Armillaria mellea

Overview

Armillaria mellea is the cause of Armillaria root rot, shoestring rot, and also plays a secondary role in disease complexes such as oak decline, maple blight, and ash dieback.

Host range

Large. Hundreds of species of trees, shrubs, vines, and forbs (herbaceous flowering plants that are not graminoids (grasses, sedges and rushes) growing in forests, along roadsides, and in cultivated areas. Among shade and ornamental trees, oaks and maples are the ones most commonly infected. Other woody plant hosts include azaleas, beeches, birches, black locust, boxwoods, cedars, currants, dogwoods, Douglas-fir, elms, firs, golden rain tree, hemlocks, hickories, hophornbeam, Katsura tree, larches, lilacs, mountainashes, pines, planetrees, poplars, privets, rhododendrons, roses, sassafras, spruces, sycamores, tree of heaven, tuliptree, willows, yews, and many fruit and nut trees. The Armillaria fungi may infect many other kinds of woody plants if conditions are favorable for infection (See Table 1).

Distribution

Cosmopolitan. A common soilborne fungus in temperate and tropical regions.

Symptoms

The symptoms of the aboveground parts are similar to those caused by other root rot diseases. The commonest symptoms are reduced growth, yellowish leaves, dieback of twigs and branches, and gradual or sudden death of the tree. Initially the infected trees are scattered but due to the spread of the fungus from its primary infection point, circular areas of diseased trees appear. Diagnostic characteristics appear at decayed areas in the bark, at the root collar, and on the roots. White mycelial fans form between the bark and wood. Because these fungi commonly inhabit roots, their detection is difficult unless characteristic mushrooms are produced around the base of the tree or symptoms become obvious in the crown or on the lower stem.

Rhizomorphs

Mycelial fan under bark of black oak

Fruiting bodies

Fruiting bodies at the base of a living oak tree

Dispersal

Under favorable conditions, mushrooms may arise from the rhizomorphs. Millions of basidiospores produced in the mushroom caps are carried by the wind to dead stumps or injured bark at the base of living plants. The rhizomorphs advance through the soil (rate dependant on climate). The spread of the disease is not so much a matter of the fungus growing toward the roots of a healthy tree or shrub as it is of a healthy plant's roots growing through the soil to wood already infected with Armillaria. Some species of the fungus or perhaps strains within species, are virulent parasites while others are opportunistic and act selectively on small or weak individual plants. Armillaria also colonizes the declining root systems of plants felled or killed by other agents.

Environmental conditions conducive to disease

Weakened trees and healthy trees, either killing them outright or predisposing them to attacks by other fungi or insects. Trees weakened by drought. Huge losses occur in orchards or vineyards planted in recently cleared forestlands or in forest tree plantations. In coastal forests, the fungus occurs commonly as a butt rotter in old trees and a decayer of dead and down trees.

Diagnostic procedure(s) used

Pure culture on malt agar

Isolation from field samples may be made from decayed wood, basidiomes, fans or rhizomorphs. Surface disinfestation is usually necessary. Rhizomorph growing tips are advantageous in that they grow faster than undifferentiated hyphae and may thus escape contaminants. Modified Weinhold’s medium, which is the defined medium for Armillaria provides good rhizomorph production. Benomyl dichloron streptomycin (BDS) and orthophenylphenate agar (OPP) media are two commonly used media that generally works well for Amillaria species. Tape mount of mycelial growth or wait for appearance of basidiocarp, thin section, and observe under microscope. Spore print is white.

In the absence of mushrooms, field identification of Armillaria root disease is based on the presence of mycelial fans, rhizomorphs and/or decay pattern (white, spongy rot of wood with zone lines or pseudosclerotial plates). Distinguishing among the species of Armillaria in the field is difficult. Species differ to some extent in cultural characteristics; however, such identifications may only be practical in regions with a limited number of Armillaria species. For the present, critical identification of cultures relies on pairings with tester strains. Although various techniques are employed most rely on the difference between cultural mat morphology of haploid single-basidiospore isolates and putatively diploid isolates from decay, fans or rhizomorphs. When sexually compatible single-basidiospore isolates of the same species are placed near each other on malt extract agar (MAE 1-3%) and allowed to grow together for over three weeks, the fluffy white mycelium may flatten, darken and become crustose. If the isolates are of different species, the mycelia remain white or light tan, continue to produce abundant aerial mycelium and do not become crustose.

Pathogen information

Classification

Physalacriaceae, Agaricales

Anamorph.

Rhizomorpha subcorticalis

Macroscopic

Positive signs are found at the trunk base or in the main roots near the root collar. White or creamy white mycellial fans develop between the bark and wood. The Armillaria fungi have a strong mushroom odor. The rhizomorphs are 1 to 3 millimeters in diameter, round or flattened and branched, and they consist of hyphal strands bundled together and enclosed within suberized cells. The cordlike rhizomorphs grow over infected roots and outward from a dead tree into the soil. Clusters of yellowish brown basidiocarps appear in late autumn after a rainy period are often speckled dark brown. The lower surface is light brown to white with radiating gills which are attached to and run a little way down the stem. The mushrooms have a persistent whitish collar or ring around the upper part of the stem. The mushrooms develop near severely diseased roots and emerge through the soil, near the base of a trunk. Spore print is white.

Microscopic

This is the only species of Armillaria that lacks clamp connections at the base of the basidia. Basidiospores are 7.2-8.9 X 5.6-6.7 µm, elliptical, smooth, not amyloid. See Key to North American species.

Management recommendations

1. Armillaria can be excluded if care is taken to insure that all planting material brought into an area is disease free. Plant only well adapted trees and shrubs in sites suited for vigorous growth.
2. Fruit trees, pine plantations, or ornamental trees and shrubs should NOT be planted in recently cleared areas where Armillaria has been a problem. These areas should be planted with nonsusceptible crops such as corn, small grains, and grasses for a few years to help eliminate the fungus. Another possibility: use the infested area for lawn, vegetable garden, rockery, or for annual and biennial flowers.
3. Clean cultivation of an orchard can help distribute Armillaria infected wood to other areas not infested with the fungus. A groundcover crop should be used to replace the procedure of clean cultivation.
4. In orchards and other areas where Armillaria is established, diseased trees and shrubs should be carefully dug up, including the stump, all large roots, stakes, or other wood harboring the fungus, and burned on the site instead of transported to a dump. All pruning wastes should be burned rather than incorporated into the soil to prevent the formation of new disease centers. Deprived of their food supply, any rhizomorphs left in the soil will soon die. Eradicating Armillaria from a site requires a thorough removal of all diseased and dead wood.
5. Plants found to be infected in only a few roots or a small part of the root collar can be saved for a time by carefully removing the soil to expose the root collar and buttress roots to aeration and drying from mid-spring to late autumn. Infected bark and wood on large roots, buttress or trunk should be excised back to healthy tissue. Replace the soil with Armillaria-free soil before the first heavy frost.
6. Maintain tree and shrub vigor by good cultural management practices: (1) regular fertilization, based on a soil test; (2) thorough watering during extended droughts; and (3) insect and disease control. Where possible, provide for adequate soil drainage in heavy, poorly drained sites. Avoid all root damage to established woody plants in areas where construction is to occur. This is particularly relevant to oak groves. Avoid soil fill and soil removal around valuable trees and shrubs.
7. If the precise source of infection is known and cannot be removed, it should be possible in some cases to prevent the rhizomorphs from reaching the trees and shrubs to be protected by sinking a sheet of heavy polyethylene vertically into the soil between diseased and healthy plant(s), provided it extends far enough laterally (several feet beyond the outer dripline) and at least a meter (3 feet) into the soil. A suitable deep ditch would have the same effect.
8. Fungicides applied to infected trees are not recommended.

Resistance or susceptibility of certain woody plants

Table 1. Resistance or Susceptibility to Armillaria Root Rot of Certain Woody Plants Adapted to Illinois

A partial listing taken largely from Resistance or Susceptibility of Certain Plants to Armillaria Root Rot, by Dr. Robert D. Raabe, Division of Agricultural Sciences, University of California, Leaflet 2591.

Immune or Highly Resistant
Abutilon or flowering maple		Black cherry		Dawn redwood		Mock-orange		Shademaster honeylocust
American sweet gum		Boxelder		English holly		Modesto ash		Shining sumac
American holly		Boxwood		French pear		Mulberry		Smoke tree
American plum		Callery pear		Ginnala maple, Amur maple		Osage orange		Southern magnolia
American chestnut		Cherry plum		Hackberry		Pawpaw		St. Johnswort (shrub form)
American or sweet elder		Chinese wisteria		Holly mahonia, Oregon grape		Pecan		Staghorn sumac
Amur cork tree		Chinese elm		Japanese pagoda tree		Planetrees or sycamore		Swamp birch
Austrian pine		Clematis		Japanese maple		Prairie crabapple		Tamarisk
Bald cypress		Colorado or white fir		Japanese flowering crabapple		Rose of Sharon		Thornless honeylocust
Bayberry		Common persimmon		Kentucky coffee tree		Russian olive, oleaster		Tree of honeylocust
Big-leaf maple, Oregon maple		Common catalpa		Maidenhair tree		Scots pine, Scotch pine		Tree of Heaven
								Tuliptree
Moderately Resistant
Black locust		European larch		Honeysuckle		Lalande pyracantha		Silk tree, mimosa
Bridal wreath		Glossy abelia, white abelia		Hybrid larch		Mazzard sweet cherry		Washington thorn
Common pear		Golden raintree		Japanese larch		Norway spruce		Yellow wood
Douglas fir		Green Japanese barberry		Japanese zelkova		Scarlet firethorn		Yew
Susceptible
American beech		English walnut		Japanese flowering cherry		Prostrate junipers		Sweet chestnut
Apple		European white birch		Katsura tree		Redbud		Tea crabapple
Bush cherry		European beech		Lilac		Rock cotoneaster		Weigela
Chinese chestnut		European hornbeam		Mahaleb cherry		Roses		Western red cedar
Chokecherry		Flowering almond		Narrowleaf firethorn		Rowal paulownia, Empress tree		Willows
Colorado blue spruce		Golden chain tree		Oakleaf hydrangea		Sargent crabapple		Siberian crabapple
Cutleaf crabapple		Gooseberry		Peach, flowering peach		Serian spruce
Eley crabapple		Grapes		Privets (except Japanese privet)		Shrubby St. Johnsworth

Key to North American species

Key to North American Armillaria species using macroscopic, microscopic, and distributional characters

Obtained from Tom Volk. Key to North American Armillaria species. Department of Biology, University of Wisconsin-La Crosse

1. Annulus lacking ................................................................A. tabescens

1. Annulus present.................................................................2

2. Pileus smooth, stipes pointed at the base, thick wooly annulus, no clamp at base of basidium or anywhere in basidiomata,

dist. mainly east of Rocky Mountains................................................................................................A. mellea

2. Pileus smooth or scaly, pointed or non-pointed stipe bases, at least some basidia basally clamped..........3.

3. Orange brown pileus, no scales, brown stipe, virtually all basidia basally clamped, second basidium emerges from clamp of first,

dist. western North America, on hardwoods................................................................................................A. nabsnona

3. Pileus brown to yellow brown, scales present or absent, more widely distributed..............................................4.

4. Annulus thick, scales on pileus, basidiomata often clustered, with pointed stipe bases................................................................5

4. Annulus cortinaceous (arachnoid, cobwebby), pileus not scaly (may have hairs), basidiomata clustered or single...........................6

5. On hardwoods, Eastern distribution, apparent distribution from Québec south to North Carolina. not known west of the

Appalachian Mountains........................................................................................................................................................................A .gemina

5. On hardwood or conifer, widely distributed through northern tier of states and throughout Canada, severely pathogenic...................................A. solidipes

6. Rare species in North America, apparently restricted to Washinton and British Columbia, on hardwoods,

often with deceptive double-appearing annulus................................................................................................................................NABS XI

6. More widely distributed, annulus arachnoid, not appearing double.......................................................................................................7

7. Some annulus cells greater than 8 µm diameter, on hardwoods in the East, on conifer in the West................................................................A. sinapina

7. All cells of annulus less than 8 µm diameter, non pathogenic species, mostly east of the Rocky Mountains, rare in the west...........................8

8. Indistinguishable from each other. A.gallica, A.calvescens

Bibliographic

• Agrios GN, 2005. Plant Pathology (5th ed). Elsevier Academic Press Publications, pp 448-452
• Arora D, 1986. Mushrooms Demystified. Ten Speed Press, p 196
• Basnayake V. Armillaria mellea(Vahl:Fr.) Kummer: Class Hymenomycetes. NC State University. Retrieved July 20, 2010, from http://www.cals.ncsu.edu/course/pp728/Armillaria/Armillaria.htm
• Petaky NR, 2001. Armillaria mellea. Department of Crop Sciences, University of Illinois. Retrieved July 20, 2010, from https://www.ipm.uiuc.edu/landturf/diseases/armillaria/index.html
• Farr DF and Rossman AY. Fungal Databases, Systematic Mycology and Microbiology Laboratory, ARS, USDA. Retrieved July 20, 2010, from http://nt.ars-grin.gov/fungaldatabases/
• Jones RK and Benson DM, 2001. Diseases in Woody Ornamentals and Trees in Nurseries. APS Press, p 264
• Sinclair WA, Lyon HH, Johnson WT, 1987. Diseases of Trees and Shrubs. Cornell University Press, p 308-310