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Published online on: 18-12-2015
Meenakshi Sharma and Saurabh Kulshrestha*
Shoolini University of Biotechnology and Management Sciences, Bajhol, Solan, Himachal Pradesh
ABSTRACT: 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 25-280C, 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.
KEYWORDS: Colletotrichum gloeosporioides; anthracnose; pathogenecity genesDownload this article as:
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Sharma M, Kulshrestha S. Colletotrichum gloeosporioides: An anthracnose causing pathogen of fruits and vegetables. Biosci Biotechnol Res Asia 2015;12(2)
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 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 25-280C 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).
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 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 μm 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, 25-280 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 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 appear 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 act 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. 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). 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 degrade 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 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 induce 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 encode 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 play 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., 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 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 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.
Table 1: Showing various genes involved in host defense as well as in pathogenesis of Colletotrichum gloeosporioides
|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||CgDN3 protein (Stephenson et al., 2000)|
|5||Chip 6||Pathogenesis, 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 development||Stephenson et al., 2005|
|9||Bcl-2||Apoptosis, mycelium, conidia, germination, pathogenesis||Bax and antiapoptotic protein (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 growth||CgOPT1protein (Chague et al., 2009)|
|13||CgRac1||Morphogenesis, nuclear division, pathogenesis||CgRac1 protein (Nesher et al., 2011)|
|14||GDH2,GS1,GLT,MEP||Induce ammonia accumulation, pathogenesis||GDH2,GS1,GLT,MEP proteins (Miyara et al., 2012)|
|15||PacC||Create alkalinize environment and regulate activity of several genes||Pac C protein (Alkan et al., 2013)|
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.
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.
- Adelusi, A.A. and Lawanson, A.O. Disease induced changes in carotenoid content of edible yam (Dioscorea ) infected by Botryodiplodia theobrontae and Aspergillus niger. Mycopathologia., 1987;98:49-58.
- Agwana, C.O., Lashermes, P., Trouslot, P., Combes, M. and Charrier, A. Identification of RAPD markers for resistance to coffee berry disease, Colletotrichum kahawae, in arabica coffee. Euphytica., 1997; 97:241-248.
- Alahakoon, P.W., Brown, A.E. and Sreenivasaprasad, S. Cross infection potential of genetic groups of Colletotrichum gloeosporioides tropical fruits. Physiol. Mol Plant Pathol., 1994;44:93-103.
- Alkan, N., Meng, X., Friedlander, G., Reuveni, E., Sukno, S., Sherman, A., Thon, M., Fluhr, R., Prusky, D. Global aspects of pacC regulation of pathogenicity genes in Colletotrichum gloeosporioides as revealed by transcriptome analysis. Mol Plant Microbe Interact., 2013;26(11) 1345-58.
- Amusa, A.N., Ikotun, T. and Bankole, J.O. Short communication: Survey of leaf spot-causing microorganisms on yam. African Crop Science Journal., 1996; 4(1):111-113.
- Amusa, N.A., Ashaye, O.A., Oladapo, M.O., and Oni, M.O. Guava fruit anthracnose and the effects on its nutritional and market values in Ibadan, World J Agric Sci., 2005;1:169-172.
- Arauz, L.F., Wang, A., Duran, J.A. and Monterre, M. Causes of post harvest losses of mango at the wholesale market level in Costa Rica. Agronomia Costarricense., 1994;18(1):47-51.
- Arauz, L.F. Mango anthracnose: Economic impact and current option for integrated management. Plant disease., 2000;86(6):600-611.
- Bailey, J.A. and Jeger, M.J. Colletotrichum: Biology, Pathology and Control. Wallingford., UK: CAB international., 1992;388
- Barbosa, M.P.M. 2001. Variabilidade patogênica de Colletotrichum graminicola isolado de milho (Zea mays ). Master’s dissertation, Escola Superior de AgriculturaLuiz de Queiroz, Piracicaba.
- Barhoom, S. and Sharon, A. cAMP regulation of “pathogenic” and “saprophytic” fungal spore germination. Fungal Genet Biol., 2004;41:317–326.
- Barhoom, S., Kupiec, M., Zhao, X., Xu, J.R. and Sharon, A. Functional characterization of cgCTR2, a putative vacuole copper transporter that is involved in germination and pathogenicity in Colletotrichum gloeosporioides. Eukaryotic Cell., 2008;7(7):1098.
- Barhoom, S. and Sharon, A. Bcl-2 proteins link programmed cell death with growth and morphogenetic adaptations in the fungal plant pathogen Colletotrichum gloeosporioides. Fungal genetics and biology., 2007;44:32-43.
- Baxter, Alice P, G.C.A Van Der Westhuizen, and Eicker A. A review of literature on the taxonomy, morphology, and biology of the fungal genus Colletotrichum. Phytophylactica., 1985; 17:15-18.
- Binyamini, N. and Nadel, M.S. Latent infection in avocado fruit due to Colletotrichum gloeosporioides. Phytopathology., 1972;62:592–594.
- Bitancounrt, A.A. Anthracnose of mango. Biologia., 1938; 4:43-45.
- Bose, S.K., Sindhan, G.S. and Pandey, B.N. Studies on the die back disease of mango in the Tarai region of Kumaon. Progressive Horticulture., 1973;5:41-53.
- Butler, E.J. Fungi and diseases in plants. Thacker Spink & Co, Calcutta and Simla, India., 1918; 547.
- CAB International, 2005. Crop protection Compendium, 2005 Edition. Wallingford, U.K: CAB International. cabicompendium.org/cpc.
- Cannon, P.F. and Simmons, C.M. Diversity and host preference of leaf endophytic fungi in the Iwokrama Forest Reserve, Guyana. Mycologia., 2002;94:210-220.
- Cannon, P.F., Bridge, P.D. and Monte,E. Linking the past, present and future of Colletotrichum In: Colletotrichum – Host Specificity, Pathology and Host-Pathogen Interaction (eds D Prusky, S Freeman, MB Dickman). APS Press, St Paul, Minnesota., 2000;1–20.
- Cardin, P.P. Annual report of the mango in Cuba. The Cuba Review., 1910; 8(5):28-29.
- Chague, V., Maor, R. and Sharon, A. CgOpt1, a putative oligopeptide transporter from Colletotrichum gloeosporioides that is involved in responses to auxin and BMC Microbiology., 2009; 9:173.
- Chakraborty, S. and Datta, S. How will plant pathogens adapt to host plant resistance at elevated CO2under a changing climate. New Phytologist., 2003;159: 733–742.
- Chilly, J., Kaplan, J.C., Gantron, S., and Kahn, A. Transcription of the dystrophin gene in human muscle and non-muscle tissues. Nature., 1988;333:858-860.
- Chitkara, S., Singh, T. and Singh, D. Histopathology of Colletotrichum dematium infected chilli seeds. Acta Botanica Indica., 1990;18:226–230.
- Choi, O., Choi, O., Kwak, Y.S., Kim, J. and Kwon, J.H. Spot Anthracnose Disease Caused by Colletotrichum gloeosporioideson Tulip Tree in Korea. Mycobiology., 2012;40(1):82–84.
- Collins, G.N. The mango in Puerto rico. U.S.D.A. Pl. Ind. Bull., 1903:28.
- Coursey, D.G. Yam storage I. A review of storage practices and information on storage losses. Stored Product Res., 1967;2:227-244.
- Darvas, J.M. and Kotze, J.M. Avocado fruit diseases and their control in South Africa. South African Avocado Growers’ Association Yearbook., 1987;10:117-119.
- Davis, R.D., Irwin, J.A.G., Cameron, D.F. and Shepherd, R.K. Epidemiological studies on the anthracnose diseases of Stylosanthes caused by C. gloeosporioides in North Queensland and pathogenic specialization within the natural fungal populations. Australian Journal Agriculture Research., 1987;38:1019-1032.
- Denoyes-Rothan, B., Guerin, G., Delye, C., Smith, B., Maymon, M. and Freeman, S. Genetic diversity and pathogenic variability among isolates of Colletotrichum species from strawberry. Phytopathology., 2003;93:219–228.
- Dickman, M. B., and Alvarez, A. M. Latent infection of papaya caused by Colletotrichum gloeosporioides. Plant Dis., 1983;67:748-750.
- Dickman, M.B. 1993. Plant disease pathogen- Colletotrichum gloeosporioides. Crop Knowledge Master, 1993 (cited 22 april 2004).http://www.extento.hawaii.edu/kbase/crop.
- Dinh, S.Q., Chongwungse, J., Pongam, P. and Sangchote, S. Fruit infection by gloeosporioides and anthracnose resistance of some mango cultivars in Thailand. Australian plant pathology., 2003;32:533-538.
- Dirou, J. and Stovold, G. 2005. Fungicide management program to control mango anthracnose. Prime fact
- Dodd, J.C., Estrada, A.B., Matcham, J., Jeffries, P. and Jeger, M.J. The effect of climatic factors on Colletotrichum gloeosporioides, causal agent of mango anthracnose, in the Philippines. Plant Pathology., 1991;40:568-575.
- Doidge, E.M. Black spot of mangoes. Farming South Africa., 1932;7:89-91.
- Drori, N., Haimovich, H.K., Rollins, J., Dinoor, A., Okon, Y., Pines, O. and Prusky, D. External pH and Nitrogen Source Affect Secretion of Pectate Lyase by Colletotrichum gloeosporioides. Appl. Environ. Microbiol., 2003;69(6):3258.
- Fagan, H.J. Strains of Colletotrichum gloeosporioides on citrus in Belize. Br. Mycol .Soc., 1980;74:643-644.
- Fawcett, H.S. Bloom blight (Gloeosporium mangiferae). Florida Agriculture Experimentation Station Report., 1907;25.
- Fitzell, R.D. Epidemiology of anthracnose disease of avocados. South African Avocado Growers Association Yearbook., 1987;10:113 -116
- Freeman, S. and Katan, T. Identification of Colletotrichum species responsible for anthracnose and root necrosis of strawberry in Israel. Phytopathology., 1997;87:516-521.
- Freeman, S., Katan, T. and Shabi, E. Characterization of Colletotrichum gloeosporioides isolates from Avocado and Almond Fruits with Molecular and Pathogenicity Tests. Applied and environment microbiology., 1995;62(3):1014–1020.
- Freeman, S., Katan, T. and Shabi, E. Characterization of Colletotrichum species responsible for anthracnose diseases of various fruits. Plant Disease., 1998;82:596-605.
- Freeman, S., Minz, D., Maymon, M. and Zveibil, A. Genetic diversity within Colletotrichum acutatum sensu Simmonds. Phytopathology., 2001;91: 586–59.
- Giblin, F. and Coates, L. Avocado fruit responses to Colletotrichum gloeosporioides (Penz) sacc. Proceedings VI World Avocado Congress (Actas VI Congreso Mundial del Aguacate)., 2007.
- Guarro, J., Svidzinski, T.E., Zaror, L., Forjaz, M.H., Gene, J. and Fischman, O. Subcutaneous hyalohyphomycosis caused by Colletotrichum gloeosporioides. Journal of Clinical Microbiology., 1998;36: 3060-3065.
- Gunnell, P.S. and Gubler, W.D. Taxonomy and morphology ofColletotrichum species pathogenic to strawberry. Mycologia., 1992;84(2):157–165.
- Gupta, S.K., Jarial, K. and Kansal, S. Colletotrichum gloeosporioides causing anthracnose in bell pepper seed crop. Journal of Plant Disease Science., 2009;4:126-127.
- Harrison, S.J., Curtis, M.D., Mclntyre, C.L., Maclean, D.J. and Manners, J.M. Differential expression of peroxidase isogenes during the early stages of infection of the tropical forage legume Stylosanthes humilis by Colletotrichum gloeosporioides. The American Phytopathological society. 1994;8(3):398-406.
- Hartill, W.F.T. Post-harvest rots of avocado in New Zealand and their control. Brighton crop protection conference., 1992;1157-67.
- Higgins, J.E. The mango in Hawaii. Agriculture Experimentation Station Bulletin., 1906;12.
- Howard, C.M. and Albregts, E.E. Anthracnose of strawberry fruit caused by Glomerella cingulata in Florida. Plant Dis., 1984;68:824-825.
- Howard, C.M., Maas, J.L., Chandler, C.K. and Albregts, E.E. Anthracnose of strawberry caused by the Colletotrichum complex in Florida. Plant Dis., 1992;76:976-981.
- Hsiang, T. and Goodwin, P.H. Ribosomal DNA sequence comparisons of Colletotrichum graminicola from turf grasses and other hosts. European Journal of Plant Pathology., 2001;107: 593–599.
- Hutvagner, G., Barta, E. and Banfalvi, Z. Isolation of sequence analysis of a cDNA and related gene for cytochrome P450 proteins from Solanum chacoense. Gene ., 1997;188:247-252.
- Jeffries, P., Dodd, J.C., Jeger, M.J. and Plumbley, R.A. The biology and control of Colletotrichum species on tropical fruit crops. Plant Pathology., 1990;39:343-366.
- Jeger, M.J., Eden-Green, S., Johanson, , Waller, J.M. and Brown, A.E. Banana diseases. In: Banana and Plantains (ed. S. Gowen). Chapman and Hall, London, UK., 1995;317-381.
- Ji, Z.P. and Guo, S.X. 1992. The occurrence characteristics of camellia anthracnose and its control. Shanxi Forest Science Technology., 1992;4:70-71.
- Kim, Y.K., Wang, Y.H., Liu, Z.M. and Kolattukudy, P.E. Identification of a hard surface contact induced gene in Colletotrichum gloeosporioides conidia as a sterol glycosyl transferase, a novel fungal virulence factor. The Plant Journal., 2002;30(2):177-187.
- Kramer-Haimovich,H., Servi, E., Katan, T., Rollins,J., Okon, Y. and Prusky, D. Effect of Ammonia Production by Colletotrichum gloeosporioides on pelB Activation, Pectate Lyase Secretion, and Fruit Pathogenicity. Environ. Microbiol., 2006;72(2):1034.
- Kulkarni, S., Benagi, V.I., Patil, P.V., Hegde, Y., Konda, C.R., and Deshpande, V.K. Sources of resistance to anthracnose in green gram and biochemical parameters for resistance. Karnataka J. Agric. , 2009;22:1123-1125.
- Kumar, D.S.S. and Hyde, K.D. Biodiversity and tissue recurrence of endophytic fungi in Tripterygium wilfordii. Fungal Diversity., 2004;17:69-90.
- Latinovic, J. and Vucinic, Z. Cultural characteristics, pathogenicity and host range of Colletotrichum gloeosporioides isolated from olive plants in Montenegro. Acta Hotriculturae (ISHS)., 2002;586:753-755.
- Lee, H.T. and Chung, H.S. Detection and transmission of seed-borne Colletotrichum gloeosporioides in red pepper, Capsicum annuum. Seed Sci. & Technol., 1995;23:533-541.
- Lenne, J.M. Colletotrichum disease in legumes. In: Colletotrichum – Biology, Pathology and Control (eds. J.A. Bailey and M.J. Jeger). CAB International, Wallingford, UK., 1992;134-166.
- Li, H.Y. and Zhang, Z.F. First Report of Colletotrichum gloeosporioides Causing Anthracnose Fruit Rot of Trichosanthes kirilowii in China. The American Phytopathological Society., 2007;91(5): 63.
- Lu, G.Z., Cannon, P.F., Reid, A. and Simmons, C.M. Diversity and molecular relationships of endophytic Colletotrichum isolates from the Iwokrama Forest Reserve, Guyana. Mycological Research., 2004;108:53-63.
- MacLean, D.J., Braithwaite, K.S., Manners, J.M. and Irwing, J.A.G. How do we identify and classify fungal pathogens in the era of DNA analysis. Advances In Plant Pathology., 1993; 10:207-244.
- Manandhar, J.B., Hartman, G.L. and Wang, T.C. Anthracnose development on pepper fruits inoculated with Colletotrichum Plant Disease., 1995;79:380-383.
- Martinez-Culebras P.V., Barrio, E., Garcia, M.D. and Querol, A. Identification of Colletotrichum species responsible for anthracnose of strawberry based on the internal transcribed spacers of the ribosomal region. Fems Microbiol. Lett., 2000;189:97-101.
- Martinez-Culebras, P.V., Querol, A., Suarez-Fernandez, M.B., Garcia-Lopez, M.D., Barrio, E. Phylogenetic relationships among Colletotrichum pathogens of strawberry and design of PCR primers for their identification. Journal of Phytopathology., 2003;151: 135–174.
- Masyahit, M., Sijam, K., Awang,Y. and Satar, M.G.M. The First Report of the Occurrence of Anthracnose Disease Caused by Colletotrichum gloeosporioides (Penz.) Penz. &Sacc. on Dragon Fruit (Hylocereus) in Peninsular Malaysia. Am. J. Applied Sci., 2009;6: 902-912.
- Mitani, A., Shiraishi, A., Uno, H.M., Haray, M.Y. and Ohashi, Y. Invivo and invitro investigations of fungal keratitis caused by Colletotrichum gloeosporioides. Jocul Pharmacol Ther., 2009;6:563-564.
- Miyara, C., Shnaiderman, X., Meng, X., Vargas, W.A., Diaz-Minguez, J.M., Sherman,A., Thon, M. and Prusky, D. 2012. Role of Nitrogen-Metabolism Genes Expressed During Pathogenicity of the Alkalinizing Colletotrichum gloeosporioides and Their Differential Expression in Acidifying Pathogens. The American Phytopathological Society., 2012;25(9):1251-1263.
- Mordue, J.E.M. Colletotrichum coccodes. CMI Descriptions of Pathogenic Fungi and Bacteria., 1967;131.
- Mori, T. Effects of temperature as the selection pressure for resistance to anthracnose crown rot (Glomerella cingulata Spaulding et Schrenk) of young strawberry seedlings. J Jpn Soc Hortic Sci., 1998;67:934-938.
- Munch,S., Lingner, U., Floss, D.S., Ludwig, N., Sauer, N. and Deising, H.B. 2008. The hemibiotrophic lifestyle of Colletotrichum Journal of Plant Physiology., 2008;165:41-51.
- Nelson, S.C. Mango anthracnose (Colletotrichum gloeosporioides).Plant disease., 2008;48.
- Nesher, I., Kokkelink, A.M.L., Tudzynski, P. and Sharon, A. Regulation of Pathogenic Spore Germination by CgRac1 in the Fungal Plant Pathogen Colletotrichum gloeosporioides. Eukaryotic Cell., 2011;10:1122-1130.
- Nguyen, T. H. P., Torbjorn, S., Bryngelsson, T. and Liljeroth, E. Variation among Colletotrichum gloeosporioides isolates from infected coffee berries at different locations in Vietnam. Plant Pathology., 2009;58 (5):898-909.
- Oh, B. J., Kim, K. D. and Kim, Y. S. Effect of cuticular wax layers of green and red pepper fruits on infection by Colletotrichum gloeosporioides. J Phytopathology ., 1999;147:547-552.
- Palo, M.A. Sclerotium seed rot and seedling stem rot of mango. The Philippines Journal Science., 1932;52(3):237-261.
- Pandey, A. Variability studies and molecular characterization of Colletotrichum gloeosporioides causing anthracnose of mango. D. thesis, A.P.S. University, Rewa, M.P. India., 2011.
- Penzig, A.G.O. Fungi agrumicoli Contribuzioneallo studio deifunghi parassiti degliagrumi. , 1882;2:385–508.
- Peterson, R.A. Mango diseases. In: Proceedings of the CSIRO 1st Australian Mango Research Workshop,CSIRO, Cairns., 1986;233-247.
- Photita, W., Lumyong, S., Lumyong, P. and Hyde, K.D. 2001. Fungi on Musa acuminatain Hong Kong. Fungal Diversity., 2001;6:99-106.
- Photita, W., Lumyong, S., Lumyong, P., Mckenzie, E.H.C. and Hyde, K.D. Are someendophytes of Musa acuminate latent pathogens? Fungal Diversity., 2004;16:131-140.
- Photita, W., Taylor, P., W. J, Ford, R., Hyde, K.D. and Lumyong, S. Morphological and molecular characterization of Colletotrichum species from herbaceous plants in Thailand. Fungal Diversity., 2005;18:117-133.
- Ploetz, C.R.L. and Prakash, O. 1997. Foliar, floral and soil borne diseases. In: The Mango (eds. Litz, R.E). CAB,International, Wallingford, UK., 1997;281-325.
- Ponte, J.J. da. Clinica de doencas de plantas. Fortaleza-CE: UFC., 1996; pp 871.
- Promputtha, I., Lumyong, S., Lumyong, P., McKenzie, E.H.C. and Hyde, K.D. Fungal succession on senescent leaves of Manglietia garrettiion Doi Suthep-Pui National Park, northern Thailand. Fungal Diversity., 2002;10:89-100.
- Prusky, D. and Saka, H. The role of epicuticular wax of avocado fruit in appressoria formation of Colletotrichum Phytoparasitica., 1989;17:140.
- Prusky, D. and Plumbley, R.A. Quiescent Infections of Colletotrichum in Tropical and Subtropical Fruits. In: Bailey JA, Jeger MJ, editors. Colletotrichum: Biology, Pathology, and Control. Wallingford: CAB International., 1992;289–307.
- Prusky, D., Plumbley, R.A. and Kobiler, The relationship between antifungal diene levels and fungal inhibition during quiescent infection of unripe avocado fruits by Colletotrichum gloeosporioides. Plant Pathol., 1991;40: 45-52.
- Sanders, G.M., Korsten, L. and Wehner, F.C. Market survey of post harvest diseases and incidence of Colletotrichum gloeosporioideson avocado and mango fruit in South Africa. Tropical 11:155-160.Science., 2000;40(4):192-198.
- Sanders, GM. and Korsten, L. Comparison of cross inoculation potential of South African avocado and mango isolates of gloeosporioides. Res., 2003;158:143-150.
- Santoso, U., Kubo, K., Ota, T., Tadokoro, T. and Maekawa, A. Nutrient composition of kopyor coconut (Cocos nucifera L.). Food Chemistry., 1996;57:299-304.
- Sattar, A. and Malik, S.A. Some studies on anthracnose of mango caused by Glomerella cingulata (Stonem.) Spauld. Sch. (Colletotrichum gloeosporioides ). India Journal Agriculture Science., 1939;1:511-521.
- Schrenk, H. and Spaulding, P. 1903. The bitter rot of apple. Science New York., 1903;17:750-751.
- Shabi, E. and Katan, T. Occurrence and control of anthracnose of almond in Israel. Plant Dis., 1983;67:1364–1366.
- Shane, W. W. and Sutton, T. B. Germination, appressorium formation, and infection of immature and mature apple fruit by Glomerella Phytopathology., 1981;71:454-457.
- Sharma, I.M., Raj, H., Kaul, J.L. and Raj, H. Studies on post harvest diseases of mango and chemical control of stem end rot and anthracnose. Indian Phytopathology., 1994;47(2):197-200.
- Sherriff, C., Whelan, M.J., Arnold, G.M., Lafey, J., Brygoo, Y., Bailey, J.A. Ribosomal DNA sequence analysis reveals new species groupings in the genus Colletotrichum. Experimental Mycology., 1994;18:121–38.
- Shih, J.,Wei, Y. and Goodwin, P.H. A comparison of the pectate lyase genes, pel-1 and pel-2, of Colletotrichum gloeosporioides f.sp. malvae and the relationship between their expression in culture and during necrotrophic infection. Gene., 2000;243(1-2):139-50.
- Simmonds, J.H. A study of the species of Colletotrichum causing ripe fruit rots in Queensland. Queensland Journal of Agriculture and Animal Science., 1965;22:437-459.
- Sivanathan, S. and Adikaram N.K.M. Biological activity of four antifungal compounds in immature avocado. Journal of Phytopathology ., 1989;125:97-109.
- Slade, S.J., Harris, R.F., Smith, C.S. and Andrews, J.H. 1987. Microcycle conidiation and spore carrying capacity of gloeosporioides on solid media. Applied and Environmental Microbiology., 1987;53, 2106-2110.
- Smith, B. J. and Black, L.L. Resistance of strawberry plants to Colletotrichum fragariae affected by environmental conditions. Plant Dis., 1987;71:834-837.
- Smith, B.J. and Black, L.L. Morphological, cultural and pathogenic variation among Colletotrichum species isolated from strawberry. Plant Disease., 1990;74: 69-76.
- Sonoda,R.M. and Pelosi, R.R. Characteristics of Colletotrichum gloeosporioides from lesions on citrus blossoms in the Indian River area of Florida. Fla. State Hortic. Soc., 1988;101:36-38.
- Sreenivasaprasad, S., Mills, P.R., Meehan, B.M., Brown, A.E. Phylogeny and systematics of 18 Colletotrichum species based on ribosomal DNA spacer sequences. Genome., 1996;39: 499–512.
- Stephenson, S.A., Stephenson, C.A., Maclean, D.J. and Mauners, J.M. CgDN24, A gene involved in hyphal development in the fungal phytopathogen Colletotrichum gloeosporioides. Microbiological Research., 2005;160 (4, 5):389-397.
- Stephenson, S.A., Hatfield, J.T., Rusu, A.G., Maclean, D.J. and Manners, J.M. 2 CgDN3: An essential pathogenicity gene of Colletotrichum gloeosporiodes necessary to avert a hypersensitive-like response in the host Stylosanthes guianensis. Molecular plant microbe interactions., 2000;13(9):929-941.
- Stevens, F.L. and Pierce A.S. Fungi from Bombay. Indian Journal Agriculture Science., 1933;3:912-916.
- Sundravadana, S., Alice, D., Kuttalam, S. and Samiyappan, R. Control of Mango Anthracnose by Azoxystrobin. Tunisian Journal of Plant Protection., 2006;1:109-11
- Sutton, B.C. The genus Glomerella and its anamorph Colletotrichum. In Colletotrichum: biology, pathology and control (eds. J.A. Bailey and M.J. Jeger). CAB International: Wallingford., 1992;1-26.
- Sutton, T. B. 1990. Bitter Rot. Pages 15-16 in: Compendium of Apple and Pear Diseases, (A.L. Jones and H. S. Aldwinckle, eds.) American Phytopathological Society, St. Paul, MN.
- Talbot, N.J., Ebbole, D.J. and Hamer, J.E. ldentification and characterization of MPG7, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea. Plant Cell., 1993;5:1575-1590
- Tang, A.M.C., Hyde K.D. and Corlett, R.T. Diversity of fungi on wild fruits in Hong Kong. Fungal Diversity., 2003;14:165-185.
- Taro, R.A. 1929. Plant disease notes from the Central Andes. Phytopathology., 1929;19: 969-974.
- Timmer, L.W., Brown, G.E., Zitko, S.E. The role of colletotrichum spp. In post harvest anthracnose of citrus and survival of C. acutatum on fruit. Plant disease., 1998;82.
- Toofanee, S.B. and Dulymamode, R. Fungal endophytes associated with Cordemoya integrifolia. Fungal Diversity., 2002;11:169-175.
- Traub, H.T. and Robinson, T.T. Improvement of subtropical fruit other than citrus. USDA bull., 1938;1589:77.
- Von Arx J.A. Die Arten der Gattung Colletotrichum Phytopath Zeitschrift., 1957;29:414-468.
- Wei, Y., Shih, J., Li, J. and Goodwin, P.H. Two pectin lyase genes, pnl-1 and pnl-2, from Colletotrichum gloeosporioides sp.malvae differ in a cellulose-binding domain and in their expression during infection of Malva pusilla. Microbiology., 2002;148:2149-2157.
- Wester, P.J. The Phillippines Island, Bureau of Agriculture Bulletin., 1911;18:60.
- Xiao, C.L., MacKenzie, S.J. and Legard, D.E. Genetic and pathogenic analyses of Colletotrichum gloeosporioides from strawberry and non cultivated hosts. Phytopathology., 2004; 94:446-453.
- Yakoby, N., Moualem, D.B., Keen, N.T., Dinoor, A., Pines, O. and Prusky, D. Colletotrichum gloeosporioides, Pel-B is an important virulence factor in avocado fruit- fungus interaction. The American Phytopathological Society., 2001;14(8):988-995.
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