Ganoderma (and rust) Dr Morag Glen Dr Anthony Francis Assoc. Prof. Caroline Mohammed

Overview Ganoderma What makes Ganodermas of interest? What defines Ganoderma as a genus? Taxonomy (briefly) Australian records of Ganoderma spp. Ganodermas and – root rot – butt rot – trunk rot Case studies involving some Australasian species. – Ganoderma australe – G. steyaertanum – G. philippii Myrtaceae rust Why rust? Rust life-cycles Puccinia psidii in America Myrtaceae rusts in Australia Hosts and impacts Photos: Dr Anthony Francis

Overview Ganoderma What makes Ganodermas of interest? What defines Ganoderma as a genus? Taxonomy (briefly) Australian records of Ganoderma spp. Ganodermas and – root rot – butt rot – trunk rot Case studies involving some Australasian species. – Ganoderma australe – G. steyaertanum – G. philippii Myrtaceae rust Why rust? Rust life-cycles Puccinia psidii in America Myrtaceae rusts in Australia Hosts and impacts Photo: CSIRO

Why Ganodermas? Medicinal qualities Aesthetic values Taxonomy Wood decay Root rot

Why Ganoderma ? Root rot – some species are highly pathogenic and have a broad host range. Butt rot – may also be the final stage of root rot Trunk decay – many species are regarded as secondary invaders of wounded or stressed trees, but may contribute to the death of old or stressed trees

What defines Ganoderma ? Ganoderma is a lignicolous basidiomycete with tough, leathery, perennial, sporocarps Ryvarden, L. & Gilbertson, R.L.1993, Syn. Fung. 6: Basidia and spores are produced in pores It is separated from other polypores on the basis of its double spore walls Photos: Dr Anthony Francis

Taxonomy (brief) Fungi, Basidiomycota, Agaricomycotina, Agaricomycetes, Polyporales, Ganodermataceae Ganoderma is a large genus - over 300 species have been described Many names are synonyms Several species are species complexes – e.g. G. australe Many names have been misapplied – e.g. G. lucidum

Taxonomy (brief) Phylogenetic analysis of DNA sequences has been helpful in resolving some of the taxonomic issues Plenty more to do

Ganoderma spp. in Australia Currently accepted names of published records (ICAF 21 species recorded in Australia Recent taxonomic studies of Australian species –Smith BJ, Sivasithamparam K (2000) Internal transcribed spacer ribosomal DNA sequence of five species of Ganoderma from Australia. Mycological Research 104, –Smith BJ, Sivasithamparam K (2003) Morphological studies of Ganoderma (Ganodermataceae) from the Australasian and Pacific regions. Australian Systematic Botany 16, G. amboinense G. annulare G. applanatum* G. australe* G. chalceum* G. chilense G. colossum G. cupreum G. gibbosum G. incrassatum* G. japonicum G. lucidum* G. mastoporum G. miniatocinctum G. ochrolaccatum* G. orbiforme* G. resinaceum G. steyaertanum* G. weberianum* G. williamsianum

Ganoderma spp. in Australia Specimens in herbaria (as recorded in the APPD) –Ganoderma applanatum (125 records) –G. australe (35 records) –G. boninense (=G. orbiforme) (1 record) –G. chalceum (22 records) –G. incrassatum (3 records) –G. lucidum (55 records) –G. ochrolaccatum (1 record) –G. steyaertanum (2 records) –G. weberianum (1 record) –G. williamsianum (4 records)

Ganoderma spp. in Australia Ganoderma applanatum (125 records) G. australe (35 records) Moncalvo and Buchanan studied the G. applanatum/G. australe species complex using ITS sequence data and vegetative compatibility tests. 96 isolates were separated into 8 clades, corresponding to VC groups and geographical origin. Cryptic speciation explains the taxonomic difficulties in resolving this species complex Moncalvo and Buchanan (2008, Mycological Research 112: )

Launceston City Council Street trees and trees in City Park Fungi were isolated from some of the wood samples. DNA extracted directly from wood (including 5 yo samples). PCR, cloning and sequencing of DNA from wood

Launceston City Council Fraxinus excelsior, Dry Street Ganoderma australe detected in DNA from wood samples. Ulmus x hollandica, Clarence Street Ganoderma australe isolated. Fagus sylvatica, City Park Ganoderma australe and Sistotrema brinkmannii isolated. Quercus robur, City Park Ganoderma australe isolated. Fraxinus excelsior, City Park Ganoderma australe isolated. Acacia melanoxylon (stump), Cataract Gorge Ganoderma australe isolated. Other fungi detected included Coniophora olivaceae and Armillaria luteobubalina

Ganoderma spp. in Australia Ganoderma boninense = G. orbiforme 1 record – Qld A major pathogen of coconuts and oil palms in SE Asia Also found on ornamental palms in the NT Photo:

Ganoderma spp. in Australia Ganoderma lucidum (55 records) G. steyaertanum (3 records) Recorded from Qld, WA, NT Found on many plant families in Australia, including –Annonaceae, Arecaceae, Araucariaceae, Caesalpiniaceae, Fabaceae, Lauraceae, Mimosaceae, Moraceae, Myrtaceae, Rutaceae, Sterculiaceae This species (G. steyaertanum) can cause root rot in Australia and Indonesia Recently found affecting sandalwood in WA Causes ‘white root rot’ in Acacia mangium in Java

Ganoderma steyaertanum at Wonogiri in Java Somatic incompatibility tests –within-tree comparison found that multiple genotypes of Ganoderma spp. were present within the root system of a single A. mangium tree –Some of these genotypes were identical to isolates recovered from the fruitbody growing on the trunk of the tree. –The presence of more than one genotype of the same fungus within a single tree indicates multiple infection events in the same tree. Ganoderma spp. in Australasia

Ganoderma philippii Aggressive root rot pathogen Hosts include: –Annatto –Cloves –Cocoa –Coffee –Guarana –Orange –Rubber –Tea –Acacia mangium

Ganoderma spp. in Australasia ACIAR funded a study to: –Confirm the identity of the main root rot pathogen –Study the mode of spread –Develop early detection methods –Develop risk predictions Riau 2 sites in PT RAPP Logas South and Langgam compartments South Sumatra 2 sites in PT MHP Deras and Selibing compartments 1 site in East Kalimantan in a PT SRH Sebulu compartment

Ganoderma spp. in Australasia Monitoring plots – 10 x 10 trees –Each site visited every 6 months –Crown health scored –Roots excavated, scored for presence/absence of root rot and isolations made

Prognosis for infected trees The largest proportion of living trees with root rot have full green crowns

Prognosis for infected sites The number of trees with root rot on all our sites is increasing

Prognosis for infected sites This increase is even more evident if we consider the age of the compartments

Predicting loss The probability of having root rot generally increases with the number of dead neighbours (DNI)

Predicting loss Regional differences in diversity and abundance of root rot

Pathology - identification Identification of Ganoderma philippii as the main causal agent of red root rot of Acacia mangium in Indonesia

Pathology - identification DNA sequencing and phylogenetic analysis of Ganoderma species. G. philippii 66 IMI E7095R* E7092 E7095B* E7094R* FRIM 95 G. subresinosum JMM ASP.1 Amauroderma rude E7366 E7070 E7113 E7079 G. philippii A. rugosum E7108 E7425 E7376 E7096R* FRIM 589 E7098 HMAS G. sp. RSH 0626 G. sp ATCC G. sp. T210 T DAR G. steyaertanum G. aff. steyaertanum UWA8 G. steyaertanum C17274 G. sp. 100 RSH 1111 G. sp. RSH 0814 G. fornicatum

Pathology - identification Ganoderma philippii specific PCR for rapid identification of isolates Which of these three isolates is Ganoderma philippii? Species-specific PCR provides rapid, confident identification. Feedback to technical staff involved with isolation and maintenance of isolates enhances skills in morphological recognition. Allowed appropriate selection of isolates for pathogenicity testing and somatic compatibility testing.

Rust Puccinia psidii Winter described in 1884 –Rust of guava (Psidium spp.) Photographs: AC Alfenas, UFV

Urediniospores Teliospore germination, basidiospore development Urediniospore germination, host penetration, haustorium development R Urediniosori Young leaf/shoot/ fruit/flower bud Aeciospore Basidiospore germination, host penetration, haustorium development Young leaf/shoot/ Fruit/flower bud Aeciospore germination, host penetration, haustorium development Young leaf/shoot/ fruit/flower bud Teliospores Urediniospore germination, host penetration Rust life-cycle

Hosts of P. psidii P. psidii has subsequently been found on a broad range of Myrtaceae species Other rust species described from Myrtaceae in South America have been synonymised with P. psidii P. psidii was confirmed on Eucalyptus citriodora in Brazil in 1944 Image

Hosts of P. psidii P. psidii became an increasing problem in eucalypt plantations in Brazil CSIRO

Hosts of P. psidii –Eucalyptus nitens –Corymbia gummifera –Eucalyptus pilularis –Eucalyptus regnans –Eucalyptus robusta –Eucalyptus saligna –Eucalyptus cloeziana –Eucalyptus deglupta –Eucalyptus diversicolor –Eucalyptus dunnii –Eucalyptus globulus –Eucalyptus grandis –Eucalyptus microcorys Host testing of Australian Myrtaceae species in Brazil Susceptible species in the eucalypt/melaleuca clades included: –Melaleuca alternifolia 5.25 – Melaleuca cajuputi subsp. cajuputi –Melaleuca leucadendra –Melaleuca nesophila 0.00 –Melaleuca quinquenervia Zauza et al Australasian Plant Pathology. 39:

Hosts of P. psidii –Angophora costata –Eucalyptus moluccana subsp. moluccana –Corymbia calophylla ‘rosea’ – Eucalyptus nitens –Corymbia citriodora –Eucalyptus obliqua –Eucalyptus paniculata –Corymbia intermedia –Eucalyptus pellita –Corymbia maculata –Corymbia tessellaris –Eucalyptus acmenoides –Eucalyptus resinifera –Eucalyptus alba –Eucalyptus acmenoides –Eucalyptus resinifera –Eucalyptus alba –Eucalyptus amplifolia var. amplifolia –Eucalyptus brassiana –Eucalyptus scias subsp. scias –Eucalyptus camaldulensis var. obtusa –Eucalyptus tereticornis –Eucalyptus urophylla –Eucalypus camaldulensis var. simulata –Eucalypus melanophloia –Eucalyptus elata –Melaleuca ericifolia –Eucalyptus guilfoylei Resistant species in the eucalypt/melaleuca clades included:

Hosts of P. psidii Susceptible species included: –Astartea heteranthera (28) WA 11 –Callistemon pachyphyllus (48) Qld –Kunzea baxteri (80) WA 0 –Pericalymma ellipticum (24) – 0 –Pilidiostigma glabrum (32) – 62.5 –Regelia ciliata (30) WA –Rhodamnia rubescens (12) – 60.5 –Rhodomyrtus psidioides (80) – 15 –Syncarpia glomulifera (60) NSW –Syzygium leumannii (4) – 50

Hosts of P. psidii Resistant species included: –Acmena smithii (40) – 97.5 –Archirhodomytus beckleri (60) NSW –Asteromyrtus dulcia (12) – 100 –Austromyrtus tenuifolia (24) NSW 100 –Decaspermum humile (40) – 87.5 –Eugenia reinwardtiana (12) – –Gossia fragrantissima (8) – 100 –Hypocalymma robustum (32) – 88 –Lophostemon confertus (22) Qld 100 –Pilidiostigma tropicum (80) – 81 –Syncarpia hillii (20) Qld –Syzygium alatoramulum (80) Qld –Syzygium australe (20) – 100 –Syzygium australe (20) NSW 95 –Syzygium fibrosum (4) – 75 –Syzygium wilsonii subsp. cryptophlebium (4) – 100

Hosts of P. psidii Rust rating scale – from Zauza et al 2010

Climatic risk modelling Booth and Jovanovic, CSIRO IN RISK AREA Eucalypt forest and woodland Rainforest – 50% World Heritage listed Melaleuca woodland

Melaleuca quinquenervia natural distribution (based on herbarium specimens) Herbarium records of Melaleuca quinquenervia

Puccinia psidii is contributing to ‘biological control’ of Melaleuca quinquenervia in the Florida Everglades

Global distribution – Puccinia psidii Hawaii – incursion in Oct 2005

Rust In April 2010, rust was found on Agonis flexuosa cv.‘Afterdark’ in NSW Photo: Dr Angus Carnegie, I&I, NSW Though it was determined by authorities to be Uredo rangelii, based on morphological characteristics, DNA sequencing of 3 gene regions has failed to find any characters that support the distinction from P. psidii The incursion was deemed ‘not feasible to eradicate’ and has subsequently been found in Queensland, with abundant teliospore production

Rust The hosts in Australia now include: Acmena sp. (lilly pilly)Agonis flexuosa (willow myrtle) 'Afterdark', 'Burgundy', 'Jeddas Dream'Austromyrtus inophloia (see Gossia inophloia)Backhousia citriodora (lemon-scented myrtle)Backhousia myrtifolia (grey myrtle)Callistemon viminalis (weeping bottlebrush)Callistemon salignus (willow bottlebrush) Callistemon 'St Mary MacKillop'Chamelaucium uncinatum (Geraldton wax)Choricarpia leptopetala (brown myrtle or rusty turpentine)Eucalyptus agglomerata (blue-leaved stringybark)Eucalyptus deanei (mountain blue gum or Deane's gum)Eucalyptus pilularis (blackbutt)Gossia gonoclada (angle-stemmed myrtle)Gossia inophloia 'Aurora' and 'Blushing Beauty' (syn. Austromyrtus inophloia)Lenwebbia prominens (southern velvet myrtle)Leptospermum rotundifolium (round-leaved tea tree)Lophomyrtus bullata 'Rainbow's End'

Rust The hosts in Australia now include: Lophomyrtus x ralphii 'Red Dragon', 'Black Stallion', 'Krinkly'Melaleuca alternifolia (tea tree)Melaleuca quinquenervia (broad-leaved paperbark)Melaleuca linariifolia 'Claret tops'Metrosideros collina 'Tahiti' and 'Fiji'Rhodamnia maideniana (smooth scrub turpentine)Rhodamnia rubescens (scrub turpentine)Rhodamnia whiteana (white malletwood)Rhodomyrtus psidioides (native guava)Syncarpia glomulifera (turpentine)Syzygium anisatum (aniseed myrtle)Syzygium apodophyllum (rex satinash)Syzygium australe 'Meridian Midget'Syzygium jambos (rose apple)Syzygium luehmannii (small-leaved lilly pilly, riberry)Syzygium luehmannii x Syzygium wilsonii 'Cascade' (lilly pilly)Tristania neriifolia (water gum)Uromyrtus lamingtonensisXanthostemon chrysanthus (golden penda)

And the list is growing… Photos: Dr Angus Carnegie, I&I, NSW Syzygium anisatum Syzygium jambos Rhodamnia rubescens