1. PaDIL Species Factsheet

Scientific Name: ostoyae (Romagn.) Herink Marasmiaceae, , Agaricomycetidae, Basidiomycetes

Common Name Live link: http://www.padil.gov.au/pests-and-diseases/Pest/Main/136613

Image Library Australian Biosecurity Live link: http://www.padil.gov.au/pests-and-diseases/

Partners for Australian Biosecurity image library

Department of Agriculture, Water and the Environment https://www.awe.gov.au/ Department of Primary Industries and Regional Development, Western Australia https://dpird.wa.gov.au/ Plant Health Australia https://www.planthealthaustralia.com.au/ Museums Victoria https://museumsvictoria.com.au/ 2. Species Information

2.1. Details Specimen Contact: Dr Jose R. Liberato - [email protected] Author: Liberato JR, Kunca A & Korhonen K Citation: Liberato JR, Kunca A & Korhonen K (2006) Armillaria root rot( )Updated on 7/23/2016 Available online: PaDIL - http://www.padil.gov.au Image Use: Free for use under the Creative Commons Attribution-NonCommercial 4.0 International (CC BY- NC 4.0)

2.2. URL Live link: http://www.padil.gov.au/pests-and-diseases/Pest/Main/136613

2.3. Facets Status: Exotic Regulated Pest - absent from Australia Group: Fungi Commodity Overview: Horticulture, Forestry Commodity Type: Timber, Fresh Fruit, Stone fruits Distribution: USA and Canada, Europe and Northern Asia, South and South-East Asia

2.4. Other Names Armillaria montagnei var. umbrinolutea Singe Armillaria obscura (Pers. ex Secr.) Herink Armillaria polymyces (Secr.) Sing. & Clem Armillariella mellea var. obscura Gillet Armillariella ostoyae Romagn. Honey

2.5. Diagnostic Notes Symptoms:

Armillaria ostoyae colonizes the root system of woody plants and causes non-specific symptoms such as reduction of shoot growth, changes in foliar characteristics, crown dieback, stress-induced reproduction, basal stem indicators (exudates, cankers, cracks, or flutes at or just above the root collar), and death. Signs of the (mycelial fans, rhizomorphs and ) can occur on the root collar and lower bole of the tree. A detailed description of these symptoms and signs is provided by Morrison et al. (1991).

Typical symptoms on pines are: The whole crown becomes brown and dies simultaneously, strong resin exudation at the root collar and white mycelial sheets under the bark. Often A. ostoyae produces increasing gaps in pine stand.

The fungi:

Pileus 5—10 cm in diameter, broad, hemispherical-campanulate or obtusely parabolic, then convex and finally plane. Surface dry, sometimes of pale colours like orange white or caramel (brown) but usually darker, with distinct scales in shades of dark reddish colors or dark brownish colour, distributed over the surface but more densely toward the centre. Margin inrolled at first then down turned, sometimes striated, entire, usually concolorous to cap but sometimes paler, often cream, flesh or camel. Flesh firm, 1-2 cm thick at the apex of the , context white. Lamellae white or cream when young, to greyish orange, cinnamon later, rather close, adnate to slightly decurrent becoming sinuate in mature specimens, thick at the point of attachment to the stipe but thinner toward the margin. Stipe central, 5-20 cm long, 1.5 cm thick at the apex, clavate when young becoming more or less equal, fibrous, context white to alabaster, often with bright yellow to greenish yellow mycelial fibres at base only, covered with fibers ranging from greyish orange, light brown, burnt sienna and hazel, staining black or sometimes mahogany, sometimes deeply striated. Annulus thick, membranous, usually white to alabaster, circled with a thick fluffy band at margin ranging from tan to chestnut, broken in many places leaving the stipe marked and covered at many locations with dark fluffy remmants concolours to ring. ivory in mass, broadly elliptical to ovate, 5.5-7 x 8-11 µm, smooth, apiculate and nonamyloid. Basidia clavate, four-spored, some with a clamp connection(*). Pleurocystidia absent. Margin of lamellae composed of three layers: a suprapellis consisting of a loose array of more or less parallel, regular, thick- walled hyphae, 5-20 x 18-55 µm; a mediopellis formed of a tight array of parallel, almost regular, very thick walled cells 4-9 x 9-64 µm, staining blue in toluidine blue; a subpellis composed of a loose array irregular, thin-walled globular cells, 9-15 x 25 µm, arranged in a complex network. Subhymenial hyphae filamentous, unclamped (**), binucleate. trama bilateral (Bérubé & Dessureault 1988).

Notes

* In natural specimens that the senior author has investigated the basidia had regularly a clamp connection (on the other hand, basidiocarps of A. ostoyae produced in pure culture have usually clampless basidia).

** In natural fruit bodies, some clamped binucleate hyphae occur in the subhymenium at the base of basidia.

1. Additional information about the colour of the basidiocarps is provided by Bérubé & Dessureault (1988).

2. According to Termorshuizen & Arnolds (1987), the names Armillariella obscura sensu Romagn., Armillaria obscura sensu Marxmuller and Armillariella polymyces sensu Sing. & Clemencon were misapplied to this pathogen.

Diagnosis:

Until the late 1970s, most plant pathologists referred to all annulate Northern Hemisphere species of Armillaria as A. mellea (sensu lato). The 'mellea complex' has been split in many species, including A. ostoyae. Reviews about the of Armillaria were provided by Watling et al. (1991) and Crop Protection Compendium (2005). Currently there are approximately 36 species of Armilla

2.6. References Anderson JB (1986) Biological species of Armillaria in North America: redesignation of groups IV and VIII and enumeration of voucher strains for other groups. Mycologia 78:837-839. Banik MT, Volk TJ, Burdsall Jr HH (1996) Armillaria species of the Olympic Peninsula of Washington state, including confirmation of North American biological species XI. Mycologia 88:492-496. Bérubé JA, Dessureault M (1988) Morphological characterization of Armillaria ostoyae and Armillaria sinapina sp. nov. Canadian Journal of Botany 66:2027- 2034. Bragaloni M, Anselmi N, Cellerino GP (1997) Identification of European Armillaria species by analysis of isozyme profiles. European Journal of 27:147-157. Crop Protection Compendium 2005 Edition. Armillaria ostoyae (armillaria root rot). CAB International, Wallingford, UK. Fox RTV (2000) Armillaria root rot: Biology, and control of honey fungus. Intercept Ltda: Andover UK). Guillaumin JJ, Anderson JB, Korhonen K (1991). Life cycle, interfertility, and biological species. In: Shaw CG, Kile GA, eds. Armillaria Root Disease. Agriculture Handbook No. 691. Washington, USA: USDA, Forest Service, 10-20. Guillaumin JJ, Anderson JB, Legrand P, Ghahari S, Berthelay S (1996) A comparison of different methods for the identification of genets of Armillaria spp. New Phytologist 133:333-343. Guillaumin JJ, Berthelay S (1981) Détermination spécifique des armillaires par la méthode des groupes de compatibilité sexuelle. Spécialisation écologique des espèces françaises. Agronomie 1:897-908. Hagle SK, Gibson KE, Tunnock S (2003) Field Guide to Diseases and Insect Pests of Northern & Central Rocky Mountain . 2nd ed. USDA Forest Service. Available online at http://www.fs.fed.us/r1-r4/spf/fhp/field_guide/index.htm. Harrington TC, Wingfield BD (1995) A PCR-based identification method for species of Armillaria. Mycologia 87:280-288. Jacobs KA, MacDonald JD, Cobb Jr FW, Wells K (1994) Identification of Armillaria species in California. Mycologia 86:113-116. Korhonen K (1980) The origin of clamped and clampless basidia in Armillaria ostoyae. Karstenia 20: 23-27. Morrison DJ, Williams RE, Whitney RD (1991) Infection, Disease Development, Diagnosis and Detection. In: Shaw III CG, Kile GA (eds) Armillaria Root Disease. Agriculture Handbook No. 691. Washington, USA: USDA, Forest Service, p. 62-75. Omdal D & Shaw III CG (1997) Armillaria root disease. In Hansen EM & Lewis KJ (eds) Compendium of diseases. APS Press: St Paul, MN. P. 13-14. Rishbeth J (1986) Some characteristics of the English Armillaria species in culture. Transactions of the British Mycological Society 85:213-218. Roll-Hansen F (1985). The Armillaria species in Europe. A literature review. European Journal of Forest Pathology 15:22-31. Romagnesi H (1970) Observations sur les Armillariella - I. Bulletin de la Société Mycologique de France 86:257-265. Schulze S, Bahnweg G (1998) Critical review of identification techniques for Armillaria spp. and Heterobasidion annosum root and butt rot diseases. Journal of Phytopathology 146:61-72. Termorshuizen A, Arnolds E (1987). On the nomenclature of the European species of the Armillaria mellea group. Mycotaxon 30:101-116. Termorshuizen AJ, Arnolds EJM (1997). Compatibility groups, species concepts and nomenclature in European Armillaria species. Mycotaxon 65:263- 272. Watling R, Kile GA, Burdsall HH (1991). Nomenclature, taxonomy and identification. In: Shaw CG, Kile GA, eds. Armillaria Root Disease. Agriculture Handbook No. 691. Washington, USA: USDA, Forest Service, 1-9. Watling R, Kile GA, Gregory NM (1982) The Armillaria - nomenclature, typification, the identity of Armillaria mellea and species differentiation. Transactions of the British Mycological Society 78:271-285. 3. Diagnostic Images

Top dieback (copyright, for use contact Pinus sylvestris saplings killed by A. ostoyae [email protected]) (Finland) (copyright, for use contact Host Symptoms: Andrej Kunca [email protected]). (www.forestryimages.org) Národné lesnícke Host Symptoms: Kari Korhonen Finnish centrum, Slovakia Forest Research Institute

Root deformation due to excess of resin flow Rhizomorphs (copyright, for use contact (copyright, for use contact [email protected]) [email protected]) Host symptoms - roots: Andrej Kunca Host symptoms - stem: Andrej Kunca (www.forestryimages.org) Národné lesnícke (www.forestryimages.org) Národné lesnícke centrum, Slovakia centrum, Slovakia

Mycelial fans under the bark – more than 2 Mycelial fans under the bark – fresh growing m up the stem. (copyright, for use contact edge (copyright, for use contact [email protected]) [email protected]) Host symptoms - stem: Andrej Kunca Host symptoms - stem: Andrej Kunca (www.forestryimages.org) Národné lesnícke (www.forestryimages.org) Národné lesnícke centrum, Slovakia centrum, Slovakia Mycelial fans under the bark (copyright, for Light orange brown color moving from the use contact [email protected]) edge to the center of the stem (copyright, for Host symptoms - stem: Andrej Kunca use contact [email protected]) (www.forestryimages.org) Národné lesnícke Host symptoms - stem: Andrej Kunca centrum, Slovakia (www.forestryimages.org) Národné lesnícke centrum, Slovakia

Basidiocarps (copyright, for use contact Basidiocarps (copyright, for use contact [email protected]). [email protected]). Pathogen : Andrej Kunca Národné lesnícke Pathogen : Andrej Kunca Národné lesnícke centrum, Slovakia centrum, Slovakia

Armillaria ostoyae, fresh fruit bodies from A. ostoyae on Pinus sylvestris sapling Pinus sylvestris in Finland (copyright, for use (Finland) (copyright, for use contact contact [email protected]). [email protected]). Pathogen: Kari Korhonen Finnish Forest Pathogen: Kari Korhonen Finnish Forest Research Institute Research Institute A. ostoyae on Pinus sylvestris sapling A. ostoyae on Pinus sylvestris sapling (Finland) (copyright, for use contact (Finland) (copyright, for use contact [email protected]). [email protected]). Pathogen: Kari Korhonen Finnish Forest Pathogen: Kari Korhonen Finnish Forest Research Institute Research Institute

Mating reactions between haploid isolates of Species identification with the aid of mating A. ostoyae (with bifactorial mating system): test. 1. A. ostoyae haploid (lower) x A. 1. Incompatible mating (incompatibility borealis haploid (intersterile – no reaction). factors A1B1 x A1B1). 2. hemicompatible I 2. A. ostoyae diploid (lower) x A. borealis (incomp. factors A1B1 x A1B2). 3. haploid (intersterile – no reaction). 3. A. hemicompatible II (incomp. factors A1B1 x ostoyae haploid x A. ostoyae haploid A2B1). 4. compatible mating, resulting in (compatible – rapid diploidisation). 4. A. diploid (incomp. factors A1B1 x ostoyae diploid (lower) x A. ostoyae haploid A2B2). (copyright, for use contact (intersterile – slow diploidisation of the [email protected]). haploid tester). (©, for use contact Pathogen: Kari Korhonen Finnish Forest [email protected]). Research Institute Pathogen: Kari Korhonen Finnish Forest Research Institute

Dried . Lamellae on the Dried basidiocarp. Lamellae on the underside of the pileus. underside of the pileus. Stereo microscope: J. R. Liberato DPI&F Stereo microscope: J. R. Liberato DPI&F Results Generated: Tuesday, September 28, 2021