Botryosphaeriaceae ocorrendo em Syzygium cordatum nativa na África do Sul e sua ameaça potencial aos eucaliptos - Pavlic - 2007 - Fitopatologia - Biblioteca Online Wiley

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Patologia das plantas / Volume 56, Edição 4 / pág. 624-636
Acesso Livre
Botryosphaeriaceae ocorrendo em Syzygium cordatum nativa na África do Sul e
sua potencial ameaça aos eucaliptos
Publicado pela primeira vez:23 de julho de 2007
https://doi.org/10.1111/j.1365-3059.2007.01608.x
Citações: 76
Abstrato
D. Pavlic, B. Chinelos, TA Coutinho, MJ Wing�eld
Oito espécies de Botryosphaeriaceae (patógenos de cancro e morte) foram identi�cadas
em Syzygium cordatum nativa na África do Sul, com base na morfologia anamorfa, dados
de sequência de rDNA ITS e análise de PCR-RFLP. As espécies identi�cadas foram
Neofusicoccum parvum, N. ribis, N. luteum, N. australe, N. mangiferae , Botryosphaeria
dothidea, Lasiodiplodia gonubiensis e L. theobromae . Sua patogenicidade em mudas de S.
cordatum e em um clone de Eucalyptus grandis  ×  camaldulensis foi determinada em
ensaios de inoculação em estufa. Isolados de todas as espécies identi�cadas, exceto um
de N. mangiferae , foram mais patogênicos no clone de Eucalyptus do que em S. cordatum
. Algumas das espécies que infectaram esses hospedeiros, como N. ribis, N. parvum e L.
theobromae , estavam entre as mais patogênicas no clone de Eucalyptus , enquanto B.
dothidea e L. gonubiensis foram as menos patogênicas. Os resultados deste estudo
ilustram que espécies de Botryosphaeriaceae de hospedeiros nativos podem representar
uma ameaça para os Eucalyptus spp. introduzidos e vice-versa .
Introdução
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 Botryosphaeriaceae cause a
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https://bsppjournals.onlinelibrary.wiley.com/authored-by/Pavlic/D.
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https://bsppjournals.onlinelibrary.wiley.com/authored-by/Pavlic/D.
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https://bsppjournals.onlinelibrary.wiley.com/authored-by/Slippers/B.
https://bsppjournals.onlinelibrary.wiley.com/authored-by/Slippers/B.
https://bsppjournals.onlinelibrary.wiley.com/authored-by/Slippers/B.
https://bsppjournals.onlinelibrary.wiley.com/authored-by/Coutinho/T.+A.
https://bsppjournals.onlinelibrary.wiley.com/authored-by/Coutinho/T.+A.
https://bsppjournals.onlinelibrary.wiley.com/authored-by/Coutinho/T.+A.
https://bsppjournals.onlinelibrary.wiley.com/authored-by/Wingfield/M.+J.
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https://bsppjournals.onlinelibrary.wiley.com/authored-by/Wingfield/M.+J.
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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 hemisphere 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 �ora
(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 introduced hosts has been recognized as a
signi�cant 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
(Wing�eld, 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 & Wing�eld, 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 plantations 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 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 �ora, identi�cation and characterization of
Botryosphaeriaceae from S. cordatum is of great concern.
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Figure 1
Open in �gure viewer PowerPoint
A map of South Africa indicating the area of natural distribution of Syzygium cordatum
(left) and sites from where isolates of the Botryosphaeriaceae identi�ed in this study were
obtained (stars, right).
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 transcribedspacer
(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
di�cult 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, identi�cation 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 Botryosphaeriaceae 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
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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 di�erent 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 ) and segments of the leaves
(3 mm ) 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-�uorescent
light and colonies resembling Botryosphaeriaceae with grey-coloured, �u�y aerial mycelium,
were selected. These colonies were transferred to 2% MEA at 25°C and stored at 5°C. All
isolates have been maintained in the Culture Collection (CMW) of the Forestry and
Agricultural Biotechnology Institute (FABI), University of Pretoria, South Africa, and
representative isolates were deposited in the collection of the Centraalbureau voor
Schimmelcultures (CBS), Utrecht, the Netherlands.
Table 1. Isolates considered in the phylogenetic study and pathogenicity trials
2
2
CMW
7772
Neofusicoccum ribis Ribis sp. New York, USA B. Slippers
& G.
Hudler
A
CMW
7054
CBS
121
N. ribis (chromagena) R. rubrum New York, USA N.E.
Stevens
A
CMW
14011
N. ribis Syzygium
cordatum
Sodwana Bay,
S. Africa
D. Pavlic D
CMW
14012
N. ribis S. cordatum Sodwana Bay,
S. Africa
D. Pavlic D
Isolatea,b Other
no.a
Identity Host Location Isolator G
IT
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https://www.ncbi.nlm.nih.gov/nuccore/DQ316072
https://www.ncbi.nlm.nih.gov/nuccore/DQ316073
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DNA extraction and ITS rDNA ampli�cation
Single conidial cultures from 21 isolates were grown on MEA for 7 days at 25°C in the dark.
Template DNA was obtained from the mycelium using the modi�ed phenol:chloroform DNA
extraction method described in Smith et al. (2001). DNA was separated by electrophoresis
on 1·5% agarose gels, stained with ethidium bromide and visualized under ultraviolet light.
DNA concentrations were estimated against λ standard size markers.
The internal transcribed spacer (ITS) regions ITS1 and ITS2, and the intermediate 5·8S gene
of the ribosomal RNA (rRNA), were ampli�ed using the primer pair ITS1 and ITS4 (White
et al., 1990). The PCR reactions were performed using the PCR protocol of Slippers et al.
(2004b). PCR products were separated in a 1·5% agarose gel, stained with ethidium bromide
and visualized under UV light. Sizes of PCR products were estimated against a 100 bp
molecular weight marker XIV (Roche Diagnostics). The PCR products were puri�ed using the
High Pure PCR Product Puri�cation kit (Roche Diagnostics).
DNA sequencing and analysis
Based on conidial morphology, the isolates of Botryosphaeriaceae from S. cordatum in South
Africa were tentatively separated into eight groups. ITS rDNA sequences were determined
for representative samples from all morphological groups (Table 1). To determine the
identity and phylogenetic relationships of these isolates, ITS sequences of known species of
the Botryosphaeriaceae were obtained from GenBank and included in the analyses
CMW
13990
N. ribis S. cordatum Sodwana Bay,
S. Africa
D. Pavlic D
CMW
13991
CBS
118822
N. ribis S. cordatum Sodwana Bay,
S. Africa
D. Pavlic D
 Culture collections: CMW = Tree Pathology Co-operative Programme, Forestry and Agricultural Biotechnology
Institute, University of Pretoria; KJ = Jacobs & Rehner (1998); ATCC = American Type Culture Collection, Fairfax, VA,
USA; BRIP = Plant Pathology Herbarium, Department of Primary Industries, Queensland, Australia; CAP = culture
collection of A.J.L. Phillips, Lisbon, Portugal; CBS = Centraalbureau voor Schimmelcultures, Utrecht, Netherlands;
ICMP = International Collection of Microorganisms from Plants, Auckland, New Zealand; ZS = Zhou & Stanosz
(2001).
a
b Isolates sequenced in this study are given in bold.
c Isolates used in pathogenicity trials.
Isolatea,b Other
no.a
Identity Host Location Isolator G
IT
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(Table 1). The puri�ed PCR products were sequenced using the same primers that were
used for the PCR reactions. The ABI PRISM™ Dye Terminator Cycle Sequencing Ready
Reaction kit (Perkin-Elmer) was used for sequencing reactions, as speci�ed by the
manufacturers. Sequence reactions were run on an ABI PRISM 3100™ automated DNA
sequencer (Perkin-Elmer).
As sequências de nucleotídeos foram analisadas usando O NAVEGADOR DE SEQUÊNCIA versão 1·0·1.
(Perkin-Elmer Applied BioSystems, Inc.) e os alinhamentos foram feitos on-line usando MAFFT
versão 5.667 ( //timpani.genome.ad.jp/~ma�t/server/ ) ( Katoh et al ., 2002 ). Aslacunas
foram tratadas como quinto caractere e todos os caracteres eram desordenados e de igual
peso. As análises �logenéticas de sequências alinhadas foram realizadas utilizando O PAUP
(Phylogenetic Analysis Using Parsimony) versão 4·0b8 ( Swo�ord, 1999 ). As árvores mais
parcimoniosas foram encontradas usando a função de busca heurística com 1000 réplicas
de adição aleatória e bissecção e reconstrução de árvores (TBR) selecionadas como o
algoritmo de troca de ramos. Galhos de comprimento zero foram derrubados e todas as
árvores múltiplas e igualmente parcimoniosas foram salvas. O suporte de rami�cação foi
determinado usando 1.000 réplicas de bootstrap ( Felsenstein, 1985 ). As árvores foram
enraizadas utilizando as sequências do GenBank de Guignardia philoprina e Mycosphaerella
africana , que estão intimamente relacionadas com Botryosphaeriaceae. Os alinhamentos
de sequências e árvore �logenética foram depositados no TreeBASE como S1412, M2541.
Análises PCR-RFLP
Técnicas de impressão digital PCR-RFLP foram aplicadas para con�rmar a identidade dos
isolados que não foram sequenciados e para identi�car os isolados que não puderam ser
separados com base nas sequências de rDNA ITS. Amplicons obtidos usando pares de
iniciadores ITS1 e ITS4, ou BOT15 (5'-CTGACTTGTGACGCCGGCTC-3') e BOT16 (5'-
CAACCTGCTCAGCAAGCGAC-3') ( Slippers et al ., 2004a ) foram digeridos com a
endonuclease de restrição Cfo I. O RFLP a mistura de reação consistiu em 10 µL de produtos
de PCR, 0,3 µL de Cfo I e 2,5 µL de tampão enzimático correspondente (Roche Diagnostics). A
mistura reaccional foi incubada a 37°C durante a noite. Os fragmentos de restrição foram
separados em gel de agarose a 1,5% conforme descrito para produtos de PCR. Os
resultados foram comparados com os de Slippers (2003 ).
Morfologia e características culturais
Os isolados de fungos foram cultivados em ágar água a 2% (WA; Biolab) com agulhas de
pinheiro esterilizadas colocadas no meio, a 25°C sob luz quase UV, para induzir a
esporulação. Os conídios liberados dos picnídios nas agulhas dos pinheiros foram montados
em lactofenol em lâminas de vidro e examinados microscopicamente. Foram realizadas dez
medições de conídios para cada isolado. Medições e fotogra�as digitais foram tiradas
usando um microscópio óptico, uma câmera digital HRc Axiocam e software acompanhante
(Carl Zeiss Ltd). A morfologia e a cor das colónias foram determinadas a partir de culturas
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cultivadas em 2% de MEA a 25°C sob luz quase UV. As cores das colônias (superfície superior
e reverso) foram comparadas com as da tabela de cores de Rayner (1970 ).
Patogenicidade
Quinze isolados, representando oito espécies de Botryosphaeriaceae isoladas de S.
cordatum nativa na África do Sul, foram utilizados neste estudo ( Tabela 1 ). Um isolado de
Botryosphaeria dothidea e dois isolados de cada uma das outras sete espécies foram
selecionados aleatoriamente para inoculações. Os isolados foram cultivados em MEA a 2% a
25°C sob luz quase �uorescente contínua durante 7 dias antes da inoculação.
Árvores de dois anos de idade de um clone de E. grandis  ×  camaldulensis (GC-540) e mudas
de S. cordatum com 1 ano de idade foram selecionadas para os ensaios de patogenicidade
em condições de estufa. Mudas de S. cordatum foram cultivadas a partir de sementes
retiradas de uma única árvore cultivada na área de Kwambonambi (província de Kwazulu-
Natal). As árvores e mudas selecionadas para inoculações foram cultivadas em vasos
externos e mantidas em estufa para aclimatação por 3 semanas antes da inoculação. As
árvores foram inoculadas durante a estação primavera-verão (setembro de 2003 a fevereiro
de 2004). A estufa foi submetida a condições naturais de dia/noite e a uma temperatura
constante de aproximadamente 25°C. Cada um dos isolados representando as diferentes
espécies foi inoculado nos caules de 10 árvores de cada espécie hospedeira. Dez árvores
também foram inoculadas com tampões de MEA estéreis para servir como controle. As 160
árvores inoculadas, 10 para cada espécie fúngica e 10 como controle, foram dispostas em
delineamento de blocos casualizados. Todo o ensaio foi repetido uma vez nas mesmas
condições, dando um total de 320 árvores inoculadas para cada espécie hospedeira.
Para as inoculações, foram feitas feridas no caule das árvores com broca de cortiça de 6 mm
de diâmetro (clone de Eucalyptus ) ou de 4 mm de diâmetro ( S. cordatum ), para retirar a
casca e expor o câmbio. As feridas foram feitas entre dois nós nos caules das árvores
aproximadamente 250 mm ( Eucalyptus ) ou 150 mm ( S. cordatum ) acima do nível do solo.
Os tampões de micélio foram retirados de culturas com 7 dias de idade cultivadas em MEA
utilizando a broca da cortiça do mesmo tamanho e foram colocados nas feridas com a
superfície micelial voltada para o câmbio. As feridas inoculadas foram seladas com �lme de
laboratório (Para�lm M, Pechiney Plastic Packaging) para evitar dessecação e contaminação.
Os comprimentos das lesões (mm) foram medidos 6 semanas após a inoculação. Os fungos
foram reisolados cortando pequenos pedaços de madeira das bordas das lesões e
plaqueando-os em MEA 2% a 25°C. Os reisolamentos foram feitos a partir de duas árvores
selecionadas aleatoriamente por isolado e espécie de árvore e de todas as árvores
inoculadas como controle.
A patogenicidade de todos os isolados inoculados no clone de Eucalyptus e S. cordatum foi
determinada com base no comprimento das lesões (mm) que se desenvolveram após 6
semanas. Não houve diferença signi�cativa entre as duas repetições dos ensaios de
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patogenicidade e os dados foram, portanto, combinados para representar um conjunto de
dados para as análises. As análises estatísticas dos dados foram realizadas utilizando o
software estatístico SAS (versão 8, SAS Institute). Os limites de con�ança de 95% foram
determinados para todas as médias com base na análise de variância do modelo completo (
ANOVA ). As diferenças entre as médias foram, portanto, consideradas signi�cativas no nível P
 ≤ 0,05.
Resultados
Análises de sequência de DNA
Fragmentos de DNA de aproximadamente 600 pb foram ampli�cados. O conjunto de dados
ITS consistia em 53 sequências de grupo interno, com G. philoprina e M. africana como
táxons de grupo externo ( Tabela 1 ). Após o alinhamento, o conjunto de dados ITS consistiu
em 593 caracteres; Foram excluídos 432 caracteres não informativos e 161 caracteres
informativos de parcimônia foram utilizados na análise. A análise de parcimônia (usando
pesquisas heurísticas) produziu 276 árvores mais parcimoniosas de 414 etapas (índice de
consistência (CI) = 0,702, índice de retenção (RI) = 0,915), uma das quais foi escolhida para
apresentação (Fig. 2 ) . .
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Figura 2
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Uma das 276 árvores mais parcimoniosas obtidas a partir de pesquisas heurísticas de
dados de sequência de rDNA ITS1, 5·8S e ITS2 (comprimento da árvore = 414 passos, CI =
0·702, RI = 0·915). Os comprimentos dos ramos, proporcionais ao número de passos, são
indicados acima dos entrenós e os valores de bootstrap (1000 réplicas) abaixo dos
entrenós. A árvore está enraizada nos táxons do grupo externo Guignardia philoprina e
Mycosphaerella africana . Os isolados sequenciados neste estudo são apresentados em
negrito.
Os isolados considerados nas análises �logenéticas formaram 12 clados, designados como
grupos I a XII ( Fig. 2 ). Esses grupos foram resolvidos em dois clados principais que
correspondiam a espécies de Botryosphaeriaceae com anamorfos semelhantes a
Fusicoccum ou semelhantes a Diplodia . O clado Fusicoccum compreendeu seis grupos que
representavam: Neofusicoccum parvum e N. ribis (grupo I) , N. mangiferae (grupo II), N.
eucalyptorum (grupo III), N. australe (grupo IV), N. luteum (grupo V ) e B. dothidea (grupo VI).
Os grupos VII e VIII representaram espécies com anamorfos de Lasiodiplodia : Lasiodiplodia
theobromae (grupo VII) e L. gonubiensis (grupo VIII). Esses dois grupos (VII e VIII) formaram
um subclado distinto (suportado por 100% do valor de bootstrap) dentro do clado Diplodia .
O outro subclado principal dentro do clado Diplodia continha quatro grupos
correspondentes a: D. mutila (grupo IX), D. corticola (grupo X), Diplodia sp. (= ' Botryosphaeria
obtusa ') (grupo XI) e Diplodia pinea (=  Sphaeropsis sapinea ) (grupo XII) ( Fig. 2 ).
Todos os isolados obtidos de S. cordatum neste estudo residiram em sete grupos ( Fig. 2 )
como segue: N. parvum e N. ribis (grupo I), N. parvum e N. ribis (grupo I) , N. mangiferae
(grupo II), N. australe (grupo IV), N. luteum (grupo V), B. dothidea (grupo VI), L. theobromae
(grupo VII) e L. gonubiensis (grupo VIII).
Análise PCR-RFLP
Os isolados que não foram identi�cados utilizando comparações de sequências de DNA
foram submetidos a análises ITS PCR-RFLP. A digestão dos produtos de PCR, obtidos
utilizando os iniciadores ITS1 e ITS4, com Cfo I produziu dois padrões de bandas distintos.
Estes per�s correspondiam aos de N. parvum / N. ribis (99 isolados) e N. luteum / N. australe
(5 isolados) como mostrado por Slippers et al . (2004b ). Para distinguir ainda mais os
isolados de N. parvum daqueles de N. ribis , os amplicons obtidos utilizando os iniciadores
BOT15 e BOT16 foram digeridos utilizando a mesma endonuclease de restrição. Os dois
padrões de bandas obtidos coincidiram com os de N. parvum (42 isolados) e N. ribis (57
isolados), conforme descrito por Slippers (2003 ). No entanto, N. luteum e N. australe não
puderam ser separados usando esta técnica.
Morfologia e características culturais
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Todos os 148 isolados de Botryosphaeriaceae de S. cordatum produziram estruturas
anamorfas em agulhas de pinheiro em WA dentro de 2 a 3 semanas. Nenhuma estrutura
teleomorfa (sexual) foi observada. Com base na morfologia dos conídios, os isolados foram
separados em oito grupos. Cinco desses grupos correspondiam a Botryosphaeriaceae com
anamorfos de Neofusicoccum ( Fig. 3a-f ), um com um anamorfo de Fusicoccum ( Fig. 3g ) e
dois com anamorfos de Lasiodiplodia ( semelhantes a Diplodia ) ( Fig. 4a, b ).
Figura 3
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Microgra�as ópticas de conídios de seis espécies de Botryosphaeriaceae com anamorfos
semelhantes a Fusicoccum : (a) Neofusicoccum parvum ; (b) N. ribis ; (c) conídios asseptados
e unisseptados de N. australe ; (d, e) conídios uni- e bisseptados aseptados e em
germinação de N. luteum ; (f) N. mangiferae ; (g) Botryosphaeria dothidea . Barras = 10 µm .
Figura 4
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Microgra�as ópticas de conídios de duas espécies de Botryosphaeriaceae com anamorfos
de Lasiodiplodia : (a) Lasiodiplodia gonubiensis ; (b) L. theobromae . Barras = 10 µm .
Amostras representativas dos grupos emergentes de comparações morfológicas foram
identi�cadas com base na comparação de sequências de rDNA ITS. Conforme descrito
anteriormente, os isolados de N. parvum e N. ribis foram separados com base em análises
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de PCR-RFLP. Exames morfológicos adicionais dos isolados, identi�cados com base em
dados de DNA, forneceram suporte para sua identidade.
As culturas de N. parvum eram inicialmente brancas com micélio aéreo e fofo, tornando-se
cinza oliváceo pálido a partir do meio da colônia após 3-4 dias; colunas de micélio formadas
no meio da colônia atingindo a tampa; as margens eram regulares; os lados opostos das
colônias eram cinza oliváceos. Os conídios eram hialinos, lisos, asseptados e fusiformes a
elipsóides (média de 420 conídios: 18,2 × 5,5 µm , l/w 3,3) ( Fig. 3a ). Os 42 isolados foram
identi�cados como N. parvum .
As colônias de N. ribis eram inicialmente brancas, tornando-se cinza oliváceo pálido a partir
do meio da colônia, com micélio aéreo espesso atingindo as tampas das placas de Petri; as
margens eram regulares; os lados opostos das colônias eram cinza oliváceos. Os conídios
eram hialinos, unicelulares, asseptados, fusiformes, ápices cônicos (médiade 570 conídios:
21 × 5,5 µm , l/w 3,8) ( Fig. 3b ). Os 57 isolados foram identi�cados como N. ribis .
A cultura do único isolado de B. dothidea identi�cado neste estudo produziu micélio oliváceo
esverdeado comprimido, com margens regulares e verso das colônias de cor cinza olivácea
a cinza-ferro. Os conidiomas foram prontamente formados no meio das colônias após 3-4
dias de incubação. Os conídios eram hialinos, lisos com conteúdo granular, asseptados,
estreitamente fusiformes (média de 10 conídios: 27,8 × 5,4 µm , l/w 5,1) ( Fig. 3g ).
Isolados de N. mangiferae produziram micélio oliváceo pálido cinza oprimido, levemente fofo
nas bordas das colônias, com margens sinuosas, e o verso das colônias era oliváceo. Os
conidiomas foram prontamente formados no meio das colônias após 3 a 4 dias e cobriram
toda a superfície das colônias em 7 a 10 dias. Os conídios eram hialinos, fusiformes (média
de 300 conídios: 14,2 × 6,3 µm , l/w 2,25) ( Fig. 3f ). Os 30 isolados foram identi�cados como
N. mangiferae .
As culturas de N. luteum eram inicialmente brancas, tornando-se cinza oliváceo pálido a
partir do meio das colônias em 3-4 dias, com micélio suprimido, moderadamente fofo no
meio e com margens regulares. Um pigmento amarelo foi perceptível após 3–5 dias de
incubação e foi visto como amarelo âmbar no verso das placas de Petri; após 5–7 dias, as
colônias tornam-se amarelo-oliváceo a cinza oliváceo. Os conidiomas foram prontamente
formados no meio das colônias em 3 a 4 dias e cobriram toda a superfície das colônias em 7
a 10 dias. Os conídios eram hialinos, fusiformes a elipsóides, às vezes irregularmente
fusiformes, lisos com conteúdo granular, unicelulares, formando um ou dois septos antes
da germinação (média de 40 conídios: 18,9 × 6,3 µ m , l/w 3,0) ( Figura 3d, e ). Os quatro
isolados foram identi�cados como N. luteum .
As culturas de N. australe eram muito semelhantes em morfologia às de N. luteum , mas o
pigmento amarelo produzido nas culturas jovens era mais brilhante e tinha uma cor
amarelo-mel quando visto do fundo das placas de Petri. Os conidiomas formaram-se
prontamente no meio das colônias em 3 a 4 dias e cobriram as superfícies das colônias em
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7 a 10 dias. Os conídios eram hialinos, fusiformes, ápices arredondados, asseptados,
raramente uniseptados (média de 70 conídios: 20,5 × 5,7 µm , l/w 3,6) ( Fig. 3c ). Estes
conídios eram em média ligeiramente mais longos e mais estreitos do que os de N. luteum ,
o que também se re�etiu numa relação l/p mais elevada. Os sete isolados foram
identi�cados como N. australe .
Isolados de L. theobromae produziram inicialmente micélio aéreo fofo branco a cinza-
esfumaçado, tornando-se cinza oliváceo pálido dentro de 5–6 dias com margens regulares;
o verso das culturas era cinza oliváceo a ferro, tornando-se azul ardósia escuro após 7 a 10
dias. Os conídios eram hialinos, asseptados, elipsóides a ovóides, de paredes espessas com
conteúdo granular (média de 50 conídios: 27 × 14,7 µm , l/w 1,85) ( Fig. 4b ). Conídios
escuros e septados típicos desta espécie não foram observados neste estudo. Os cinco
isolados foram identi�cados como L. theobromae .
Os isolados de L. gonubiensis foram semelhantes em morfologia de cultura aos de L.
theobromae. Os conídios de L. gonubiensis eram inicialmente hialinos, unicelulares, elipsóides
a obovóides, de paredes espessas e conteúdo granular, arredondados no ápice e
ocasionalmente truncados na base. Os conídios envelhecidos tornaram-se canela a sépia
com estrias longitudinais, formando um a três septos (média de 20 conídios: 33,9 × 18,9 µm ,
l/w 1,8) ( Fig. 4a ). Os dois isolados foram identi�cados como L. gonubiensis .
Patogenicidade
All Botryosphaeriaceae isolates tested for pathogenicity on the E. grandis × camaldulensis
clone (GC-540) produced lesions within 6 weeks. No lesions developed on trees inoculated
with sterile MEA plugs as controls. The fungi re-isolated from the lesions that developed on
trees were the same as those used for inoculations. The original Botryosphaeriaceae species
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were re-isolated from all trees chosen for re-isolations. No Botryosphaeriaceae were re-
isolated from the controls.
Statistical analyses showed that the mean lesion length for the majority of isolates used in
the trial di�ered signi�cantly from that of the controls (Fig. 5a). The longest lesions were
produced by isolates of L. theobromae, while the size of lesions produced by B. dothidea and
L. gonubiensis were not signi�cantly di�erent to those of the controls (Fig. 5a). The mean
lesion lengths for di�erent strains of the same Botryosphaeriaceae species were not
signi�cantly di�erent, except for the isolates of L. theobromae. Thus, L. theobromae isolate
CMW 14116 was signi�cantly more pathogenic than isolate CMW 14114 (Fig. 5a).
Figure 5
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Mean lesion lengths (mm) for each isolate of di�erent species of the Botryosphaeriaceae
6 weeks after inoculations on (a) Eucalyptus grandis × camaldulensis clone GC-540 and (b)
Syzygium cordatum. Bars represent 95% con�dence limits for each isolate. C = Control;
Botryosphaeria dothidea (CMW14009), Neofusicoccum parvum (CMW14097, 14030); N. ribis
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(CMW13992, 14031); N. australe (CMW13987, 14013); Lasiodiplodia theobromae
(CMW14116, 14114); L. gonubiensis (CMW14077, 140780); N. mangiferae (CMW14102,
14034); N. luteum (CMW14071, 14073).
All Botryosphaeriaceae isolates inoculated on S. cordatum saplings produced lesions within 6
weeks. However, the mean lesion lengths produced by majority of the isolates were not
signi�cantly di�erent from those of the controls (Fig. 5b). Some trees inoculated as controls
also developed small lesions, but no Botryosphaeriaceae could be re-isolated from these
lesions, which appeared to represent wound reactions. The fungi re-isolated from the
lesions on trees inoculated with fungal mycelium were the same as those used for
inoculations. The longest lesions were produced by one isolate of N. mangiferae (CMW
14034) and the mean lesion length obtained for this isolate was signi�cantly greater than
that of the other isolate (CMW 14102) of the same species (Fig. 5b). However, there were no
statistically signi�cant di�erences between the lesion lengths for the di�erent isolates of the
other species of Botryosphaeriaceae (Fig. 5b). The mean lengths of lesions producedby one
isolate of N. ribis (CMW 13992) and one isolate of L. theobromae (CMW 14116) were also
signi�cantly di�erent from that of the control (Fig. 5b). All the other isolates inoculated onto
S. cordatum saplings produced lesions that were not signi�cantly di�erent from those of the
controls (Fig. 5b).
Isolates of all the Botryosphaeriaceae used in this study, except those of N. mangiferuae,
were more pathogenic on the Eucalyptus clone than on S. cordatum. Analyses of variance
showed that the interactions between mean lesion length produced by the species of
Botryosphaeriaceae on the Eucalyptus clone and those on S. cordatum were statistically
signi�cant (P ≤ 0·001).
Discussion
Eight species of the Botryosphaeriaceae were identi�ed on native S. cordatum in South Africa
in this study. They were N. ribis, N. parvum, N. luteum, N. australe, N. mangiferae, B. dothidea,
L. theobromae and L. gonubiensis. The isolates were identi�ed based on ITS rDNA sequence
data, PCR-RFLP analysis and anamorph morphology. With the exception of B. dothidea and L.
gonubiensis, this is the �rst report of all of these species of Botryosphaeriaceae on native S.
cordatum. All eight species had the ability to infect and cause lesions on the stems of a E.
grandis × camaldulensis clone and S. cordatum in glasshouse trials. Although lesions
produced by most of the isolates on S. cordatum saplings were not signi�cantly di�erent
from those on the controls, the pathogens could be re-isolated from these lesions. In the
case of some species, such as N. ribis, L. theobromae and F. mangiferae, one isolate did not
produce lesions that di�ered from those of the control, while the other isolate did. From
these data, and knowledge of the fungi on other hosts, it was concluded that this group of
fungi could be regarded as potential pathogens of Syzygium. However, apart from the
isolates of B. dothidea and L. gonubiensis, all the other Botryosphaeriaceae in this study
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produced lesions on the Eucalyptus clone that were signi�cantly di�erent from those of the
controls. They should be considered as potential threats to plantation grown Eucalyptus spp.
in South Africa.
Neofusicoccum ribis was the dominant species collected from native S. cordatum in South
Africa in this study. This fungus represented 38% of all isolates obtained and was found in
most of the areas surveyed. This abundant and wide distribution on a native host might
indicate that this species is native to this region. Neofusicoccum ribis has been reported from
Eucalyptus spp. (Myrtaceae) in its native range in Australia and on non-native Eucalyptus spp.
in plantations (Old & Davison, 2000), but has not been identi�ed on Eucalyptus spp. in South
Africa (Slippers et al., 2004a). These identi�cations should, however, be interpreted with
caution, as the distinction between N. parvum and N. ribis had not been recognized at the
time of these studies (Slippers et al., 2004a). Furthermore, N. ribis as identi�ed in this study
(using RFLPs) was also interpreted as representing the N. ribis sensu lato group rather than
strictly conspeci�c populations with the type isolates of this species, as identi�ed by Slippers
(2003). Further analyses using sequence data for additional gene regions and other variable
markers will be required to more clearly characterize populations and potential cryptic
species in this group. Neofusicoccum ribis was one of the most pathogenic species of the
Botryosphaeriaceae on the Eucalyptus clone in this study. This fungus should thus be
considered as a potentially important pathogen of Eucalyptus spp. in South Africa.
Isolates of N. parvum represented 28% of the total number of isolates obtained in this study.
Recent studies showed that N. parvum is an important and widely distributed pathogen of
non-native Eucalyptus plantations in South Africa (Slippers et al., 2004b). The wide
distribution of N. parvum on non-native and native Myrtaceae in South Africa raises
intriguing questions, such as whether these populations are native or introduced and how
they might be interacting with each other. The movement of this pathogen between these
important host groups represents a potential threat for both groups and should be further
investigated. Isolates of N. parvum used in this study also developed only slightly smaller
lesions than those of closely related N. ribis, illustrating its potential threat to Eucalyptus
plantations in South Africa.
Only one isolate obtained from S. cordatum was identi�ed as B. dothidea (anamorph
Fusicoccum aesculi). This species is one of the most commonly reported members of the
Botryosphaeriaceae from a wide variety of hosts, including Eucalyptus spp. (von Arx &
Muller, 1954; Smith et al., 2001). While B. dothidea was considered to be an important
canker pathogen of Eucalyptus spp. in South Africa (Smith et al., 1994), some of these
isolates that were the most pathogenic (Smith et al., 2001) were re-identi�ed as N. parvum
(Slippers et al., 2004b). Botryosphaeria dothidea was seldom encountered on Eucalyptus spp.
in other studies on this host (Slippers et al., 2004b) and results of the present study suggest
that it is probably not an important pathogen of this tree.
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24/03/24, 19:40 Botryosphaeriaceae ocorrendo em Syzygium cordatum nativa na África do Sul e sua ameaça potencial aos eucaliptos - Pavlic …
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High numbers of isolates from S. cordatum were identi�ed as N. mangiferae. This species is
best known as a pathogen of mango (Mangifera indica) worldwide, particularly in Australia
(Johnson et al., 1992). Neofusicoccum mangiferae was earlier reported under di�erent names
from mango in South Africa (Darvas, 1991). Interestingly, however, a recent comprehensive
study of Botryosphaeriaceae from mango plantations in South Africa, using a combination of
DNA-based techniques and morphological data, did not report this species (Jacobs, 2002).
The fact that this fungus is highly pathogenic on S. cordatum might imply that it has been
introduced into South Africa on other woody plants. Studies focused on the origin of N.
mangiferae are likely to yield intriguing results, relevant to commercial forestry and to the
protection of natural biodiversity in South Africa.
Neofusicoccum luteum and phylogenetically closely related N. australe were identi�ed on S.
cordatum in this study, but have not been recorded on Eucalyptus spp. in South Africa.
Neofusicoccum australe is a recently described species (Slippers et al., 2004c) and the present
study is the �rst to consider the pathogenicity of this fungus on Eucalyptus. Neofusicoccum
luteum was highly pathogenic to the Eucalyptus clone and its occurrence on the related S.
cordatum in South Africa is of concern. Neofusicoccum luteum and N. australe were not the
most commonly encountered species of the Botryosphaeriaceae on S. cordatum, but their
presence alone provides su�cient evidence that they are well established in the country.
Two Lasiodiplodia species were identi�ed in this study. Lasiodiplodia theobromae was isolated
from S. cordatum in subtropical areas of South Africa. This fungus is an opportunistic
pathogen with an extremely wide host range, including more than500 host plants, mostly in
tropical and subtropical regions (Punithalingam, 1976), and has previously been isolated
from exotic Acacia, Eucalyptus and Pinus spp. in South Africa (Crous et al., 2000; Burgess
et al., 2003). Lasiodiplodia theobromae was the most pathogenic species to the Eucalyptus
clone in this study. Although the two isolates of L. theobromae displayed di�erent levels of
pathogenicity, both were highly pathogenic. Lasiodiplodia theobromae might be considered a
potentially important pathogen of Eucalyptus in South Africa and studies to consider its
pathogenicity to di�erent species and hybrid clones would be warranted. Another
Lasiodiplodia species isolated from S. cordatum was recently described as L. gonubiensis
(Pavlic et al., 2004) and was isolated from a geographical region with a moderate climate
where L. theobromae was absent. Lasiodiplodia gonubiensis was only very mildly pathogenic
to the Eucalyptus clone, even though it is most closely related to the highly pathogenic L.
theobromae.
Os resultados deste estudo fornecem uma visão interessante sobre a diversidade de
Botryosphaeriaceae que ocorre em S. cordatum nativa na África do Sul. Alguns destes fungos
parecem ser patógenos potencialmente importantes de Eucalyptus spp. e inquéritos futuros
deverão reconhecer este facto. Claramente, estudos adicionais como o aqui apresentado,
considerando a patogenicidade destes fungos, serão necessários para melhor compreender
a sua importância. Este estudo enfatiza a ameaça de infecção cruzada de espécies de
Botryosphaeriaceae com Myrtaceae nativas e introduzidas. Num estudo recente, Burgess et
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al . (2006 ) mostraram que não há restrição ao movimento de N. australe entre eucaliptos
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Botryosphaeriaceae são, portanto, planeados para fornecer mais informações sobre o seu
movimento entre hospedeiros nativos e cultivados na África do Sul.
Reconhecimentos
Agradecemos à Fundação Nacional de Pesquisa (NRF), aos membros do Programa
Cooperativo de Proteção de Árvores (TPCP), à iniciativa THRIP do Departamento de
Comércio e Indústria e ao Departamento de Ciência e Tecnologia (DST)/Centro de Excelência
da NRF em Tree Health Biotechnology (CTHB), África do Sul pelo apoio �nanceiro.
Agradecemos também ao Dr. BE Eisenberg que forneceu as análises estatísticas.
Referências 
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