressum; the group of M. rachodes; M. procera plus two closely related species; all other species are paraphyletic throughout the phylogram, in different topologies (the tree with the highest -ln likelihood value is given in Fig. 2). The consensus tree also is highly unresolved, and only the lineages of Micropsalliota and Allopsalliota, Leucoagaricus meleagris and L. americanus, and L. leucothites and M. nympharum respectively have a bootstrap support higher than 70% (consensus tree not shown; bootstrap values given in Fig. 2).
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, enforcing the two Endoptychum species together and enforcing a monophyletic clade containing all Macrolepiota, Chlorophyllum, and Agaricus species are significantly less likely.
Analyses of the combined ITS and LSU dataset –
The combined dataset was tested for incongruence with the partition homogeneity test, as implemented in PAUP* 4.0b8, as advocated by Cunningham (1997). The original ITS-dataset was incongruent with the LSU-dataset (P = 0.0200), because of the placement of Allopsalliota geesterani. This species is a sister species of Micropsalliota spec. in the phylogram, based on the LSU-data set, but appears in the Leucoagaricus-Leucocoprinus lineage in the analyses of the ITS-data set. The position of this species based on morphological characters is also rather enigmatic; it shares characters with Agaricus and Micropsalliota (Nauta 1999) and has some chemical reactions in common with Leucoagaricus americanus and its allies. A similar situation was found in the analyses of several molecular datasets illuminating the phylogeny of the tribus Triticeae within the Gramineae (Mason-Gamer and Kellogg 1996), where the position of Triticum monococcum caused incongruence. After removal of A. geesterani in these datasets, the two datasets were congruent (P = 0.4100) and were used for further analysis.
The combined dataset of ITS and LSU sequences yields 287 parsimony-informative characters (out of 1883); 20 most-parsimonious trees could be recovered, with a length of 988 (CI = 0.4615, CR = 0.2969), and all show the same four lineages as derived from the ITS-data set (the strict consensus tree is given in Fig. 3). These phylograms differ from the ones based on ITS data only in the fact that lineages 3 and 4 are now sister groups. Leucoagaricus hortensis is a sister taxon of the Endoptychum agaricoides-Chlorophyllum clade in half of the phylograms, and a sister group to the M. rachodes clade in the other 10 phylograms. The bootstrap support for Lineage 1 is 100%, 75% for Lineage 2, and 95% for Lineage 4; again Lineage 3 gets very low bootstrap support (<50 %). All four lineages are present in the consensus tree (Fig. 3) in the same topology as in the individual most parsimonious trees.
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Adding morphological data to the data set or treating the gaps as fifth characters does not change the topology of the trees (data not shown), although bootstrap values might change slightly.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The phylograms based on the ITS sequences, and ITS-LSU-data (Figs. 1 and 3), show two distinct clades within Macrolepiota, viz. lineages 2 and 4, which do not form a monophyletic group. However, topological constraints forcing the two lineages together (analyses of all three data sets) that result in one monophyletic "big" Macrolepiota clade is neither significantly better, nor worse, than the two-clade option. These alternatives cannot be discriminated on the present molecular grounds alone.
Morphological considerations –
The number of morphological characters of mushrooms available for a phylogenetic analysis on the generic level is unfortunately very small in general. Nevertheless, several morphological characters do support recognition of lineages 2 and 4 at genus level. (i) The veil structure is hymenidermal in Lineage 2 (with clavate to lageniform terminal elements) versus trichodermal (all elements cylindrical and elongate) in Lineage 4; (ii) a stipe covering is absent in Lineage 2, although present in all taxa of Lineage 4, giving the stipes of the species a striking, banded appearance; (iii) the spores of the taxa of Lineage 2 lack either a germ pore, or have a truncate to rounded apex, without a hyaline cap covering the germ pore; the pore is caused by a depression of the episporium (Meléndez-Howell 1967); the spores of the Lineage 4 taxa always have a rounded apex, with a germ pore, covered by a hyaline cap; the germ pore in this case is caused by an interruption of the episporium, and it is filled by a refringent plug (Meléndez-Howell 1967).
The data suggest that representatives of Lineage 2 are more thermophilic or thermotolerant than those of Lineage 4. Lineage 2 includes species with a wide distribution in the tropics, or with a preference for compost heaps.
All agaricoid taxa of lineages 2 and 4 share the general Macrolepiota features: The basidiocarps are relatively big and fleshy (though the two undescribed taxa basal to Lineage 4 form relatively small basidiocarps), with a more or less complex annulus on the stipe, made up of both universal and partial veil remnants. The spores of all taxa are ellipsoid to amygdaloid-ellipsoid, and relatively large (8.0–22 µm long).
Presence or absence of clamp connections previously was considered a good character to distinguish sections within the genus Macrolepiota (Singer 1986, Pázmány 1985). In our observations, clamp connections were found, at least at the base of the basidia, in almost all investigated taxa of Lineage 4 (they are absent to rare in collections belonging to the complex of M. mastoidea (Vellinga 2001)). Clamp connections are absent or rare in some taxa of Lineage 2, e.g., Chlorophyllum molybdites (Sundberg 1971), and absent in others (M. venenata, E. agaricoides, and M. spec. nov. A (senior author pers obs). In short, clamp connections are present and absent in both lineages, as indicated in Fig. 3, and clearly this character cannot be used to distinguish the two lineages.
Taxonomic implications – Morphological characters, particularly features of the covering layers, and the spore apex, provide the decisive factor to rule out the "big" Macrolepiota clade alternative and to regard the two lineages as separate genera.
Lineage 4 comprises the type species of Macrolepiota, M. procera, and keeps the name Macrolepiota. Macrolepiota in this restricted sense comprises section Macrolepiota and section Macrosporae with subsections Excoriatae Bon and Microsquamatae (Pázmány) Bellù & Lanzoni of the infrageneric classification advocated by Bon (1993).
Lineage 2 is more diverse, with relatively long-branch lengths in the phylograms based on the sequence data, and the species morphologically are more diverse than those in Lineage 4. Lineage 2 is made up of Macrolepiota section Laevistipedes (Pázmány) Bon, M. globosa, the genus Chlorophyllum, Leucoagaricus hortensis, and Endoptychum agaricoides. Macrolepiota neomastoidea is basal to this lineage. Moreno et al (1995) concluded on morphological grounds that Chlorophyllum and Macrolepiota should be merged, the only differences between the two genera being the different spore color. The green pigments in Chlorophyllum spores obscure the staining reactions that nevertheless are similar to those of spores of Macrolepiota species. Moreno et al (1995) used the name Macrolepiota for the combined group, though the genus name Chlorophyllum (Massee 1898) predates Macrolepiota (Singer 1948) by 50 years.
Endoptychum agaricoides is the type species of the genus Endoptychum (Czernajew 1845), which means that Lineage 2 should be called Endoptychum, because it is the oldest generic name available. However, it would be infelicitous to call Lineage 2 Endoptychum, because this name is associated in usage and etymology with the secotioid habit of only one taxon in Lineage 2. Furthermore, the name is not well known and has been used for species now shown to belong to several genera (discussed further below). Vellinga and De Kok (2002) officially proposed to conserve Chlorophyllum against Endoptychum.
Akers and Sundberg (1997) placed the species Leucoagaricus hortensis in the genus Leucoagaricus on account of the absence of the germ pore, despite the presence of clamp connections. In all analyses, that position is significantly worse than including L. hortensis within Lineage 2, the M. rachodes-Chlorophyllum-Endoptychum clade.
Macrolepiota nympharum is shown to belong to neither of the two Macrolepiota lineages, but to be a sister taxon of Leucoagaricus leucothites. Migliozzi and Bizzi (1994) suggested on morphological grounds that M. nympharum (as M. puellaris) was an intermediate between Macrolepiota and Leucoagaricus. The structure of the pileus covering is much looser than in Macrolepiota species; the shape of the cheilocystidia and, in particular, the absence of clamp connections support placement in Leucoagaricus (see also Vellinga 2001).
The position of Endoptychum –
It is not a new observation that secotioid fungi do not form a monophyletic group but are either mutants of normally agaricoid taxa (Hibbett et al 1994) or recently derived from diverse agaricoid and boletoid ancestors. Endoptychum depressum and E. agaricoides both recently are derived from representatives of Agaricales, it appears. In such cases, taxonomic conclusions have been drawn in different ways. Kretzer and Bruns (1997) combined the genera Gastrosuillus Thiers and Suillus Gray, but Redhead et al (2001) kept Montagnea Fr. and Coprinus Pers. s. str. as separate genera within the Agaricaceae. Endoptychum depressum in Lineage 1 is morphologically an Agaricus species in which the lamellae are not exposed and the basidia do not actively discharge spores. It is closely related to Agaricus arvensis. The name Agaricus depressus Léveillé, used for a small marasmioid species from Java, Indonesia, predates a new combination by at least 150 years, so the new name Agaricus inapertus Vellinga is proposed; basionym: Endoptychum depressum Singer & A.H. Sm. in Brittonia 10: 216. 1958.
Endoptychum agaricoides is a sister taxon of Macrolepiota globosa and Chlorophyllum molybdites. Conard (1915) had presumed a close relationship with Agaricus campestris, because of similarities in development, although this opinion was disputed strongly by Lohwag (1924), who interpreted the agaricoid fungi as derived from secotioid forms. A relationship with Chlorophyllum already was suggested by Singer and Smith (1958), on account of similar spore colors. The spores of E. agaricoides, the secotioid member of Lineage 2, are greenish to yellowish brown under the microscope, not gray-green like the spores of Chl. molybdites. A germ pore is lacking or vaguely visible. Young, uncolored spores have all the characteristic staining reactions: red in Congo Red, blue in Cotton Blue, red-brown in Melzer's reagent, and with a pink inner wall in Cresyl Blue. Clamp connections are absent at the base of the basidia and on hyphal septa, and the hymenophoral trama hyphae are inflated, character states shared with Chl. molybdites.
Singer and Smith (1958) listed two more Endoptychum species: E. melanosporum (Berk.) Singer & A.H. Sm. with black spores, and E. arizonicum (Shear & Griffiths) Singer & A.H. Sm. with white, globose spores, and clamp connections in the trama (senior author pers obs). These taxa await sequencing for correct taxonomic placement.
Taxa other than the ones studied here putatively belonging to the Chlorophyllum lineage are M. abrubtibulba (Heim) Heinem., M. brunnea (Farlow & Burt) S. Wasser, M. venenata, M. subrhacodes Murrill, and probably Chlorolepiota mahabaleshwarensis Sathe & Deshpande.
Classification above genus level –
Current molecular data also show that recognition of two families, Lepiotaceae for the non-brown-spored taxa and Agaricaceae for brown-spored taxa, cannot be justified, just as shown in earlier papers (e.g., Johnson 1999, Moncalvo et al 2000). In fact, Lineage 2 appears to be more closely related to the brown-spored genus Agaricus than to the white-spored genera Leucoagaricus and Leucocoprinus, despite discordant morphological data, such as the structure of the trama (regular in Agaricus versus trabecular in Chlorophyllum, Macrolepiota, Leucoagaricus and Leucocoprinus) and the structure of the pileus coverings.
Classification of the family Agaricaceae into three tribus has to be reconsidered. Division into two tribus, Lepioteae and Agariceae, seems to be better supported by the current molecular data, but analysis of data in the family as a whole is better suited to resolving the intrafamilial classification. Coprinus comatus (O.F. Müll. : Fr.) Pers. and C. sterquilinus (Fr. : Fr.) Fr., and their secotioid allies Montagnea arenarius (DC.) Zeller, and Podaxis Desv. should be included in these analyses (Hopple 1994, Johnson 1999) and so should gasteroid taxa in the Lycoperdaceae (Hibbett et al 1997, Krüger et al 2001, Moncalvo et al 2002).
Molecular and morphological characters in Lineage 3, the Leucoagaricus-Leucocoprinus assemblage, are highly diverse, and our datasets do not warrant any conclusions on this lineage because a relatively small number of representatives have been chosen for a comparison with Macrolepiota and Chlorophyllum.
In conclusion – The three questions raised in the introduction now can be answered. The genus Macrolepiota has to be emended and now is restricted to species with trichodermal pileus covering, a stipe covering made up of hymeni-trichodermal patches, and spores with a rounded apex with a covered germ pore. Macrolepiota procera, M. dolichaula, M. mastoidea and allies belong here. A second genus comprises Endoptychum agaricoides, Chlorophyllum molybdites, M. globosa, Leucoagaricus hortensis and the group of M. rachodes. The agaricoid members are characterized by a hymenidermal pileus covering, a smooth stipe, and often truncate spores with an uncovered germ pore, or the germ pore might be absent. We suggest that the generic name Chlorophyllum is appropriate for this lineage, pending the outcome of a proposal submitted to Taxon. Toxic species group together in the latter genus, Although they do not constitute a separate clade. It also is shown that secotioid taxa, formerly in the genus Endoptychum, belong to different genera: E. depressum in the genus Agaricus, and E. agaricoides in Chlorophyllum (proposal pending).
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Accepted for publication September 30, 2002.
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LITERATURE CITED |
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