The Meruliaceae of Russia. II. Panus

The history of taxonomical study of the genus Panus Fr. (Meruliaceae, Polyporales, Basidiomycota) is considered. A current revision of the genus in Russia was carried out. Two species of the genus Panus were recorded in various regions of Russia, Panus conchatus (Bull.) Fr. and P. lecomtei (Fr.) Corner. For P. conchatus, the lateral ecotype with conchiform pileus and rather dark wine-red to lilac-brown surface is more characteristic. Two main deviations from such a neutral type were described: 1) the chromatic one, characterized by light-colored (red or clay-yellow), usually conchiform pilei [P. conchatus var. inconstans (Pers.) Zmitr., Bondartseva, Perevedentseva, Myasnikov et Kovalenko] and 2) the growth one, characterized by a central (often bulbous) stipe, funnel-shaped cap and strongly inrolled margin [P. conchatus var. torulosus (Pers.) Zmitr., Bondartseva, Perevedentseva, Myasnikov et Kovalenko]. For P. lecomtei, the ecotype having small eccentric to lateral elegant stipe is considered. However, the stipe shape and size are variable. The stipe can be either central – rather small, with a bulbous base [P. lecomtei var. semirudis (Singer) Zmitr., Bondartseva, Perevedentseva, Myasnikov et Kovalenko], or strongly elongated [P. lecomtei var. stipitata (Malk.) Zmitr., Bondartseva, Perevedentseva, Myasnikov et Kovalenko]. Four new combinations, P. conchatus var. inconstans, P. conchatus var. torulosus, P. lecomtei var. semirudis, and P. lecomtei var. stipitata were suggested. It was concluded that Panus represents rather well-delimited genus belonging to merulioid phylogenetic radiation, whose morphotype on essential features of its organization is trametoid, but superficial habitual features make it closer to the lentinoid one. Its essential features are the abundance of fibrohyphae which form textura intricata, slowly growing basidiocarps and strictly lamellate hymenophore. Apparently, such an adaptive structure was generated at arid and warm climatic zones, and only 2 species, P. conchatus, and P. lecomtei, have been irradiated into temperate latitudes. The substrate spectrum of these fungi is determined by their insensitivity to substrate moistening and best ability to colonize hardwood, so the greatest number of their finds can be made on stumps and large remnants of stand-formers of corresponding forest areas. In Russia, a reliable association of Panus species to Betula spp. and Populus spp. was revealed. An ecotypic differentiation of the genus Panus is related to the quality of substrate colonized. The basidiocarps, growing over top cuts of the stumps, are characterized by strong central stipe (P. conchatus var. torulosus, P. lecomtei var. semirudis), whereas basidiocarps with sublateral attachment are common on fallen logs. Certain chromatic adaptations (P. conchatus var. inconstans) are associated with an insolation regime of the habitat. During last years, the Panus representatives have attracted an interest in biomedical research development. Their resource potential estimation should proceed from the fact that within Russian territory, such areas as Middle Belt of European Russia, North Caucasus, Altai and other regions of Southern Siberia are promising for replenishing the strains of P. conchatus and P. lecomtei.


Introduction
This paper continues a taxonomical survey on the genera of Meruliaceae (Polyporales, Basidiomycota) presented in Russian mycobiota (Zmitrovich et al., 2016), and it is devoted to an interesting genus Panus Fr., for a long time considering first within Pleurotaceae, later within Polyporaceae families, but in fact being closely related to the genera Cerrena Gray and Steccherinum Gray of merulioid phylogenetic radiation.
An important episode in Panus taxonomy is related to the works by Singer. In 1951, on the basis of complex similarities between Lentinus, Panus, and Polyporus Fr., this mycologist has united three genera with such genera as Pseudovafolus Pat., Mycobonia Pat., Phyllotopsis E.-J. Gilbert et Donk ex Singer, and Pleurotus (Fr.) P. Kumm. in the family Polyporaceae (Singer, 1951). Considering the Lentinus lepideus (Fr.: Fr.) Fr. as type species for Lentinus (the more correct modern typification is L. crinitus L.), Singer unites all the small-spored species within the genus Panus. Thereafter he has reissued this system three times without essential changing of the concept (Singer, 1962(Singer, , 1975(Singer, , 1986. Corner (1981) has differentiated the genera Lentinus and Panus on the basis of the branching pattern of skeletal hyphae which are organized as dendrites with an inflated axial element in Lentinus and stay unbranched in Panus. In 1983, Pegler has published a monograph on the genus Lentinus, which includes according to this author the Panus-union as a subgenus, but basing on Corner's principles. Within the Lentinus subgenus there are considered species with branched and swollen sclerohyphae, whereas the Panus subgenus unites the species with fibrohyphae (Pegler, 1983).
In the period of molecular taxonomy (Ko, Jung, 1999;Grand, 2004;Larsson, 2007;Lee, Lim, 2010;Miettinen, Larsson, 2011;Zmitrovich, Malysheva, 2013) it was shown that the genus Panus sensu Corner is substantially distant from Lentinus (core Polyporaceae), but closely related to the genus Cerrena Gray (large merulioid phylogenetic radiation). Within the framework of "splitter's approach", even two closely related families -Cerrenaceae and Panaceae -have been described (Justo et al., 2017), although we believe that the preservation of the "large Meruliaceae" lies in canvas of more balanced classification of the Polyporales.
Distracting from macromorphology, it can be seen that Cerrena and Panus have much in common: e. g. unbranched fibrohyphae, highly characteristic sclerified elements protruding the hymenium, traditionally called as sclerocystidia or metuloids in the genus Panus, and as pseudocystidia in the genus Cerrena, finally, rather similar basidia and basidiospores. It should be emphasized the absence of any inflated hyphal elements (characteristic feature of representatives of Lentinus and Polyporus s. l.) in all tissues of representatives of the genus Panus. This feature, as well as rather slow growth of the basidiomata with the formation of solid and often twisting stipe of textura intricata, allows to interpret Panus-like morphotype consider only superficially similar to lentinoid one. It is rather a unique adaptive structure combining true lamellate hymenophore and trametoid growth and tissues organization. Studies on hymenophore development in Panus conchatus, P. lecomtei, and P. fulvus (Hibbett et al., 1993) also confirm this conclusion.
The aim of the present paper is detailed characterization of the genus Panus in Russia, including a modern morphological elaboration, survey of intraspecies polymorphism, substrate preferences and resource potential, considering that some species of this genus are known as promising subject for biomedical research, since produce panepoxidone and isopanepoxidone, substances that has an inhibitory effect on a number of inflammatory chemokines secreted by cancer tissues (Erkel et al., 1996;Shotwell et al., 2000).

Materials and Methods
The macroscopic descriptions were based on a study of fresh and dried specimens. The materials of the herbaria of Komarov Botanical Institute (St. Petersburg, LE) and Perm State National Research University (PERM) were studied. Microscopic preparations were mounted from dried material in Melzer's solution, 10 % ammoniacal Congo Red and 5 % aqueous solution of KOH, using a LOMO Micmed-6 light microscope. The hyphal system was revealed and described according to updated technique (Zmitrovich et al., 2009). The size of mature spores was measured on 30 spores in distilled water and Melzer's solution. Basidiocarp solitary or caespitose, medium-sized to large, slowly growing, tough and persistant, originating from a woody substratum or from sclerotium, of lentioid habitus with gymnocarpic development. Pileus convex, then depressed to umbilicate, tough with dry, with hirsute, fibrillose-squamulose, squamose, or glabrous surface. Margin mostly inrolled, even, or radially ribbed. Hymenophore lamellate. Gills of 2-4 levels, decurrent, rarely furcate, moderately spaced to densely crowded; edge entire. Stipe central to lateral and very reduced, stiff, solid, continuous with the pileus. Context fibrous, toughfleshy to coriaceous, mostly thin. Spore print white to cream colour.
On dying and dry trees, fallen logs, stumps and large fallen branches of trees and shrubs, presumable angiosprems. Causes a white rot. Worldwide, more abundant in the tropics.
Type specimen is deposited in Friesian herbarium of the Uppsala University Museum of Evolution (UPS) (Ryvarden, 1991).
Differential generic suggestions. The genus Lentinus Fr. has a superficial resemblance, but differs by skeleto-binding hyphae with inflated axial segment (all the Panus representatives have uninflated skeletals). The genus Lignomyces R. H. Petersen et Zmitr. is superficially similar too, but differs by monomitic hyphal system with strongly inflated hyphal segments and a dorsal stem attachment (Petersen et al., 2015). Phylogenetically related genus Cymatoderma Jungh. differs by podoscyphoid habitus and the presence of ventricose hymenial gloeocystidia. Phylogenetically related genus Cerrena differs by daedaleoid/trametoid habitus and less elongated (in median) basidiospores.
Ecology and substrata. All the Panus representatives are rather thermophilic, xerotolerant and non-sensitive to substrate watercut, why they are especially often found on large logs and stumps, without allocation of strict substrate specificity. On the other hand, they have not very high enzymatic activity and are generally not adapted to deep decomposition of coniferous wood. This circumstance, as well as their attraction to large-scale tree residues, are the reasons that in zonal biomes they are most often associated to deciduous stand formers (mostly Betula and Populus in the temperate-boreal zone, and Quercus and Fagus in the nemoral zone), although they readily colonize many other trees.
Type of rot. All the Panus representatives cause a white rot. Oxidative enzymes were carefully investigated in Panus lecomtei and P. conchatus (Zhang et al., 2006;Zhou et al., 2014). It was shown that purified enzymes of these fungi belong to the laccases family, due to the following observations: 1) the enzyme exhibited a broad substrate pattern, 2) oxygen was used as an oxidative agent, while there was no H 2 O 2 to initiate the catalytic oxidation, and 3) the determined N-terminal primary structure of the enzyme exhibited a high degree of similarity with the corresponding laccases sequences.
Secondary metabolites and perspectives in biomedical research. A metabolite of great application value, panepoxidone has been detected in P. lecomtei by Erkel group (Erkel et al., 1996). Such metabolite as isopanepoxidone has been isolated from P. conchatus by Shotwell et al. (2000), and this substance has a similar effect reducible to the prevention of degradation of inhibiting particles of NF-κB (IκBα) that inactivate this transcriptional factor. NF-κB chemokine represents the main pro-inflammatory factor, constitutionally associated with cancer progression (Zmitrovich, 2015), therefore such substance as panepoxidone is a prospective subject for biomedical research, whereas the Panus species have a great resource value.
Also, it should be mentioned the production of pink-lilac pigment complexes by both tropical and temperate Panus representatives which were noted already by Miller (1967), but yet were not chemically fractioned.
Specifics of Panus-like morphotype. Basidiocarp development in the Panus representatives was studied by Hibbett et al. (1993), whereas their hyphal differentiation was studied by Zmitrovich et al. (2009). As it was shown, the hymenophore differentiation in Panus involves the periclinal growth of context hyphae below a closed surface palisade of hymenial elements, resulting in a cantharelloid appearance and radiate trama. This pattern is qualitatively different from that in Lentinus s. str., which suggests that lamellae of Panus and Lentinus are not homologous. P. conchatus and P. lecomtei basidiocarps have short stipes, whereas P. fulvus basidiocarps have an elongate stipe, and develop from a pseudosclerotium. P. conchatus sporocarps developed an ephemeral partial veil that was obliterated during basidiocarp expansion, whereas primordia of P. lecomtei are initially gymnocarpic. Analysis of hyphal system of all the tropical representatives of the genus indicates the rigorous dimitism of mature basidiocarp, whereas in P. conchatus and P. lecomtei the hyphae sclerify slower, while mature basidiocarps include the hyphal elements on different stages of maturation (Zmitrovich et al., 2009). The absence of physalohyphae determining the accelerated growth of agaricoid basidiocarps makes the growth of Panus representatives more monotonous and slow, what, in combination with its hyphal structure, brings Panus-like morphotype together with trametoid one. However, the hymenophore of Panus is a classical lamellate that indicates a surprising convergence among agaricomycetes.
S u b s t r a t a: on many hardwoods, especially Betula spp. and Populus tremula, rarely on conifers (Pinus sylvestris).
C u l t u r a l c h a r a c t e r i s t i c s: Hibbett et al. (1993); Johnson, Methven (1994); Grand (2004).
G e n e r a l d i s t r i b u t i o n: EUROPE (Austria, Belarus, Belgium, Bulgaria, Denmark, Estonia, Finland, France, Germany, Latvia, Lithuania, Norway, Russia, Scotland, Spain, Sweden, Ukraine); AFRICA (Ethiopia); ASIA (Armenia, Georgia, Japan, Korea, Russia); NORTH AMERICA (Canada, Mexico, USA), CENTRAL AMERICA (Costa Rica); SOUTH AMERICA (Equador); AUSTRALIA and OCEANIA (Australia) (Pegler, 1983;Panus conchatus.., 2018). D i s t r i b u t i o n i n R u s s i a: see Table 1. Association with Trametes multicolor. According to our observations made on the Karelian Isthmus clear cuttings, Panus conchatus often settles on stumps, primarily colonized by Trametes multicolor (Schaeff.) Jülich (Fig. 2). Within ten records made for Betula stumps on the Karelian Isthmus clear cuttings, seven ones have contained an indication of the joint presence of Panus conchatus and Trametes multicolor. The latter species is an active producer of laccase and is characterized by high growth rate (Zmitrovich et al., 2017). Apparently, their primary delignification and moistening of wood by T. multicolor creates a niche for Panus conchatus, carrying out a deeper substrate delignification. The pair in question certainly echoes with another pair, Antrodiella pallescens/Fomes 36 Zmitrovich I. V. et al. The Meruliaceae of Russia. II. Panus fomentarius, described for dead wood in boreal forests (Spirin, 2002).
Nomenclature. Two names sanctioned by Fries (1821) were considered in the literature as a fit basionyms of this species, Agaricus conchatus (Bulliard, 1787) and A. torulosus (Persoon, 1801). Since both names are sanctioned by Fries and there is no any doubt in their synonymy, the combination based on A. conchatus name, i. e. Panus conchatus (Fries, 1838), has a priority.
From type variety differs by clay-buff, carneous of rufescent color of the upperside. Basidiocarps of conchoid appearance, the stipe often reduced and then the hymenophore is subporoid at the base. The microstructures vary as in a neutral type. I c o n .: Malkovský (1932: fig. 2, 3, 6 ut Panus flabelliformis).
From type variety is distinguished by long lateral or eccentric stipe and spathulate pilei. Upperside is strongly strigose, color usually fading to cinnamon. The microstructures vary as in a neutral type (Fig. 6). The problem of Lentinus martianoffianus. This problematic species was described by Thümen (1877) with reference to Kalchbrenner, and its authentic material kept in Kew Herbarium (K). There is a single specimen, collected on Populus balsamifera by Martianoff near Minussinsk in 1880 and distributed within exsiccate series by Thümen (Fung. Exot. Dec. 21).
Since the molecular testing of any Kew material is prohibited, only the morphological description may be considered on, which unambiguously indicates the close relationships of this taxon with Panus lecomtei-coll. Only basidiospores are something diverse, since are not ovoid, but rather ellipsoidalcylindrical. Malkovský (1932) has considered Lentinus martianoffianus as a synonym of Panus rudis, whereas Pegler (1983) has abstained from synonymization procedure. In any case, this taxon belongs to the genus Panus, although there have been attempted to associate this name with the Lentinus