Doi: 10. 1111/j. 1365-3059. 2007. 01608. x 2007 The Authors



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Plant Pathology

 

 (2007) 



 

56

 

, 624–636



Doi: 10.1111/j.1365-3059.2007.01608.x

 

© 2007 The Authors 



 

624


 

Journal compilation © 2007 BSPP

 

Blackwell Publishing Ltd



 

Botryosphaeriaceae occurring on native 



 

Syzygium cordatum

 

 



in South Africa and their potential threat to 

 

Eucalyptus

 

D. Pavlic



 

a

 



*, B. Slippers

 

b



 

, T.  A. Coutinho

 

a

 



 and M.  J. Wingfield

 

a



 

a

 



Department of Microbiology and Plant Pathology; and 

 

b



 

Department of Genetics, Forestry and Agricultural Biotechnology Institute (FABI), 

Faculty of Natural and Agricultural Sciences, University of Pretoria, Pretoria, 0002, South Africa 

 

Eight species of the Botryosphaeriaceae (canker and dieback pathogens) were identified on native 



 

Syzygium cordatum

 

in South Africa, based on anamorph morphology, ITS rDNA sequence data and PCR-RFLP analysis. The species



identified were 

 

Neofusicoccum parvum, N. ribis, N. luteum, N. australe, N. mangiferae

 



 

Botryosphaeria dothidea,

Lasiodiplodia gonubiensis

 

  and 



 

L. theobromae

 

. Their pathogenicity on 



 

S. cordatum

 

  seedlings and a 



 

Eucalyptus

grandis

 

 



 

×

 



 

 

camaldulensis

 

 clone was determined in glasshouse inoculation trials. Isolates of all identified species, except



one of 

 

N. mangiferae

 

, were more pathogenic on the 



 

Eucalyptus

 

 clone than on 



 

S. cordatum

 

. Some of the species that



cross-infected these hosts, such as 

 

N. ribis, N. parvum

 

 and 



 

L. theobromae

 

, were amongst the most pathogenic on the



 

Eucalyptus

 

 clone, while 



 

B. dothidea

 

 and 



 

L. gonubiensis

 

 were the least pathogenic. Results of this study illustrate that



species of the Botryosphaeriaceae from native hosts could pose a threat to introduced 

 

Eucalyptus

 

 spp., and 



 

vice versa

 

.



 

Keywords

 

: Botryosphaeriaceae, 



 

Eucalyptus

 

 spp., host association, indigenous tree, latent pathogen, 



 

Myrtaceae

 

 



 

Introduction

 

The Botryosphaeriaceae (Dothideales) is comprised of



fungal species that have a wide geographic distribution

and extensive host range, including 



 

Eucalyptus

 

  spp.



(Myrtaceae) (von Arx & Müller, 1954; Crous 

 

et al

 

.,



2006). These fungi are latent and opportunistic pathogens

that occur as endophytes in symptomless plant tissues and

they can cause rapid disease development when plants are

exposed to unsuitable environmental conditions such

as drought, freezing, hot or cold winds, hail wounds or

damage caused by insects or other pathogens (Fisher



 

et al

 

., 1993; Smith 



 

et al

 

., 1996). Species of the Botry-



osphaeriaceae cause a wide variety of symptoms on all

parts of 



 

Eucalyptus

 

 trees and on trees of all ages, but are



mostly associated with cankers and dieback followed by

extensive production of kino, a dark-red tree sap, and in

severe cases mortality of trees (Smith 

 

et al

 

., 1994, 1996;



Old & Davison, 2000).

The Myrtaceae is a predominantly southern hemi-

sphere angiosperm family that accommodates more than

3000 species, largely distributed in the tropical and

temperate regions of Australasia, as well as Central and

South America (Johnson & Briggs, 1981). Species of the

Myrtaceae also form an integral part of the Southern

African indigenous flora (Palgrave, 1977). In this context,

the most widespread myrtaceous tree in South Africa is

 

Syzygium cordatum

 

 (Palgrave, 1977). 



 

Eucalyptus

 

 species,



native Australasian Myrtaceae, are the most widely grown

trees in commercial forestry plantations, particularly in the

tropics and southern hemisphere, including South Africa.

Movement of pathogens between native and intro-

duced hosts has been recognized as a significant threat to

plant communities (Slippers 



 

et al

 

., 2005). Because of



the potential threat of native pathogens to non-native

 

Eucalyptus

 

 plantations, various recent studies considered



fungal pathogens on native hosts in areas where 

 

Eucalyptus

 

spp. are intensively planted (Wingfield, 2003; Burgess



 

et al

 

., 2006). These studies showed that pathogens which



can cause severe diseases on 

 

Eucalyptus

 

 spp. also occur on



native plants and thus pose a threat to 

 

Eucalyptus

 

 spp.



Where plantations of non-native 

 

Eucalyptus

 

  spp



 

.

 

  are



established amongst closely related native myrtaceous

trees, pathogens could cross-infect either the native or

introduced host group and cause serious diseases (Burgess

& Wingfield, 2001). For example, the rust fungus 



 

Puccinia

psidii

 

, which occurs on a variety of native Myrtaceae in



South America, has become one of the main pathogens on

exotic 


 

Eucalyptus

 

 spp. in that area (Coutinho 



 

et al

 

., 1998).



In South Africa, species of the Botryosphaeriaceae are

amongst the most important canker pathogens in planta-

tions of non-native 

 

Eucalyptus

 

 spp., causing twig dieback,



branch and stem cankers and mortality of diseased trees

(Smith 


 

et al

 

., 1994). These fungi have also recently been



 

*E-mail: draginja.pavlic@fabi.up.ac.za



 

Accepted 12 December 2006

 

Plant Pathology

 

 (2007) 



 

56

 

, 624–636



 

Botryosphaeriaceae on Myrtaceae in South Africa

 

625



 

PPA_1608

 

reported as endophytes from native South African trees



closely related to 

 

Eucalyptus

 

, such as 



 

S. cordatum

 

 and



 

Heteropyxis natalensis

 

 (Smith 



 

et al

 

., 2001). The 



 

Eucalyptus

 

plantations mostly occur in the eastern part of the country



where 

 

S. cordatum

 

 is widely distributed (Palgrave, 1977;



Anonymous, 2002; Fig. 1). Thus, Botryosphaeriaceae

that occur on this native tree could pose a threat to exotic



 

Eucalyptus

 

 spp. and 



 

vice versa

 

. However, there have not



been any detailed studies on Botryosphaeriaceae on

native hosts closely related to 



 

Eucalyptus

 

 in South Africa.



Because of the economic importance of 

 

Eucalyptus

 

plantations, as well as the need to protect native flora,



identification and characterization of Botryosphaeriaceae

from 


 

S. cordatum

 

 is of great concern.



Recent studies combined morphological characteristics

and DNA sequence data to distinguish and identify

species within the Botryosphaeriaceae (Denman 

 

et al

 

.,



2000;  Zhou & Stanosz, 2001; Crous 

 

et al

 

., 2006).



Molecular approaches most commonly used to study

Botryosphaeriaceae are comparisons of sequence data

from the internal transcribed spacer (ITS) gene region of

the rDNA operon (Denman 



 

et al

 

., 2000; Zhou & Stanosz,



2001). However, some closely related or cryptic species of

the Botryosphaeriaceae have been difficult to distinguish

based on single gene genealogies. Comparisons of sequence

data for multiple genes or gene regions were thus used to

discriminate between these species (Slippers 

 

et al

 

., 2004a,



c). Furthermore, identification of large numbers of species

has been facilitated by PCR restriction fragment length

polymorphism (RFLP) techniques (Slippers 

 

et al

 

., 2004b).



The aims of this study were to identify Botryosphaer-

iaceae occurring on native 



 

S. cordatum

 

 in South Africa,



based on ITS rDNA sequence data, PCR-RFLP analysis

and anamorph morphology. Isolates belonging to the

Botryosphaeriaceae on 

 

S. cordatum

 

 and 



 

Eucalyptus

 

 were



also compared, with special attention given to overlaps

and the potential for cross infection. The pathogenicity

of the Botryosphaeriaceae isolates from 

 

S. cordatum

 

was furthermore tested on both a 



 

Eucalyptus

 

 clone and



 

S. cordatum

 

 in glasshouse trials.



 

Materials and methods

 

Isolates

 

Isolates used in this study were collected in surveys of



Botryosphaeriaceae on native 

 

S. cordatum

 

  in different



geographical regions of South Africa, in 2001 and 2002

(Table 1, Fig. 1). The 148 isolates that were collected from

11 

 

S. cordatum

 

 sites during these surveys form the basis



of this study. Between 5 and 45 trees were sampled from

each site. From each tree, isolations were made from

dying twigs and symptomless, visually healthy twig and

leaf tissues. Leaves and twig portions (5 cm in length)

were washed in running tap water and surface sterilized

by placing them sequentially for 1 min in 96% ethanol,

undiluted bleach (3·5–5% available chlorine) and 70%

ethanol, then rinsed in sterile water. Treated twig portions

were halved and pieces from the pith tissue (2 mm

 

2



 

) and


segments of the leaves (3 mm

 

2



 

) were placed on 2% malt

extract agar (MEA; 2% malt extract, 1·5% agar; Biolab)

in Petri dishes. Following incubation for 2 weeks at 20

 

°

 



C

under continuous near-fluorescent light and colonies

resembling Botryosphaeriaceae with grey-coloured, fluffy

aerial mycelium, were selected. These colonies were trans-

ferred to 2% MEA at 25

 

°



 

C and stored at 5

 

°

 



C. All isolates

Figure 1 A map of South Africa indicating the area of natural distribution of Syzygium cordatum (left) and sites from where isolates of the 

Botryosphaeriaceae identified in this study were obtained (stars, right).


 

Plant Pathology

 

 (2007) 



 

56

 

, 624



–636

 

626



 

D. Pavlic 

 

et al.



 

PP

A_1608

 

Table 1



 

Isolates considered in the phylogenetic study and pathogenicity trials

GenBank 

ITS


Isolate

 

a,b



 

Other no.

 

a

 



Identity

Host


Location

Isolator


CMW 7772

 

Neofusicoccum ribis

Ribis

 

 sp.



New York, USA

B. Slippers & G. Hudler

AY236935

CMW 7054


CBS 121

 

N. ribis

 

 (chromagena)



 

R. rubrum

 

New York, USA



N.E. Stevens

AF241177


CMW 14011

 

N. ribis

Syzygium cordatum

 

Sodwana Bay, S. Africa



D. Pavlic

DQ316072


 

CMW 14012

 

N. ribis

S. cordatum

 

Sodwana Bay, S. Africa



D. Pavlic

DQ316073


 

CMW 13990

 

N. ribis

S. cordatum

 

Sodwana Bay, S. Africa



D. Pavlic

DQ316074


 

CMW 13991

 

CBS 118822



 

N. ribis

S. cordatum

 

Sodwana Bay, S. Africa



D. Pavlic

DQ316075


 

CMW 14016

 

 



 

N. ribis

S. cordatum

 

Kwambonambi, S. Africa



D. Pavlic

DQ316079


 

CMW 14031

 

c

 

N. ribis

S. cordatum

 

Kwambonambi, S. Africa



D. Pavlic

DQ316076


 

CMW 14025

 

N. ribis

S. cordatum

 

Kwambonambi, S. Africa



D. Pavlic

DQ316080


CMW 13992

 

c



 

N. ribis

S. cordatum

 

Sodwana bay, S. Africa



D. Pavlic

CMW 9081


ICMP 8003

 

Neofusicoccum parvum

Populus nigra

 

New Zealand



G.J. Samuels

AY236943


CMW 9078

ICMP 7925



 

N. parvum

Actinidia deliciosa

 

New Zealand



S.R. Pennycook

AY236940


CMW 994

ATCC 58189



 

N. parvum

Malus sylvestris

 

New Zealand



G.J. Samuels

AF243395


CMW 9071

 

N. parvum

Ribes

 

 sp.



Australia

M.J. Wingfield

AY236938

CMW 10122



 

N. parvum

Eucalyptus grandis

 

Mpumalanga, S. Africa



H. Smith

AF283681


 

CMW 14030

 

c

 

N. parvum

S. cordatum

 

Kwambonambi, S. Africa



D. Pavlic

DQ316077


 

CMW 14029

 

CBS 118832



 

N. parvum

S. cordatum

 

Kwambonambi, S. Africa



D. Pavlic

DQ316078


CMW 14097

 

c

 

N. parvum

S. cordatum

 

St. John’s Port, S. Africa



D. Pavlic

CMW 7801


BRIP 23396

 

Neofusicoccum mangiferae

Mangifera indica

 

Australia



G.I. Johnson

AY615187


CMW 7024

BRIP 24101



 

N. mangiferae

M. indica

 

Australia



G.I. Johnson

AY615185


CMW 13998

CBS 118821



N. mangiferae

S. cordatum

Sodwana Bay, S. Africa

D. Pavlic

DQ316081


CMW 14005

N. mangiferae

S. cordatum

Sodwana Bay, S. Africa

D. Pavlic

DQ316082


CMW 14102

c

N. mangiferae

S. cordatum

Sodwana Bay, S. Africa

D. Pavlic

DQ316083


CMW 14034

c

N. mangiferae

S. cordatum

Kwambonambi, S. Africa

D. Pavlic

CMW 9072


Neofusicoccum australe

Acacia sp.

Melbourne, Australia

J. Roux & D. Guest

AY339260


CMW 6837

N. australe

Acacia sp.

Batemans Bay, Australia

M.J. Wingfield

AY339262


CMW 1110

N. australe

Widdringtonia nodiflora

Cape province, S. Africa

W.J. Swart

AY615166


CMW 1112

N. australe

W. nodiflora

Cape province, S. Africa

W.J. Swart

AY615167


CMW 3386

N. australe

Wollemia nobilis

Queensland, Australia

M. Ivory

AY615165


CMW 14074

N. australe

S. cordatum

East London, S. Africa

D. Pavlic

DQ316089


CMW 13986

CBS 118839



N. australe

S. cordatum

Sodwana Bay, S. Africa

D. Pavlic

DQ316085


CMW 13987

c

N. australe

S. cordatum

Sodwana Bay, S. Africa

D. Pavlic

DQ316086


CMW 14013

c

N. australe

S. cordatum

Sodwana Bay, S. Africa

D. Pavlic

DQ316087


CMW 9076

ICMP 7818



Neofusicoccum luteum

Malus domestica

New Zealand

S.R. Pennycook

AY236946


CMW 992

KJ 93·52


N. luteum

Actinidia deliciosa

New Zealand

G.J. Samuels

AF027745


CMW 10309

CAP 002


N. luteum

Vitis vinifera

Portugal


A.J.L. Phillips

AY339258


CMW 14071

c

CBS 118842



N. luteum

S. cordatum

East London, S. Africa

D. Pavlic

DQ316088


CMW 14073

c

N. luteum

S. cordatum

East London, S. Africa

D. Pavlic

DQ316090


CMW 10125

Neofusicoccum eucalyptorum

E. grandis

Mpumalanga, S. Africa

H. Smith

AF283686


CMW 11705 

N. eucalyptorum

E. nitens

South Africa

B. Slippers

AY339248


Plant Pathology

 (2007) 


56

, 624


–636

Botryosphaeriaceae on Myrtaceae in South Africa

627


PP

A_1608

CMW 9075


ICMP 8019

Botryosphaeria dothidea

P. nigra

New Zealand

G.J. Samuels

AY236950


CMW 8000

B. dothidea

Prunus sp.

Crocifisso, Switzerland

B. Slippers

AY236949


CMW 14009

c

CBS 118831



B. dothidea

S. cordatum

Sodwana Bay, S. Africa

D. Pavlic

DQ316084


CMW 10130

Lasiodiplodia theobromae

Vitex donniana

Uganda


J. Roux

AY236951


CMW 9074

L. theobromae

Pinus sp.

Mexico


T. Burgess

AY236952

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