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Colletotrichum gloeosporioides: An Anthracnose Causing Pathogen of Fruits and Vegetables

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Colletotrichum species are present in both tropical and subtropical regions of the world. But Colletotrichum gloeosporioides is most important pathogen and belongs to order melanconiales. The complete genome of this pathogen is not yet sequenced but various genes are identified which involved in pathogenesis and host defense. The optimum temperature for growth of this pathogen is 25-28°C, and pH 5.8-6.5. It is usually inactive in dry season but during favorable conditions it causes anthracnose disease to large number of economic crops amongst which mango anthracnose is important as far as losses caused by pathogen is concerned. First of all pathogen establish interaction with host by producing melanized appressorium and then penetrate the host cuticle. After penetration, infection vesicles and primary hyphae are formed. Later, secondary hyphae developed and spread to kill the host cell. Colletotrichum gloeosporioides follows the hemibiotrophic mode of infection where, biotrophic and necrotrophic phases are sequentially occur. The pathogen produced lesions on leaves, fruit and other parts of plant. Finally these lesions become dark and form concentric ring pattern. Colletotrichum gloeosporioides is also known to infect humans but only few incidents of such infections are known. A number of fungal genes have been identified using mutant screen, which plays role in different stages of infection and can be used as potential targets to devise strategies for controlling anthracnose disease in fields. This review focuses on up to date knowledge of all aspects of C. gloeosporioides biology.
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BIOSCIENCES BIOTECHNOLOGY RESEARCH ASIA, August 2015. Vol. 12(2), proof
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Colletotrichum gloeosporioides: An Anthracnose
Causing Pathogen of Fruits and Vegetables
Meenakshi Sharma and Saurabh Kulshrestha*
Faculty of Applied Sciences and Biotechnology, Shoolini University of Biotechnology
and Management Sciences, Bajhol, Solan, India.
(Received: 02 March 2015; accepted: 04 April 2015)
Colletotrichum species are present in both tropical and subtropical regions of the
world. But Colletotrichum gloeosporioides is most important pathogen and belongs to order
melanconiales. The complete genome of this pathogen is not yet sequenced but various genes are
identified which involved in pathogenesis and host defense. The optimum temperature for growth
of this pathogen is 25-28°C, and pH 5.8-6.5. It is usually inactive in dry season but during
favorable conditions it causes anthracnose disease to large number of economic crops amongst
which mango anthracnose is important as far as losses caused by pathogen is concerned. First
of all pathogen establish interaction with host by producing melanized appressorium and then
penetrate the host cuticle. After penetration, infection vesicles and primary hyphae are formed.
Later, secondary hyphae developed and spread to kill the host cell. Colletotrichum
gloeosporioides follows the hemibiotrophic mode of infection where, biotrophic and necrotrophic
phases are sequentially occur. The pathogen produced lesions on leaves, fruit and other parts
of plant. Finally these lesions become dark and form concentric ring pattern. Colletotrichum
gloeosporioides is also known to infect humans but only few incidents of such infections are
known. A number of fungal genes have been identified using mutant screen, which plays role in
different stages of infection and can be used as potential targets to devise strategies for controlling
anthracnose disease in fields. This review focuses on up to date knowledge of all aspects of C.
gloeosporioides biology.
Key words: Colletotrichum gloeosporioides, anthracnose, pathogenicity genes.
Colletotrichum gloeosporioides is a
ubiquitous pathogen. It belongs to the order
melanconiales. This fungus infects
monocotyledons (turf grass) to higher
dicothyledons (cashew trees). C.
gloeosporioides is widely distributed and
common plant pathogen in the world (Sutton,
1992; Cannon et al., 2000). The fungus is more
abundant in tropical and subtropical regions than
in temprate (CAB international 2005).This
pathogen infects about 470 different host genera.
The pathogen also causes post-harvest problems
(Prusky and Plumbley,1992) and also act as
endophytic strains which are isolated from
symptomless plant parts (Cannon and Simmons,
2002; Lu et al., 2004; Photita et al., 2004, 2005).
C. gloeosporioides was proposed for the
first time as Vermicularia gloeosporioides by
Penzig 1882. C. gloeosporioides was first
reported at Deodoro, Brazil in 1937 on S. humilis
and in India, it was first reported by Butler 1918
on coffee. Glomerella cingulata is the sexual
stage (teleomorph) while the asexual stage
(anamorph) is called C. gloeosporioides (Schrenk
2
and Spaulding, 1903). There are various species
come under genus Colletotrichum but only C.
graminicola and C. higginsianum genomes were
completely sequenced. C. gloeosporioides
genome is under study but various genes have been
identified which involve in pathogenesis and host
defense mechanism.
It requires 25-28°C temperature, pH
5.8-6.5 for better growth. This pathogen is
inactive in dry season and switches to active stages
when encountered favorable environmental
conditions. It involves hemibiotrophic mode of
infection where both phases, biotrophic and
necrotrophic phases occur sequentially. Various
medium preparations were employed for the
growth and sporulation of C. gloeosporioides
including Potato dextrose agar, lima bean agar,
malt extract agar and oat meal agar.
Traditionally the identification and
characterization of Colletotrichum spp were
relied on differences in morphology features such
as colony color, size, and shape of conidia and
appressorium, optimal temperature for growth,
growth rate, presence or absence of setae (Von
Arx, 1957; Smith and Black, 1990; Gunnel and
Gubler, 1992; Sutton, 1992). Now molecular
techniques provide alternative methods for
taxonomic studies and are important tools in
solving the problem of species delimitation
(Maclean et al., 1993)
Germination in C. gloeosporioides
follows two routes: “pathogenic” and
“saprophytic” (Barhoom and Sharon, 2004).
Pathogenic germination takes place on plants or
on a hydrophobic surface and is characterized by
fast mitosis followed by development of a single
germ tube. This process is initiated immediately
and results in the formation of appressoria.
Saprophytic germination occurs in rich medium.
It takes a much longer period of time and is
characterized by development of two germ tubes
that emerge from opposite sides of the spore.
These germ tubes do not form appressoria, and
these germinated spores do not infect plants.
These two germination routes in C.
gloeosporioides are regulated by different
signaling pathways such as: saprophytic
germination involved cAMP pathways while
pathogenic germination is cAMP independent.
C. gloeosporioides causes anthracnose
disease on a wide variety of fruits, including
almond, avocado, apple, Arabica coffee, guava,
mango, strawberry, papaya, banana, passion fruit,
citrus, grapes and cashews (Simmonds, 1965;
Hartill, 1992 ; Alahakoon et al., 1994 ;Timmer et
al., 1998; Agwana et al., 1997; Freeman et al.,
1998; Martinez-Culebras et al., 2000, 2003;
Sanders and Korsten 2003; Xiao et al., 2004;
Amusa et al., 2005; Nelson 2008). It causes
considerable damage to large number of crops
such as cereals, coffee, legumes (Bailey and
Jeger, 1992;Lenne, 1992) and tropical, subtropical
fruits such as avocado, banana, mango (Mordue,
1967; Jeffries et al., 1990). Colletotrichum spp
are also found on decaying wild fruits (Tang et
al., 2003). Under a high concentration of CO2,
there is increase in fecundity (spores produced
per lesion area) observed and this may increase
the severity and spread of disease (Chakraborty
and Datta, 2003)
Colletotrichum species that cause
serious plant disease are also commonly isolated
as endophytes from healthy plants, and have been
identified as saprobes on dead plant material
(Photita et al., 2001, 2004; Promputtha et al.,
2002; Toofanee and Dulymamode, 2002; Kumar
and Hyde, 2004). The symptoms such as small,
dark lesions appear on leaves, fruits and flowers
of the infected plant which finally produce
concentric ring pattern.
Phylogenetic relationships in
Colletotrichum genus is successfully achieved by
using ITS1 and ITS2 regions (Sherriff et al., 1994;
Sreenivasaprasad et al., 1996; Freeman et al.,
2001; Hsiang and Goodwin, 2001; Denoyes
Rothan et al., 2003; Martinez-Culebras, et al.,
2000, 2003).
Morphology
There are more than 600 synonyms of
C. gloeosporioides showed many morphological
and physiological variations reported by Von Arx
(1957). Palo (1932), described the morphology
of the fungus and the spores were irregular and
appear as brown to black dots. The acervuli were
highly variable in size, shape and exude pink
masses of conidia when mature under moist
conditions (Sattar and Malik, 1939).
Conidia were straight, cylindrical and
oval and borne on distinct well developed hyaline
conidiophores (Sattar and Malik, 1939). Bose et
3
al., 1973, observed the size of conidia varied
from 11-16 x 4-6 µm and 13.8 x 4.8 µm, broad
oblong with rounded ends 14.0 x 3.7 µm reported
by Simmonds, 1965, formae speciales of C.
gloeosporioides was observed by Sutton, 1992
and also recognized the species as a
heterogeneous group with a great variation in
morphology.
Ji and Guo, 1992 described the current
method for the detection and identification of C.
gloeosporioides and C. oleifera. This method
depends on isolation of pure cultures on nutrient
media followed by morphological examination of
the isolates.
Baxter et al., 1985 defined C.
gloeosporioides aggregate by using
morphological methods and reported that conidia
were cylindrical with rounded ends and less than
4.5 ¼m in diameter. These features are not
reliable because Colletotrichum spp frequently
produce different shape and sizes secondary
conidia.
Environment condition for growth of
pathogen
Environmental conditions favors the
pathogen growth are temperature, 25-28° C being
optimum, pH range of 5.8 to 6.5 and high
humidity. Activity of this pathogen depend upon
weather, Colletotrichum is inactive in dry season.
Ponte 1996, observed that sunlight, low humidity
and temperature extremes (below 180 C or greater
than 250) rapidly inactivate spores. Spores are
released from acervuli when there is an abundance
of moisture. The pathogen persists on and in seed,
trash and weed hosts and is dispersed locally by
water splash, air currents, insects, or other forms
of contact (CAB international 2005 crop
protection compendium). In general, infection is
favored at temperatures ranging from 20 to 30°C.
Davis et al., 1987 reported the range between 20-
30°C as the optimum temperature for the growth
and sporulation of C. gloeosporioides on mango.
C. gloeosporioides required free water
or relative humidity above 95 per cent for conidial
germination and appressorium formation. Pandey
2011, observed that temperature and moisture
requirements for infection have also been used
to build forecasting systems for mango
anthracnose a vital component for the disease
management.
In vitro culture
Various growth parameters of C.
gloeosporioides were studied using solid media
such as effect of concentration and composition
of media, inoculums density and temperature on
the spore carrying capacity and microcycle
conidiation. Slade et al., 1987, compared spore
production of C. gloeosporioides on solid media
with liquid media.
C. gloeosporioides grow well on PDA
(potato dextrose agar) and CWA (coconut watery
endosperm) which contain appropriate amounts
of carbohydrates, proteins, minerals and lipids
(Santoso et al., 1996).
Aerial mycelium growth is better on
the Richard’s, Brown’s agar and better sporulation
occur on oat meal, corn meal agar along with
abundant development of acervuli in rings and few
setae in C. gloeosporioides. Glutamic acid and
alanine supported maximum growth and
sporulation of C. gloeosporioides. The growth
is completely inhibited at 10°C.
Light is not necessary but enhance
sporulation, pH 6 (for growth and sporulation)
and germination is better on a more acidic
medium. Czapek’s and yeast extract agar medium
give maximum growth.
Mode of infection
C. gloeosporioides follows the
hemibiotrophic mode of infection where,
biotrophic and necrotrophic phases are
sequentially occur. First of all pathogen establish
interaction with host by producing melanized
appressorium and then penetrate the host cuticle.
After penetration, infection vesicles and primary
hyphae are formed. These structures are somewhat
similar to haustoria (formed by powdery mildews
and rust fungi) do not cause any harm to host. This
stage of infection is called biotrophic phase. Later,
necrotrophic secondary hyphae developed and
spread to kill the host cell (Munch et al., 2008)
Anthracnose caused by Colletotrichum
gloeosporioides
C. gloeosporioides causes anthracnose
disease to variety of crops worldwide. It is a
disease of the foliage, stems, fruits and causes
pre-harvest and post-harvest losses in mango,
papaya, guava, custard apple, pomegranate and
other subtropical fruit crops. Anthracnose is
favored by wet, humid, warm conditions and
4
spread by infected seeds, rain splash and moist
winds. It often result in fruit drop and fruit rot
(infonet-biovision.com).
Anthracnose is caused by fungi that
produce conidia within black fungal fruiting
bodies called acervuli. Other species are also
responsible for most anthracnose disease. First,
lesion appears as small, dark spots on stolons and
petioles. With age these lesions become large in
diameter. Brownish areas are formed by the
conidial masses that cover the lesion center and
are frequently produced in a concentric ring
pattern (Ponte, 1996) (infonet-biovision.com).
Host range and crop loss
Life cycle of this pathogen starts by
germination of spores on the plant surface to form
melanized infection structures called appressoria
followed by penetration of host tissue. At this
point thick infection hypaes are produced in
primary infected cells, this stage is called as
biotrophic stage of infection. After this the
fungus suddenly switches to necrotrophic phase
of infection which is characterized by formation
of thin secondary hyphaes, which originated from
the primary hyphaes and it is these secondary
hyphae which starts colonizing the nearby cells,
and ultimately leads to development of visible
lesions at the site of infection. Finally the spores
are formed on the surface of infected tissue and
then they are dispersed by insect, air current and
water splash to start another infection cycle.
C. gloeosporioides infects about 470
different host genera but some economic
important crops such as: avocado, mango, beans,
cashews, cassava, citrus plant, cotton, cow-pea,
cucumber, eggplant, green gram, mango, onion,
pepper, pumpkin, papaya, sorghum, soybean,
tomato, watermelon, wheat, yam, zucchini/
courgette, cucurbit, cereals, legumes and spinach.
Amongst them mango anthracnose is very
important from Indian prospective.
Anthracnose caused by C.
gloeosporioides was reported from several parts
of the world. Bitter rot of apple (Malus sylvestris
Mill) caused by Glomerella cingulata and C.
gloeosporioides was reported in North Carolina
orchards. The disease was first observed during
the end of June and may cause 100% fruit rot by
mid-august (Shane and Sutton, 1981).
Fruit rot of apple and pear was caused by
C. gloeosporioides and C. acutatum in the
Southern, Central and Mid Atlantic regions of the
United States and in most countries where these
fruits are grown (Sutton 1990).
C. gloeosporioides was reported to
cause both pre and post harvest anthracnose on
avocado in several countries including Australia
(Fitzell, 1987), Israel (Binyamini and Nadel,
1972), South Africa (Darvas and Kotze, 1987) and
Sri Lanka (Sivanathan and Adikaram, 1989)
primarily as a quiescent pathogen (Jefferies et
al., 1990).
Almond and avocado are also reported
to be infected by C. gloeosporioides in Israel
(Binyamini and Nadel, 1972; Shabi and Katan,
1983). This fungus acts as a post-harvest pathogen
in avocado and in almond it infect the young
fruits). Prusky and Saka, 1989; Prusky et al., 1991
observed that germination and appressorium
formation of C. gloeosporioides spores in
avocado fruits may be triggered by chemical
signals from the surface wax .The pathogen causes
severe yield losses and having different optimal
growth temperature (Freeman et al., 1995). The
site of infection in avocado is primarily the fruits,
but infections may also appear on leaves and stems
but it does not attack avocado flowers (Nelson,
2008). Anthracnose caused by C. gloeosporioides
was also reported on avocado in Australia, South
Africa (Giblin and Coates, 2007) and banana
(Jeger et al., 1995).
In Belize, the three strains of C.
gloeosporioides such as: cgm, cgc and cgp was
observed on citrus. cgm and cgc were non-
pathogenic to citrus flowers (Fagan, 1980). In
Florida, the fast growing and slow growing strains
of C. gloeosporioides caused post bloom fruit
drop (Sonoda and Pelosi, 1988). C.
gloeosporioides also causes infection on Dragon
fruit (Hylocereus spp.) in Peninsular Malaysia
(Masyahit et al., 2009).
Trichosanthes kirilowii Maxim, a
species within the gourd family, is cultivated in
China for its edible seeds and medicinal roots. In
2000, there was a heavy loss due to fruit rot
caused by C. gloeosporioides (Li and Zhang,
2007). Anthracnose is highly destructive disease
of lupins. It was first found in Western Australia
in 1996 and infect almost all species of lupins.
5
But 10-100% crop loss was observed in albus
lupins and 10-50% in narrow leafed lupins
(www.hannafords.com).
Post harvest disease of mango was also
reported to be caused by C. gloeosporioides
(Ploetz and Prakash, 1997). It was first reported
from Puerto Rico (Collins, 1903) and later from
Hawaii (Higgins, 1906), Florida (Fawcett, 1907),
Cuba (Cardin, 1910), Philippines (Wester, 1911),
Columbia (Taro, 1929), South Africa (Doidge,
1932), Brazil (Bitancounrt, 1938), United States
(Traub and Robinson, 1938) and Pakistan (Sattar
and Malik, 1939). In India, this disease of mango
was reported by Stevens and Pierce, 1933 and
currently, it is widely distributed in the entire
mango growing states of the India causing huge
economic loss.
It affects both vegetative and
reproductive structure. Initial infection starts
from leaves and spreads to flowers causing
blossoms blight, which destroys inflorescence
leading to considerable reduction in fruit set and
yield loss. The disease incidence from different
countries has been reported to be 32% in South
Africa (Sanders et al., 2000), 64.6% in Cost Rica
during 1990 (Arauz et al., 1994) and could reach
almost 100% in fruit produced under wet or very
humid condition (Arauz, 2000). In India, Himachal
Pradesh, during 1990-92, post harvest decay due
to anthracnose was 29.6% (Sharma et al., 1994).
C. gloeosporioides causes anthracnose which is
the most important biological constraint to mango
production in South East Asia resulting in
substantial yield loss (Dodd et al., 1991).
There are several mango varieties like
Alphonso, Baramasi, Carabao, Carrie Early Gold,
Keaw, Kent, Kishen Bhog, Rad, Saigon, Tommy
Atkins and Van Dyke are resistant to infection
caused by C. gloeosporioides. (Peterson, 1986;
Dinh et al., 2003).
Infection on oil coffee berries in
Vietnam was observed and finally pathogen
characterize as C. gloeosporioides by employed
morphological and molecular methods (Nguyen
et al., 2009). In September 1995, C.
gloeosporoides was observed on olive on the
southern Montenegrin coast near Ulcinj
(Latinovic and Vucinic, 2002). Brazil, one of the
largest onion producers in the world observed
onion anthracnose caused by C. gloeosporioides
(Barbosa, 2001). 17% of papaya fruits were
affected by anthracnose disease in Hawaii,
rounded, water soaked, and sunken lesions
appeared on the body of the ripened fruits. These
lesions are referred to as “chocolate spots”
(Dickman and Alvarez, 1983).
Microsclerotia formed sparsely by C.
gloeosporioides and play an important role in
survival (Baxter et al., 1985). Survival of mycelia
and stromata in colonized pepper seeds have also
been reported (Manandhar et al., 1995). The
pathogen readily colonizes the seed coat and
peripheral layers of endosperm even in
moderately colonized seeds. Heavily colonized
seeds had abundant inter and intra-cellular
mycelium and acervulli in seed coat endosperm
and embryo, showing disintegration of
parenchymatous layers of the seed coat and
depletion of food material in endosperm and
embryo (Chitkara et al., 1990). C.
gloeosporioides was reported that it transmits
from endosperm tissue to hypocotyls and radicals
in red pepper (Lee and Chung, 1995).
Pepper anthracnose is caused by C.
capsici and C. gloeosporioides in the hot humid
tropics of Asia. They reduce marketable yields
of pepper (Manandhar et al., 1995). Recently,
Park and Kim reported that five anthracnose fungi-
C. gloeosporioides, C. dematium, C. coccodes,
C. acutatum and Glomerella cingulata are
pathogenic to different tissue of pepper plants.
Among these species C. gloeosporioides was the
predominant species causing anthracnose on
pepper fruits. Purple and ripe red fruit stage
developed more anthracnose than the immature
stages (Oh et al., 1999). During 2005 and 2006,
C. gloeosporioides was isolated from diseased
samples of bell pepper (Capsicum annuum)
collected from various districts of Himachal
Pradesh, India. This was the first report of C.
gloeosporioides on bell pepper from Himachal
Pradesh (Gupta et al., 2009).
Three species of Colletotrichum such as:
C. gloeosporioides, C. fragariae, or C. acutatum
were observed to cause crown rot of strawberry
(Freeman and Katan, 1997; Howard and Albregts,
1984; Howard et al., 1992). In United State
(southeastern) infection by C. fragariae and C.
gloeosporioides is favored by warm, moist
conditions (Mori, 1998; Smith and Black, 1987).
6
Tulip tree (Liriodendron chinense) has been
widely cultivated in Korea and infection of C.
gloeosporioides was detected by mycological
characteristics, pathogenicity, internal transcribed
spacer sequence. This was the first report on
anthracnose disease caused by C.
gloeosporioides on tulip trees in Korea (Choi et
al., 2012). Yam a stable crop in tropical,
subtropical Africa, Central South America, parts
of Asia, the Carribean and Pacific islands
(Coursey, 1967; Adelusi and Lawanson, 1987).
Water yam (D. alata) is thought to be more
susceptible to anthracnose than other yams (Plant
Protection Service Secretariat of the Pacific
Community, 2002). Other fungi were also
associated with yam leaf-spot (Amusa et al.,
1996).
Genes involved in host defence and in
pathogenesis of Colletotrichum gloeosporioides
During colonization in host tissue, C.
gloeosporioides create alkalinizes surroundings.
The transcription factor, pacC, is a regulator of
pH-controlled genes and is essential for
successful colonization. PacC up-regulates 478
genes and down-regulates 483 genes, comprising
5% of the fungal genome including; transporters,
antioxidants and cell wall degrading enzymes
(Alkan et al., 2013).
Genes involved in host defense
Pel-B gene is a virulent gene and encodes
for pectate lyase (Yakoby et al., 2001). This
enzyme degrades the plant cell wall and its
expression can be easily seen in necrotrophic
phase of infection. The expression of this gene
also induce host defense mechanism. Pectate
lyase expression is strongly affected by
alkalinization. Alkalinization occurs naturally
during fruit ripening, where the pH of the pericarp
increases from 5.2 to 6.1 and pathogen also helps
in increase the amount of ammonia accumulated
by the host. This increase pH may change the
expression of pacC, the terminal component of
Table 1. Showing various genes involved in host defense as well as in pathogenesis of Colletotrichum gloeosporioides
S.No Gene Function Encode (Reference)
1 Shpx2,Shpx5,Shpx6,Shpx12 Host defense Shpx2,5,6 12 protein (Harrison et al ., 1994)
2 PepCYP Host defense PepCYP protein (Hutvagner et al., 1997)
3 Cap 20 Host pathogenesis Cap-20 protein (Chilly et al., 1998)
4 CgDN3 Host pathogenesis Pathogenesis, CgDN3 protein (Stephenson et al., 2000)
5 Chip 6 conidial germination,
appressorium formation Chip 6 protein (Kim et al., 2002)
6 Pnl-1,Pnl-2 Pathogenesis Cellulose binding domain, pectin lyase (Wei
et al., 2002)
7 Pel-B Degrade plant cell wall Pectate lyase (Drori et al., 2003; Kramer-
Haimovich et al., 2006)
8 CgDN24 Pathogenesis , hyphal Stephenson et al., 2005
development
9 Bcl-2 Apoptosis, mycelium, conidia, Bax and antiapoptotic protein
germination, pathogenesis (Barhoom and Sharon, 2007)
10 CgCTR2 Putative copper transporter CgCTR2 protein (Barhoom et al., 2008)
11 Pel-1,Pel-2 Pathogenesis Pectic lyase (Shih et al., 2008)
12 CgOPT1 Spore germination, mycelium CgOPT1protein (Chague et al., 2009)
growth
13 CgRac1 Morphogenesis, nuclear division, CgRac1 protein (Nesher et al., 2011)
pathogenesis
14 GDH2,GS1,GLT,MEP Induce ammonia accumulation, GDH2,GS1,GLT,MEP proteins (Miyara
pathogenesis et al., 2012)
15 PacC Create alkalinize environment Pac C protein (Alkan et al., 2013)
and regulate activity of several
genes
7
the pH-dependent genes which is known to
regulate the expression of Pel-B gene (Kramer-
Haimovich et al., 2006; Drori et al., 2003).
Pel-B mutants do not secrete PLB and
exhibited 25% lower pectate lyase and pectin
lyase activities and 15% higher polygalacturonase
activity. In addition, these Pel-B mutants induced
a significantly higher host phenylalanine ammonia
lyase activity as well as the antifungal diene,
which is indicative of higher host resistance
(Yakoby et al., 2001).
PepCYP gene encodes a protein
homologous to cytochrome P450 containing
a‘heme-binding domain. PepCYP gene expression
is higher in the incompatible interaction than in
the compatible interaction. The induction of
PepCYP gene is up-regulated by wounding or
jasmonic acid treatment during ripening. PepCYP
gene product play a role in the defense
mechanism when the fungus invades and colonizes
the epidermal cells of fruits in the incompatible
interaction during the early fungal infection
process. Sequence comparison showed that
PepCYP protein shared highest homology to the
CYPs.ch from a Solanum Chacoense line rich in
glycoalkaloids (Hutvagner et al., 1997).
There are four distinct cDNAs such as:
Shpx2, Shpx5, Shpx6, Spx12 isolated from a
cDNAs library of S. humilis contain deduced
amino acid sequence motifs characteristics of
peroxidases. The mRNAs of Shpx2 and Shpx6 but
not Shpx5, Shpx12 are also induced by wounding
(Harrison et al., 1994).
Gene involved in pathogenesis
CgRac1 gene is a major regulator of
asymmetric development of C. gloeosporioides
and encodes CgRac1 protein which is involved in
the regulation of morphogenesis, nuclear division
and pathogenic germination. CgRac1 protein is
abundant in conidia and hyphal tips (Nesher et al.,
2011). During plant infection, C.
gloeosporioides produces high level of IAA in
axenic culture. CgOPT1 gene is necessary for full
virulence and its expression can be enhanced by
addition of IAA (auxin). CgOPTI gene encode a
protein contains 752 amino acids and has mass
of 84.9 kDa and pI of 8.89. The gene includes
three exons separated by two introns of 58 and
73 bp. In resting spores the expression of
CgOPT1 is very low and enhanced in spore
germination and reduced again in mycelia
development (Chague et al., 2009).
There are several nitrogen-metabolism
genes such as: GDH2, GS1, GLT, and MEP are
differentially expressed during colonization by
C. gloeosporioides and induces ammonia
accumulation and pathogenicity (Miyara et al.,
2012). Bcl-2 protein is observed in C.
gloeosporioides and its expression determine the
programmed cell death and fungal development.
There are two Bcl-2 proteins such as: Bax protein
and anti-apoptotic bcl-2 protein. The Bax protein
expression leads to apoptotic-like cell death,
while expression of the anti-apoptotic Bcl-2
protein leads to prolonged cell longevity and
protected the fungus from stresses. In short these
two proteins expression cause drastic changes in
processes such as mycelium growth, conidia
production, conidial germination, and fungal
pathogenicity (Barhoom and Sharon, 2007).
C. gloeosporioides requires copper at
the initial stages of pathogenesis, germination and
the CgCTR2, a putative vacuolar copper
transporter involved in regulating cellular copper
balance during the process. This transporter is
highly expressed in resting spores (Barhoom et
al., 2008).
C. gloeosporioides expressed Pel-1 and
Pel-2 during infection to host. These genes
encodes for pectic lyase activity began at the end
of the biotrophic phase and increased in the
necrotrophic phase of infection. Initial pH
condition and carbon sources affects the
expression of Pel-1 and Pel-2. The expression
of these genes are higher in MCWE (mallow cell
wall extract) broth than in any other broths or
MCWE is better inducer for the expression of
Pel-1 and pel-2 (Shih et al., 2000).
Cap20 gene is expressed during
appressorium formation induced by host signal
in C. gloeosporioides. This gene encode 183
amino acid polypeptide and plays significant role
in infection to host. The Cap20 expression was
observed by a sensitive reverse transcriptase PCR
method (Chilly et al., 1998) in the various layers
of the fruit as infection proceeded into the fruit.
The mpg1 gene from Magnaporthe grisea is
involved in appressorium formation (Talbot et al.,
8
1993) and did not show any homology with
Cap20. There are two pectin lyase genes, Pnl-1
and Pnl-2 cause infection to host. Pnl-1 encode a
cellulose binding domain (CBD), which is
common in cellulases and xylanases, where as
Pnl-2 encodes a pectin lyase that lacks a CBD.
The expression of Pnl-2 gene is observed in the
necrotrophic phase of infection and expression
of Pnl-1 is observed in both nectrotrophic and
biotrophic phase of infection. Glucose affects the
expression of these genes and expression of Pnl-
2 is relatively low during infection, because it may
be more sensitive to catabolite repression (Wei
et al., 2002).
Chip 6 gene encodes a protein with
homology to sterol glycosyl transferase and
induced by hard surface contact of the conidia of
C. gloeosporioides and encodes a protein with
homology to sterol glycosyl transferase. This
transferase plays an important role in
pathogenesis and involved in conidial
germination, appressorium formation (Kim et al.,
2002). CgDN3 gene of C. gloeosporioides
plays an important role in pathogenesis and
required to avert a hypersensitive-like response
by a compatible host. This gene is induced by
nitrogen starvation in axenic culture and is
expressed at the early stages of infection. The
gene encodes a protein of 74 amino acids that
contains a predicted 18 amino acid signal
sequence for secretion of a basic 54 amino acid
mature protein with weak homology to an internal
region of plant wall-associated receptor kinases
(Stephenson et al., 2000).
CgDN24 gene encodes cDNA and is
induced by nitrogen starvation in axenic culture.
The cDNA comprises of 905 bp and predicted a
215 amino acids protein. CgDN24 gene plays no
role in pathogenesis and is necessary for normal
hyphal development in axenic culture (Stephenson
et al., 2005). Table 1 demonstrates the current
status of known genes involved in pathogenesis
of C. gloeosporioides and host defense.
Infection in Humans
C. gloeosporioides is very rare pathogen
in humans but there are few cases have been
reported:
A patient of 56 years age, developed a
subcutaneous nodule of left fore arm and elbow
after traumatic injury. Numerous irregularly
shaped, hyaline, septate, branched hyphae were
observed throughout the tissue. When these
hyphae get cultured on PDA and Sabouraud’s
glucose agar, fungus grew. Finally it was identified
as C. gloeosporioides (Guarro et al., 1988).
A patient of 82 years old was suffering
from myelodysplastic syndrome and after
contract surgery of left eye, patient developed
fungal kerratitis. When corneal of patient cultured
on media, it grew well and identified as C.
gloeosporioides (Mitani et al., 2009).
Management of Colletotrichum gloeosporioides
Non-chemical control
Non-chemical control involves the
effective dips of infected plant or crop in hot
water having temperature around 480C for
approximately 20 minutes. This method is not that
much effective to eliminate infection of C.
gloeosporioides completely.
Chemical control
Chemical method involves the use of
fungicide spray in orchard having infected plants
or crops present. Fungicide spray was not
recommended in rainy season. Fungicide spray
applies at the interval of 14-28 days in the orchard
is an effective control of this pathogen.
There are various types of fungicides
used such as: post-harvest and pre-harvest. Post-
harvest fungicide generally used as spray or dips
to those crops which are already infected with C.
gloeosporioides. This method is employed to
those fruits and crops which are shipped to
overseas market (Dickman, 1993).
There are various fungicides which are
used as pre-harvest fungicides e.g. copper
hydroxide, mancozeb, and copper sulfate products
(these are routinely used from flowering through
to harvest). Prohloraz fungicide is used when
weather conditions favours the infection of C.
gloeosporioides (Dirou and Stovold, 2005).
Azoxystrobin is one of the strobilurin
class fungicide was evaluated both in vitro and in
vivo conditions. Azoxystrobin completely inhibit
mycelia growth. Azoxystrobin at 1, 2 and 4 ml/l
suppressed the development of both panicle and
leaf anthracnose. Sundravadana et al., 2006
observed total control of mango anthracnose with
azoxystrobin.
9
CONCLUSION
Anthracnose disease caused by
Colletotrichum gloeosporioides is a major cause
of concern among farmers not only in India but
around the world as it causes huge pre and post
harvest looses to a number of fruit and vegetable
crops. The only method to control anthracnose is
by timely fungicide spray, which also raises
environmental and health concerns. Another way
is to use varieties resistant against the infection
caused by C. gloeosporioides. In order to devise
effective control measures the importance of
better understanding about the mechanism of
Collecotrichum infection has been felt and as a
result of that a number of genes involved in
Colletotrichum pathogenesis and host defense
has been worked out. But still a lot of work needs
to be done before any environment friendly and
consistent control strategy to come into
existence. The use of mycoviruses to control
fungal infection has been proposed recently for a
number of fungal diseases but it has never been
worked out in case of anthracnose pathogen
Colletotrichum. The study on mycoviruses
infecting Colletotrichum is also need of the time
as it has lot of potential for being an environment
friendly method for fungal disease control.
ACKNOWLEDGEMENT
The authors would like to thank Prof. P.
K. Khosla, Hon’ble Vice-Chancellor, Shoolini
University of Biotechnology and Management
Sciences, Solan and Foundation for Life Sciences
and Business Management (FLSBM), Solan for
providing financial support and necessary
facilities.
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... The optimum temperature for germination and infestation of conidia is approximately 25-30 °C with moisture and pH 5.8-6.5 [32]. This condition is crucial at the beginning of infection and is generally critical for the successful development of C. gloeosporioides [33]. ...
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... One of the diseases with greatest economic importance in mango (Mangifera indica L.) farming is anthracnosis or cankers, caused by the fungus Colletotrichum gloeosporioides (Sharma and Kulshrestha, 2015). During postharvest, this disease appears as small, rounded lesions, brown to black in color, with undefined outlines that are slightly sunken into the fruit's flesh. ...
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Fungal endophytes associated with leaves of the endemic plant Cordemoya integrifolia have been studied. The diversity and frequency of endophytic fungi in young and old leaves of Cordemoya integrifiola occurring inside and outside the Maccabhé Conservation Management Area (CMA) were investigated. Endophyte assemblages examined were quite diverse, consisting of 26 fertile fungal taxa and one sterile morphospecies. Pestalotiopsis sp. and Penicillium sp. were the dominant taxa. Differences were observed between the endophytic communities isolated from different tissues and tissues of different ages. Old leaves supported more endophytes than relatively younger ones. Likewise, more endophytic fungi were recorded in the veins and petioles than in the intervein tissues.
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Fungal endophytes associated with leaves of the endemic plant Cordemoya integrifolia have been studied. The diversity and frequency of endophytic fungi in young and old leaves of Cordemóya integrifiola occurring inside and outside the Maccabhé Conservation Management Area (CMA) were investigated. Endophyte assemblages examined were quite diverse, consisting of 26 fertile fungal taxa and one sterile morphospecies. Pestalotiopsis sp. and Penicillium sp. were the dominant taxa. Differences were observed between the endophytic communities isolated from different tissues and tissues of different ages. Old leaves supported more endophytes than relatively younger ones. Likewise, more endophytic fungi were recorded in the veins and petioles than in the intervein tissues.