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Chilli anthracnose disease caused by Colletotrichum species

Article in Journal of Zhejiang University SCIENCE B · November 2008

DOI: 10.1631/jzus.B0860007 · Source: PubMed

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764 Than et al. / J Zhejiang Univ Sci B 2008 9(10):764-778

Journal of Zhejiang University SCIENCE B

ISSN 1673-1581 (Print); ISSN 1862-1783 (Online)
www.zju.edu.cn/jzus; www.springerlink.com
E-mail: [email protected]

Review:
Chilli anthracnose disease caused by Colletotrichum species

Po Po THAN1,2, Haryudian PRIHASTUTI3,4, Sitthisack PHOULIVONG3,5,6,

Paul W.J. TAYLOR2, Kevin D. HYDE†‡1,3
(1International Fungal Research and Development Centre, the Research Institute of Resources Insect,
Chinese Academy of Forestry, Kunming 650224, China)
(2BioMarka, School of Agriculture and Food Systems, University of Melbourne, Victoria 3010, Australia)
(3Fungal Research Group, School of Science, Mae Fah Luang University, Tasud, Chiang Rai 57100, Thailand)
(4Department of Biotechnology, Faculty of Agriculture, Brawijaya University, Malang 65145, Indonesia)
(5Mushroom Research Centre, 128 Moo 3 T. Pa Pae, A. Mae Taeng, Chiang Mai 50150, Thailand)
6
( Department of Plant Science, Faculty of Agriculture, National University of Laos, Vientiane, Lao PDR)
†
E-mail: [email protected]
Received Aug. 5, 2008; revision accepted Aug. 18, 2008

Abstract: Anthracnose disease is one of the major economic constraints to chilli production worldwide, especially in tropical
and subtropical regions. Accurate taxonomic information is necessary for effective disease control management. In the Colleto-
trichum patho-system, different Colletotrichum species can be associated with anthracnose of the same host. Little information is
known concerning the interactions of the species associated with the chilli anthracnose although several Colletotrichum species
have been reported as causal agents of chilli anthracnose disease worldwide. The ambiguous taxonomic status of Colletotrichum
species has resulted in inaccurate identification which may cause practical problems in plant breeding and disease management.
Although the management and control of anthracnose disease are still being extensively researched, commercial cultivars of
Capsicum annuum that are resistant to the pathogens that cause chilli anthracnose have not yet been developed. This paper reviews
the causal agents of chilli anthracnose, the disease cycle, conventional methods in identification of the pathogen and molecular
approaches that have been used for the identification of Colletotrichum species. Pathogenetic variation and population structure of
the causal agents of chilli anthracnose along with the current taxonomic status of Colletotrichum species are discussed. Future
developments leading to the disease management strategies are suggested.

Key words: Capsicum annuum, Disease management, Identification, Taxonomy, Pathogenicity

doi:10.1631/jzus.B0860007 Document code: A CLC number: S432

INTRODUCTION 2005). Typical anthracnose symptoms on chilli fruit

include sunken necrotic tissues, with concentric rings
Colletotrichum is one of the most important of acervuli. Fruits showing blemishes have reduced
plant pathogens worldwide causing the economically marketability (Manandhar et al., 1995).
important disease anthracnose in a wide range of In the Colletotrichum patho-system, different
hosts including cereals, legumes, vegetables, peren- Colletotrichum species can be associated with an-
nial crops and tree fruits (Bailey and Jeger, 1992). thracnose of the same host (Simmonds, 1965; Free-
Among these hosts, chilli (Capsicum spp.), an im- man et al., 1998; Cannon et al., 2000). Anthracnose
portant economic crop worldwide (Poulos, 1992), is of chilli has been shown to be caused by more than
severely infected by anthracnose which may cause one Colletotrichum species including C. acutatum
yield losses of up to 50% (Pakdeevaraporn et al., (Simmonds), C. capsici (Syd.) Butler and Bisby, C.
gloeosporioides (Penz.) Penz. and Sacc., and C. coc-
‡
Corresponding author codes (Wallr.) S. Hughes (Simmonds, 1965;
 Than et al. / J Zhejiang Univ Sci B 2008 9(10):764-778 765

Johnston and Jones, 1997; Kim et al., 1999; differences between the English-speaking countries)
Nirenberg et al., 2002; Voorrips et al., 2004; Sharma and type of fruits. The term “chilli” in most of the
et al., 2005; Pakdeevaraporn et al., 2005; Than et al., world refers exclusively to the smaller, hot types of
2008). Capsicum (Wikipedia, 2007).
There is little information concerning the inter- Capsicum contains approximately 20~27 species,
actions between the complexes of species involved in 5 of which are domesticated: C. annuum, C. baccatum,
chilli anthracnose (Than et al., 2008). This informa- C. chinense, C. frutescens, and C. pubescens, and are
tion is necessary for plant breeding purposes and cultivated in different parts of the world. Among the
disease management. Some Colletotrichum species five species of cultivated Capsicum, C. annuum is one
respond differently to various control measures, e.g., of the most common cultivated crops worldwide
C. acutatum was found to be moderately susceptible (Tong and Bosland, 1999) followed by C. frutescens
to the fungicide, benzimidazole, while C. gloeo- (Bosland and Votava, 2003).
sporioides was highly susceptible (Peres et al., 2004). Chilli has many culinary advantages. It com-
Correct and accurate identification will thus ulti- prises numerous chemicals including steam-volatile
mately lead to more effective disease control and oils, fatty oils, capsaicinoids, carotenoids, vitamins,
management, e.g., selecting appropriate fungicides, protein, fibre and mineral elements (Bosland and
or long lasting resistant cultivars (Whitelaw-Weckert Votava, 2003). Many chilli constituents are important
et al., 2007). for nutritional value, flavor, aroma, texture and color.
The current taxonomic status of Colletotrichum Chillies are low in sodium and cholesterol free, rich in
species is unclear (Sreenivasaprasad and Talhinhas, vitamins A and C, and are a good source of potassium,
2005). The broad host range of many species has folic acid and vitamin E. Fresh green chilli peppers
caused problems for plant pathologists who need to contain more vitamin C than citrus fruits and fresh red
identify specific plant pathogens to control disease. chilli has more vitamin A than carrots (Osuna-García
Molecular techniques have provided additional data et al., 1998; Marin et al., 2004). Two chemical groups
to aid the naming of fungi, and have been applied to produced by chilli are capsaicinoids and carotenoids.
taxonomically difficult genera including Fusarium The capsaicinoids are alkaloids that make hot chilli
(O′Donnell et al., 1998; Maxwell et al., 2005), pungent. A large number of carotenoids provide high
Pestalotiopsis (Jeewon et al., 2002; 2003; 2004; Lui nutritional value and the color to chilli (Britton and
et al., 2007), Mycosphaerella and its anamorphs Hornero-Méndez, 1997; Hornero-Méndez et al., 2002;
(Crous et al., 2000; Mancini et al., 2006), but to a Pérez-Gálvez et al., 2003).
lesser extent to Colletotrichum (Sreenivasaprasad et
al., 1996; Moriwaki et al., 2002; Photita et al., 2005;
Du et al., 2005). The management and control of CONSTRAINTS TO CHILLI PRODUCTION
anthracnose diseases are still being extensively re-
searched. This paper reviews the host ‘chilli’ as well Chilli is considered to be one of the most im-
as the causal agents of the chilli anthracnose, their portant crops in the tropics. The area cultivated with
pathogenic variability and approaches leading to the chilli worldwide is about 1 700 000 ha for producing
disease management. fresh chilli, and around 1 800 000 ha for producing
dried chilli; a total area of 3 729 900 ha with a total
production of 20 000 000 t (FAO, 2003). The most
HOST: CHILLI important producers and exporters of chilli include
China, India, Mexico, Morocco, Pakistan, Thailand
The genus Capsicum was originated in the and Turkey. Diseases caused by fungi, bacteria and
American tropics and has been propagated throughout viruses are the major constraints to chilli production.
the world including the tropics, subtropics, and also Anthracnose disease caused by Colletotrichum species,
temperate regions (Pickersgill, 1997). The fruit of bacterial wilt caused by Pseudomonas solanacearum,
Capsicum has a variety of names, such as ‘chilli’, and mosaic disease caused by chilli veinal mottle virus
‘chilli pepper’ or ‘pepper’ depending on place (i.e., (CVMV) or cucumber mosaic virus (CMV) are the
766 Than et al. / J Zhejiang Univ Sci B 2008 9(10):764-778

most serious destructive diseases of chilli (Isaac, conidial masses (Fig.1). Under severe disease pressure,
1992). lesions may coalesce. Conidial masses may also occur
Anthracnose disease caused by Colletotrichum scatteredly or in concentric rings on the lesions. Many
species is one of the most economically important studies have concluded that disease management
diseases reducing marketable yield from 10% to 80% practices are often inadequate to eliminate the diseases.
of the crop production in some developing countries, Breeding to develop the long-lasting resistant varieties
particularly in Thailand (Poonpolgul and Kumphai, has also not been successful due to involvement of
2007). Anthracnose is mainly a problem on mature multiple Colletotrichum species in anthracnose infec-
fruits, causing severe losses due to both pre- and tion.
post-harvest fruit decay (Hadden and Black, 1989;
Bosland and Votava, 2003).

ANTHRACNOSE DISEASE

Anthracnose, derived from a Greek word

meaning ‘coal’, is the common name for plant dis-
eases characterized by very dark, sunken lesions,
containing spores (Isaac, 1992). Generally, anthrac-
nose disease is caused by Colletotrichum species Fig.1 Anthracnose symptoms on chilli fruits
which belongs to the Kingdom Fungi; Phylum As-
comycota, Class Sordariomycetes; Order Phyllacho- Causal agents of chilli anthracnose
rales; and Family Phyllachoraceae. The anamorphs In the Colletotrichum patho-system, different
are Glomerella species. Anthracnose of chilli was Colletotrichum species can be associated with anthr-
first reported from New Jersey, USA, by Halsted acnose of the same host (Simmonds, 1965; Freeman
(1890) in 1890 who described the causal agents as et al., 1998; Cannon et al., 2000). Colletotrichum
Gloeopsorium piperatum and Colletotrichum nigrum. species causing anthracnose of chilli have been re-
These taxa were then considered as synonyms of C. ported from different countries and regions (Table 1).
gloeosporioides by von Arx (1957). Although these species have been the subject of nu-
Anthracnose causes extensive pre- and post- merous investigations, there remain many gaps in the
harvest damage to chilli fruits causing anthracnose knowledge of the disease process and understanding
lesions. Even small anthracnose lesions on chilli fruits of the complex relationships between the species
reduce their marketable value (Manandhar et al., involved. Kim et al.(2004) reported that different
1995). Many post-harvest diseases of fruit exhibit the species cause diseases of different organs of the chilli
phenomenon of quiescence in which symptoms do plant; for example, C. acutatum and C. gloeo-
not develop until the fruit ripens. Colletotrichum sporioides infect chilli fruits at all developmental
species are the most important pathogens that cause stages, but usually not the leaves or stems, which are
latent infection (Jeffries et al., 1990). Appressoria are mostly damaged by C. coccodes and C. dematium.
known to form adhesive disks that adhere to plant Leaf anthracnose of chilli seedlings caused by C.
surfaces and remain latent until physiological changes coccodes was first reported in chilli growing in a field
occur in fruits (Bailey and Jeger, 1992). Appressoria in Chungnam Province of Korea in 1988 (Hong and
that formed on immature fruits may remain quiescent Hwang, 1998). Different Colletotrichum species may
until ontogenic changes occur in the fruits (Prusky also play an important role in different diseases of
and Plumbley, 1992). Anthracnose disease can occur mature stages of chilli fruit as well. For example, C.
on leaves, stems, and both pre- and post-harvest fruits capsici is widespread in red chilli fruits, whereas C.
(Isaac, 1992). Typical fruit symptoms are circular or acutatum and C. gloeosporioides have been reported
angular sunken lesions, with concentric rings of to be more prevalent on both young and mature green
acervuli that are often wet and produce pink to orange fruits (Hong and Hwang, 1998; Kim et al., 1999).
 Than et al. / J Zhejiang Univ Sci B 2008 9(10):764-778 767

Table 1 Reported causal agents of chilli anthracnose

Countries and regions Causal agent Reference
Australia Colletotrichum acutatum, C. atramentarium, C. dematium, C. Simmonds, 1965
gloeosporioides var. minor, C. gloeosporioides var. gloeosporioides
India C. capsici Maiti and Sen, 1979;
Paul and Behl, 1990
Indonesia C. acutatum, C. capsici, C. gloeosporioides Voorrips et al., 2004
Korea C. acutatum, C. gloeosporioides, C. coccodes, C. dematium Park and Kim, 1992
Myanmar (Burma) Gloeosporium piperatum E. and E., C. nigrum E. and Hals Dastur, 1920
Papua New Guinea C. capsici, C. gloeosporioides Pearson et al., 1984
New Zealand C. coccodes Johnston and Jones, 1997
Taiwan C. acutatum, C. capsici, C. gloeosporioides Manandhar et al., 1995
Thailand C. acutatum, C. capsici, C. gloeosporioides Than et al., 2008
UK C. acutatum, Glomerella cingulata Adikaram et al., 1983
USA C. acutatum Roberts et al., 2001
Vietnam C. acutatum, C. capsici, C. gloeosporioides, C. nigrum Don et al., 2007

Anthracnose caused by C. coccodes does not result in allowing the disease to spread from plant to plant
severe epidemics on chilli fruits (Hong and Hwang, within the field (Roberts et al., 2001).
1998). C. gloeosporioides, the predominant species Initial infection by Colletotrichum species in-
on chilli in Korea, was differentiated into G and R volves a series of processes including the attachment
strains by isozyme analysis of esterase, leucine amino of conidia to plant surfaces, germination of conidia,
peptidase, phosphatase and glutamine oxalocetic production of adhesive appressoria, penetration of
trasminase (Park et al., 1987). plant epidermis, growth and colonization of plant
Colletotrichum species can survive in and on tissue and production of acervuli and sporulation
seeds as acervuli and micro-sclerotia (Pernezny et al., (Bailey and Jeger, 1992; Prusky et al., 2000). An-
2003). Survival of mycelia and stomata in colonized thracnose is mainly a problem on mature fruits,
chilli seeds had been reported (Manandhar et al., causing both pre- and post-harvest fruit decay re-
1995). It has been shown that the pathogen readily sulting severe economic losses (Hadden and Black,
colonizes the seed coat and peripheral layers of the 1989; Bosland and Votava, 2003). Appressoria that
endosperm even in moderately colonized seeds. formed on immature fruits may remain quiescent until
Heavily colonized seeds had abundant inter- and the fruits mature or ripen.
intracellular mycelia and acervuli in the seed coat
endosperm and embryo, showing disintegration of Disease cycle and epidemiology of anthracnose
parenchymatous layers of the seed coat and depletion Environmental factors play a major role in the
of food material in endosperm and embryo (Chitkara development of disease epidemics. The relationships
et al., 1990). among rainfall intensity, duration and crop geometry
Fungi can overwinter on alternative hosts such as and the dispersal of inoculum possibly lead to dif-
other solanaceous or legume crops, plant debris and ferent levels of disease severity (Dodd et al., 1992).
rotten fruits in the field (Pring et al., 1995). Colleto- The effects of temperature often interact with other
trichum species naturally produce micro-sclerotia to factors, such as leaf surface wetness, humidity, light
allow dormancy in the soil during the winter or when or competitive microbiota (Royle and Butler, 1986).
subjected to stressful conditions, and these mi- The duration of the surface wetness, however, ap-
cro-sclerotia can survive for many years (Pring et al., pears to have the most direct influence on the ger-
1995). During warm and wet periods, conidia from mination, infection and growth of the pathogen on the
acervuli and micro-sclerotia are splashed by rain or host. Generally infection occurs during warm, wet
irrigation water from diseased to healthy fruit and weather. Temperatures around 27 °C and high hu-
foliage. Diseased fruit acts as a source of inoculum, midity (a mean of 80%) are optimum for anthracnose
768 Than et al. / J Zhejiang Univ Sci B 2008 9(10):764-778

disease development (Roberts et al., 2001). appressoria (e.g., predominantly biotrophic disease
Colletotrichum species utilize diverse strategies cycle on citrus leaves).
for invading host tissues, which vary from intracel- (2) Subcuticular intramural necrotrophy with
lular hemibiotrophy to subcuticular intramural ne- hyphal development within periclinal and anticlinal
crotrophy (Bailey and Jeger, 1992). Colletotrichum walls of epidermal host cells which are swollen and
species produce a series of specialized infection wider apart (e.g., predominantly necrotrophic disease
structures such as germ tubes, appressoria, intracel- cycle on strawberry).
lular hyphae, and secondary necrotrophic hyphae (3) Hemibiotrophic interaction with infection
(Perfect et al., 1999). These pathogens infect plants vesicles and broad primary hyphae within host cells.
by either colonizing subcuticular tissues intramurally Inter- and intracellular hyphal growth could be seen
or being established intracellularly. The preinfection as the subsequent necrotrophic phase (e.g., combina-
stages of the both are very similar, in which conidia tion of biotrophy and necrotrophy but mostly a
adhere to and germinate on the plant surface, pro- biotrophic disease cycle on blueberry fruits).
ducing germ tubes that form appressoria which in turn (4) Hemibiotrophic and subcuticular, intra- and
penetrate the cuticle directly (Bailey and Jeger, 1992). intercellular development of C. acutatum (e.g., com-
Following penetration, the pathogens that colonize bination of biotrophy and necrotrophy but mostly a
the intramural region beneath the cuticle invade in a necrotrophic disease cycle on almond leaves and
necrotrophic manner and spread rapidly throughout fruits).
the tissues (O′Connell et al., 1985). There is no de- There are only a few detailed studies on pene-
tectable biotrophic stage in this form of parasitism. In tration and colonization by Colletotrichum species on
contrast, most anthracnose pathogens exhibit a chilli. Kim et al.(2004) noticed that there was no
biotropic infection strategy initially by colonizing the biotrophic infection vesicle found during the infec-
plasmalemma and cell wall intracellularly. After the tion process of C. gloeosporioides in susceptible
biotrophic state, intracellular hyphae colonize one or chilli (C. annuum cv. jejujaerae). Epidermal cyto-
two cells and subsequently produce secondary ne- plasm became condensed and small vacuoles in-
crotrophic hyphae (Bailey and Jeger, 1992). These creased and cell destruction extended to the subepi-
pathogens are therefore regarded as hemibiotrophs or dermal cells of the plant, which are likely to be
facultative biotrophs (Kim et al., 2004). For example, damaged by the pathogen enzymes. At later stages of
C. gloeosporioides on avocado, chilli and citrus can infection, tissues were colonized inter- and intracel-
produce both types of colonizations: intracellular lularly by the pathogen. This structural feature indi-
biotrophy at an early stage and intramural necrotro- cated that the infection was governed by necrotrophic
phy later (O′Connell et al., 2000). fungal growth.
Although the mechanisms developed by Colle- Colletotrichum species are generally able to
totrichum species appear similar in prepenetration survive in or on seeds and one of the ways that an-
events, there are differences between species in the thracnose is introduced to the chilli field is through
later mechanisms such as spore adhesion, melaniza- infected transplants (Manandhar et al., 1995). C.
tion and cutinization in penetration of the plant cuticle capsici infection of chilli was shown to have two
by the appressoria. For example, the host-pathogen pathways: invasion through the seed coat and inva-
interaction of C. acutatum appears to be more sion through the openings of the testa (Jewsakun,
biotrophic than that of some other species such as C. 1978). Jewsakun (1978) mentioned that C. capsici
gloeosporioides (Wharton and Diéguez-Uribeondo, caused root rot of seedlings; however, whether chilli
2004). Based on studies with C. acutatum on specific anthracnose can be seed-transmitted, and the role of
hosts, four types of interactions or infection strategies seed infection and seedling infection in pre- and post-
were described by Peres et al.(2005) as follows: emergence damage of chilli plants are still question-
(1) Biotrophic growth of C. acutatum with sec- able. We have found that C. acutatum can infect chilli
ondary conidiation in which conidia germinate to seeds either by reducing the germination rates or by
form appressoria and quiescent infections, and sec- causing damping off of seedlings. However, very
ondary conidia are formed after germination of the little is known about the disease cycle of the patho-
 Than et al. / J Zhejiang Univ Sci B 2008 9(10):764-778 769

gens that cause anthracnose in chilli. There are still environmental factors. Most fungal phylogenetic
several questions to be answered. studies utilized sequences from the ribosomal gene
cluster, since they were present in large numbers as
tandem repeats and evolved as a single unit (Mitchell
IDENTIFICATION OF COLLETOTRICHUM SPE- et al., 1995). In particular, sequence analysis of the
CIES internal transcribed spacer (ITS) regions which lie
between the 18S and 5.8S genes and the 5.8S and 28S
Conventional methods genes, has proved useful in studying phylogenetic
Accurate identification of Colletotrichum species relationships of Colletotrichum species because of
along with the knowledge of populations responsible their comparative variability (Sreenivasaprasad et al.,
for epidemics are essential for developing and im- 1994; 1996; Moriwaki et al., 2002; Photita et al.,
plementing effective disease control strategies 2005). Apart from ITS region, sequence analysis of
(Freeman et al., 1998). Traditionally, identification protein coding genes such as partial β-tubulin gene,
and characterization of Colletotrichum species have has also been applied to resolve phylogenetic rela-
been based on morphological characters, such as size tionships among C. acutatum species complexes
and shape of conidia and appressoria; existence of (Sreenivasaprasad and Talhinhas, 2005). Sequences
setae; the teleomorph state and cultural characters of introns from two genes (glutamine synthase and
such as colony colour, growth rate and texture (von glyceraldehyde-3-phosphate dehydrogenase) were
Arx, 1957; Smith and Black, 1990). These criteria also used to evaluate a diverse collection of isolates of
alone, however, are not always adequate for species C. acutatum (Guerber et al., 2003). C. acutatum iso-
identification due to overlap in morphological char- lates clustered into groups (Guerber et al., 2003;
acters and phenotypic variation among species under MacKenzie et al., 2008; Peres et al., 2008). These
different environmental conditions. Conidial shape groups might represent phylogenetically distinct
has been applied as a reliable means of discriminating species of C. acutatum sensu lato (Guerber et al.,
certain species; for example, conidial shape has dif- 2003). Yun et al.(1999) stated that, because of the
ferentiated Colletotrichum species pathogenic to high intra-species variability and the low inter-species
strawberry (Denoyes and Baudry, 1995). However, in variability, MAT1-2 mating type sequences gave
other cases, identification can be complicated because strong support for branches, allowing differentiation
of overlapping ranges of conidial morphology and of closely related Cochliobolus spp. whose relation-
variation in colony characteristics (Adaskaveg and ships were not resolved by ITS sequences alone.
Hartin, 1997). Correct taxonomic identification is Consequently, Du et al.(2005) confirmed that
important in disease management such as choosing MAT1-2 mating type was useful in differentiating the
appropriate fungicides (Whitelaw-Weckert et al., groups of isolates from the species complexes (C.
2007). For instance, it could be seen in different re- graminicola, C. gloeosporioides and C. acutatum).
sponses of C. acutatum and C. gloeosporioides to However, there is no report concerning the use of
benzimidazole-based fungicides (Peres et al., 2004). these genes to differentiate between the Colleto-
trichum species involved in chilli anthracnose.
Molecular genetics approach A combined application of molecular diagnostic
To overcome the inadequacies of traditional tools along with traditional morphological charac-
morphology based identification schemes, DNA se- terization is an appropriate and reliable approach for
quence analyses have been used to characterize and studying Colletotrichum species complexes (Cannon
analyze the taxonomic complexity of Colletotrichum et al., 2000). Than et al.(2008) differentiated isolates
(Sreenivasaprasad et al., 1996; Moriwaki et al., 2002; of chilli anthracnose from Thailand into three species:
Du et al., 2005; Photita et al., 2005; Than et al., 2008). C. acutatum, C. capsici and C. gloeosporioides, based
Cannon et al.(2000) stated that data derived from on morphological characterization, sequencing based
nucleic acid analyses should provide the most reliable on rDNA-ITS region and partial beta tubulin gene and
framework to build a classification of Colletotrichum, pathogenicity testing. Hong and Kim (2007) reported
as DNA characters were not directly influenced by that Korea isolates of C. acutatum were phyloge-
770 Than et al. / J Zhejiang Univ Sci B 2008 9(10):764-778

netically separated from the global groups of C. the pathogen population is therefore a prerequisite for
acutatum A1 to A8 based on the sequences in partial accurate assessment of durable resistant germplasm in
beta-tubulin 2 (exons 3-6). Restriction fragment breeding programs (Abang, 2003). Taylor and Ford
length polymorphisms (RFLP) of ITS region resulting (2007) suggested that knowledge of pathotype diver-
from AluI, RsaI and BamHI digestions have also been sity is important when choosing the appropriate iso-
employed to differentiate Colletotrichum species lates to screen for resistance in plant breeding pro-
from chilli anthracnose in Taiwan region (Sheu et al., grams.
2007). Four species of Colletotrichum were identified We have studied pathogenic variation among 10
by ITS-RFLP fingerprinting and observation of un- isolates of C. acutatum against 7 cultivars including
distinguishable isolates of Colletotrichum from their reportedly susceptible species of Capsicum (Capsi-
studies indicated the various inter- and intra-species cum annuum ‘Bangchang’) (Mongkolporn et al.,
variations in Colletotrichum species. Ratanacherdchai 2004a) and resistant species such as Capsicum
et al.(2007) distinguished C. capsici and C. gloeo- chinense ‘PBC 932’ (AVRDC, 1999; 2003; Mong-
sporioides causing chilli anthracnose in Thailand kolporn et al., 2004a), Capsicum baccatum ‘PBC 80’
using random amplified polymorphic DNA (RAPD) and ‘PBC 81’ in Thailand. This revealed two patho-
markers. types based on qualitative differences in infection of a
reported resistant genotype, C. baccatum genotype
‘PBC 81’. Interestingly, of 10 isolates assayed, the
PATHOGENIC VARIABILITY OF COLLETO- genotype showed complete resistance against 5 iso-
TRICHUM SPECIES lates tested, whereas it showed a highly susceptible
reaction to the other 5 isolates tested. Sharma et
When any of the progeny exhibits a characteris- al.(2005) studied the pathogenic variability in C.
tic that is different from those present in the ancestral capsici in India and proposed that 15 pathotypes of C.
individuals or descent individuals, this individual is capsici existed among 37 isolates from different chilli
called a variant (Agrios, 2005). This may involve a growing regions from Himachal Pradesh in India.
change in any conceivable biological characteristic, However, these pathotype differences were based on
such as color, shape, growth rate and reproduction quantitative differences in host reaction, i.e., level of
rate. In the case of pathogens, changes in host range aggressiveness.
may occur, i.e., it may be able to infect a variety of the Taylor et al.(2007) defined the pathotype as “a
host plant or cultivar not previously infected by the subclass or group of isolates distinguishable from
ancestor, or in virulence, i.e., it may produce a milder others of the same species by its virulence on a spe-
or much more severe disease than the ancestors cific host (genotype), i.e., a qualitative difference in
(Agrios, 2005). This is the way that resistance of a disease severity” and the aggressiveness as “the
plant variety is ‘broken down’ (Agrios, 2005). The natural variation in virulence or level of disease
spread of a resistant genotype capable of escaping a (measured quantitatively) within the pathogen popu-
current prevalent pathogen will be challenged by a lation.” According to Taylor and Ford (2007), there
new parasitic strain that harbors a virulent gene which might be confusion as to whether true pathotype dif-
is capable of overcoming that resistance (McDonald ferences exist, or whether the differences observed in
and Linde, 2002). Compatibility of plant-pathogen disease severity are a measure of the natural distribu-
interactions is often governed by the gene-for-gene tion of aggressiveness within a population, ranging
model in many pathosystems (Flor, 1971). This sug- from low to high. However, the level of aggressive-
gests a continuous co-evolutionary change in both ness of isolates is also an important consideration in
host and parasite. resistance breeding programmes and disease control
Some pathogen populations are known to be management. Genotypes with partial resistance
pathogenitically diverse, and the diversity seems to be would result in lower level of infection which even-
due to continuous generation of novel pathogenic tually will decrease the inoculum amount in the field
variations (Taylor and Ford, 2007). Information on to limit the potential of epidemics.
pathogen diversity and the geographic distribution of Several studies (AVRDC, 1999; Yoon et al.,
 Than et al. / J Zhejiang Univ Sci B 2008 9(10):764-778 771

2004) have screened C. acutatum, which is the very In general, organisms reproduce by means of a
virulent species (Than et al., 2008), against chilli sexual process. Variation in progeny is introduced
genotypes and found that Capsicum baccatum geno- primarily through segregation and recombination of
type ‘PBC 80’ is a genetic resource pool for resistance genes in meiotic division of the zygote (Agrios, 2005).
to anthracnose. We have also confirmed this. This However, in the case of anamorphic fungi such as
genotype is assumed to be useful for studying genet- Colletotrichum, reproduction is mainly or exclusively
ics of resistance and practical breeding in chilli pep- vegetative (Katan, 2000). Parasexual reproduction, by
per. However, we found that another genotype of C. which a system of genetic recombination can occur
baccatum, ‘PBC 81’, showed high susceptibility to within fungal heterokaryon, will likely lead to varia-
some C. acutatum isolates. This would make it ques- tion. The new variants come into existence, which
tionable as to whether C. baccatum species are a may be identical in appearance to that of the ancestral
useful genetic resource pool for breeding for resis- types, but behave differently as far as disease pro-
tance to anthracnose. duction is concerned (Agrios, 2005).
In contrast to C. baccatum, susceptibility of the In recent decades, molecular markers have been
C. annuum cultivars has been reported in several widely used to measure the variation in a pathogen
studies (Mongkolporn et al., 2004b; Park, 2007). In population. Random amplified polymorphic DNA
addition, Capsicum chinense ‘PBC 932’ has been (RAPD), simple sequence repeat (microsatellite), inter
reported as a resistant variety to Colletotrichum cap- simple sequence repeat (ISSR), amplified fragment
sici and hence has been introgressed with C. annuum length polymorphism (AFLP), and genomic DNA
‘Bangchang’ to produce F1 progeny (AVRDC, 2003). RFLP, are among the most frequently used neutral
However, Yoon et al.(2004) and Than et al.(2008) genetic markers in population genetic studies (Brown
found that the ‘PBC 932’ was highly susceptible to C. et al., 1996; Milgroom, 1996; McDonald, 1997).
acutatum isolates. Nevertheless, this information Despite its importance, there have only been a
about highly susceptible reaction of ‘PBC 932’ will few studies concerning the diversity of Colleto-
help chilli breeders to be aware of the potential for trichum species associated with chilli anthracnose.
breaking down its resistance to C. acutatum. Sharma et al.(2005) found a variable population of C.
capsici causing fruit rot/die back or anthracnose of
chilli in the northwestern region of India based on
POPULATION STRUCTURE AND MOLECULAR differential inoculation tests and RAPD analysis. In
MARKER TECHNIQUES contrast, examination of C. acutatum from a limited
collection of isolates from chilli anthracnose epi-
The genetic structure of plant pathogen popula- demics in Brazil, Korea, Taiwan region and the US
tions, the potential for gene flow and long distance indicated that they belonged to a single group based
dispersal, and the relative contribution of sexual and on mtDNA-RFLP analysis (Correll et al., 2007). They
asexual reproduction have direct inference with ag- also found that most isolates (36 out of 43) examined
ricultural ecosystems (McDonald and McDermott, from the various countries and regions belonged to a
1993; McDonald, 1997). Abang (2003) stated that single vegetative compatibility group (VCG). As the
genetic population structure refers to the amount and sexual stages of C. acutatum have never been found in
distribution of genetic variation within and between nature (Wharton and Diéguez-Uribeondo, 2004), the
populations. For example, how rapidly a pathogen asexual reproduction mode of C. acutatum is likely to
can evolve could be indicated by the amount of ge- be an important role in its population structure.
netic variation maintained within a population and
then which may eventually be used to predict how
long a control measure is probable to be effective DISEASE MANAGEMENT OF CHILLI AN-
(McDonald and Linde, 2002). Pathogens with large THRACNOSE
genetic variations are assumed to adapt faster to
fluctuating environments (e.g., resistant genes and Bailey (1987) and Agrios (2005) recommended
fungicides). integrated management techniques, as no single spe-
772 Than et al. / J Zhejiang Univ Sci B 2008 9(10):764-778

cific management program could eliminate chilli thracnose resistant C. chinense ‘CM 021’. The ge-
anthracnose. Effective control of Colletotrichum netic purity of the F1 was proven by using molecular
diseases usually involves the use of a combination of marker analysis. Recently, Voorrips et al.(2004) have
cultural control, biological control, chemical control found one main quantitative trait locus (QTL) with
and intrinsic resistance (Wharton and Diéguez- high significance and large effects on resistance and
Uribeondo, 2004). three other QTLs with smaller effects on the F2
population (cross between C. annuum and C.
Cultural practices chinense) on the traits they tested, such as infection
Pathogen-free chilli seed should be planted and frequency, the true lesion diameter and overall lesion
weeds eliminated. Crops should be rotated every 2~3 diameter after inoculation with C. gloeosporioides in
years with crops that are not alternative hosts of the study of resistance to anthracnose disease in In-
Colletotrichum. Transplants should be kept clean by donesia.
controlling weeds and solanaceous volunteers around
the transplant houses. The field should have good Use of chemicals
drainage and be free from infected plant debris. If Chemicals are the most common and practical
disease was previously present, crops should be ro- method to control anthracnose diseases. However,
tated away from solanaceous plants for at least 2 years fungicide tolerance often arises quickly, if a single
(Roberts et al., 2001). Sanitation practices in the field compound is relied upon too heavily (Staub, 1991).
include control of weeds and volunteer chilli plants. The fungicide traditionally recommended for an-
Choosing cultivars that bear fruit with a shorter rip- thracnose management in chilli is Manganese ethyl-
ening period may allow the fruit to escape infection enebisdithiocarbamate (Maneb) (Smith, 2000), al-
by the fungus. Wounds in fruit from insects or other though it does not consistently control the severe form
means should be reduced to the extent possibly be- of anthracnose on chilli fruit. The strobilurin fungi-
cause wounds provide entry points for Colletotrichum cides azoxystrobin (Quadris), trifloxystrobin (Flint),
spp. and other pathogens such as bacteria that cause and pyraclostrobin (Cabrio) have recently been la-
soft rot. At the end of the season, infected plant debris beled for the control of anthracnose of chilli, but only
from the field must be removed or deep ploughed to preliminary reports are available on the efficacy of
completely cover crop diseases (Agrios, 2005). these fungicides against the severe form of the disease
(Alexander and Waldenmaier, 2002; Lewis and
Use of resistant cultivars Miller, 2003). The disease can be controlled under
The use of resistant varieties not only eliminated normal weather conditions with a reasonable spray
losses from diseases, but also eliminated chemical program. However, there are numerous reports of
and mechanical expenses of disease control (Agrios, negative effects of using chemicals on farmers’ in-
2005). Some genetic resources resistant to anthrac- come and health, and toxic contamination to the en-
nose in chilli have been independently reported from vironment, particularly in developing countries
different countries and regions (Kim W.G. et al., 1986; (Voorrips et al., 2004).
Kim B.S. et al., 1987; Park et al., 1987; Hong and
Hwang, 1998; Pae et al., 1998; AVRDC, 1999; Yoon Use of biofungicides
and Park, 2001). In particular, some lines of C. bac- The control of chilli anthracnose fruit rot has, for
catum show strong resistance to the pathogen, and many years, relied on chemicals and resulted in many
pathogen inoculation resulted in no or limited lesions undesirable problems. There is a need to incorporate
on the chilli fruits (Yoon, 2003). However, to date, no alternative control components that are effective in
strong resistance has been found in Capsicum an- field. Biological control of fruit rot and dieback of
nuum, which is the only species grown worldwide chilli with plant products tested in many laboratories
(Park, 2007). Mongkolporn et al.(2004a) carried out a and field trials showed that the crude extract from
genetic study of anthracnose resistance to C. capsici, rhizome, leaves and creeping branches of sweetflag
which was expressed in the interspecific cross of Thai (Acorus calamus L.), palmorosa (Cymbopogon mar-
susceptible C. annuum cv. ‘Bangchang’ and an- tinii) oil, Ocimum sanctum leaf extract, and neem
 Than et al. / J Zhejiang Univ Sci B 2008 9(10):764-778 773

(Azadirachia indica) oil could restrict growth of the management of disease through breeding of patho-
anthracnose fungus (Jeyalakshmi and Seetharaman, gen-resistant cultivars has only had limited success
1998; Korpraditskul et al., 1999). Among the bio- due to frequent breakdown of resistance under field
fungicides used against the fungus Colletotrichum conditions. Commercial cultivars of Capsicum an-
spp. on chilli fruit, Charigkapakorn (2000) found that nuum resistant to the pathogens that cause anthrac-
the most effective control was sweetflag crude extract nose have not yet been developed (Park, 2007).
when applied in two intervals when the majority of Nevertheless, high levels of resistance to the Colle-
the plants were at the first bloom stage and at the totrichum species that infect chilli have been found in
mature bloom stage. some species of Capsicum, for instance, C. baccatum.
Current research is focusing on introgression of this
Biological control resistance into susceptible commercial cultivars of C.
So far, biological control methods for chilli an- annuum (AVRDC, 2003; Pakdeevaraporn et al.,
thracnose disease have not received much attention. 2005). Recently in Thailand, Mongkolporn et
The potential for biological control of Colletotrichum al.(2004a) have studied the inheritance of resistance
species had been suggested as early as in 1976 by to anthracnose specifically caused by Colletotrichum
Lenné and Parbery (1976). Jeger and Jeffries (1988) capsici, in a Capsicum annuum population estab-
also stressed the possibilities of biological control of lished from a cross between accession ‘83-168’ and
post-harvest fruit diseases by using Pseudomonas cv. ‘KKU-Cluster’, and their progenies. They ob-
fluorescens. Antagonistic bacterial strains (DGg13 served a promising dominant gene responsible for the
and BB133) were found to effectively control C. resistance to C. capsici. Voorrips et al.(2004) found
capsici, the major anthracnose pathogen in Thailand one main QTL with high significance and strong
(Intanoo and Chamswarng, 2007). It is also believed resistance against C. gloeosporioides associated with
that Trichoderma species are able to effectively chilli anthracnose disease in Indonesia.
compete for surface area, thereby reducing pathogen Although there are currently extensive research
infection success (Jeffries and Koomen, 1992; on disease control management including breeding
Maymon et al., 2004). Trichoderma species have programs for resistant cultivars to anthracnose, the
been applied to control Colletotrichum species in current status of the chilli anthracnose disease still
chilli (Boonratkwang et al., 2007), strawberries requires improvement. There remain many questions
(Freeman et al., 2001), and citrus in Belize (Moretto to be answered concerning characterization of Col-
et al., 2001) with concomitant disease reduction. letotrichum species associated with anthracnose; in
Other biological control agents that have been tested particular species present in different countries and
for efficacy against C. acutatum include Bacillus regions; pathogenetic or genetic diversity of Colleto-
subtilis and Candida oleophila (Wharton and trichum species worldwide; infection processes and
Diéguez-Uribeondo, 2004). the disease cycle of Colletotrichum species leading to
effective disease control and resistant plant breeding.

ASPECTS TO CURRENT STATUS OF CHILLI References

ANTHRACNOSE DISEASE MANAGEMENT Abang, M.M., 2003. Genetic diversity of Colletotrichum
gloeosporioides Penz. causing anthracnose disease of
yam (Dioscorea spp.) in Nigeria. Bibliotheca Mycologia,
Management and control of the anthracnose 197:20-33.
disease are still under extensive research (Yoon et al., Adaskaveg, J.E., Hartin, R.J., 1997. Characterization of Col-
2004). Among disease control management, the use letotrichum acutatum isolates causing anthracnose of
of resistant cultivars is the cheapest, easiest, safest almond and peach in California. Phytopathology, 87(9):
and most effective means of controlling the disease. 979-987. [doi:10.1094/PHYTO.1997.87.9.979]
Adikaram, N.K.B., Brown, A., Swinburne, T.R., 1983. Ob-
This is not only to eliminate losses from the disease
servations on infection of Capsicum annuum fruit by
but also decrease the cost of chemical and mechanical Glomerella cingulata and Colletotrichum capsici.
control, as well as reduce contamination of the envi- Transactions of the British Mycological Society, 80:
ronment from the use of toxic chemicals. However, 395-401.
774 Than et al. / J Zhejiang Univ Sci B 2008 9(10):764-778

Agrios, G.N., 2005. Plant Pathology, 5th Ed. Academic Press, the First International Symposium on Chilli Anthracnose.
San Diego, p.922. National Horticultural Research Institute, Rural Devel-
Alexander, S.A., Waldenmaier, C.M., 2002. Management of opment of Administration, Republic of Korea, p.20.
Anthracnose in Bell Pepper. Fungicide and Nematicide Crous, P.W., Aptroot, A., Kang, J.C., Braun, U., Wingfield,
Tests [Online]. New Fungicide and Nematicide Data M.J., 2000. The genus Mycoshaerella and its anamorphs.
Committee of the American Phytopathological Society. Studies in Mycology, 45:107-121.
Vol. 58, p.49. Available from http://apsjournals.apsnet. Dastur, J.F., 1920. Glomerella cingulata (Stoneman) Spald
org/doi/abs/10.1094/PDIS.2004.88.11.1198 (Accessed and its conidial form, Gloesporium piperatum E. and E.
25/12/2007). [doi:10.1094/FN58] and Colletotrichum nigrum E. and Hals. on chillies and
AVRDC (Asian Vegetable Research and Development Centre), Carica papaya. Annals of Applied Biology, 6(4):245-268.
1999. Off-Season Tomato, Pepper, and Eggplant. Pro- [doi:10.1111/j.1744-7348.1920.tb06472.x]
gress Report for 1998. Asian Vegetable Research and Denoyes, B., Baudry, A., 1995. Species identification an
Development Centre, Taiwan, China. pathogenicity study of French Colletotrichum strains
AVRDC (Asian Vegetable Research and Development Centre), isolated from strawberry using morphological and cul-
2003. AVRDC Progress Report for 2002. Asian Vegetable tural characteristics. Phytopathology, 85(1):53-57.
Research and Development Centre, Taiwan, China. [doi:10.1094/Phyto-85-53]
Bailey, J.A., 1987. Phytoalexins: A Genetic View of Their Dodd, J.C., Estrada, A., Jeger, M.J., 1992. Epidemiology of
Significance. In: Day, P.R., Jellis, G.J. (Eds.), Genetics Colletotrichum Gloeosporioides in the Tropics. In: Bailey,
J.A., Jeger, M.J. (Eds.), Colletotrichum: Biology, Pa-
and Plant Pathogenesis. Blackwell, Oxford, p.13-26.
thology and Control. CAB International, Wallingford,
Bailey, J.A., Jeger, M.J. (Eds.), 1992. Colletotrichum: Biology,
p.308-325.
Pathology and Control. Commonwealth Mycological In-
Don, L.D., Van, T.T., Phuong Vy, T.T., Kieu, P.T.M., 2007.
stitute, Wallingford, p.388.
Colletotrichum spp. Attacking on Chilli Pepper Growing
Boonratkwang, C., Chamswarng, C., Intanoo, W., Juntharasri, in Vietnam. Country Report. In: Oh, D.G., Kim, K.T.
V., 2007. Effect of Secondary Metabolites from Tricho- (Eds.), Abstracts of the First International Symposium on
derma Harzianum Strain Pm9 on Growth Inhibition of Chilli Anthracnose. National Horticultural Research In-
Colletotrichum Gloeosporioides and Chilli Anthracnose stitute, Rural Development of Administration, Republic
Control. Proceeding of the 8th National Plant Protection of Korea, p.24.
Conference. Naresuan University, Phisanulok, Thailand, Du, M., Schardl, C.L., Vaillancourt, L.J., 2005. Using mat-
p.323-336. ing-type gene sequences for improved phylogenetic reso-
Bosland, P.W., Votava, E.J., 2003. Peppers: Vegetable and lution of Colletotrichum species complexes. Mycologia,
Spice Capsicums. CAB International, England, p.233. 97(3):641-658. [doi:10.3852/mycologia.97.3.641]
Britton, G., Hornero-Méndez, D., 1997. Carotenoids and FAO (Food and Agriculture Organization of the United Na-
Colour in Fruits and Vegetables. In: Tomás-Barberán, tions), 2003. FAO Production Yearbook 2001. FAO,
F.A., Robins, R.J. (Eds.), Photochemistry of Fruits and Rome, 55(170):333.
Vegetables. Clarendon Press, Oxford, England, p.11-28. Flor, H.H., 1971. Current status for the gene-for-gene concept.
Brown, A.E., Sreenivasaprasad, S., Timmer, L.W., 1996. Annual Reviews of Phytopathology, 9:275-296.
Molecular characterization of slow-growing orange and Freeman, S., Katan, T., Shabi, E., 1998. Characterization of
key lime anthracnose strains of Colletotrichum from cit- Colletotrichum species responsible for anthracnose dis-
eases of various fruits. Plant Disease, 82(6):596-605.
rus as C. acutatum. Phytopathology, 86(5):523-527.
[doi:10.1094/PDIS.1998.82.6.596]
[doi:10.1094/Phyto-86-523]
Freeman, S., Minz, D., Maymon, M., Zveibil, A., 2001. Ge-
Cannon, P.F., Bridge, P.D., Monte, E., 2000. Linking the Past,
netic diversity within Colletotrichum acutatum sensu
Present, and Future of Colletotrichum Systematics. In:
Simmonds. Phytopathology, 91(6):586-592. [doi:10.1094/
Prusky, D., Freeman, S., Dickman, M. (Eds.), Colleto-
PHYTO.2001.91.6.586]
trichum: Host specificity, Pathology, and Host-pathogen Guerber, J.C., Liu, B., Correll, J.C., Johnston, P.R., 2003.
Interaction. APS Press, St. Paul, Minnesota, p.1-20. Characterization of diversity in Colletotrichum acutatum
Charigkapakorn, N., 2000. Control of Chilli Anthracnose by sensu lato by sequence analysis of two gene introns,
Different Biofungicides. Thailand. Available from http:// mtDNA and intron RFLPs and mating compatibility.
www.arc-avrdc.org/pdf_files/029-Charigkapakorn_18th. Mycologia, 95(5):872-895. [doi:10.2307/3762016]
pdf (Accessed 24/06/2008). Hadden, J.F., Black, L.L., 1989. Anthracnose of Pepper
Chitkara, S., Singh, T., Singh, D., 1990. Histopathology of Caused by Colletotrichum spp. Proceeding of the Inter-
Colletotrichum dematium infected chilli seeds. Acta national Symposium on Integrated Management Practices:
Botanica Indica, 18:226-230. Tomato and Pepper Production in the Tropics. Asian
Correll, C.J., Cornelius, K., Feng, C., Ware, S.B., Gabor, B., Vegetable Research and Development Centre, Taiwan,
Harp, T.L., 2007. Overview of the Phylogenetics Species p.189-199.
Concept in Colletotrichum as it Relates to Chilli An- Halsted, B.D., 1890. A new anthracnose of pepper. Bulletin of
thracnose. In: Oh, D.G., Kim, K.T. (Eds.), Abstracts of the Torrey Botanical. Club., 18:14-15.
 Than et al. / J Zhejiang Univ Sci B 2008 9(10):764-778 775

Hong, J.K., Hwang, B.K., 1998. Influence of inoculum density, Johnston, P.R., Jones, D., 1997. Relationships among Colleto-
wetness duration, plant age, inoculation method, and trichum isolates from fruit-rots assessed using rDNA se-
cultivar resistance on infection of pepper plants by Col- quences. Mycologia, 89(3):420-430. [doi:10.2307/37610
letotrichum cocodes. Plant Disease, 82(10):1079-1083. 36]
[doi:10.1094/PDIS.1998.82.10.1079] Katan, T., 2000. Vegetative Compatibility in Colletotrichum.
Hong, J.K., Kim, D.H., 2007. Taxonomic Characteristics of In: Prusky, D., Freeman, S., Dickman, M. (Eds.), Colle-
Colletotrichum spp. and their Teleomorphs Causing An- totrichum: Host Specificity, Pathology, and Host-
thracnose of Chilli Pepper. In: Oh, D.G., Kim, K.T. (Eds.), pathogen Interaction. APS Press, St. Paul, Minnesota,
Abstracts of the First International Symposium on Chilli p.45-55.
Anthracnose. National Horticultural Research Institute, Kim, B.S., Park, K.S., Lee, W.S., 1987. Search for resistance
Rural Development of Administration, Republic of Korea, to two Colletotrichum species in pepper (Capsicum spp.).
p.31. Journal of Korean Society and Horticultural Science,
Hornero-Méndez, D., Costa-García, J., Mínguez-Mosquera, 28:207-213.
M.I., 2002. Characterization of carotenoids high-producing Kim, K.D., Oh, B.J., Yang, J., 1999. Differential interactions
Capsicum annuum cultivars selected for paprika produc- of a Colletotrichum gloeosporioides isolate with green
tion. Journal of Agricultural and Food Chemistry, 50(20): and red pepper fruits. Phytoparasitica, 27:1-10.
5711-5716. [doi:10.1021/jf0256236] Kim, K.K., Yoon, J.B., Park, H.G., Park, E.W., Kim, Y.H.,
Intanoo, W., Chamswarng, C., 2007. Effect of Antagonistic 2004. Structural modifications and programmed cell
Bacterial Formulations for Control of Anthracnose on death of chilli pepper fruits related to resistance responses
Chilli Fruits. Proceeding of the 8th National Plant Pro- to Colletotrichum gloeosporioides infection. Genetics
tection Conference. Naresuan University, Phisanulok, and Resistance, 94:1295-1304.
Thailand, p.309-322. Kim, W.G., Cho, E.J., Lee, E.J., 1986. Two strains of Colle-
Isaac, S., 1992. Fungal Plant Interaction. Chapman and Hall totrichum gloeosporioides Penz. causing anthracnose of
Press, London, p.115. pepper fruits. Korean Journal of Plant Pathology,
Jeewon, R., Liew, E.C.Y., Hyde, K.D., 2002. Phylogenetic 2:107-113.
relationships of Pestalotiopsis and allied genera inferred Korpraditskul, V., Rattanakreetakul, C., Korpraditskul, R.,
from ribosomal DNA sequences and morphological Pasabutra, T., 1999. Development of Plant Active Sub-
characters. Molecular Phylogenetics and Evolution, 25(3): stances from Sweetflag to Control Fruit Rot of Mango for
378-392. [doi:10.1016/S1055-7903(02)00422-0] Export. In: Proceeding of Kasetsart University Annual
Jeewon, R., Liew, E.C.Y., Simpson, J.A., Hodgkiss, I.J., Hyde, Conference. Kasetsart University, Bangkok, p.34.
K.D., 2003. Phylogenetic significance of morphological Lenné, J.M., Parbery, D.G., 1976. Phyllosphere antagonists
characters in the taxonomy of Pestalotiopsis species. and appressoria formation in Colletotrichum gloeo-
Molecular Phylogenetics and Evolution, 27(3):372-383. sporioides. Transactions of the British Mycological So-
[doi:10.1016/S1055-7903(03)00010-1] ciety, 66:334-336.
Jeewon, R., Liew, E.C.Y., Hyde, K.D., 2004. Phylogenetic Lewis, I.M.L., Miller, S.A., 2003. Evaluation of Fungicides
evaluation of species nomenclature of Pestalotiopsis in and a Biocontrol Agents for the Control of Anthracnose
relation to host association. Fungal Diversity, 17:39-55.
on Green Pepper Fruit, 2002. Nematicide Test Report
Jeffries, P., Koomen, I., 1992. Strategies and Prospects for
[Online]. New Fungicide and Nematicide Data Committee
Biological Control of Diseases Caused by Colletotrichum.
of the American Phytopathological Society. Vol. 58, p.62.
In: Bailey, J.A., Jeger, M.J. (Eds.), Colletotrichum: Bi-
Available from http://apsjournals.apsnet.org/doi/abs/10.
ology, Pathology and Control. Commonwealth Myco-
1094/PD-90-0397?cookieSet=1andjournalCode=pdis (Ac-
logical Institute, Wallingford, p.337-357.
cessed 25/12/2007). [doi:10.1094/FN58]
Jeffries, P., Dodd, J.C., Jegerand, M.J., Plumbley, R.A., 1990.
Lui, A.R., Xu, T., Guo, L.D., 2007. Molecular and morpho-
The biology and control of Colletotrichum species on
logical description of Pestalotiopsis hainanensis sp. nov.,
tropical fruit crops. Plant Pathology, 39(3):343-366.
[doi:10.1111/j.1365-3059.1990.tb02512.x] a new endophyte from a tropical region of China. Fungal
Jeger, M.J., Jeffries, P., 1988. Alternative to chemical usage Diversity, 24:23-26.
for disease management in the post-harvest environment. MacKenzie, S.J., Peres, N.A., Barquero, M.P., Arauz, L.F.,
Aspects of Applied Biology, 17:47-57. Timmer, L.W., 2008. Host range and genetic relatedness
Jewsakun, S., 1978. Serology, Seed Transmission on An- of Colletotrichum acutatum isolates from fruit crops and
thracnose Disease of Pepper and Effect of Foliar Fungi- leatherleaf fern in Florida. Phytopathology, in press.
cides to the Causal Pathogens. MS Thesis, Kasetsart Maiti, S., Sen, C., 1979. Fungal Diseases of Betel Vine. Pro-
University. ceedings of the National Academy of Science of the
Jeyalakshmi, C., Seetharaman, K., 1998. Biological control of United States of America. Vol. 25, p.150-157.
fruit rot and die-back of chilli with plant products and Manandhar, J.B., Hartman, G.L., Wang, T.C., 1995. An-
antagonistic microorganisms. Plant Disease Research, thracnose development on pepper fruits inoculated with
13:46-48. Colletotrichum gloeosporioides. Plant Disease, 79:
776 Than et al. / J Zhejiang Univ Sci B 2008 9(10):764-778

380-383. cologia, 94(2):307-320. [doi:10.2307/3761809]

Mancini, N., Perotti, M., Ossi, C.M., Cavallero, A., Matuka, S., O′Connell, R.J., Bailey, J.A., Richmond, D.V., 1985. Cytology
Paganoni, G., Burioni, R., Rama, P., Clementi, M., 2006. and physiology of infection of Phaseolus vulgaris by
Rapid molecular identification of fungal pathogens in Colletotrichum lindemuthianum. Physiologial Plant Pa-
corneal samples from suspected keratomycosis cases. thology, 27(1):75-98. [doi:10.1016/0048-4059(85)900
Journal of Medical Microbiology, 55(11):1505-1509. 58-X]
[doi:10.1099/jmm.0.46638-0] O′Connell, R.J., Perfect, S., Hughes, B., Carzaniga, R., Bailey,
Marin, A., Ferreres, F., Tomás Barberán, F.A., Gil, M., 2004. J.A., Green, J., 2000. Dissecting the Cell Biology of
Characterization and quantization of antioxidant con- Colletotrichum Infection Processes. In: Bailey, J.A., Jegar,
stituents of sweet pepper (Capsicum annuum L.). Journal M.J. (Eds.), Colletotrichum: Biology, Pathology, and
of Agricultural and Food Chemistry, 52(12):3861-3869. Control. CAB International, Wallingfords, UK, p.57-77.
[doi:10.1021/jf0497915]
O′Donnell, K., Cigilink, E., Nirenberg, H.I., 1998. Molecular
Maxwell, A., Jackson, S.L., Dell, B., Hardy, G.E., 2005. systematic and phylogeography of the Giberella fujikuroi
PCR-identification of Mycospharella species associated species complex. Mycologia, 90(3):465-493. [doi:10.
2307/3761407]
with leaf diseases of Eucalyptus. Mycological Research,
Osuna-García, J.A., Wall, M.W., Waddell, C.A., 1998. En-
109(9):992-1004. [doi:10.1017/S0953756205003539]
dogenous levels of tocopherols and ascorbic acid during
Maymon, M., Minz, D., Barbul, O., Zveibil, A., Elad, Y.,
fruits ripening of New Mexican-type chilli (Capsicum
Freeman, S., 2004. Identification to species of Tricho-
annuum L.) cultivars. Journal of Agricultural and Food
derma biocontrol isolates according to ap-PCR and ITS
Chemistry, 46(12):5093-5096. [doi:10.1021/jf980588h]
sequence analyses. Phytoparasitica, 32:370-375.
Pae, D.H., Yoon, J.Y., Lee, J.M., 1998. Screening for resis-
McDonald, B.A., 1997. The population genetics of fungi: tools
tance to Colletotrichum gloeosporioides using detached
and techniques. Phytopathology, 87(4):448-453. [doi:10.
1094/PHYTO.1997.87.4.448]
fruits in pepper (Capsicum annuum) by high-pressure
McDonald, B.A., McDermott, J.M., 1993. The population spray. Journal of Korean Society and Horticultural Sci-
genetics of plant pathogenic fungi. Bioscience, 43(5): ence, 39:690-692.
311-319. [doi:10.2307/1312063] Pakdeevaraporn, P., Wasee, S., Taylor, P.W.J., Mongkolporn,
McDonald, B.A., Linde, C., 2002. The population genetics of O., 2005. Inheritance of resistance to anthracnose caused
plant pathogens and breeding strategies for durable re- by Colletotrichum capsici in Capsicum. Plant Breeding,
sistance. Euphytica, 124(2):163-180. [doi:10.1023/A:10 124(2):206-208. [doi:10.1111/j.1439-0523.2004.01065.x]
15678432355] Park, H.G., 2007. Problems of Anthracnose in Pepper and
Milgroom, M.G., 1996. Recombination and the multiloci Prospects for its Management. In: Oh, D.G., Kim, K.T.
structure of fungal populations. Annual Review of Phy- (Eds.), Abstracts of the First International Symposium on
topathology, 34(1):457-477. [doi:10.1146/annurev.phyto. Chilli Anthracnose. National Horticultural Research In-
34.1.457] stitute, Rural Development of Administration, Republic
Mitchell, J.R., Roberts, P.J., Moss, S.T., 1995. Sequence or of Korea, p.19.
structure? A short review on the application of nucleic Park, K.S., Kim, C.H., 1992. Identification, distribution, and
acid sequence information to fungal taxonomy. Mycolo- etiological characteristics of anthracnose fungi of red
gist, 9:67-75. pepper in Korea. Korean Journal of Plant Pathology,
Mongkolporn, O., Dokmaihom, Y., Kanchana-udomkarn, C., 8:61-69.
Pakdeevaraporn, P., 2004a. Genetic purity test of F1 hy- Park, W.M., Park, S.H., Lee, Y.S., Ko, Y.H., 1987. Differen-
brid Capsicum using molecular analysis. Journal of Hor- tiation of Colletotrichum spp. causing anthracnose on
ticultural Science and Biotechnology, 79:449-451. Capsicum annuum L. by electrophoretic method. Korean
Mongkolporn, O., Thierry, J., Kanchana-udomkarn, C., Lin, Q., Journal of Plant Pathology, 3:85-92.
2004b. Genetic analysis of resistance to pepper anthrac- Paul, Y.S., Behl, M.K., 1990. Some studies on bell pepper
nose caused by Colletotrichum capsici. Thai Journal of anthracnose caused by Colletotrichum capsici and its
Agricultural Science, 35:259-264. control. Seed Research, 1:656-659.
Moretto, K.C.K., Gimenes-Fernandes, N., Dos Santos, J.M., Pearson, M.N., Bull, P.B., Speke, H., 1984. Anthracnose of
2001. Influence of Trichoderma spp. on Colletotrichum Capsicum in Papua, New Guinea; varietal reaction and
acutatum mycelial growth and morphology on infection associated fungi. Tropical Pest Management, 30:
of ‘Tahiti’ lime detached flowers. Summa Phytopatholo- 230-233.
gia, 27(4):357-364. Peres, N.A.R., de Souza, N.L., Peever, T.L., Timmer, L.W.,
Moriwaki, J., Tsukiboshi, T., Sato, T., 2002. Grouping of 2004. Benomyl sensitivity of isolates of Colletotrichum
Colletotrichum species in Japan based on rDNA se- acutatum and C. gloeosporioides from citrus. Plant Dis-
quences. Journal of General Plant Pathology, 68(4): ease, 88(2):125-130. [doi:10.1094/PDIS.2004.88.2.125]
307-320. [doi:10.1007/PL00013096] Peres, N.A., Timmer, L.W., Adaskaveg, J.E., Correll, J.C.,
Nirenberg, H.I., Feiler, U., Hagedorn, G., 2002. Description of 2005. Life cycles of Colletotrichum acutatum. Plant
Colletotrichum lupini comb. nov. in modern terms. My- Disease, 89(8):784-796. [doi:10.1094/PD-89-0784]
 Than et al. / J Zhejiang Univ Sci B 2008 9(10):764-778 777

Peres, N.A., MacKenzie, S.J., Peever, T.L., Timmer, L.W., Agricultural Sciences. Available from http://edis.ifas.
2008. Postbloom fruit drop of citrus and key lime an- ufl.edu/PP104 (Accessed 25/12/2007).
thracnose are caused by distinct phylogenetic lineages of Royle, D.J., Butler, D.R., 1986. Epidemiological Significance
Colletotrichum acutatum. Phytopathology, 98(3):345- of Liquid Water in Crop Canopies and its Role in Disease
352. [doi:10.1094/PHYTO-98-3-0345] Forecasting. In: Ayres, P.G., Boddy, L. (Eds.), Water,
Pérez-Gálvez, A., Martin, H.D., Sies, H., Stahl, W., 2003. Fungi and Plants. Cambridge University Press, Cam-
Incorporation of carotenoids from paprika oleoresin into bridge, p.139-156.
human chylomicron. British Journal of Nutrition, 89(6): Sharma, P.N., Kaur, M., Sharma, O.P., Sharma, P., Pathania,
787-793. [doi:10.1079/BJN2003842] A., 2005. Morphological, pathological and molecular
Perfect, S.E., Hughes, H.B., O′Connell, R.J., Green, J.R., 1999. variability in Colletotrichum capsici, the cause of fruit rot
Colletotrichum: a model genus for studies on pathology of chillies in the subtropical region of north-western India.
and fungal-plant interactions. Fungal Genetics and Bi- Journal of Phytopathology, 153(4):232-237. [doi:10.
ology, 27(2-3):186-198. [doi:10.1006/fgbi.1999.1143] 1111/j.1439-0434.2005.00959.x]
Pernezny, K., Roberts, P.D., Murphy, J.F., Goldberg, N.P., Sheu, Z., Chenand, J., Wang, T., 2007. Application of
2003. Compendium of Pepper Diseases. The American ITS-RFLP Analysis for Identifying Colletotrichum Spe-
Phytopathological Society, St. Paul, Minnedota, p.73. cies Associated with Pepper Anthracnose in Taiwan. In:
Photita, W., Taylor, P.W.J., Ford, R., Lumyong, P., McKenzie, Oh, D.G., Kim, K.T. (Eds.), Abstracts of the First Inter-
H.C., Hyde, K.D., 2005. Morphological and molecular national Symposium on Chilli Anthracnose. National
characterization of Colletotrichum species from herba- Horticultural Research Institute, Rural Development of
ceous plants in Thailand. Fungal Diversity, 18:117-133. Administration, Republic of Korea, p.32.
Pickersgill, B., 1997. Genetic resources and breeding of Cap- Simmonds, J.H., 1965. A study of the species of Colleto-
sicum spp. Euphytica, 96(1):129-133. [doi:10.1023/A:100 trichum causing ripe fruit rots in Queensland. Queensland
2913228101] Journal Agriculture and Animal Science, 22:437-459.
Poonpolgul, S., Kumphai, S., 2007. Chilli Pepper Anthracnose Smith, B.J., Black, L.L., 1990. Morphological, cultural, and
in Thailand. Country Report. In: Oh, D.G., Kim, K.T. pathogenic variation among Colletotrichum species iso-
(Eds.), Abstracts of the First International Symposium on lated from strawberry. Plant Disease, 74(1):69-76.
Chilli Anthracnose. National Horticultural Research In- [doi:10.1094/PD-74-0069]
stitute, Rural Development of Administration, Republic Smith, K.L., 2000. Peppers. In: Precheur, R.J. (Ed.), Ohio
of Korea, p.23. Vegetable Production Guide. Ohio State University Ex-
Poulos, J.M., 1992. Problems and Progress of Chilli Pepper tension, Columbus, Ohio, p.166-173.
Production in the Tropics. In: Hock, C.B., Hong, L.W., Sreenivasaprasad, S., Talhinhas, P., 2005. Genotypic and
phenotypic diversity in Colletotrichum acutatum, a cos-
Rejab, M., Syed, A.R. (Eds.), Proceedings of the Con-
mopolitan pathogen causing anthracnose on a wide range
ference on Chilli Pepper Production in the Tropics. Kuala
of hosts. Molecular Plant Pathology, 6(4):361-378.
Lumpur, Malaysia, p.98-129.
[doi:10.1111/j.1364-3703.2005.00291.x]
Pring, R.J., Nash, C., Zakaria, M., Bailey, J.A., 1995. Infection
Sreenivasaprasad, S., Mills, P., Brown, A., 1994. Nucleotide
process and host range of Colletotrichum capsici.
sequence of the rDNA spacer 1 enables identification of
Physiological and Molecular Plant Pathology, 46(2):
isolates of Colletotrichum as C. acutatum. Mycological
137-152. [doi:10.1006/pmpp.1995.1011] Research, 98:186-188.
Prusky, D., Plumbley, R.A., 1992. Quiescent Infections off Sreenivasaprasad, S., Mills, P., Meehan, B.M., Brown, A.,
Colletotrichum in Tropical and Subtropical Fruits. In: 1996. Phylogeny and systematics of 18 Colletotrichum
Bailey, J.A., Jeger, M.J. (Eds.), Colletotrichum: Biology, species based on ribosomal DNA spacer sequences. Ge-
Pathology, and Control. CAB International Wallingford, nome, 39(3):499-512. [doi:10.1139/g96-064]
p.289-307. Staub, T., 1991. Fungicide resistance: practical experience and
Prusky, D., Koblier, I., Aridi, R., Beno-Moalem, D., Yakoby, antiresistance strategies and the role of integrated use.
N., Keen, N.T., 2000. Resistance Mechanisms of Sub- Annual Review of Phytopathology, 29(1):421-442. [doi:
tropical Fruits to Colletotrichum gloeosporioides. In: 10.1146/annurev.py.29.090191.002225]
Bailey, J.A., Jeger, M.J. (Eds.), Colletotrichum: Biology, Taylor, P.W.J., Ford, R., 2007. Diagnostics, genetics diversity
Pathology, and Control. CAB International Wallingford, and pathogenic variation of ascochyta blight of cool
p.232-244. season food and feed legumes. European Journal of Plant
Ratanacherdchai, K., Wang, H.K., Lin, F.C., Soytong, K., Pathology, 119(1):127-133 [doi:10.1007/s10658-007-91
2007. RAPD analysis of Colletotrichum species causing 77-x]
chilli anthracnose disease in Thailand. Journal of Agri- Taylor, P.W.J., Mongkolporn, O., Than, P.P., Montri, P.,
cultural Technology, 3:211-219. Ranathunge, N., Kanchana-udonkarn, C., Ford, R.,
Roberts, P.D., Pernezny, K., Kucharek, T.A., 2001. Anthrac- Pongsupasamit, S., Hyde, K.D., 2007. Pathotypes of
nose caused by Colletotrichum sp. on pepper [Online]. Colletotrichum spp. Infecting Chilli Peppers and Mecha-
Journal of University of Florida/Institute of Food and nisms of Resistance. In: Oh, D.G., Kim, K.T. (Eds.), Ab-
 778 Than et al. / J Zhejiang Univ Sci B 2008 9(10):764-778

stracts of the First International Symposium on Chilli isolates from grape in subtropical Australia. Plant Pa-
Anthracnose. National Horticultural Research Institute, thology, 56(3):448-463. [doi:10.1111/j.1365-3059.2007.
Rural Development of Administration, Republic of Korea, 01569.x]
p.29. Wikipedia, 2007. Capsicum [WWW]. Wikimedia Foundation,
Than, P.P., Jeewon, R., Hyde, K.D., Pongsupasamit, S., Inc., USA. Available from http://en.wikipedia.org/wiki/
Mongkolporn, O., Taylor, P.W.J., 2008. Characterization Capsicum (Accessed 25/12/2007).
and pathogenicity of Colletotrichum species associated Yoon, J.B., 2003. Identification of Genetic Resource, Inter-
with anthracnose disease on chilli (Capsicum spp.) in specific Hybridization and Inheritance Analysis for
Thailand. Plant Pathology, 57(3):562-572. [doi:10.1111/ Breeding Pepper (Capsicum annuum) Resistant to An-
j.1365-3059.2007.01782.x] thracnose. Ph.D. Thesis, Seoul National University, Ko-
Tong, N., Bosland, P.W., 1999. Capsicum tovarii, a new rea.
member of the Capsicum complex. Euphytica, 109(2): Yoon, J.B., Park, H.G., 2001. Screening method for resistance
71-72. [doi:10.1023/A:1003421217077] to pepper fruits anthracnose: Pathogen sporulation, in-
von Arx, J.A., 1957. Die Arten der Gattung Colletotrichum oculation methods related to inoculum concentrations,
Cda. Phytopathologische Zeitschrift, 29:414-468. post-inoculation environments. Journal of Korean Soci-
Voorrips, R.E., Finkers, R., Sanjaya, L., Groenwold, R., 2004. ety and Horticultural Science, 42:382-393.
QTL mapping of anthracnose (Colletotrichum spp.) re- Yoon, J.B., Yang, D.C., Lee, W.P., Ahn, S.Y., Park, H.G.,
sistance in a cross between Capsicum annuum and C. 2004. Genetic resources resistant to anthracnose in the
chinense. Theoretical and Applied Genetics, 109(6): genus Capsicum. Journal of Korean Society and Horti-
1275-1282. [doi:10.1007/s00122-004-1738-1] cultural Science, 45:318-323.
Wharton, P.S., Diéguez-Uribeondo, J., 2004. The biology of Yun, S.H., Berbee, M.L., Yoder, O.C., Turgeon, B.G., 1999.
Colletotrichum acutatum. Anales del Jardin Botanico de Evolution of the fungal self-fertile reproductive life style
Madrid, 61:3-22. from self-sterile ancestors. Proceedings of the National
Whitelaw-Weckert, M.A., Curtin, S.J., Huang, Steel, R.C.C., Academy of Science of the United States of America,
Blanchard, C.L., Roffey, P.E., 2007. Phylogenetic rela- 96(10):5592-5597. [doi:10.1073/pnas.96.10.55 92]
tionships and pathogenicity of Colletotrichum acutatum

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