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Morphological and molecular characterization of two novel species of Agaricus section Xanthodermatei

     INRA, MYCSA (Mycologie et sécurité des aliments), BP 81, 33883 Villenave d’Ornon cedex, France

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS TAXONOMY DISCUSSION LITERATURE CITED

 

Agaricus specimens collected in France belong to two novel entities resembling small forms of A. moelleri and A. xanthodermus, two common species in section Xanthodermatei. Molecular (IT1+ITS2 DNA sequence) and morphological comparisons between eight presumed similar taxa of the section support the elevation of both entities to species rank. The new entities are described as A. parvitigrinus and A. xanthodermulus. They form a group with A. laskibarii, a rare species also recently described from France, and A. californicus, a North-American species. The well known A. moelleri and A. xanthodermus are the most related species among the studied sample. Like other species of the section, both new species have a phenolic odor and are probably toxic.

Key words: Basidiomycetes, Agaricus, section Xanthodermatei, ITS, systematics

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS TAXONOMY DISCUSSION LITERATURE CITED

 
Within the framework of the phylogenetic analysis of the genus Agaricus, section Duploannulati Wasser ex Wasser sensu restr. Kerrigan, Challen et Callac had been proposed (Challen et al 2003) and an analysis of the section Xanthodermatei Singer is in preparation. With this aim, during the past four years, we focussed collecting in the field species of section Xanthodermatei. Thus we collected several times in western France specimens belonging to two entities resembling respectively A. moelleri Wasser (= A. praeclaresquamosus A.E. Freeman) and A. xanthodermus Genev., but much smaller. Both names represent taxa belonging to section Xanthodermatei and are among the most abundant species of Agaricus in France. The little sporophores we collected clearly are related to section Xanthodermatei, with their phenolic odor and yellow discoloration on handling, but the small cap diameter up to 3 or 4 cm is unusual in this section. Such specimens must have be taken for A. moelleri or A. xanthodermus or for specimens of A. pseudopratensis (Bohus) Wasser, which is the only small species of section Xantodermatei known in Europe except the tropical species A. endoxanthus Berk. et Br. that recently was found in Spain (Parra et al 2002) and the not well known Psalliota nigricans Velen. We compared morphological traits and sequences of the internal transcribed spacers (ITS1 and ITS2) of the nuclear rDNA of these small specimens with a group that included (i) three taxa morphologically similar: A. moelleri, A. xanthodermus, and A. xanthodermus var. macrosporus Aparici et Mahiques; (ii) the typically small sized species A. pseudopratensis; and (iii) two small to medium size species: A. laskibarii L.A. Parra et Arrillaga and A. californicus Peck. Agaricus laskibarii is a medium size species recently described from western France (Parra and Arrillaga 2002, Arrillaga Anabitarte 2004); A. californicus is a North American species that can be small (Peck 1895, Kerrigan 1986). Of the about 20 taxa of section Xanthodermatei sequenced to date that will be treated separately in a further phylogenetic analysis of the section, only A. laskibarii and A. californicus have a sequence highly similar to those of the new entities. In addition to their small to medium size, this represents another reason to include them in the present study. We conclude that our small specimens represent collections of two novel species described here as A. parvitigrinus and A. xanthodermulus.

	MATERIALS AND METHODS

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Specimens and sequencing.— – We used 18 specimens belonging to eight taxa of section Xanthodermatei, and one specimen of A. bisporus ( J.E. Lange) Imbach (section Duploannulati) as outgroup. The origin of the samples included in this analysis and their GenBank accession numbers are listed (TABLE I). DNA sequences of A. bisporus RWK 1885 and A. californicus ecv 2139-CA already were available in GEN-BANK. The other specimens, including A. laskibarii LAPAG 115 and A. xanthodermus var. macrosporus MES 1577 (both provided by L.A. Parra), were examined at INRA Bordeaux. Except for LAPAG 115 (sequence provided by R.W. Kerrigan), sequences were obtained at INRA as follows: Tissue cultures were performed on compost-extract agar medium. DNA extraction was made from lyophilized mycelium or pieces of cap with the RPN8510 Nucleon Phytopure plant DNA extraction kit (Amersham Pharmacia Biotech). To characterize the strains with ITS1 and ITS2 sequences of the nuclear rDNA, a single product was amplified with ITS4 and ITS5 primers (White et al 1990). PCR products were sequenced directly with big dye-terminator chemistry on ABI Prism (Applied Biosystems) DNA sequencers. The region used in comparisons was confirmed by double-stranded sequence; it started 5'-TTGAATTATG, finished 5'-YTT GAATGYT and spanned a maximum length of 655 bases that included the ITS1, the 5.8S rDNA gene and the ITS2.

Dissimilarity analysis.— – Analyses were performed with the tools available in Infobiogen (http://www.infobiogen.fr/index.html). Alignment was performed with version 1.8 of Clustal W (Higgins and Sharp 1988). The distance matrix and the phenogram were performed with the DNADIST program (with the F84 model) and the Fitch program of the PHYLIP software package (Felsenstein 1993).

	RESULTS

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Phenotype analysis.— – Sporophore height (cap diameter smaller or larger than 5.5 cm), spore size (on average shorter or longer than 6.5 µm) and pileipellis aspect (squamules) are the most distinctive traits separating the taxa of section Xanthodermatei considered here, except A. californicus that can be intermediary. Morphological traits are reported (TABLE II). Cap diameter is not indicated in the original diagnosis (Genevier 1876) for A. xanthodermus, and we retained the size generally given in the literature. We must note that Wasser (2002) indicates 2–12 cm; we have never seen such small specimens of A. xanthodermus except those we describe here as A. xanthodermulus. A. xanthodermulus appears well characterized by its small cap diameter, long spores and the lack of squamules (TABLE II). Agaricus parvitigrinus is characterized by its small cap diameter and its dark gray squamules; these traits make this species easy to distinguish from all the other taxa except A. pseudopratensis, which differs by its brown squamules and the frequently rufescent flesh. More subtle traits must be examined to differentiate the latter two species (i.e., the sporophore silhouette which is spindly for A. parvitigrinus and squat for A. pseudopratensis).

View this table: [in this window] [in a new window]   TABLE II. Morphological comparison between A. parvitigrinus, A. xanthodermulus, and six other taxa of section Xanthodermatei. Morphological traits are taken from our own observations, from Agaricus monographs (Cappelli 1984, Kerrigan 1986, Nauta 2001, Wasser 2002), or from the original description of the species (Genevier 1876, Peck 1895, Aparici et Mahiques 1996, Parra et Arrillaga 2002)

View larger version (181K): [in this window] [in a new window]   FIGS. 2–7. Sporophores. 2. Agaricus parvitigrinus CA 212 in the field. 3. Agaricus parvitigrinus CA 176. 4. Agaricus parvitigrinus HOLOTYPE CA 158. 5. Agaricus xanthodermulus HOLOTYPE CA 160. 6. Agaricus xanthodermulus CA 174 in the field. 7. Agaricus xanthodermulus CA 204. Photos J. Guinberteau (2–5 and 7) et G. Dupuy (6). Scale bars: 2–7 = 5 cm.

	TAXONOMY

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS TAXONOMY DISCUSSION LITERATURE CITED

View larger version (11K): [in this window] [in a new window]   FIG. 8. Spores, basidia, and cheilocystidia of Agaricus parvitigrinus. Scale bar = 10 µm.

Pileus at first trapezoid-convex with the cap margin often pleated before the dehiscence, becoming truncately conical, later expanding to plano-convex with the discal part remaining flat, sometimes with low umbo; 1.6–5(6) cm diam and 4–5 mm thick; pilei-pellis uniformly bistre sepia at the center, gradually breaking up into appressed fibrillose squamules of less than 1 mm of width or length. These dark grayish squamules are scattered and well distinct from the white background. At maturity the center remains always bistre sepia, while the cap margin sometimes becomes completely white. On handling surface becomes yellow then ferruginous. Margin slightly exceeding the lamellae.

Lamellae free, ca. 14/cm at 1 cm from stipe, at first light pink, later grayish chocolate, margin not distinctive.

Stipe glabrous, often curved, subequal, progressively thicker toward the base that is bulbous, sometimes abruptly; 4–6(10) cm long x 3–5 mm thick (6–10 mm at the bulb); white becoming yellow then ferrugineous on handling; rhizomorphs sometimes visible.

Veils: universal veil not detected; partial veil thick, membranous, forming a pendant annulus, often with radial squamules on the underside, these occasionally arranged as a cogwheel; annulus sometimes loosened itself from the stipe.

Context white, light yellow when sectioned, fading away soon. The pileus easily breaking free from the stipe. Odor unpleasant, phenolic like ink. Schaeffer reaction negative.

Spores dark brown at maturity, cylindrical-ellipsoid, (4.6–)5.5–6.7(–7.4) x 3.4–4.4(–5.2) µm, mean = 6.0 x 3.8 µm (N = 30 x 4), L/W = 1.61; apiculus visible. Basidia tetrasporic (some bisporic), clavate, 18–25 x 7–9 µm; sterigmata 3 µm long. Cheilocystidia clavate to sphero-pedunculate, 11–21 x 5–10 µm. Presence of pileipellis hyphae entirely colored by a light brown pigment apparently parietal incrusting; dark brown vacuoles lacking.

Characteristic internal transcriber spacer polymorphism.— – The four sequenced specimens of A. parvitigrinus (CA 157, CA 158, CA 176 and CA 212) have identical ITS1 and ITS2 sequences. Agaricus parvitigrinus can be distinguished from its three neighbor species, A. laskibarii L.A. Parra et Arrillaga, A. californicus Peck and A. xanthodermulus sp. nov. (see below), by ITS polymorphisms at positions 36–38, 59, 120, 414 and 550 of its own sequence (respectively: ctggctTtCaggagc, gcctgtTtggact, ggaagcAggtcaa, cttggtGttccga and agaactAtttgcg).

Habitat, distribution, occurrence.— – Isolated, gregarious or caespitose in mixed deciduous wood (Carpinus, Robinia, Sambucus, Euonymus) on sandy alluvial soil. Western France, extent of range unknown, probably limited.

Specimens examined.— – All collections from mixed deciduous wood (Carpinus, Robinia, Sambucus, Euonymus), FRANCE, Gironde, Villandraut-Prechac: 21 Oct 2000, CA 277; 7 Oct 2001, CA 157, GENBANK xxx; 7 Oct 2001, CA 158, HOLOTYPE (LIP), GENBANK xxx; 27 Oct 2002, CA 176, GEN-BANK xxx; 15 Sep 2003, CA 212 GENBANK xxx. Mycelium cultures of CA 157, CA158 and CA 176 are available at INRA Bordeaux. All specimens were collected by J. Guinberteau; specimen CA 212 was collected with P. Callac and R.W. Kerrigan.

Etymology.— – The epithet ‘parvitigrinus’ is a contraction of ‘parvus’ and ‘tigrinus’ that respectively refers to the small size of the sporophore and to the spotted aspect of the cap with colored squamules scattered on a white background, as in the case of Lentinus tigrinus.

Agaricus xanthodermulus Callac et Guinberteau, sp. nov. FIGS. 5–7 and 9

View larger version (12K): [in this window] [in a new window]   FIG. 9. Spores, basidia, and cheilocystidia of Agaricus xanthodermulus. Scale bar = 10 µm.

Pileus at first cuboidal, helmet-shaped, becoming truncately conical to conico-convex, opening slowly and irregularly, finally expanding to plano-convex remaining plane on the disc, sometimes with a low umbo; 1.5–5(6) cm diam, 4–5 mm thick; pileipellis smooth to subglabrous, uniformly white or gray, sensitive to the environment: often discoloring in grayish brown progressively from the top to the edge, sometimes breaking up into squamules and/or radially fissured. On handling surface becomes yellow. Margin exceeding the lamellae.

Lamellae free, ca 17/cm at 1 cm from stipe, at first light pink, later grayish chocolate, margin not distinctive.

Stipe glabrous, bumpy, satiny, often flexuous and curved at the base, subequal, progressively thicker toward the bulbous base, sometimes abruptly; 3–7(10) cm long x 3–7 mm thick (6–10 mm at the bulb); white, becoming yellow on handling; rhizomorphs sometimes visible.

Veils: universal veil not detected; partial veil thick, membranous, forming a pendant annulus, sometimes with radial squamules on the underside, these occasionally arranged as a cogwheel.

Context white, light yellow, more strongly so in the bulb when sectioned, soon fading. Odor unpleasant, phenolic, like ink. Schaeffer reaction negative.

Spores dark brown at maturity, ellipsoid to oblong, (5.7–)6.6–7.8(–8.6) x (4.0)4.5–5.5(–6.3) µm, mean = 7.3 x 5.0 µm (N = 30 x 4), L/W = 1.46; apiculus visible. Basidia tetrasporic, cavate, 18–27 x 6–8 µm; sterigmata 2.5 µm long. Cheilocystidia infrequent, clavate to spheropedunculate, sometimes in chains, 12– 20 x 7–11 µm.

Characteristic internal transcriber spacer polymorphism.— – The four examined specimens of A. xanthodermulus (CA 160, CA 174, CA 188 and CA 204) have identical ITS1 and ITS2 sequences. Agaricus xanthodermulus can be distinguished from the three neighbor species, A. laskibarii L.A. Parra et Arrillaga, A. californicus Peck, and A. parvitigrinus sp. nov. (see above), by the characteristic ITS polymorphism tatgttTttcatt at position 222 of its own sequence.

Habitat, distribution, occurrence.— – Isolated to gregarious in mixed deciduous wood, in coniferous wood or in rich grassland, on sandy soil. Western France, extent of range unknown, possibly relatively abundant.

Specimens examined.— – FRANCE, Gironde, Villandraut-Prechac, mixed deciduous wood (Carpinus, Robinia, Sambucus, Euonymus), 7 Oct 2001, CA 160, J. Guinberteau, HOLOTYPE (LIP), GENBANK xxx; FRANCE, Charente Maritime, Oléron Island, rich grassland, 21 Oct 2002, CA 174, G. Dupuy, GENBANK xxx; FRANCE, Gironde, Le Verdon, under Pinus pinaster and Quercus ilex, 9 Nov 2002, CA 188, J. Guinberteau, GENBANK xxx; FRANCE, Charente Maritime, Oléron Island, rich grassland, 12 Nov 2002, CA 204, G. Dupuy, GENBANK xxx. Mycelium cultures of the four collection are available at INRA Bordeaux.

Etymology.— – The ‘xanthodermulus’ epithet means ‘small xanthodermus’, indicating that the new species looks like a miniature A. xanthodermus.

	DISCUSSION

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A. parvitigrinus looks like a miniature A. moelleri with a more slender silhouette and with the cap squamules more scattered making its cap globally lighter. In the same way A. xanthodermulus looks like a miniature A. xanthodermus but has significantly larger spores, unless one considers A. xanthodermus var. macrosporus. This variety differs from A. xanthodermulus by its much larger cap and the greater width of its cheilocystidia (6–21 µm vs 6–8 µm). Their truncately conical form, odor of ink and yellow discoloring on handling put all four species together in section Xanthodermatei. Within this section the main characteristics of both new species are their small sporophores and their spindly silhouette; moreover, they can be distinguished from each other by their own characteristics: dark grayish, minute squamules for A. parvitigrinus and large spores for A. xanthodermulus.

The other small species of section Xanthodermatei described in Europe are A. pseudopratensis, A. endoxanthus and Psalliota nigricans. Agaricus pseudopratensis differs from both new species by its "stature squat, measurements resembling those of Agaricus campester" (Bohus 1971) and by its context often becoming somewhat reddish. It also can be distinguished from A. xanthodermulus by its smaller spores. Agaricus endoxanthus differs from both new species by the presence of vacuoles containing an abundant dark brown pigment in the pileipellis hyphae; this also characterizes other small tropical species of the Xanthodermatei—like A. rotalis K.R. Peterson, Desjardin et Hemmes (Peterson et al 2000) and A. termiticola Heinem. (Heineman 1980). Psalliota nigricans Velen. 1921 (= Agaricus meleagris var. nigricans [Velen] Pilát 1951) has been described briefly as a small species (cap 3–5 cm diam); the specimen drawn by Velenovsky (1921) looks like A. parvitigrinus with a more inflated bulb. However we do not consider Psalliota nigricans as a synonym because its spores are significantly shorter (4–5 µm vs 5.5–6.7 µm for A. parvitigrinus) and this cannot be verified because the type collection does not exist. We also note its grassy site, while A. parvitigrinus was collected in wood. Agaricus velenovskyi Pilát 1968 (= Agaricus meleagris var. nigricans [Velen] Pilát sensu Pilát, 1951, pro parte [quoad descr. & specimina], excl. typo) has a cap 5–11 cm diam and therefore typically is not small. This species that we suspect to be synonym or close to A. xanthodermus (see Cappelli 1984) also can be distinguished from A. parvitigrinus by its cap, which is white and not ornamented at first, and by its grassy habitat (Pilát 1968).

The dissimilarity analysis shows that both new species are close to A. laskibarii and A. californicus. Agaricus laskibarii differs by its larger cap and its habitat in the dunes; it differs also from A. parvitigrinus by the absence of squamules and from A. xanthodermulus by its smaller spores. Agaricus californicus, which can have a small cap diameter, differs by a pileus with a grayish brown (or "brownish-purple", according to Peck 1895) disk without squamules (or "somewhat squamulose", according to Kerrigan 1986) and by fainter phenolic odor and yellow discoloring on handling.

Agaricus pilatianus (Bohus) Bohus that is probably a synonym of A. iodosmus Heineman, is a large species distributed in the Mediterranean area, but a small variant was described from the Netherland (Nauta 2001). The cylindrical stipe with a triangular annulus that characterizes this species differs from the generally bulbous stipe with a pendant membranous annulus observed in both new species.

We have known both new entities for several years, and we have observed that mycologists often have mistaken them for small or slender forms of A. moelleri, A. xanthodermus or A. pseudopratensis. This confusion also exists in the literature (i.e., we consider that the photo 544 p.192 [A. pseudopratensis var. niveus] in Arrillaga Anabitarte [2004] represents in fact specimens of A. xanthodermulus). We primarily hesitated to describe both new entities at the varietal rank. However molecular comparisons show that both new species diverge from these three species. The level of divergence is much greater, for example, than the divergence found between sister species of section Duploannulati (Challen et al 2003) like A. bisporus and A. subfloccosus ( J. Lange) Pilát that differ at about 10–14 sequence sites (R.W. Kerrigan pers comm). Finally, all morphological and molecular comparisons reinforce the concepts of these new entities and support their elevation to the species rank.

In the Fitch phenogram A. xanthodermulus, A. parvitigrinus, A. laskibarii and A. californicus form a group. We note that this group is made up of small to medium size species. Among them, to our surprise, A. xanthodermulus and A. laskibarii are close to each other. The slight difference between the sequences of A. xanthodermulus and A. laskibarii (polymorphisms at three positions) was reinforced by the fact that the specimen of A. laskibarii was heteromorphic at four other sequence sites, while the four specimens of A. xanthodermulus had identical sequences without any heteromorphism, although the collections came from relatively distant sites in western France. The collection of A. laskibarii has been found in the same region (at about 120 km from a site of A. xanthodermulus); other collections would be useful to interpret the origin of this heteromorphism, but this species seems particularly rare. We also note that, among the three polymorphic sites for which the two species diverge, two characterize A. laskibarii while the remaining one characterizes A. xanthodermulus among all the studied species. On the other hand, the morphological differences between these two species are relatively important. They are in fact more pronounced than the differences between the two abundant species A. moelleri and A. xanthodermus, which mainly differ by the presence/absence of squamules, while their sequences differ by only two polymorphisms. Such a small divergence is of the same order of the maximum difference we observed between specimens belonging to a same species in the analysis of section Duploannulati (Challen et al 2003). Pairs of species as close as A. laskibari/A. xanthodermulus or A. moelleri/A. xanthodermus possibly reflect relatively recent processes of speciation in the Xanthodermatei. The phylogenetic analysis of section Xanthodermatei is in progress and will let us compare better the evolutionary processes.

In conclusion, among the species of the Agaricus section Xanthodermatei there exist now in Europe four species having a cap diameter smaller than 5.5 cm (generally 3–4 cm), Agaricus pseudopratensis and A. endoxanthus, and two new species, A. parvitigrinus, which probably is rare, and A. xanthodermulus, which is relatively more abundant than its larger, rare sister species A. laskibarii. Phenol, p-quinol and other phenolic metabolites are constituents of A. moelleri and A. xanthodermus in sufficient quantity to account for their immediate toxicity and their phenolic odor (Gill and Strauch 1984, Wood et al 1998). Both new species have a phenolic odor and probably are toxic.

View larger version (30K): [in this window] [in a new window]   FIG. 1. Fitch phenogram for ITS1 and ITS2 sequences of 16 specimens of Agaricus belonging to seven species of section Xanthodermatei, including two new species A. xanthodermulus and A. parvitigrinus, and of one specimen of A. bisporus used as outgroup. The tree is unrooted.

	ACKNOWLEDGMENTS

	FOOTNOTES

 
Accepted for publication December 1, 2004.

¹ Corresponding author. E-mail: callac{at}bordeaux.inra.fr

	LITERATURE CITED

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Felsenstein J. 1993. PHYLIP: phylogeny interference package, version 3.5c. Department of Genetics, University of Washington, Seattle.

Gill M, Strauch RJ. 1984. Constituents of Agaricus xanthodermus Genevier: the first naturally endogenous azo compound and toxic phenilic metabolites. Z. Naturforsch 39c:1027–1029.

Heinemann P. 1980. Les genres Agaricus et Micropsalliota en Malaisie et en Indonésie. Bull Jard bot Belg 50: 3–68.

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———, Villarreal M, Esteve-Raventos F. 2002. Agaricus endoxanthus una specie tropicale trovata in Spagna. Rivista di Micologia 45(3):225–233.

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———. 1968. De Agarico velenovskyi sp. Nov. [= Agaricus meleagris var. nigricans (Velen.?) Pilát 1951]. Ceska Mykologie 22(2):81–86.

Velenovsky J. 1921. Psalliota nigricans p 563–564. In: Ceske houby. Praha. 950 p.

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