10E -

Armillaria root rotA new disease of cut- flower

proteas in South Africa

INTRODUCTION

Armillaria spp. are voracious pathogens of tree s andshrubs throughout the world. They survive either aspathogens, saprobes or perthobes (an organism ableto utilis e de ad ti s sues in living hosts) of woodymaterial(Gregory et al. ,1991). As facu lt at ivenecrotrophs (pathogens) these fun gi kill living tissuesof woody hosts and then utilise the tissues as a nutrientsour ce (Kilc et a l., 1991). In th e sap rob ic mode,Armillaria spp. 3fC wood decomposers aiding therecycling of nutri ents in ecosystems. Pathogeni cA rmi ll aria spp. ca us e major los s e s to for e str y(espec ially nati ve fores ts but also to co mme rcialplantations) world-wide, and also occur on fruit treesand ornamental plants. They have cause d losses toProteaceae in Africa (Kenya, Tanzania, South Mrica),Australia, Madeira, New Zeal and, United State s ofAmerica (California, Hawaii ) and Zimbabwe. In someof these countrie s where A rmillaria root rot occursin commercial cut-flower plantations , losses arc ofgreat econom ic s ignificanc e to producers. Thi sdisease has nev er been recorded on indigenousProteaceae in South Africa, although it was noted onAustralian Proteaceae growing in this country(Doidge, 1950) . Thus, in South Afri ca Armillaria hasnot po sed a threat to either the natural flora or tocommercial production of Proteaceae.In a recent investigatio n into the cause of decline anddeath of Protea scolymocephala (L.) Reichard, atKirstenbosch, we were surprised to discover typic alsigns of Armillaria root rot. The significance of thisfinding for conser vation and Proteaceae farmers needsto be assessed. General information about the genu sArmillaria, and the diseases that it causes, is providedhere. Other than reporting this dis ease for the firsttime, we also discuss the significance of this recordto the Protea industry in South Afr ica.

s. Denman ', M .P.A . Ccetaee",

B.D. Wingfield', M.J. Wingfield'

and P. W. Crous '.

I Deportment of Plant Pathology, University of

Stellenbosch. Privote Bog XI, Motieland 7602.

2Departme nt of Genetics, Tree Patholo gy Co­operative Programm e (TPCP) , Fore str y and

Agriculturol Biot echnology Institute (FABI),

University of Pret orio, Pretoria 0002.

JDepartment of Microbiology and Plant Pathology,

Tree Pathology Co-operotive Progromme (TPCP) ,

Forestry and Agricultural Biotechnology Institute

(FABI), University of Pretoria, Pretoria 0002 .

Taxonomy and IdentificationThe ta xonomy of Armilloria has been

problematic mainly because it was assumed

that Armillaria mel/eo (Vah l:Fr.) Kummer

sensu lato (in the widest sense) wa s 0

pleo morphic (multiple formed) species that

occurred in Asia, Europe and North America

(Singer 19 5 6 ). This res ulted in d ifferent

species being lumped together under the

name A. mel/ea . Thus Armillaria root- and

butt-rot was frequently incorrectly attributed

to A. mel/ea . Although this might seem to

be a rather academic matter, it is important

to know the correct species identification of

the pathogen that affects spe cific crops .

This ensures that appropriate disease

control and management practices can be

se lected and imp lemented.

With the d iscove ry of mating co m pa t ibility t e sts

(H intikko, 19 7 3 ) and the a dvent of molecu lar

techniques as an aid to species identification, the

taxono mic uncerta inties within Armillaria are bei ng

re so lved . Cu rre nt ly, Volk a nd Bur d sh oll ( 1995)

recog nise A. melleo as th e type (or representative)

of the ge nus and accept 38 spec ies . Acco rding to

Volk a nd Burdsall (20 00) t he genus Armillaria, is

reserved for facu ltat ively paras it ic (non-ob ligate)

root- an d butt-rot fungi t hat produce rhizomorphs .

IdentificationArmillaria is an Agaric (0 so-ce lled mushroo m or

toadstoo l [Ken d rick 19 9 2] ) and th e fruitbodies

(basid iome s or, more sim ply, m ushrooms) when

produced, are one of the ways this fungus can be

identified (Fig . 10) . The main compon ent 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 colou r from yellow, honey-beige

to tawny or cigar brown (Wat ling et 01., 19 9 1).

Fig. la . Basidiomes (fruitbodies I mushrooms) of Armillaria mellea

fou nd on decaying oak trees in the Company Gardens in Cape Town

T he stipe is cent ra lly situ a ted in the cop, fibrous

to fle shy, often becoming ho llow with maturity. An

a nnulus (0 me mbranous ring/ve il of tissue) preva ils

on t he stipe (Fig . 1b) and fruitbod ie s may arise

from white fan- like mycelium (Fig . 2) or from black

rh izomorphs (Fig . 3). The rh izomorphs ore un usua l

macroscopic features that are comprised of hard,

block, me lon ised cells which form long string-like

structu res under the gro und, from which the

common term "shoe -string" rhizomorphs, takes its

nome . Rh izomorphs enab le the pathogen to

spread f ro m pla nt to p lant th rough the soi l.

Armillaria can be cultured in a Petri dish containing

cultu re medium where the rhizomorphs are often seen

(Fig. 4).

Insid e the cop of Armillaria f ruiti ng bo d ies, th e

la me llae or gi lls th a t ca rry th e spores of t he fungus

are ivory co loured init ially but become dark with age

(Wat ling et 01., 1991) . The spore print (mode by

p lac ing t h e cop of the m ushroom, gi lls fac ing

downwards, on a piece of coloured paper overn ight)

is white . T he basidiomes usually arise at the base

of infected trees an d shrubs and occur as solitary

individuals or in clusters.

Fig. lb . A basidiome (fruitbody I mushroom) of Armillaria mellea ­

note the annulus (or ve il of tissue ) on the st ipc

However, basidiomes are produced seasonally, and

therefore a re often not present for identificat ion

pu rposes . 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

com patib ility between sing le spore c u ltu res of

Armillar ia, and t h e deve lopment of mol e cula r

techniques have recently aided species differentiation

in this g e n us ( Ha rrington and Wingfie ld, 1995,

Coetzee et 01 ., 2 0000) . The lock of fo rmation of

rhizomorphs and scarcity of basidiomes in Afri can

species ma kes identification difficult in these regions

(Swift, 1968). Therefore, the morphologica l features

that are present must be studied, and mating tests

between single spore isolates and sequencing of

various parts of the pathogen's genome must be carried

out to relia bly identify the fungus to species leve l. The

latter of these techn iques is expensive and specialised

expertise is required to carry out tests.

Fig. 2. Whi te, fan-like mycelium of Armillaria bel ow the bark of

an infected Protea scolymocephala plant found in Kirs tenbosch

G arde ns , Cape Town .-

Fig . 3 . Black sh oe-s tr ing I boot-lace r hizo mor phs ofA rmillaria be low tbe bark of an inf ected Spruce tree in

Scotland

Fig. 4. Armillaria from infected Prutea scolym ocephala , cultured in a

Pe tr i di sh . The long sp idery ou tgrowths are the rh izomorph s

Epidem iology

Armillaria thr ives in mo ist conditions (Porter et ot ,

19 9 6 ) b ut is re s t rict ed by excess ively wet,

waterlogged, co ld, or dry condit ions (Kile et 01. ,

199 1). Infect ion 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 impl ica t io ns for

fa rme rs pla nting young pla nts in o ld stands where

p lants ha ve d ied as a re sult of infe ct io n by thi s

pa t hogen, a nd the infected roots rema in in the so il.

Althou gh rhizom o rp hs do na t require wounds or

weakened poin ts in root tissues to initia te infection,

roots with t hese afflictions can all serve as infect ion

co urts (Morr iso n et a/., 199 1). Stu mps of fe lled trees

can be infected by bas idiaspores (Rishbeth, 19 70)

but thi s is considered a fa irly uncommon event and

there is n o ev idence to support t he id e a tha t

basidiospores infect roots directly (Redfern and Filip,

19 9 1).

Armillaria on Proteaceae throughout theworldThere are not many records of Arm illaria spp . on

Proteaceae throughout the world . Howeve r, th is

pathogen has be en reco rded f rom a number of

co untries. These include Australia (von Broemb se n,

1989; Forsbe rg, 1993; Porter et 0/., 1996), Califo rnia

(Forr et 0/., 1989), Hawaii (Loemmlen and Bego 1974),

Kenya (Anonymous , 1960) Madeira (Rodriguez, 2000),

New Zea la nd (Pen nycook, 1989), South Africa (Doidge ,

195 0), Tonzonio (Anono mous, 196 0) a nd Zimbabwe

(Musuko et 0/., 199 8).

In Australia Arm illaria JuteobuboJino Wat ling & Kile is

the main species that causes root rot of Proteaceae

(Kile et of., 1983, Pearce et ol., 1986 , Shives, 1989,

von Broembsen et ol., 1989 ). The dist ribution of this

disease on Proteaceae in Aust ralia is very wide, ranging

from Dwellingu p, Monjimup, Pem berton and Perth in

the west, to th e south and east regions . In Sydney,

South African Proteaceae ore especia lly susceptible to

A. futeabubolina (Pw. Crous pers. obs. ). The first above

ground symptoms often shown by infect ed plants are

undersized leaves that drop prematurely (Porter et 0/.,

1996). Sig ns of the pa thogen includ e th e creom­

coloured web of mycelium below the bark, block "shoe­

string" rhizomorphs that a lso form below the bark a nd

run a long the roots and in the soil. Hon ey colou red

mushrooms may occu r at the base of infected plants

(Porter et 0 /., 1996). Proteoceous hosts known to be

infe cted with A. luteobubalina in Australia include

Banksia gran dis Willd an d B. seminuda (A.s . George )

Rye, (Pea rce et of., 1986, Shives. 19 89), Grevillea

robusta R. Br., (Kile et 0/., 1983, Shives , 1989) an d

Hakea prostrata R. Br. (Kile et of., 1983, Shives, 1989),

and severa l members of the genus Protea (P.W. Crous

pe rs. obs. ). An un ide ntified Armilla ria sp. has a lso

been recorded on Dryandra palycepha la Benth (Shives,1989).

According to Laemmlen a nd Bego ( 1974), Bega (1962)

made the first report of A mel/eo in Hawa ii, when he

fou nd this pathogen on G_ robusta . However, no

bas idiomes (mushrooms) of Armillaria ha ve eve r been

found on the island (Loemm len a nd Bego, 1974). In

view of the recent ad vances in the ta xonom y and species

ide ntification of this genus, th e identifica t ion of th is

pathogen on Proteaceae in Ha wa ii, probably needs

to be re assess e d. O n an oth er is la nd whe re

Proteaceae ar e cu ltivate d, namely Modeiro, Armillaria

ha s been isolated from Protea ceou s hosts, but the

pa thog en has not yet been identified to species level

(Moura and Rodrigues, 2000).

--~.- ----.- ..-...-.._-.-.-.---=.---_._-.---:...=-

Interestingly, a num ber of differen t species of Armillaria

have been reported on Proteac eae from New Zea land .

Both Armillaria /imonea (Stevenso n) Boesew inke l a nd

Armillaria no vae -ze/andiae (Ste venson) Herink. were

found on Knightia exce/sa R.Br. a nd the latter was also

reported on G. robusta (Pen nycook, 1989).

Africa n reco rds of Armillaria on Protea ceae a re very sca nt

but th e fungus ha s been record ed on G. robusto in

Kenya and Ta nza nia (Anonomyous, 1960) as well os in

So uth Afric a ( Doidge, 1950) . In Zim babwe on

unidentified Armilforia sp . has been reporte d from Q

Protea sp (Musuko et 0/., 1998) .

Armillaria in Sout h Afric aUntil now the only record of Armillaria on Proteaceae in

So ut h Africa, was o n G. rabusta (Doidg e , 1950, ).

According to Coetzee et 0/ ., (Coetzee et 0 /., 20000)

only two species of Armillaria a re thu s far known occ ur

in South Africa, Armillaria fuscipes Petch a nd A . me/leo.

In view of the recent ad vances in the taxonomy of

Armillaria , previous records (pre-1996) of this fun gu s

should be referred to mere ly as Armilforia sp. because

the spe cies identity is no long er ce rta in. A rmilla ria

fU5cipes is an importa nt pat hogen of pines (Coetzee et

0/ ., 20000), especially in the northern ports of the

country. The on ly relia ble record of A. mel/eo in South

Africa is on oak trees in the Comp a ny Ga rdens in the

centre of Cape Town where it was ap parently introdu ced

by eoriy settlers (Coetzee et 0/., 2000b). Arm illa ria sp.

(originally as Armiflaria mellea) has been recorded as 0

pathogen on Aroucoria brazi/iana A. Rich. (mo nke y

puzzle trees) (Doidge 1950 ), on Cedrefa odorata Linn.

(West Indian ced a rs) (Doidge 1950), Cupressus /usitanica

(cypress) (Doidge 1950), De/onix reg ia Rof. (fla mboyant

trees) (Doidge 1950), Eriobatrya japonica (Thunb.) Lind!.

(Ioquats) ) (Doidge 1950), Euco /yptus panicufota Sm .

(Doidge 1950), Grevillea robusta (Doidge 1950), Parinari

cu ra t ell ifo /ia (Mo bo lo plum) (Doid ge 195 0 ), Musa

cavendishii Lomb. (ban anas) (Brodrick, 1971 ), Pinus spp.

(Doidg e 1950), Q ue rcus spp. (oa ks) (Doidge 1950 ),

s yzygium ge rrardii (Ho rv. Ex Hook. f . ) Burtt. Da vy

(forest wote rwoo d) (Doidge 1950), a nd Toano cil iata

M.J. Roe m. (toon trees) (Doidge 1950 ). Armillaria

sp . (o riginolly a s A. m ell ea) wos also re po rte d by

Doid ge ( 1950) on severa l ot her hosts, but as th e se

re po rts we re unconfi rmed they we re not listed by

Doidg e et 0/., 195 3, Gorter, 197 7 or Crous et 0/.,

200 0

In 1996 A. mellea, a deva stating pathogen of ma ny

woody species wo rld -wid e wa s ide ntifie d in t he

"Compa ny Gardens" in the centre of Ca pe Town on

oa k t rees (Coetzee e t a/ ., 2000b). An int rig uing

sto ry of ho w t h is fu ngu s must ha ve be e n

int rod uced into Cape Town du ring the ea rly Ca pe

Dutch settlement (1652) on one of the potted plants

(suc h as citrus or gra pevine) is presented by Coetzee

et 0/. (2000b). Ifthe hypot hes is proposed by Caetzee

et 0/. (2000b) is correct, and this fung us has not

been reported else where in the Western Cape until

now, the spread of th is pat hogen ha s obviously been

con ta ined up to the presen t.

Armillaria on Proteaceae in SouthAfrica - A ne w recordDeclining P. sco/ymocepha/a plants were encounte red

in th e plan ted beds a t Kirst en bos ch Na ti o nal

Botanical Gardens, Ki rstenbosch, Cape Town in May

2000. The leaves of affecte d 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). Isola t io ns were ma de and the pathog e n was

obtained in culture (Fig. 4). Cultures are ma inta ined

in the Depa rt ment of Plant Pa t ho log y cu lture

co llection, Univers ity of Ste llenbosch Private Ba g

X l , Matieland 7600 - Culture numbers STE-U 3773

an d STE-U 3774. No fruiting structures (basidia mes)

Fig . 5 . A Protea scolymocephala pl ant infected with Armillaria in

Kirst enbosch Ga rd ens. Note the chlorotic lowe r leaves and dead

branches

were present nor were rh izomorphs obse rve d, thus

identification to species level will have to be derived from

molecular studies . This work is unde rway a nd the results

prom ise to be most intriguing. One possibility is th at the

exot ic A. mel/eo ha s esca ped from the Company Ga rdens

an d ente red Kirstenbosch . Alternat ively, t his cou ld be

another species of Armillaria an d possib ly even something

new for South Africa.

Fi g. 6 . A Prot ea scolym ocephala p lant in fec t ed wi t h Armillaria in

Kir ste nbosch Gar dens . Not e the chlorotic lowe r leaves, de ad br anc hesand 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. 7. Wh ite mycelial fans typical of Armillaria present below the bark in

the crown reg io n of P. scolymocephala plants infect ed with Armillaria in

Kir stenbosch Gardens

-------------- -- -----------_ .~-----

DiscussionArm illaria is a seriou s root rot pathogen of man y woody

hosts a nd in South Africa, th e most serious rootpathogen on Proteaceae that we have had to contendwith th us far is Phyt ophthora cinnamomi Ra nds,although in the past two years Fusarium wilt ca usedby Fusa rium oxysporum Schlecht . ha s become aproblem. Does thi s new record mean that we now

hove a third serious root pathogen that we need to

keep in check? In order to answer this que stion Q

few facts need to be esta blished . Firstly the speciesidentifica tio n of the Arm illaria able to infect P.scolymocepho/la must be resolved. The host rangeof this pat hogen must be established and then thebig challenge will be to answer the question of howth is pat hoge n a ppeared in Kirsten bosch Ga rde ns.Once these facts are establis hed it will be easi er toestimate the potentia l impact of this pathogen to

the South Africa n Proteaceae indust ry. However, if thefu ngu s is Armillaria m e l/eo, th ere may be se rio usimplications for indigenous vegetation on Ta ble Mountaina nd it will be essential to era dicate this pat hogen beforeit beco mes a thre a t to bot h nat u ral a nd c ultiva tedProteaceae in the Western Cape.The flowerbeds at Kirstenbosch a re co vered with barkchips that help retain soil moisture and whe n th eydecompose th ey return nutrients to th e soil, they a lso he lpprevent soil erosion and made rate the tem perature of th esoil. Armillaria spp . are common wood rotting fungi thusit is quite possible that this pathoge n wos introduced intoKi rstenbosch Ga rdens on the bar k chips that have beenst rewn over the flower beds. Growers need to be warnedof the potentia l risk involved with the practice of coveringbeds with bark chips espec ia lly lf they were de rived fromdiseased, rotted or dead trees or shrubs .

AcknowledgementsWe th an k Dr J Taylor for her co n tri b ut ion o f lite ra tur e res ources and fo r reviewing the ma n uscr ip t. We also thank Ioland e Roux and Ja mesTown send who b rou ght thi s d ise ase to O UT at te ntio n and ass is ted with field co llect ions.

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