Armillaria mellea
Template:Short description Template:Speciesbox Template:Mycomorphbox Armillaria mellea, commonly known as honey fungus, is an edible basidiomycete fungus in the genus Armillaria. It is a plant pathogen and part of a cryptic species complex of closely related and morphologically similar species. It causes Armillaria root rot in many plant species and produces mushrooms around the base of trees it has infected. The symptoms of infection appear in the crowns of infected trees as discoloured foliage, reduced growth, dieback of the branches and death. The mycelium is capable of producing light via bioluminescence.
The mushroom is widely distributed in temperate regions of the Northern Hemisphere. It typically grows on hardwoods but may be found around and on other living and dead wood or in open areas.
TaxonomyEdit
The species was originally named Agaricus melleus by Danish-Norwegian botanist Martin Vahl in 1790; it was transferred to the genus Armillaria in 1871 by Paul Kummer.<ref name="urlMycoBank: Armillaria mellea"/> Numerous subtaxa have been described:
| Name | Authority | Year |
|---|---|---|
| var. camerunensis | Henn.<ref name="Hennings 1895"/> | 1895 |
| var. flava | Peck<ref name="Peck 1897"/> | 1897 |
| var. glabra | Gillet<ref name="Gillet 1874"/> | 1874 |
| var. javanica | Henn.<ref name="Hennings 1900"/> | 1900 |
| var. maxima | Barla<ref name="Barla 1887"/> | 1887 |
| var. radicata | Peck<ref name="Peck 1891"/> | 1891 |
| var. viridiflava | Barla<ref name="Barla 1887"/> | 1887 |
| subsp. nipponica | J.Y.Cha & Igarashi<ref name="Cha 1995"/> | 1995 |
| f. rosea | Calonge & M.Seq.<ref name="Calonge 2003"/> | 2003 |
| f. sabulicola | A. Ortega & G. Moreno<ref>MycoBank #584201</ref> | 2010 |
MycoBank also lists f. mellea, subsp. mellea, and var. mellea as current with a "(?)".<ref name=mycosearch/>
Reclassified speciesEdit
Armillaria mellea once included a range of species with similar features that have since been reclassified. The following are reassigned subtaxa, mostly variety-level entries from the 19th century:<ref name="Ross-Davis 2012"/>
| Name | Authority | Year | Current name |
|---|---|---|---|
| var. minor | Barla<ref name="Barla 1887"/> | 1887 | A. mellea (variety simply discarded) |
| var. bulbosa | Barla<ref name="Barla 1887"/> | 1887 | A. lutea |
| var. exannulata | Peck<ref name="Peck 1893"/> | 1893 | Desarmillaria tabescens |
| var. laricina | (Bolton) Barla<ref name="Barla 1887"/> | 1887 | A. laricina |
| var. obscura | Gillet<ref name="Gillet 1874"/> | 1874 | A. ostoyae |
| var. sulphurea | (Weinm.) Fr.<ref name="Karsten 1879"/> | 1879 | Agaricus sulphureus Weinm. (?)<ref>Question mark from MycoBank. Not to be confused with Agaricus sulphureus Bull,. which is a synonym for Tricholoma sulphureum. Some sources instead just assign to A. mellea, discarding the variety part.</ref> |
| var. tabescens | (Scop.) Rea & Ramsb. | 1917 | Desarmillaria tabescens |
| var. versicolor | (With.) W.G.Sm.<ref name="Smith 1908"/> | 1908 | A. versicolor Withering 1801 |
Common namesEdit
It is commonly known as honey fungus, stump mushroom, stumpie, honey mushroom, pipinky or pinky,Template:Citation needed
DescriptionEdit
The basidiocarp of each has a smooth cap Template:Convert in diameter,<ref name=":5" /> convex at first but becoming flattened with age often with a central raised umbo, later becoming somewhat dish-shaped. The margins of the cap are often arched at maturity and the surface is sticky when wet. Though typically honey-coloured, this fungus is rather variable in appearance and sometimes has a few dark, hairy scales near the centre somewhat radially arranged. The gills are white at first, sometimes becoming pinkish-yellow or discoloured with age, broad and fairly distant, attached to the stipe at right angles or are slightly decurrent. The flesh of the cap is whitish and has a sweetish odour and flavour with a tinge of bitterness.
The stipe is of variable length, up to about Template:Convert long and Template:Convert in diameter. It is fibrillose and of a firm spongy consistency at first but later becomes hollow. It is cylindrical and tapers to a point at its base where it is fused to the stipes of other mushrooms in the clump. It is whitish at the upper end and brownish-yellow below, often with a very dark-coloured base. There is a broad persistent skin-like ring attached to the upper part of the stipe. This has a velvety margin and yellowish fluff underneath and extends outwards as a white partial veil protecting the gills when young.
Under the microscope, the spores are approximately elliptical, 7–9 by 6–7 μm, inamyloid with prominent apiculi (short, pointed projections) at the base. The spore print is white. The basidia (spore-producing structures) lack basal clamps.<ref>Template:Cite book</ref><ref name="Kuo">{{#invoke:citation/CS1|citation |CitationClass=web }}</ref>
The main part of the fungus is underground where a mat of mycelial threads may extend for great distances. They are bundled together in rhizomorphs that are black in this species.<ref name="Kuo" /> The fungal body is not bioluminescent but its mycelia are luminous when in active growth.<ref name="Desjardin 2008" />
Similar speciesEdit
In addition to a number of reclassified species, Armillaria gemina lacks the yellow cap background and A. nabsnona has a darker hue.<ref name="audu">Template:Cite book</ref>
Distribution and habitatEdit
Armillaria mellea is widespread in northern temperate zones. It has been found throughout North America,<ref name="audu" /> and in Europe and northern Asia. It has been introduced to South Africa. It grows parasitically on a large number of broadleaf trees. It fruits in dense clusters at the base of trunks or stumps.<ref name="Roberts 2011" />
EcologyEdit
Armillaria mellea prefers moist soil and lower soil temperatures<ref name=":1">{{#invoke:citation/CS1|citation |CitationClass=web }}</ref> but it can also withstand extreme temperatures, such as forest fires, due to the protection of the soil.<ref name=":0">{{#invoke:citation/CS1|citation |CitationClass=web }}</ref> It is found in many kinds of landscapes, including gardens, parks, vineyards, tree production areas, and natural landscapes.<ref name=":1" />
Armillaria mellea typically is symbiotic with hardwood trees and conifers,<ref name=":0" /> including orchards, planted forests, vineyards,<ref>{{#invoke:citation/CS1|citation |CitationClass=web }}</ref> and a few herbaceous plants.<ref name=":1" /> It infects new hosts through rhizomorphs<ref name=":2" /><ref name=":3" /> and basidiospores.<ref>{{#invoke:citation/CS1|citation |CitationClass=web }}</ref> It is rare for basidiospores to be successful in infecting new hosts and often colonize woody debris instead,<ref name=":1" /> but rhizomorphs, however, can grow up to ten feet long in order to find a new host.<ref name=":3" />
There are few signs, and they are often difficult to observe. The most prominent sign is honey-coloured mushrooms at the base of the infected plant.<ref name=":2">{{#invoke:citation/CS1|citation |CitationClass=web }}</ref> Additional signs include white, fan-shaped mycelia and black rhizomorphs with diameters between Template:Convert.<ref name=":1" /> These usually are not as noticeable because they occur beneath the bark and in the soil, respectively.<ref name=":1" /> The symptoms are much more numerous, including slower growth, dieback of branches, yellowing foliage,<ref name=":2" /> rotted wood at base and/or roots, external cankers, cracking bark, bleeding stem, leaf wilting, defoliation, and rapid death.<ref name=":1" /> Leaf wilting, defoliation, and dieback occur after the destruction of the cambium.<ref name=":1" />
It is one of the most common causes of death in trees and shrubs in both natural and cultivated habitats, and cause steady and substantial losses.
Disease cycleEdit
Armillaria mellea infects both through basidiospore<ref name=":3">{{#invoke:citation/CS1|citation |CitationClass=web }}</ref> and penetration of host species by rhizomorphs<ref name=":2" /> which can grow up to Template:Convert long per year<ref>Template:Cite journal</ref> to find new, living tissue to infect.<ref name=":3" /> However, infection of living host tissue through basidiospores is quite rare.<ref name=":1" /> Two basidiospores must germinate and fuse to be viable and produce mycelium.<ref name=":1" /> In the late summer and autumn, Armillaria mellea produces mushrooms with notched gills, a ring near the cap base, and a white to golden color.<ref name=":0" /> They do not always appear,<ref name=":1" /> but when they do they can be found on both living and dead trees near the ground.<ref name=":1" /> These mushrooms produce and release the sexually created basidiospore which is dispersed by the wind.<ref name=":1" /> This is the only spore-bearing phase. The fungus overwinters as either rhizomorphs or vegetative mycelium.<ref>{{#invoke:citation/CS1|citation |CitationClass=web }}</ref> Infected wood is weakened through decay in roots and tree base after destruction of the vascular cambium and underlying wood.<ref name=":1" />
Trees become infected when rhizomorphs growing through the soil encounter uninfected roots. Alternatively, when infected roots come into contact with uninfected ones the fungal mycelium may grow across. The rhizomorphs invade the trunk, growing between the bark and the wood and causing wood decay, growth reduction and mortality. Trees that are already under stress are more likely to be attacked but healthy trees may also be parasitized. The foliage becomes sparse and discoloured, twig growth slows down and branches may die back. When they are attacked, the Douglas-fir, western larch and some other conifers often produce an extra large crop of cones shortly before dying. Coniferous trees also tend to ooze resin from infected areas whereas broad-leaved trees sometimes develop sunken cankers. A growth of fruiting bodies near the base of the trunk confirms the suspicion of Armillaria root rot.<ref>{{#invoke:citation/CS1|citation |CitationClass=web }}</ref>
In 1893, the American mycologist Charles Horton Peck reported finding Armillaria fruiting bodies that were "aborted", in a similar way to specimens of Entoloma abortivum. It was not until 1974 that Roy Watling showed that the aborted specimens included cells of both Armillaria mellea and Entoloma abortivum. He thought that the Armillaria was parasitizing the Entoloma, a plausible hypothesis given its pathogenic behaviour.<ref>{{#invoke:citation/CS1|citation |CitationClass=web }}</ref> However, a 2001 study by Czederpiltz, Volk and Burdsall showed that the Entoloma was in fact the microparasite. The whitish-grey malformed fruit bodies known as carpophoroids were the result of E. abortivum hyphae penetrating the Armillaria and disrupting its normal development.<ref name="Czederpiltz 2001"/>
The main part of the fungus is underground where a mat of mycelial threads may extend for great distances. The rhizomorphs of are initiated from mycelium into multicellular apices of rhizomorphs, which are multicellular vegetative organs that exclude soil from the interior of the rhizomorph tissues. The rhizomorphs spread through far greater distances through the ground than the mycelium. The rhizomorphs are black in this species.<ref name=Kuo/> The fungal body is not bioluminescent but its mycelia and rhizomorphs are luminous when in active growth.<ref name="Desjardin 2008"/> A. mellea producing rhizomorphs is parasitic on woody plants of many species, including especially shrubs, hardwood and evergreen trees. In one example, A. mellea spread by rhizomorphs from an initially infected tree killed 600 trees in a prune orchard in 6 years. Each infected tree was immediately adjacent to an already infected one, the spread by rhizomorphs through the tree roots and soil.<ref>(Piper and Fletcher, 1903, Wash. Age. Exp. Sat. But., 59: 1–14); cited in Rhizomorph Development in A. mellea, Ph.D. thesis, by Philip Snider(1957), Farlow Herbarium Library Harvard Univ., 20 Divinity Ave., Cambridge, Mass.</ref>
ManagementEdit
There are fungicides or management practices that will kill A. mellea after infection without damaging the infected plant, but these practicies are still being studied.<ref>Template:Cite journal</ref> There are practices that can extend the life of the plant and prevent further spreading. The best way to extend the plant life is to improve the host condition through supplemental watering and fertilization.<ref name=":2" /> To prevent further spread, it is recommended to regulate irrigation to avoid water stress, keep the root collar dry, control defoliating pathogens, remove stumps, fertilize adequately, avoid physical root damage and soil compaction, and to not plant trees that are especially susceptible to the disease in places where A. mellea has been recorded.<ref name=":1" /> There is also some evidence that biological control using the fungus genus Trichoderma may help. Trichoderma is a predator of A. mellea and is often found in woodchips.<ref name=":1" /> Therefore, chipping or grinding dead and infected roots will give Trichoderma its preferred habitat and help it proliferate. Solarization will also create an ideal habitat as dry soil and higher soil temperatures are preferable for Trichoderma but poor conditions for A. mellea.<ref name=":1" />
EdibilityEdit
Armillaria mellea mushroom are considered good edibles, though not preferred by some, and the tough stalks are usually excluded.<ref name=":5">Template:Cite book</ref> They are best collected when young and thoroughly cooked.<ref name="tfb">Template:Cite book</ref> Some individuals have reported "allergic" reactions that result in stomach upsets. Some authors suggest not collecting mushrooms from the wood of various trees, including hemlock, buckeye, eucalyptus, and locust.Template:Citation needed They may have been used medicinally by indigenous peoples as a laxative.<ref>Template:Cite book</ref>
The mushrooms have a taste that has been described as slightly sweet and nutty, with a texture ranging from chewy to crunchy, depending on the method of preparation. Parboiling mushrooms before consuming removes the bitter taste present in some specimens, and may reduce the amount of gastrointestinal irritants.<ref>Template:Cite book</ref> According to one guide, they must be cooked before eating.<ref>Template:Cite book</ref> Drying the mushrooms preserves and intensifies their flavour, although reconstituted mushrooms tend to be tough to eat.<ref name="Kuo 2007" /> The mushrooms can also be pickled and roasted.
CultivationEdit
Cultivation of A. mellea started with cultivation of its mycellia, which is used to support the cultivation of Gastrodia elata, a non-photosynthetic plant used in traditional Chinese medicine. This kind of cultivation has been present since 1994 and uses pieces of wood inoculated with the fungus.<ref>{{#invoke:citation/CS1|citation |CitationClass=web }}</ref> In 2017, farmers from Heilongjiang succeeded in producing fruiting bodies (mushrooms) through cultivation.<ref>{{#invoke:citation/CS1|citation |CitationClass=web }}</ref> By 2019, the spent myceliated wood from Gastrodia cultivation is routinely used to seed new wood for mushroom production.<ref>{{#invoke:citation/CS1|citation |CitationClass=web }}</ref>
ChemistryEdit
Several bioactive compounds have been isolated and identified from the fruit bodies. The triterpenes 3β-hydroxyglutin-5-ene, friedelane-2α,3β-diol, and friedelin were reported in 2011.<ref name="Guo 2011"/> Indole compounds include tryptamine, Template:Nowrap and serotonin.<ref name="Muszynska 2011"/>
The fungus produces cytotoxic compounds known as melleolides. Melleolides are made from orsellinic acid and protoilludane sesquiterpene alcohols via esterification. A polyketide synthase gene, termed ArmB, was identified in the genome of the fungus, which was found expressed during melleolide production. The gene shares c. 42% similarity with the orsellinic acid synthase gene (OrsA) in Aspergillus nidulans. Characterization of the gene proved it to catalyze orsillinic acid in vitro. It is a non-reducing iterative type-1 polyketide synthase. Co-incubation of free orsellinic acid with alcohols and ArmB showed cross-coupling activity. Therefore, the enzyme has transesterification activity. Also, there are other auxiliary factors suspected to control substrate specificity.<ref>Lackner et al., 2013</ref> Additionally, halogen modifications have been observed. Overexpression of annotated halogenases (termed ArmH1-5) and characterization of the subsequent enzymes revealed in all five enzymes the chlorination of mellolide F. In vitro reactions of free standing substrates showed that the enzymes do not require auxiliary carrier proteins for substrate delivery.<ref>Wick et al., 2015</ref>