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Researches on Russulaceous Mushrooms-An Appraisal Reported to Provide Some Non-Nutritional Benefits to Tree 1932, 1940) and Beardslee (1918)

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Researches on Russulaceous Mushrooms-An Appraisal Reported to Provide Some Non-Nutritional Benefits to Tree 1932, 1940) and Beardslee (1918) 63 KAVAKA47 : 63 - 82 (2016) Researches on Russulaceous Mushrooms-AnAppraisal N.S.Atri,Samidha Sharma* , Munruchi Kaur Sainiand Kanad Das ** Department of Botany, PunjabiUniversity, Patiala 147002, Punjab, India. *Department of Botany, Arya College, Ludhiana 141001, Punjab, India. **Botanical Survey of India, Cryptogamic Unit, P.O. BotanicGarden, Howrah 711103, India Corresponding author email: [email protected] (Submitted onAugust 10, 2016 ;Accepted on October 2, 2016) ABSTRACT Russulaceae is one among the large families of the basidiomycetous fungi. Some significant studies during the last decade on their systematics and molecularphylogenyresulted in splittingof well knownmilkcapgenusLactarius s.l.andinclusionof number of gastroid and resupinate members under its circumscription. Presently, there are seven genera (including agaricoid, gasteroid and resupinate members) in this family viz. RussulaPers. , Lactarius Pers. , Lactifluus (Pers.) Roussel, Cystangium Singer & A.H. Smith , Multifurca Buyck & Hofst., Boidinia Stalper & HjortstamandPseudoxenasma K.H.Larss.&Hjortstamspreadover 1248+ recognisedspeciestheworldover.Outof atotalofabout 259 + species/taxaofRussulacousmushrooms,146taxaofRussula ,83taxaof Lactarius ,27taxaof Lactifluus ,2speciesof Boidinia and1speciesof Multifurca are documented from India. In this manuscript an appraisal of the work done on various aspects of the members of the family Russulaceae including their taxonomic, molecular,phylogenetic, scanning electron microscopic, ectomycorrhizal, nutritional and nutraceutical aspects has been attempted. Keywords: Russulaceae, taxonomy, phylogeny, SEM, ECM, nutritional, nutraceutical, review INTRODUCTION taxa ofRussula and 83 taxa of Lactarius, 27 taxa of Lactifluus (Pers.) Roussel are known. (Atri et al ., 1994; Das and Sharma, The familyRussulaceae Lotsy is one of the 12 families under 2005; Bhattet al ., 2007; Das 2009; Das et al ., 2010, 2013, orderRussulales Krisel ex P.M. Kirk, P.F. Cannon & J.C. 2015; Das and Verbeken, 2011, 2012; Lathaet al ., 2016; David (Kirket al ., 2008). The family was established by Roze Sharmaet al ., 2016; Paloi et al ., 2015, 2016; Dutta et al ., (1876) as Russulariéés (nom. nud. ), which was subsequently 2015; Khatuaet al ., 2015,Wisitrassameewong et al ., 2016). validated asRussulaceae by Lotsy (1907). The members of this family are most diverse, containing a remarkable variety The other genera listed in the family are Lactifluus, of carpophore forms ranging from resupinate to pleurotoid, CystangiumSinger & A.H. Smith (Miller et al ., 2001), pileate and stipitate with lamellate or gasteroid hymenophore. Multifurca(Buyck et al ., 2008), Boidinia Stalper & Hjortstam Four distinct phylogenetic clades are identified within andPseudoxenasma K.H. Larss. & Hjortstam (Larsson and Russulaceae by molecular phylogenetic analysis of Larsson, 2003). The gasteroid genusCystangium is known ribosomal gene (nrITS and nrLSU) and part of a protein- only from Australia and South America. It shares many coding gene (RPB2) (Buycket al ., 2008). Thevast majority of characteristics withRussula and Lactarius. At present, there the known species in the familyRussulaceae are agaricoid are 32 species ofCystangium known throughout the world belonging to the traditional generaRussula Pers. and (Kirket al ., 2008). Genus Multifurca is characterized by Lactarius Pers., which are reported to form a monophyletic regularly forked, narrow, orange, pinkish-orange to honey clade together with their gasteroid and pleurotoid relatives yellow gills, very small spores with a faint, obscurely to (Milleret al ., 2006). The bright color of genus Russula and distinctly sub-reticulate ornamentation and inamyloid latex exuding feature of genusLactarius probably lead suprahialer spot. Presently only 5 species of this genus are Persoon (1797) to name these two genera.Russula appeared documented worldwide (Kirket al ., 2008) and only 1 species first as tribeRussula Fr. and Lactarius appeared as the tribe M. roxburghiae Buyck & Hofst. is known from India. GalorrheusFr. of the genus Agaricus L. as circumscribed by Boidinia is a widespread polyphyletic genus represented only Fries (1821). Later, Gray (1821) elevated the tribe to generic by 10 species (Kirket al ., 2008). It is a wood inhabiting status and bothRussula and Lactarius have maintained a fungus that strictly forms thin resupinate basidiomata on remarkable continuity to the present since then. Multigene coniferous wood. Dhingraet al . (2012) documented 2 species based phylogenies of familyRussulaceae reveals that ofBoidinia , namely B. furfuracea (Bers.) Stalpers & Lactariusand Russula are not supported as two monophyletic Hjortstam andB. lacticolor (Bers.) Hjortstam & Ryvarden clades (Buycket al ., 2008). It has been documented that the from India.Pseudoxenasma is another resupinate member genusRussula appears to be monophyletic only when a small represented only by one species,P. verrucisporum K.H. group of species representing subsectionOchricompacta of Larss. & Hjortstam from Sweden (Kirket al ., 2008). It grows genusRussula is removed, as these forms an independent on fallen branches and trunks as well as on dead but still clade whereRussula and Lactarius are mixed. A new genus attached branches ofPicea Dietrich. in humid forest. None of Multifurca Buyck & Hofst. was described to accommodate the species ofCystangium and Pseudoxenasma have been such representatives (Buycket al ., 2008). Apart from the taxa documented yet from India. Most of the members of that belong to genusMultifurca , the genus Lactarius also Russulaceaeincluding species of Russula , Lactarius and contains two clades, a larger and a smaller one with only 20% Lactifluusare found closely associated with trees of Quercus taxa (Verbeken et al., 2011). There are 750 species of genus L.,Lithocarpus Blume, Rhododendron L. , Shorea Roxb. ex. Russulaand 450 species of genus Lactarius documented C.F.Gaertn,Pinus L ., Cedrus Trew., Abies Miller, Picea, etc. worldwide (Kirket al ., 2008). As compared from India, 146 Besides forming symbiotic association, these fungi are also 64 Researches on Russulaceous Mushrooms-An Appraisal reported to provide some non-nutritional benefits to tree 1932, 1940) and Beardslee (1918). Schaeffer (1952) seedlings. Little work has been undertaken on the described 68 species in his monographic work from Europe characterization of ectomycorrhiza of this particular group of and provided a key for the identification of 104 taxa of the fungi in India. genusRussula . Schaeffer (1952) recognized 3 sections (Compactae , Gratae and Ingratae ) and 15 undersections Some of the members of familyRussulaceae including under this genus. Hesler (1960, 1961a, b) described 193 Russula paludosaBritzelm., R. xerampelina (Schaeff.) Fr., R. species ofRussula from North America. Singer (1926) lepidaFr., Cystangium sessile (Massee and Rodway) Singer published a monograph on the genusRussula which he &A.H.Smith are reported to be medicinally important (Wang revised in 1932. Singer (1986) in his treatise “Agaricales in et al., 2007; Lovy et al., 2000; Bougher and Lebel, 2001). modern taxonomy” recognized 317 species ofRussula under Some of the species, includingRussula delica Fr. and 11 sections, namelyPelliculariae Heim. , Delicoarchaeae Lactarius deliciosus (L.) Gray, are reported to possess Sing., Plorantes Bat. ex. Sing. , Crassotunicatae (Sing.) antioxidant and antimicrobial properties (Barroset al ., 2007a, Sing., Compactae Fr. , Pachycystides Singer , b,c; Türkoğlu et al ., 2009; Sharma, 2015). Some of the MetachromaticaeSinger , Decolorantes (R. Maire) Singer , species, includingLactarius deliciosus (L.) Gray, L. IngrataeQuél. , Rigidae Fr. and Russula . Romagnesi (1967) sanguifluus(Paulet) Fr., L. resimus (Fr.) Fr., L. scrobiculatus was one of the prominent contributors onRussula from (Scop.) Fr., L. torminosus (Schaeff.) Pers. , L. piperatus (L.) Europe. He published a detailed monograph containing 190 Pers., L. edulis Buyck , L. gymnocarpoides Verbeken , L. species and 92 varieties of European and African species of longisporusVerbeken , L. xerampelinus Karhula & Verbeken, Russula. He divided the genus into 9 sections ( Compactae Russula brevipesPeck. , R. cyanoxantha (Schaeff.) Fr. and R. Fr.,Heterophyllae Fr. , Ingratae Quélet , Piperinae Quélet , virescens (Schaeff.) Fr., are most sought after from edibility IncrustataeRomagn. , Tenellae Quélet , Polychromae R. point of view (Verbekenet al ., 2000; Atri et al ., 1997, Maire, Coccinae Romagn. and Insidiosae Quélet). Pearson 2010a,b). (1948) treated 66 species ofRussula from Britain in 8 I. TAXONOMIC STUDIES sections, namely Lactariodes, Rigidae, Resilientes, Foetentes, Ochraceae, Acrae, Subacraeand Gratae . Rayner To begin with, this family was classified under the order (1968-1970) studied British species ofRussula and described Agaricales Undrew. (Singer, 1962, 1975, 1986; Smith, 1949, 112 species of the genus under 2 divisions, namely 1973; Pegler 1977; Stuntze, 1977). However, some of the Compactaeand Genuinae . Antoine (1973) designed a key for workers including Kühner (1980) and Kreisel (1969) raised 96 species ofRussula from Eastern France. An outstanding the family to the rank of order asRussulales . Much earlier monographic work was published by Sarnari (1998) on the Bucholtz (1902) has already attempted to separate this family EuropeanRussula . It deals with the critical analysis of all of from orderAgaricales primarily because of the relationship the various nomenclature
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