Armillaria Root Rot a New Disease of Cut- Flower Proteas in South Africa

Home , Armillaria, Knightia (plant), Protea scolymocephala

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Armillaria root rot A new disease of cut- flower proteas in South Africa

s. Denman', M .P.A . Ccetaee", B.D. Wingfield', M.J. Wingfield' INTRODUCTION and P. W. Crous '.

Armillaria spp. are voracious pathogens of tree s and I Deportment of Plant Pathology, University of shrubs throughout the world. They survive either as Stellenbosch. Privote Bog XI, Motieland 7602. pathogens, saprobes or perthobes (an organism able 2Departme nt of Genetics, Tree Patholo gy Co to utilise dead ti s sues in living hosts) of woody operative Programme (TPCP), Fore stry and material(Gregory et al. ,1991). As facultat ive Agriculturol Biot echnology Institute (FABI), necrotrophs (pathogens) these fun gi kill living tissues University of Pret orio, Pretoria 0002. of woody hosts and then utilise the tissues as a nutrient JDepartment of Microbiology and Plant Pathology, sour ce (Kilc et al., 1991). In th e sap robic mode, Tree Pathology Co-operotive Progromme (TPCP) , Armillaria spp. 3fC wood decomposers aiding the Forestry and Agricultural Biotechnology Institute recycling of nutri ents in ecosystems. Pathogenic (FABI), University of Pretoria, Pretoria 0002. A rmill aria spp. ca us e major los s e s to for e stry (especially nati ve forests but also to co mme rcial plantations) world-wide, and also occur on fruit trees and ornamental plants. They have cause d losses to Taxonomy and Identification Proteaceae in Africa (Kenya, Tanzania, South Mrica), The taxonomy of Armilloria has been Australia, Madeira, New Zeal and, United States of problematic mainl y because it was assumed America (California, Hawaii ) and Zimbabwe. In some that Armillaria mel/eo (Vahl:Fr.) Kummer of these countries where Armillaria root rot occurs sensu lato (in the widest sense) wa s 0 in commercial cut-flower plantations, losses arc of pleomorphic (multiple formed) species that great economic s ignificanc e to producers. This disease has nev er been recorded on indigenous occurred in Asia, Europe and North America Proteaceae in South Africa, although it was noted on (Singer 19 5 6 ). This resulted in d ifferent Australian Proteaceae growing in this country species being lumped together under the (Doidge, 1950). Thus, in South Afri ca Armillaria has name A. mel/ea. Thus Armillaria root- and not po sed a threat to either the natural flora or to butt-rot was frequently incorrectly attributed commercial production of Proteaceae. to A. mel/ea . Although this might seem to In a recent investigatio n into the cause of decline and death of Protea scolymocephala (L.) Reichard, at be a rather academic matter, it is important Kirstenbosch, we were surprised to discover typic al to know the correct species identification of signs of Armillaria root rot. The significance of this the pathogen that affects spe cific crops. finding for conservation and Proteaceae farmers needs This ensures that appropriate disease to be assessed.General information about the genu s control and management practices can be Armillaria, and the diseases that it causes, is provided se lected and imp lemented. here. Other than reporting this dis ease for the first time, we also discuss the significance of this record to the Protea industry in South Africa. With the d iscove ry of mating co m pa t ibility tests Armillaria can be cultured in a Petri dish containing (H intikko, 19 7 3 ) and the a dvent of molecular culture medium where the rhizomorphs are often seen techniques as an aid to species iden tification, the (Fig. 4). taxono mic uncertainties within Armillaria are bei ng Insid e the cop of Armillaria fruiti ng bo d ies, th e re so lved. Cu rrent ly, Volk a nd Bur d sh oll ( 1995) la me llae or gills th at ca rry th e spores of t he fungus recog nise A. melleo as th e type (or representative) are ivory co loured initially but become dark with age of the ge nus and accept 38 spec ies . According to (Wat ling et 01., 1991). The spore print (mode by Volk a nd Burdsall (20 00) t he genus Armillaria, is p lacing t h e cop of the m ushroom, gi lls facing reserved for facu ltatively parasitic (non-obligate) downwards, on a piece of coloured pap er overnight) root- an d butt-rot fungi t hat produce rhizomorphs. is white . T he basidiomes usually arise at the base of infected trees an d shrubs an d occur as solitary individuals or in clusters. Identification Armillaria is an Agaric (0 so-celled mushroo m or toadstool [Ken d rick 19 9 2] ) and th e fruitbodies (basidiome s or, more sim ply, m ushrooms) when produced, are one of the ways this fungus can be identified (Fig. 10) . The main component po rts of m ushrooms are t he cop (pi leus) a nd the sta lk (stipe) . and both of these m a y have other characteristic features. Th e pileus of Armillaria is fleshy and ra nges in colour from yellow, honey-beige to tawny or cigar brown (Wat ling et 01., 19 9 1).

Fig. lb . A basidiome (fruitbody I mushroom) of Armillaria mellea note the annulus (or veil of tissue) on the stipc

However, basidiomes are produced seasonally, and therefore a re often not present for identification purposes. The web of tough, white mycelium that is found below the bark of infected plants (Fig. 2) is characteristic of Armillaria. Recognition of the taxonomic significance of mating Fig. la. Basidiomes (fruitbodies I mushrooms) of Armillaria mellea fou nd on decaying oak trees in the Company Gardens in Cape Town com patibility between single spore c u ltu res of Armillaria, and t h e development of mol e cula r T he stipe is cent ra lly situ ated in the cop, fibrous techniques have recently aided species differentiation to fle shy, often becoming ho llow with maturity. An in this g e n us (Ha rrington and Wingfie ld, 1995, a nnulus (0 me mbranous ring/ve il of tissue) preva ils Coetzee et 01 ., 2 0000). The lock of fo rmation of on t he stipe (Fig. 1b) and fruitbod ie s may arise rhizomorphs and scarcity of basidiomes in Afri can from white fan-like mycelium (Fig. 2) or from black species ma kes identification difficult in these regions rh izomorphs (Fig. 3). The rh izomorphs ore un usual (Swift, 1968). Therefore, the morphologica l features macroscopic features that are comprised of hard, that are present must be studied, and mating tests block, me lon ised cells which form long string-like between single spore isolates and sequencing of structu res under t he gro und, from which the various parts of the pathogen's genome must be carried com mon term "shoe -string" rhizomorphs, takes its out to reliably identify the fungus to species level. The nome. Rh izomorphs enable the pathogen to latter of these techn iques is expensive and specialised spread fro m plant to p lant through the soil. expertise is required to carry out tests. Fig. 2. White, fan-like mycelium of Armillaria bel ow the bark of an infected Protea scolymocephala plant found in Kirs tenbosch G ardens, Cape Town .-

Fig . 3. Black sh oe-str ing I boot-lace rhizo morphs of A rmillaria be low tbe bark of an infected Spruce tree in Scotland

Epidemiology Armillaria thr ives in mo ist conditions (Porter et ot, 19 9 6 ) b ut is re st rict ed by excessively wet, waterlogged, cold, or dry conditions (Kile et 01. , 1991). Infection can ta ke plac e throug h the soil by rhizomorph contact with roots, or by mycelium from infe cted roo ts colo nising healthy roo ts that are in close proxi.mity to t he infected ones (via root to root contact) (Garraway et 01. , 1991 ; Morrison et 01., 19 91 ). Th is fa ct holds serious implicat io ns for fa rme rs pla nting young pla nts in o ld stands where plants ha ve d ied as a re sult of infe ctio n by this pa t hogen, a nd the infected roots rema in in the soil. Although rhizomo rp hs do na t require wounds or weakened poin ts in root tissues to initiate infection, roots with t hese afflictions can all serve as infection co urts (Morriso n et a/., 199 1). Stu mps of fe lled trees can be infected by basidiaspores (Rishbeth, 19 70) but thi s is considered a fa irly uncommon event and there is no ev idence to support t he id e a that basidiospores infect roots directly (Redfern and Filip, Fig. 4. Armillaria from infected Prutea scolym ocephala, cultured in a 19 9 1). Petri di sh. The long sp idery outgrowths are the rhizomorph s --~.- ----.- ..-...-.._-.-.-.---=.---_._-.---:...=-

Armillaria on Proteaceae throughout the Interestingly, a num ber of differen t species of Armillaria world have been reported on Proteac eae from New Zealand. There are not many records of Arm illaria spp. on Both Armillaria /imonea (Stevenso n) Boesew inke l a nd Proteaceae throughout the world.Howeve r, th is Armillaria no vae -ze/andiae (Ste venson) Herink. were pathogen has been recorded f rom a number of found on Knightia exce/sa R.Br. a nd the latter was also co untries. These include Australia (von Broemb se n, reported on G. robusta (Pennycook, 1989). 1989; Forsbe rg, 1993; Porter et 0/., 1996), California Africa n reco rds of Armillaria on Protea ceae a re very sca nt (Forr et 0/., 1989), Hawaii (Loemmlen and Bego 1974), but the fungus ha s been record ed on G. robusto in Kenya (Anonymous, 1960) Madeira (Rodriguez, 2000), Kenya and Ta nza nia (Anonomyous, 1960) as well os in New Zeala nd (Pen nycook, 1989), South Africa (Doidge , So uth Afric a ( Doidge, 1950). In Zim babwe on 195 0), Tonzonio (Anono mous, 196 0) a nd Zimbabwe unidentified Armilforia sp . has been reported from Q (Musuko et 0/., 199 8). Protea sp (Musuko et 0/., 1998). In A ustralia Arm illaria JuteobuboJino Wat ling & Kile is the main species that causes root rot of Proteaceae Armillaria in Sout h Afric a (Kile et of., 1983, Pearce et ol., 1986 , Shives, 1989, Until now the only record of Armillaria on Proteaceae in von Broembsen et ol., 1989 ). The distribution of this So ut h Africa, was o n G. ra busta (Doidge, 1950,). disease on Proteaceae in A ustralia is very wide, ranging According to Coetzee et 0/ ., (Coetzee et 0/., 20000) from Dwellingu p, Monjimup, Pem berton and Perth in only two species of Armillaria a re thu s far known occ ur the west, to th e south and east regions. In Sydney, in South Africa, Armillaria fuscipes Petch a nd A . me/leo. South African Proteaceae ore especia lly susceptible to In view of the recent ad vances in the taxonomy of A. futeabubolina (Pw. Crous pers. obs. ). The first above Armillaria, previous records (pre-1996) of this fun gu s ground symptoms often shown by infected plants are should be referred to mere ly as Armilforia sp. because undersized leaves that drop prematurely (Porter et 0/., the spe cies identity is no longer ce rtain. A rmilla ria 1996). Signs of the pathogen includ e the creom fU5cipes is an importa nt pat hogen of pines (Coetzee et coloured web of mycelium below the bark, block "shoe 0/ ., 20000), especially in the northern ports of the string" rhizomorphs that also form below the bark a nd country. The on ly reliable record of A. mel/eo in South run a long the roots and in the soil. Hon ey colou red Africa is on oak trees in the Comp a ny Ga rdens in the mushrooms may occu r at the base of infected plants centre of Cape Town where it was ap parently introdu ced (Porter et 0/., 1996). Proteoceous hosts known to be by eoriy settlers (Coetzee et 0/., 2000b). Arm illaria sp. infected with A. luteobubalina in Australia include (originally as Armiflaria mellea) has been recorded as 0 Banksia gran dis Willd an d B. seminuda (A.s . George ) pathogen on Aroucoria brazi/iana A. Rich. (mo nke y Rye, (Pearce et of., 1986, Shives. 19 89), Grevillea puzzle trees) (Doidge 1950 ), on Cedrefa odorata Linn. robusta R.Br.,(Kile et 0/., 1983, Shives, 1989) an d (West Indian ced a rs) (Doidge 1950), Cupressus /usitanica Hakea pro strata R. Br. (Kile et of., 1983, Shives, 1989), (cypress) (Doidge 1950), De/onix regia Rof. (fla mboyant and severa l members of the genus Protea (P.W. Crous trees) (Doidge 1950), Eriobatrya japonica (Thunb.) Li nd!. pe rs. obs. ). An un ide ntified Armilla ria sp. has a lso (Ioquats) )(Doidge 1950), Euco /yptus panicufota Sm . been recorded on Dryandra palycepha la Benth (Shives, (Doidge 1950), Grevillea robu sta (Doidge 1950), Parinari 1989). cu ra t ell ifo/ia (Mo bo lo plum) (Doid ge 195 0 ), Musa According to Laemmlen a nd Bego ( 1974), Bega (1962) cavendishii Lomb. (ban anas) (Brodrick, 1971 ), Pinus spp. made the first report of A mel/eo in Hawaii, when he (Doidg e 1950), Que rcus spp.(oa ks) (Doidge 1950 ), fou nd this pathogen on G_ robusta. However, no s yzygium ge rrardii (Ho rv.Ex Hook. f .) Burtt. Da vy (forest wote rwoo d) (Doidge 1950), a nd Toano ciliata basidiomes (mushrooms) of Armillaria ha ve eve r been M.J. Roe m. (toon trees) (Doidge 1950). A rmillaria found on the island (Loemm len a nd Bego, 1974). In sp . (o riginolly a s A. m ell ea) wos also re po rted by view of the recent ad vances in the ta xonomy and species Doid ge ( 1950) on severa l ot her hosts, but as these ide ntification of this genus, the identifica tion of th is re po rts we re unconfirmed they we re not listed by pathogen on Proteaceae in Ha wa ii, probably needs Doidge et 0/., 195 3, Gorter, 197 7 or Crous et 0/., to be re assesse d. O n anoth er is la nd whe re 200 0 Proteaceae ar e cu ltivate d, namely Modeiro, Armillaria ha s been isolated from Proteaceou s hosts, but the In 1996 A. mellea, a deva stating pathogen of ma ny pathog en has not yet been identified to species level woody species wo rld -wid e wa s identified in t he (Moura and Rodrigues, 2000). "Compa ny Gardens" in the centre of Ca pe Town on oa k t rees (Coetzee et a/., 2000b). An intrig uing were present nor were rh izomorphs observe d, thus sto ry of ho w t h is fu ngu s must ha ve be e n identification to species level will have to be derived from introd uced into Cape Town du ring the early Ca pe molecular studies. This work is unde rway a nd the results Dutch settlement (1652) on one of the potted plants prom ise to be most intriguing. One possibility is th at the (suc h as citrus or gra pevine) is presented by Coetzee exotic A. mel/eo ha s esca ped from the Company Ga rdens et 0/. (2000b). Ifthe hypot hes is proposed by Caetzee an d entered Kirstenbosch. Alternatively, t his could be et 0/. (2000b) is correct, and this fung us has not another species of Armillaria an d possib ly even something been reported else where in the Western Cape until new for South Africa. now, the spread of this pat hogen ha s obviously been conta ined up to the presen t.

Armillaria on Proteaceae in South Africa - A ne w record Declining P. sco/ymocepha/a plants were encounte red in the planted beds a t Kirst en bos ch Na ti o nal Botanical Gardens, Ki rstenbosch, Cape Town in May 2000. The leaves of affected plants were chlorotic and the plants did not look healthy (Figs. 5 a nd 6) . When the infected plants were removed fro m the soi l t he roots we re blackened (not unlike typical Phytophthora root rot symptoms) a nd there was a la ck of feeder roots. Upon cutt ing into the crown t issue, wh ite myceli um typ ica l of the Armillaria myce lial fans was present in the cambial region (Fig. 7). Isolat io ns were ma de and the pathoge n was obtained in culture (Fig. 4). Cultures are ma inta ined in the Depart ment of Plant Pat ho log y cu lture co llection, Univers ity of Ste llenbosch Private Ba g Xl , Matieland 7600 -Culture numbers STE-U 3773 Fi g. 6. A Prot ea scolymocephala p lant in fected wit h Armillaria in Kir ste nbosch Gar dens. Not e the chlorotic lowe r leaves, de ad br anches an d STE-U 3774. No fruiting structures (basidia mes) and unhe althy ap pea rance of th e plan t. The wh ite mycelial fans can be seen below th e bark on the main root of the plant

Fig. 5. A Protea scolymocephala plant infected with Armillaria in Fig. 7. Wh ite mycelial fans typical of Armillaria present below the bark in Kirst enbosch Ga rdens. Note the chlorotic lowe r leaves and dead the crown reg io n of P. scolymocephala plants infected with Armillaria in branches Kir stenbosch Gardens ------_ . ~-----

Discussion Arm illaria is a seriou s root rot pathogen of man y woody the South Africa n Proteaceae industry. However, if the hosts a nd in South Africa, th e most serious root fu ngus is Armillaria m el/eo, th ere may be se rio us pathogen on Proteaceae that we have had to contend implications for indigenous vegetation on Ta ble Mountain with th us far is Phyt ophthora cinnamomi Ra nds, a nd it will be essential to era dicate this pat hogen before although in the past two years Fusarium wilt ca used it beco mes a threa t to both nat u ral a nd c ultiva ted by Fusa rium oxysporum Schlecht . ha s become a Proteaceae in the Western Cape. problem. Does thi s new record mean t hat we now The flowerbeds at Kirstenbosch a re covered with bark hove a third serious root pathogen that we need to chips that help retain soil moisture and whe n th ey keep in check? In order to answer this que stion Q decompose they return nutrients to the soil, they a lso help few facts need to be esta blished . Firstly the species prevent soil erosion and made rate the tem perature of the identifica tio n of the Arm illaria able to infect P. soil. Armillaria spp. are common wood rotting fungi thus scolymocepho/la must be resolved. The host range it is quite possible that this pathoge n wos introduced into of this pat hogen must be established and then the Ki rstenbosch Ga rdens on the bar k chips that have been big challenge will be to answer the question of how strewn over the flower beds. Growers need to be warned th is pat hoge n a ppeared in Kirsten bosch Ga rde ns. of the potential risk involved with the practice of covering Once these facts are establis hed it will be easi er to beds with bark chips especially lf they were de rived from estimate the potentia l impact of this pathogen to diseased, rotted or dead trees or shrubs .

Acknowledgements We th an k Dr J Taylor for her co n tri b ution o f lite ratur e res ources and fo r reviewing the ma n uscr ip t. We also thank Ioland e Roux and Ja mes Town send who b rou ght thi s d ise ase to O UT atte ntio n and ass isted with field co llections.

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