In addition to these typicalagaricoid forms, the family contains species with fruitbodies that are laterally striped (pleurotoid), closed (secotioid orgasteroid), or crust-like (corticioid).Molecular phylogenetics has demonstrated close affinities between species with very different fruitbody types and has discovered new, distinctlineages.
The family Russulaceae was firstvalidly named in 1907 by Dutch botanistJohannes Paulus Lotsy,[4] who included three genera:Russula,Lactarius, andRussulina (now considered a synonym ofRussula). He emphasised features such as the granularflesh, thick gills, spinyspores, and milkyhyphae and rounded cells (sphaerocytes).[1] A prior usage of "Russulariées" by French mycologistErnst Roze in 1876[5] is not considered a valid publication, since the proper Latin termination for the family rank specified in article 18.4 of thenomenclature code was not used.[4][6]
Synonyms of Russulaceae include:Ernst Albert Gäumann's Lactariaceae (1926),Fernand Moreau's Asterosporaceae (1953),[2] andDavid Pegler and Thomas Young's Elasmomycetaceae (1979). The latter family was proposed to contain species with statismosporic (non-forcibly discharged) and symmetric spores, including the gasteroid generaElasmomyces,Gymnomyces,Martellia, andZelleromyces. Calonge and Martín reduced the Elasmomycetaceae to synonymy with the Russulaceae when molecular analysis confirmed the close genetic relationship between the gasteroid and agaricoid genera.[3]
Historically, thegilled mushrooms of the family Russulaceae were classified with other gilled species in the orderAgaricales,[7] but microscopical studies of spore and fruitbody flesh features raised the possibility that they were more closely related with certain "lower fungi" presenting nongilled,crust-like fruitbodies.[2][8][9] The use ofmolecular phylogenetics confirmed that these morphologically diverse fungi form a distinct lineage, first termed the "russuloidclade"[10][11] and today classified as orderRussulales in the classAgaricomycetes.[12] The family'ssister group within the order appears to be the crust-likeGloeocystidiellaceae.[13]
Phylogeny of the Russulaceae; dashed lines indicate uncertain placement.[10][13][14][15]
A 2008 molecular phylogenetic study clarified the relationships among the mushroom-forming species of the family.[15] The authors demonstrated the existence of four distinct lineages of gilled mushrooms, which led to the description ofMultifurca as a new genus separated fromRussula[15] and the segregation ofLactifluus fromLactarius.[16][17]
Genera with closed fruitbodies within the family areform taxa instead of natural groups:Arcangeliella,Gastrolactarius, andZelleromyces are phylogenetically part ofLactarius, whileCystangium,Elasmomyces,Gymnomyces,Macowanites, andMartellia belong toRussula.[3][16] Nevertheless, some of these genus names are still in use, as many of the concerned species have not yet formally been synonymised withLactarius orRussula.[18]
The crust-like generaBoidinia,Gloeopeniophorella, andPseudoxenasma, formerly placed in theCorticiaceae or Gloeocystidiellaceae, are now classified in the Russulaceae and basal to the clade of mushroom-forming species described above.[13][18] Studies have so far failed to clearlycircumscribe and place these genera within the family.[10][13][14]Boidinia in its current extent ispolyphyletic, with some species not falling into the Russulaceae.[10]
Altogether, the Russulaceae comprise around 1,900 accepted species.[18]Russula is by far the largest genus with c. 1,100 species,Lactarius has c. 550,Lactifluus c. 120,Boidinia 13,Multifurca 6,Gloeopeniophorella 6, andPseudoxenasma 1 species.[18][19] Closed-fruitbody species not yet synonymised withLactarius orRussula (see above) account for some 150 species.[18]
New species in the Russulaceae continue to be described from various regions, such as the US,[20] Guyana,[21] Brazil,[22] Patagonia,[23] Togo,[24] Sri Lanka,[25] or Thailand.[25] It has been estimated that the real number ofRussula species in North America alone (currently around 400 described) might be as high as 2000.[26]Cryptic species may increase true diversity: some morphologically well-defined species, especially inLactifluus, have been shown to actually encompass several phylogenetic species.[27][28][29]
Theagaricoid species inLactarius,Lactifluus,Multifurca, andRussula are readily distinguished from other gilled mushrooms by the consistency of their flesh, which is granular, brittle and breaks easily, somewhat like a piece of chalk.[1][30] Russulaceae never have avolva,[30] but apartial veil can be found in some tropical species.[31][32] Gills areadnate todecurrent, and the colour of thespore print ranges from white to ochre or orange[15][33] (with the brown-sporedLactarius chromospermus as an exception).[34]
Caps can be dull to very colourful, the latter especially inRussula;[33] their size ranges from 17 mm diameter or less inRussula campinensis[35] to 30 cm (12 in) inLactifluus vellereus.[33] Concentrically ringed (zonate) caps occur in allMultifurca[15] and severalLactarius species.[33] Laterally striped (pleurotoid) fruitbodies exist in some, mainly tropicalLactifluus andRussula species.[35][36][37][38] Taste is a distinguishing characteristic in many species, from mild to very acrid.[33] A conspicuous feature of the "milk-caps" inLactarius, Lactifluus, andMultifurca furcata is thelatex or "milk" their fruitbodies exude when bruised.[15][30]
Thesecotioid andgasteroid species inLactarius andRussula are derived from agaricoid forms.[15][39] Secotioid species still have a stipe but the cap does not open fully, while in gasteroid species, fruitbodies are completely closed and the stipe is reduced; in both cases, the spore-bearing structure is made up of convoluted gills that are more or less crowded andanastomosed.[39] These closed-fruitbody species represent a continuum of secotioid to gasteroid,above-ground tobelow-ground fruitbodies, with spores forcibly discharged or not.[25][39][40] Secotioid or gasteroidLactarius exude latex just like their agaricoid relatives.[3][25][40]
Thecorticioid species ofBoidinia,Gloeopeniophorella, andPseudoxenasma develop crust-like fruitbodies with a smooth, porous, or flaky surface and grow on tree logs or dead branches.[10][41][42][43]
Spores ofLactarius rubidus, showing ornamentation with a blue, amyloid stain reaction that is typical for Russulaceae
All Russulaceae, including the corticioid species, are characterised by spherical to ellipticbasidiospores with a faint to very distinct (e.g. warty, spiny, or crested) ornamentation thatstains bluish-black withMelzer's reagent (anamyloid stain reaction).[10][30]Basidia (spore-bearing cells) are usually club-shaped and four-spored.[44] Russulaceae species do not haveclamp connections.[45]
Characteristic cells with an oily content (gloeocystidia) are found in thehymenium. In Russulaceae, these show a positive colour reaction when treated with sulfoaldehydes (sulfovanillin is mostly used).[10][30] They are also present in the hyphal sheath of ectomycorrhizal roots colonised by Russulaceae.[14]
The feature responsible for the brittle fruitbody structure in the mushroom-forming species are globular cells, calledsphaerocytes orsphaerocysts, that compose the flesh (trama) alongside the usualhyphae.[30] Sometimes, these cells are clustered, and the position and arrangement of these clusters differs among genera.[30]
Another particular trama cell type arelactiferous hyphae (alsolactifers). These are hyphae carrying the "milk" or "latex" exuded by themilk-caps; they react positively with sulfoaldehydes, form an abundantly branched system in the trama and end aspseudocystidia in the hymenium.[30] In general, onlyLactarius,Lactifluus andMultifurca furcata possess lactifers.[15] InRussula, similar hyphae can sometimes be observed in the trama, but these are not as abundantly branched as real lactifers and do not extend into the hymenium as pseudocystidia.[30] This traditional distinction line between the "milk-caps" andRussula is however less evident in some tropical species presenting intermediate states.[36]
Zonate caps are a feature of several species of Russulaceae inLactarius andMultifurca.
Some characteristics of the mushroom-forming genera (marked with * below) can be less obvious or absent in tropical species.[15][36] Distinguishing betweenLactarius andLactifluus based on morphology alone is quite difficult, as clearsynapomorphies for both genera have yet to be identified.[17] Most field guides treat the two genera together, often becauseLactifluus is not yet recognised as a separate genus.[33][46]
Boidinia: corticioid; loose texture; surface smooth, with pores, or flaky; spores spherical with spiny to warty ornamentation.[10][41] Note that the genus is polyphyletic and needs to be redefined.[10]
Gloeopeniophorella: corticioid; surface almost smooth; hyphae without clamp connections; thick-walled cystidia (metuloids) and gloeocystidia present; spores with wrinkled (rugose) ornamentation.[43]
Lactarius: agaricoid or gasteroid; exuding latex*; caps sometimes zonate, viscose or glutinate, but never annulate; rarely thick-walled cells in cuticles of the cap (pileipellis) and the stipe (stipitipellis) and sphaerocytes in the gills.[15][17]
Lactifluus: agaricoid or pleurotoid; exuding latex*; caps never zonate, viscose or glutinate, but sometimes annulate; thick-walled cells in cap and stipe cuticles; often sphaerocytes in the gill trama.[15][17]
Multifurca: agaricoid; caps zonate (also visible in cut through trama); gills regularly forked; onlyM. furcata exuding latex; spore print orange; spores very small; microscopical trama and hymenium features very variable.[15]
Pseudoxenasma: corticioid; wax-like texture; gloeocystidia with spherical apical appendices; basidia developing laterally on hyphae (pleurobasidia); spores broadly ellipsoid to roughly spherical, with warty ornamentation.[42]
Russula: agaricoid, gasteroid or pleurotoid; never exuding latex; caps often brightly coloured with stipe and gills much paler; caps not zonate*; spore print white, cream, ochre, or orange; no true lactiferous hyphae*; sphaerocytes abundant in gill, cap, and stipe trama.[15][30]
The Russulaceae as a whole have a worldwide distribution, but patterns differ among genera.Russula is the most widespread, found in North,[47][48] Central[49][50] and South America,[32][51] Europe,[33] temperate[52][53] and tropical Asia,[54][55] Africa,[56] and Australasia.[36][57][58] It is the only Russulaceae genus that occurs in theNothofagus zone of temperate South America.[59]
Lactarius is mainly known from the north temperate zone, but some species also occur in tropical Asia and Africa.[17]Lactifluus has a more tropical distribution thanLactarius, with most species known from tropical Africa, Asia, South America, and Australasia, but some also occurring in the north temperate zone.[17]Multifurca is the rarest among the four mushroom genera, known only from some punctual records in North and Central America, Asia, and Australasia.[15][19]
Species ofLactarius,Lactifluus, andRussula have repeatedly beenintroduced with trees outside their native range: An overview article lists introductions in Chile, Argentina, Uruguay, Brazil, the US, Great Britain, the Faroe Islands, South Africa, China, Thailand, and New Zealand.[60]
Among the corticioid genera,Pseudoxenasma is only known from Europe.[61] In contrast,Boidinia species have been found in Europe,[62] Taiwan,[63] and Japan,[41] andGloeopeniophorella species in North America,[64] South America,[43][65] Europe,[66] West Africa,[65] Taiwan,[63] Australia,[43] and New Zealand.[43]
Ectomycorrhizal Russulaceae are found in a wide variety of habitats ranging from high latitudes to the tropics.
The generaLactarius,Lactifluus,Multifurca andRussula form a mutualisticectomycorrhizal rootsymbiosis with trees and shrubs, exchanging mineral nutrients forphotosynthetic sugar. They are one of several fungal lineages that have evolved such a lifestyle and are sometimes referred to as the "/russula-lactarius" clade in the scientific literature.[67] Worldwide, they are one of the most frequently encountered lineages on ectomycorrhizal roots.[68] While some tropical species were initially believed to be parasitic, the observation that species fruiting on tree trunks do form ectomycorrhiza in tropical Guyana supports the view of an exclusively symbiotic lineage.[35]
Some Russulaceae are associated withmyco-heterotrophic plants of the Ericaceae subfamilyMonotropoideae, formingmonotropoid mycorrhiza.[91][92] This is anepiparasitic relationship, where the heterotrophic plant ultimately derives its carbon from the primary, ectomycorrhizal plant partner of the fungus.[92] The association is often very specific, with the heterotrophic plants only associating with selected fungus partners, including Russulaceae.[91][93]
Russulaceae are also an important group oforchid mycorrhizal fungi.[94] This symbiosis is mutualistic in the case of green orchids,[89] but a partly or fully epiparasitic relationship in the case of myco-heterotrophic[95][96] andmixotrophic[97] orchids, respectively. In some cases, the association with Russulaceae is, as in monotropoid mycorrhiza, very specific: the Mediterranean orchidLimodorum abortivum predominantly associates withRussula delica and closely related species;[97] inCorallorhiza maculata, different genotypes of the same species have distinctRussula partners.[95]
The corticioid species inBoidinia,Gloeopeniophorella, andPseudoxenasma aresaprotrophic,wood-degrading fungi that develop ondead wood.[10] Their early-branching positions in the phylogeny suggests this has been the ancestral trophic mode of the Russulaceae, and that the mycorrhizal lifestyle(see above) evolved later.[10] The saprotrophic nature of these species has been questioned, based on the observation that other inconspicuous, crust-forming fungi are ectomycorrhizal;[14] a subsequent author reaffirms nevertheless that "[n]one of the corticioid species in the family shows any sign of mycorrhizal activity."[13]
Hypogeous fruitbodies, or fruitbodies developing below ground, occur inLactarius andRussula and have previously been considered as distinct genera (seeSystematics and taxonomy: Internal systematics). As such species are especially diverse in some warm and dry regions, e.g. in Spain,[3] California,[98] or Australia,[57] below-ground fruiting has been interpreted as an adaptation to drought.[39] However, hypogeous Russulaceae are also known from cold temperate regions[23][99] and tropical rainforest.[25] The fact that hypogeous species in the Russulaceae do not form their own lineages but are scattered inRussula orLactarius shows that this type of fruiting evolved several times.[25] It is believed that these changes are evolutionarily quite recent.[25]
Russulaceae fruitbodies are subject toparasitisation by other fungi. The genusAsterophora develops on old fruitbodies of the mushroom species in the family,[46] as doesDendrocollybia racemosa on at leastRussula crassotunicata.[100] Fruitbodies ofLactifluus orRussula species otherwise hot-tasting and unpalatable are regarded as choice edibles in North America when infected by the "lobster mushroom"Hypomyces lactifluorum.[46] Heterotrophic plants, includingorchids ormonotropoids, also parasitise ectomycorrhizal Russulaceae and their plant partners – see above,Other types of mycorrhiza.
As with most fungi,[101] little information is available on the threat of extinction for Russulaceae species, and they have not been assessed in theInternational Union for the Conservation of Nature's Red List.[102] However, national lists contain some species ofLactarius,Lactifluus andRussula, indicating that they have small populations and are endangered, e.g. in Great Britain,[103] Switzerland,[104] the Czech Republic,[105] and New Zealand.[106]
Although data on Russulaceae themselves are scarce, more is known about the habitats they occur in, especially for the ectomycorrhizal species which depend on their host plants: Several of these habitats are affected by loss or degradation, such as peatlands,[107] Mediterranean forests and scrub[108] or tropical African dry woodland.[109] Similarly, dead wood, the habitat of the corticioid Russulaceae, is rare in many exploited forests and needs special management.[110]
Recent studies have found some traditional Russulaceae species to comprise several cryptic species (seeSystematics and taxonomy: Species diversity). This may imply that distribution range and population size for each of such distinct species are smaller than previously thought.[111]
Lactarius indigo and anotherLactarius species for sale on a market in Guatemala
Several species ofLactarius,Lactifluus andRussula are valued as excellent edible mushrooms. This is the case for example for the north temperate speciesLactarius deliciosus,Lactifluus volemus, orRussula vesca, and other species are popular in other parts of the world, e.g.Lactarius indigo in Mexico, orLactifluus edulis in tropical Africa.[112] Some species, likeRussula vesca, can even be eaten raw.[113] The brittle texture ofRussula fruitbodies makes them different from other mushrooms and is not appreciated by some.[114]
Cultivation of edible Russulaceae, as in other ectomycorrhizal fungi, is challenging, since the presence of host trees is required. In spite of this difficulty, the EuropeanLactarius deliciosus has been successfully grown in "mushroom orchards" in New Zealand.[122]
Fruitbodies of Russulaceae have been the subject ofnatural product research, and different classes of organic compounds have been isolated from them.
Aroma compounds are responsible for the particular odour or taste in some species, e.g.sotolon in thefenugreek-smellingLactarius helvus,[123] or the similarquabalactone III inLactarius rubidus which causes a maple syrup-like odor in dried specimens.[124]Pigments have been isolated from brightly coloured species, e.g. (7-isopropenyl-4-methylazulen-1-yl)methyl stearate from the blueLactarius indigo[125] orrussulaflavidin and a derivative from the yellowRussula flavida.[126] SomeRussula species contain pigmentedpteridine derivatives calledrussupteridines that are not found in the milk-caps.[127]Sesquiterpenes are characteristic secondary metabolites of many Russulaceae, especially milk-caps which have been quite intensively studied.[128][129] They are thought to be responsible for the hot taste in many species and may have deterrent, antifeeding functions in nature.[128]
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