TYPE Review
PUBLISHED 24 August 2023
DOI 10.3389/fmicb.2023.1168203
Mango anthracnose disease: the 
OPEN ACCESS current situation and direction for 
EDITED BY
Lei Huang,  future research
Purdue University, United States
REVIEWED BY
Porfirio Gutierrez-Martinez,  Aboagye Kwarteng Dofuor 
1*, Naa Kwarley-Aba Quartey 2, 
Instituto Tecnológico de Tepic, Mexico  Angelina Fathia Osabutey 3, Akua Konadu Antwi-Agyakwa 4, 
Livio Torta,  
University of Palermo, Italy Kwasi Asante 5, Belinda Obenewa Boateng 5, 
*CORRESPONDENCE Fred Kormla Ablormeti 5, Hanif Lutuf 6, Jonathan Osei-Owusu 7, 
Aboagye Kwarteng Dofuor  
 akdofuor@uesd.edu.gh Joseph Harold Nyarko Osei 8, William Ekloh 9, Seyram Kofi Loh 10, 
RECEIVED 17 February 2023 Joseph Okani Honger 11, Owusu Fordjour Aidoo 1 and 
ACCEPTED 03 August 2023
24 August 2023 Kodwo Dadzie Ninsin 
1
PUBLISHED 
1
CITATION  Department of Biological Sciences, School of Natural and Environmental Sciences, University of 
Dofuor AK, Quartey NK-A, Osabutey AF, Environment and Sustainable Development, Somanya, Ghana, 
2 Department of Food Science and 
Antwi-Agyakwa AK, Asante K, Boateng BO, Technology, Faculty of Biosciences, College of Science, Kwame Nkrumah University of Science and 
3
Ablormeti FK, Lutuf H, Osei-Owusu J, Technology, Kumasi, Ghana,  Department of Agribusiness, School of Business, Presbyterian University, 
Abetifi-Kwahu, Ghana, 4Osei JHN, Ekloh W, Loh SK, Honger JO,  Entomology Division, Cocoa Research Institute of Ghana, Akim Tafo, Ghana, 
5
Aidoo OF and Ninsin KD (2023) Mango  Coconut Research Program, Oil Palm Research Institute, Council for Scientific and Industrial Research, 
anthracnose disease: the current situation and Sekondi-Takoradi, Ghana, 
6 Crop Protection Division, Oil Palm Research Institute, Council for Scientific 
direction for future research. and Industrial Research, Kade, Ghana, 
7 Department of Physical and Mathematical Sciences, School of 
Front. Microbiol. 14:1168203. Natural and Environmental Sciences, University of Environment and Sustainable Development, 
doi: 10.3389/fmicb.2023.1168203 Somanya, Ghana, 
8 Department of Parasitology, Noguchi Memorial Institute for Medical Research, 
College of Health Sciences, University of Ghana, Accra, Ghana, 9 Department of Biochemistry, School of 
COPYRIGHT Biological Sciences, College of Agriculture and Natural Sciences, University of Cape Coast, Cape Coast, 
© 2023 Dofuor, Quartey, Osabutey, Antwi- Ghana, 10 Department of Built Environment, School of Sustainable Development, University of 
Agyakwa, Asante, Boateng, Ablormeti, Lutuf, Environment and Sustainable Development, Somanya, Ghana, 11 Soil and Irrigation Research Centre, 
Osei-Owusu, Osei, Ekloh, Loh, Honger, Aidoo College of Basic and Applied Sciences, School of Agriculture, University of Ghana, Accra, Ghana
and Ninsin. This is an open-access article 
distributed under the terms of the Creative 
Commons Attribution License (CC BY). The Mango anthracnose disease (MAD) is a destructive disease of mangoes, with 
use, distribution or reproduction in other 
forums is permitted, provided the original estimated yield losses of up to 100% in unmanaged plantations. Several strains 
author(s) and the copyright owner(s) are that constitute Colletotrichum complexes are implicated in MAD worldwide. 
credited and that the original publication in this All mangoes grown for commercial purposes are susceptible, and a resistant 
journal is cited, in accordance with accepted 
academic practice. No use, distribution or cultivar for all strains is not presently available on the market. The infection can 
reproduction is permitted which does not widely spread before being detected since the disease is invincible until after a 
comply with these terms. protracted latent period. The detection of multiple strains of the pathogen in 
Mexico, Brazil, and China has prompted a significant increase in research on the 
disease. Synthetic pesticide application is the primary management technique 
used to manage the disease. However, newly observed declines in anthracnose 
susceptibility to many fungicides highlight the need for more environmentally 
friendly approaches. Recent progress in understanding the host range, molecular 
and phenotypic characterization, and susceptibility of the disease in several 
mango cultivars is discussed in this review. It provides updates on the mode 
of transmission, infection biology and contemporary management strategies. 
We suggest an integrated and ecologically sound approach to managing MAD.
KEYWORDS
mango disease, anthracnose, epidemiology, detection, host range, management 
strategies, Colletotrichum gloeosporioides
Frontiers in Microbiology 01 frontiersin.org
Dofuor et al. 10.3389/fmicb.2023.1168203
1. Introduction a country; for example, in the northeast of Brazil, where C. asianum, 
C. fructicola, C. tropicale, C. karstii, and C. dianesei are present (Lima 
Mango anthracnose disease (MAD) is a worldwide disease et al., 2013a,b) highlights the importance of this review. We also provide 
that is extremely destructive to mangoes before and after harvest. an update on the taxonomic status of the Colletotrichum taxa linked with 
The disease damages the infected mango trees, leading to low various MAD, which has changed since the introduction of 
yield and quality of fruits. MAD can cause a 100% loss of yield in molecular techniques.
orchards that are not well taken care of and where the 
environment is good for the disease to spread. The disease occurs 
in almost all regions that produce the crop, and its high economic 2. History and geographical 
losses have prompted a wealth of research focusing on distribution of mango anthracnose
postharvest  losses (Cheng et  al., 2022; Silué et  al., 2022), 
damage  (Wu et  al., 2022), characterization (Ismail and Globally, Colletotrichum species was first reported by Corda (1831). 
El-Ganainy, 2022), diagnosis and classification (Alberto et al., Since then, the disease has been infecting many crops and trees, 
2022; Patil et  al., 2022; Prabu and Chelliah, 2022), genomics including mangoes worldwide (Figure 1; Ciofini et al., 2022). MAD 
(Ciofini et al., 2022; Kumari et al., 2022), control (Evangelista- occurs in several countries, including Côte d’Ivoire, Ethiopia, Ghana, 
Martínez et  al., 2022; Liang et  al., 2022) and resistance Nigeria, South Africa in Africa; Australia in Oceania; Bangladesh, China, 
management (Janamatti et al., 2022). India, Indonesia, Taiwan in Asia; and Colombia, Mexico, and Peru in the 
The Colletotrichum species complex is responsible for the Americas. The disease mainly affects the leaves, tissues, peduncle, 
fungal disease known as MAD. Weir et  al. (2012) used pedicle, twig, stem, fruit, and pulp. Different species of MAD may 
morphological and molecular techniques to determine that be part of a complex or just a singleton, and these fungal infections have 
roughly twenty-two species and one subspecies make up the been reported in different countries. Members of the Colletoctrichum 
C. gloeosporioides complex. However, several C. gloeosporioides genus are the predominant pathogens that cause MAD. They are made 
isolates in various locations worldwide are characterized by up of about 200 species that are tentatively placed into 15 species 
characteristic black, expanding lesions on mango plant parts, complexes and singletons (Talhinhas et al., 2018; Guevara-Suarez et al., 
including fruits, leaves, flowers, petioles, twigs, and stems. Many 2022). Several mango species tolerant to anthracnose diseases have been 
of these isolates, including C. alienum, C. fructicola, C. siamense, determined through screening after inoculating these mango species 
C. tropicale, and C. asianum, have significantly damaged millions with Colletotrichum asianum (Grice et  al., 2022). Moreover, many 
of mango trees in Mexico, China, and India (Weir et al., 2012; Li working groups from different geographical regions or countries, such 
et  al., 2019; Tovar-Pedraza et  al., 2020). In the United  States, as Ethiopia and Nigeria, while studying the MAD distribution, 
C. aeschynomenes, C. musae, and C. nupharicola are associated symptoms, pathogenicity, etiology, incidence, and severity, have also 
with anthracnose in mangoes (Su et al., 2011; Weir et al., 2012). reported MAD infections of different parts of mango (Awa et al., 2012; 
Several articles such as Ciofini et al. (2022), Paudel et al. (2022), Chala et al., 2014; Tucho et al., 2014; Benatar et al., 2021). Ismail et al. 
Jenny et  al. (2019), Honger et  al. (2015), Nelson (2008), and (2015) reported the recovery of C. gloeosporioides, C. kahawae subsp. 
Arauz (2000) have reviewed MAD. However, all the reviews have ciggaro, and C. karstii for the first time in Italy.
a narrow focus on particular geographical areas, including Reports of the C. gloeosporioides species complex, including 
Ghana  (Kankam et  al., 2022) and India (Maske et  al., 2022). C. alienum, C. asianum, C. fructicola, C. siamense, and C. tropicale, 
Though the economic impacts and management of the disease in were identified in Mexico in 2019 (Tovar-Pedraza et al., 2020). Among 
many countries have been investigated by different authors (e.g., these, C. alienum was reported for the first time in Mexico. The 
Arauz, 2000), these studies were confined to a small C. alienum infections have spread into many anthracnose disease 
geographical region. endemic areas; for instance, it was reported in China in 2020 (Ahmad 
In contrast to previous articles on mango anthracnose, this review et  al., 2021). Another type of MAD discovered in 2019 was the 
provides a concise summary of the current state of knowledge about Colletotrichum scovillei (Qin et al., 2019). Table 1 further explains the 
MAD from a global viewpoint, including the most up-to-date history and distribution of MAD.
information on its history, economic importance, epidemiology, early 
detection methods and management strategies. It highlights the rapid 
diagnosis of MAD using a computer vision system and a species- 3. Economic importance of mango 
specific PCR assay to slow down the spread of the disease into disease- anthracnose
free areas. The biological relationships between the pathogen, 
environmental conditions, and host plant susceptibility have been MAD represents the most severe fungal disease restricting the 
better understood due to early detection technologies, genome cultivation and commercialization of mango fruits internationally. 
sequencing, and machine learning. C. gloeosporioides, the disease’s causative organism, represents one of 
This review is well-timed because MAD is spreading rapidly to MAD’s most economically important agents that can impact the sorting, 
disease-free countries like Indonesia (Benatar et al., 2021), Vietnam (Li packaging, shipping, storage, and sale of mango fruits (Bhagwat et al., 
et al., 2020) and Cuba (Manzano León et al., 2018). MAD continues to 2015). In many regions, pre-harvest infections from organisms like 
be a severe problem in many regions; for instance, the detection of new fungi, viruses, bacteria, and nematodes have led to low mango harvests 
strains in Peru (Vilcarromero-Ramos et al., 2022) and China (Ahmad (Chowdhury and Rahim, 2009). MAD is one example of a postharvest 
et al., 2021) threatens the livelihood of millions of people that depend on disease that drastically reduces fruit quality, leading to substantial 
the crop. The potential of different strains of the fungus coexisting within economic losses (Akem, 2006). The economic and scientific importance 
Frontiers in Microbiology 02 frontiersin.org
Dofuor et al. 10.3389/fmicb.2023.1168203
FIGURE 1
Global map of mangoes production and known distribution records for mango anthracnose [refer to Table 1 for further details (FAOSTAT, 2021)].
of postharvest damage from MAD is that it lowers fruit quality and shelf Humid climates are also ideal for the spread of anthracnose fungus 
life, thereby influencing export quality standards (Kankam et al., 2022). (Arauz, 2000; Akem, 2006). The disease has a prevalence of about 100% 
MAD typically causes yield losses through a decline in either in fruits grown in damp or very humid environments (Arauz, 2000; 
the quantity or quality of harvested mango fruits. According to local Akem, 2006; Chowdhury and Rahim, 2009). MAD can also induce 
reports, MAD poses a severe threat to Ghana’s mango crop, causing postharvest deterioration, leading to the fruit being rejected by consumers.
a 30% output loss in one of its districts (Honger et al., 2014). Similar MAD is widely recognized as a significant challenge to southern 
to how anthracnose disease is responsible for roughly 39% of yield Ethiopia’s mango farming business’s sustainability (Chala et al., 2014). 
loss in mango cultivation in India (Prakash and Srivastava, 1987). Mango exporting countries like Ghana suffer the most as a result of 
MAD causes a 30–60% annual loss of mango, with potential damage the disparity in revenue between export and local markets, despite 
of 100% under ideal conditions (Kamle and Kumar, 2016). In this, producers and sellers continue to sell low-quality fruits on the 
Gondunglegi, Indonesia, yield loss due to anthracnose was reported local market (Kankam et al., 2022).
to be 50.28% by Kumari et al. (2017) and Arauz (2000), while in The expense of controlling MAD could have repercussions for the 
Himachathe l Pradesh, India, the postharvest loss was reported to economy. Farmers have used a variety of fungicides to prevent the 
be  29.6% from 1990 to 1992 (Sharma and Verma, 2007). In fungus from spreading. Smallholder farmers, who may lack the capital 
Hyderabad, 20 to 30% of mango fruits rotted due to to invest in such suggested management tactics, may profoundly feel 
C. gloeosporioides. According to Hossain and Ahmed (1994), MAD the economic effects of these controls. In addition, fungi can become 
and stem end rot diseases account for a 25–30% loss in mango yield resistant to fungicides if too many are used, necessitating the use of 
in Bangladesh. Mangoes in Thailand were lost at a rate of 62.8% more potent or hazardous compounds.
during harvest and 63.2% in the markets due to MAD, according to 
research by Sardsud et al. (2003). Anthracnose can cause a 30–60% 
annual loss in China’s mango harvest (Li et al., 2019). 4. Symptoms of mango anthracnose
Severe problems in nurseries and orchards may appear under 
crowded and moist conditions (Lai and Simon, 2013). The incidence MAD is among the most widespread diseases that can attack 
may increase significantly under favorable environmental conditions. mango at any time, whether when it is still in the field, in 
Damage to foliage, a reduction in flower production, and yield losses transportation, or storage. Mango orchards may show symptoms of 
have all been attributed to C. gloeosporioides. the disease on the mango trees’ leaves, twigs, and fruits (Figure 2). It 
Frontiers in Microbiology 03 frontiersin.org
Dofuor et al. 10.3389/fmicb.2023.1168203
TABLE 1 History and geographical distribution of the mango anthracnose disease.
Year Pathogen/ Pathogen/ Host Part Distribution Comment(s) References
Strain (Species Strain Affected
Complex) (Singleton 
Species)
2012 Colletotrichum Colletotrichum Mango fruit Nigeria First report of Colletotrichum Awa et al. (2012)
gloeosporioides gloeosporioides gloeosporioides in southwest 
Nigeria
2014 C. gloeosporioides C. gloeosporioides Leaves, fruits Ethiopia Tucho et al. (2014)
2014 C. gloeosporioides C. gloeosporioides Mango fruit Ethiopia Chala et al. (2014)
2015 C. gloeosporioides C. gloeosporioides Panicles, leaves, fruits Ghana Honger et al. (2015)
2015 C. gloeosporioides C. gloeosporioides Mango fruit Nigeria Onyeani and Amusa 
(2015)
2015 C. gloeosporioides C. asianum Mango fruit South Africa Sharma et al. (2013)
2015 C. gloeosporioides C. C. gloeosporioides C. Mango leaves and fruits Italy First report of C. Ismail et al. (2015)
acutatum kahawae subsp. ciggaro gloeosporioides, C. kahawaw 
C. karstii subsp. ciggaro, C. karstii in Italy
2018 C. gloeosporioides C. gloeosporioides Panicles, leaves, branch Bangladesh Uddin et al. (2018)
terminals of mango
2018 C. gloeosporioides C. asianum, C. Mango leaves China First report of these pathogens Mo et al. (2018) and 
fructicola, and C. in the Guangxi province, China Tovar-Pedraza et al. 
siamense (2020)
2018 C. gloeosporioides C. gloeosporioides Mango flower, mango India
leaves, mango fruit
2019 C. gloeosporioides C. gloeosporioides Leaves, fruits Côte d’Ivoire First reported in 1951 and Dembele et al. (2019)
identified in 1979
2019 C. gloeosporioides C. alienum Mango peels, mango China First report of this pathogen in Ahmad et al. (2021)
fruit pulps China
2019 C. gloeosporioides, C. C. asianum, C. Mango leaves, mango China Aside C. asianum, C. fructicola, Li et al. (2019)
boninense cliviicola, C. fruits C. scovillei and C. siamense, all 
cordylinicola, C. the other C. spp. were being 
endophytica, C. reported to infect mangoes for 
fructicola, C. the first time in China. 
gigasporum, C. However, this was the first 
gloeosporioides, C. report of C. cordylinicola, C. 
karsftii, C. liaoningense, endophytica, C. gigasporum, C. 
C. musae, C. scovillei, liaoningense and C. musae 
C. siamense and C. infecting mangoes worldwide
tropicale
2019 C. scovillei Mango leaves China First report of C. scovillei Qin et al. (2019)
infecting mangoes in China
2019 C. gloeosporioides C. gloeosporioides Mango fruit China Feng et al. (2019)
2019 C. gloeosporioides C. gloeosporioides Mango fruit Mexico First report of antagonistic Reyes-Perez et al. 
mechanisms of the marine (2019)
bacterium, Stenotrophomonas 
rhizophila, against anthracnose 
disease in mango
2020 C. gloeosporioides C., C. asianum, C. Mango tissues Mexico First report of all five species in Tovar-Pedraza et al. 
fructicola, C. siamense, Mexico and the first report of C. (2020)
and C. tropicale alienum MAD worldwide
2021 C. gloeosporioides C. asianum Mango fruit Indonesia First report of C. asianum Benatar et al. (2021)
2022 C. gloeosporioides C. asianum Mango leaves Australia Grice et al. (2022)
(Continued)
Frontiers in Microbiology 04 frontiersin.org
Dofuor et al. 10.3389/fmicb.2023.1168203
TABLE 1 (Continued)
Year Pathogen/ Pathogen/ Host Part Distribution Comment(s) References
Strain (Species Strain Affected
Complex) (Singleton 
Species)
2022 C. acutatum, C. C. acutatum, C. Mango flower, mango Colombia, Guevara-Suarez et al. 
boninense, C. godetiae, C. leaves, mango fruit Equador (2022)
gigasporum, C. laticiphilum, C. (Equador – 
gloeosporioides, C. tamarilloi Colletotrichum 
orbiculare acutatum, C. 
tamarilloi)
2022 C. gloeosporioides, C. C. gloeosporioides, and Mango flower, mango India Kadam et al. (2002)
acutatum C. acutatum leaves, mango fruit, 
twig
2022 C. gloeosporioides C. asianum Mango fruit Peru First report of C. asianum Vilcarromero-Ramos 
infecting mangoes in Peru et al. (2022)
2022 C. gloeosporioides C. gloeosporioides Mango fruit Taiwan Liang et al. (2022)
can also be found on the blossoms (Uddin et al., 2018). The disease’s lesions that are sometimes clustered near the leaf apex. While 
symptoms show up as oval or irregular brown to deep brown sunken anthracnose leaf spots are large, scab disease spots are tiny and cause 
point-sized spots of varying sizes spread all over the leaf surface, the leaf to become distorted and wrinkled before falling off 
most prominently on young leaves but also on older leaves. As the prematurely. A powdery fungus growth coating on the leaves also 
leaves age, these spots develop into larger lesions that are either characterizes powdery mildew disease.
circular or irregular in shape and surrounded by a red halo (Qin Black-banded or black velvety mycelial growth on leaf veins and 
et al., 2019). midribs is a telltale sign of disease (Gautam et al., 2017), while red rust 
The fungus can produce blossom blight on the inflorescence. is characterized by small, circular lesions that appear on the top leaf 
Lengthy lesions ranging from dark grey to black can appear in the surfaces and coalesce toward the midribs (Patrice et al., 2020). Stem 
stalk. The panicles and open flowers also develop tiny black spots that end rot is a disease that affects fruits and causes these fruits to turn 
eventually grow and kill the plant. Flowers that have been blighted black at the stem end, eventually spreading to cover about half of the 
become brittle and dark brown to black (Alemu et al., 2014). The fruit. Though the damaged skin retains its firmness, the rot sets into 
fungus sometimes invades the twigs, stems and branches of the mango the pulp, which gives off a foul odor. Additionally, water-soaked sores 
tree. Symptoms on twigs manifest as small, expanded oval and on fruits progressively develop into cankers, which break open and 
necrotic lesions that eventually consolidate and disperse. The fungus release a gummy slime due to bacterial canker disease. Conversely, 
can invade twigs during severe infections and cause dieback (Tovar- MAD causes black spots, which are initially spherical, then transform 
Pedraza et al., 2020). into big irregular blotches across the entire fruit while in storage. 
MAD is most common on immature fruits and during transport Large, gaping crevices form at these sites, allowing the fungus to eat 
and storage but can occur at any stage during the fruit’s life cycle. The its way deep into the fruit (Sefu et al., 2015).
young fruits are either aborted or mummified, and infection on larger The necrotic regions on the twigs become increasingly longer and 
fruits may remain latent or dormant until the ripening of the fruit, black due to the twig blight disease. The leaves begin to drop and 
where black, sunken necrotic lesions appear on the fruit peel and eventually dry out and fall off. Very immature branches begin to dry 
increase rapidly in size (De Souza et al., 2013). Tear staining, caused out from the tips down. Dieback disease causes twigs to wilt and die 
by spore-laden water droplets from diseased twigs and leaves from the top down, especially in older trees, and then leaves to wilt 
spreading across the fruit and infecting the surface, is another and die, giving the impression of a fire scorch (Saeed et al., 2017). 
symptom of anthracnose damage to fruit (Mabbett, 2014). Several Young, green twigs get discolored and black, eventually dying from 
other diseases attack the mango plant aside from anthracnose. Some the top down (Malik et al., 2014). Mango twigs eventually succumb to 
of these diseases have symptoms similar to anthracnose, and others MAD during extremely severe outbreaks and vice versa.
have distinct symptoms. A couple of such equally important diseases For powdery mildew, the distinguishing symptoms of the disease 
of mango are compared with anthracnose. are whitish powdery fungus growth coating on flowers. Affected 
Alternaria leaf spot disease is similar to anthracnose disease flowers and young fruits that have reached marble size may drop 
because it mostly attacks the young, tender leaves and is prematurely (Ajitomi et al., 2020). The panicles and open flowers also 
characterized by brown spots. Anthracnose, however, shows up as develop tiny black spots that eventually grow and kill the plant. 
irregular, oval-shaped spots all over the leaf ’s surface while in Flowers affected by anthracnose are dry and dark brown to black in 
Alternaria leaf spot, typical round spots are uniformly distributed hue (Rosman et  al., 2019). It is estimated that the disease causes 
across the leaf ’s lamina and more noticeable on the leaf ’s underside. 30–60% damage economically, which can climb to 100% in fruits 
Symptoms of bacterial canker disease on leaves include yellowing produced during humid seasons or at the commencement of rains 
and eventual leaf drop, as well as wet, irregular to angular, elevated (Kamle and Kumar, 2016).
Frontiers in Microbiology 05 frontiersin.org
Dofuor et al. 10.3389/fmicb.2023.1168203
FIGURE 2
Symptoms of mango anthracnose disease and cultural and morphological features of C. gloeosporioides causing anthracnose disease of mango. 
(A,B) Symptomatic leaves and twigs, (C) symptomatic mature leaves, (D) the alligator skin effect symptoms on unripe fruit, (E) typical sunken spot 
symptoms of mango anthracnose, (F) a ripe fruit with the pericarp removed to show the penetration of the dark lesions of the anthracnose disease 
on the fruit pulp, (G) white mycelial growth on PDA showing presence of acervuli ring in the middle of the culture, and (H) short conical spores with 
rounded edges (H). Mg × 200.
MAD causes the most harm in wet environments during the calmodulin-dependent serotonin-threonine phosphatase (Zhou 
flowering and fruit-setting periods. Flowering and early fruit Z. et al., 2017), targets a wide range of downstream effectors including 
development are susceptible to mango infections (Sarkar, 2016). enzymes, other proteins, and transcription effectors. Thus, triggered 
Some cutting-edge strategies for early diagnosis of anthracnose by a host of stimuli, the two pathways regulate basic cell function and 
disease in mangoes include the application of Modified Rotational stress response. Like other pathogenic fungi that attack plants, 
Kernel Transform Features (Ullagaddi and Raju, 2017), C. gloeosporioides secret proteolytic enzymes such as pectate lyase 
computational biology, and image processing analytic methods (PEL), endopolygalacturonase (PG) and pectin lyase (PNL) (Zhou 
(Khan et al., 2019). Z. et  al., 2017). These essential pathogenic functionaries can 
depolymerize polysaccharides present in the primary cell wall of the 
host during infection and colonization (Zhou Z. et al., 2017). Zhou 
5. Biochemical and molecular Z. et al. (2017) reported that C. gloeosporioides required the ABC 
characterization of pathogen (ATP-binding cassette) protein CgABCF2 for appressorial formation 
and plant infection as well as for sexual and asexual reproduction.
Conserved signal transduction pathways control fungi growth, Many of the studies conducted on C. gloeosporioides depend on 
development, and reproduction (Cannon et al., 2012; Gan et al., 2013). evidence from previous works which stated that the sequence data in 
The mitogen-activated protein (MAP) kinase cascades have been the domain 2 (D2) region of the rDNA could efficiently reveal 
shown to be responsible for the infection-related morphogenesis in information about the type of leucyl-tRNA synthetase (LARS) and 
pathogenic fungi like C. gloeosporioides (Yong et  al., 2013; Zhou relationships within C. gloeosporioides (Cannon et al., 2012; Sharma 
Z. et  al., 2017). Yong et  al. (2013), in their study isolated and et al., 2013). A recent study caused mutations within the WT strain 
characterized the MAK kinase gene Cgl-SLT2 from C. gloeosporioides, W16 of C. gloeosporioides via ATMT (Agrobacterium tumefaciens-
and indicated the full involvement of MAPK in conidiation, Mediated Transformation) to study genes associated with conidiation 
appressorium formation, polarized growth, and the pathogenicity of (Wu et al., 2016). The insertional mutagenesis populations were then 
the filamentous fungus. The MAPK cascade, which consists of three isolated, and conidiation assays were conducted on 59 conidial 
conserved kinases, the MAP kinase (MAPK), MAP kinase kinase production-variation transformants (Wu et  al., 2016). The study 
(MEK), and MAP kinase kinase kinase (MEKK), is a pivotal signaling conclusively found the oligopeptide transporter (Opt) to be involved 
pathway sensing and relaying extracellular signals to control gene in C. gloeosporioides conidiation. The team also identified 19 putative 
expression (Yong et al., 2013). The fungal MAPK cascade together genes including CgOPT2 (oligopeptide transporter protein), CgMCT1 
with the calcium-calcineurin pathway, which functions via (monocarboxylate transporter protein), CgCOP9 (Cop9 signalosome 
calmodulin, the Ca2+ binding protein, calcineurin, and the subunit 6 protein), CgMRP1 (multidrug resistance- associated protein 
Frontiers in Microbiology 06 frontiersin.org
Dofuor et al. 10.3389/fmicb.2023.1168203
5), CgRXT2 (Rxt2-like protein) and CgRRN3 (specific transcription At least three major infection strategies are implicated in the 
initiation factor RRN3). Interestingly, while the WT strain W16 molecular pathogenesis of plant fungal pathogens. Fungal strategies 
contained 19 genes, 11 of these genes were not detected in T-DNA may involve preventing host recognition, inhibiting host defense 
insertional mutants that were also sequenced (Wu et al., 2016). The mechanisms, and hijacking host cellular machinery (Rodriguez-
team inferred from the observational differences in phenotypes that Moreno et al., 2018). Specifically, to penetrate the plant host, pathogenic 
variations in conidiation and production of albino hyphae could fungi may secrete cell wall-degrading carbohydrate-active enzymes 
be attributed to the absence of those 11 genes (Wu et al., 2016). such as glycoside hydrolases, glycosyltransferases, polysaccharide 
Early in the 20th century, research teams successfully isolated and lyases, carbohydrate esterases, and redox enzymes (Lombard et al., 
characterized phenotypes of C. gloeosporioides using morphological 2014). Plant fungi may also modify the components of their cell walls 
features. Relying on morphology of appressoria and conidiomata through the accumulation of specialized carbohydrates to prevent 
conidia dimensions, three biological groups within the degradation by plant chitinases (Fujikawa et al., 2012) or the secretion 
C. gloeosporioides complex were determined (Sharma and Kulshrestha, of carbohydrate-binding effectors to inhibit chitin-mediated host 
2015). These were C. gloeosporioides var. gloeosporioides which had response (de Jonge et al., 2010; Sanchez-Vallet et al., 2013).
unlobed or slightly lobed appressoria and conidial widths of Moreover, pathogenic fungi can hijack the host defense system by 
4.5–5.5 μm; C. gloeosporioides var. minor of similar appearance but subversion of reactive oxygen species, modification of host pH, 
with mean conidial widths of 3.0–4.2 μm, and a third phenotype that regulation of hormone signaling, and inhibition of host proteases 
closely matches the definitions classifying C. crassipes with lobed (Rodriguez-Moreno et al., 2018). In most of these infection cycles, 
appressoria and conidial widths of 4.5–5.5 μm (Wu et al., 2016). fungal effector proteins, secondary metabolites, host-specific toxins, 
On the molecular level, phylogenetic relationships in the and small RNAs (sRNA) are increasingly gaining prominence as 
Colletotrichum spp. have been successfully identified through critical regulators and mediators in the mechanism of molecular 
sequencing in the internal transcribed spacers 1 and 2 (ITS1 and ITS2) pathogenesis (Rodriguez-Moreno et al., 2018).
regions and glyceraldehyde-3-phosphate dehydrogrenase (GAPDH) Colletotrichum gloeosporioides is typically dormant in the dry 
gene (Sharma and Kulshrestha, 2015; Pardo-De la Hoz et al., 2016). season, especially during extremes of temperature, low humidity, and 
Using an additional genomic region, ApMat, the three strains identified sunlight (Sharma and Kulshrestha, 2015). However, optimal growth 
in the C. gloeosporioides complex were refined and confirmed (Doyle of the pathogen is favored at high humidity, pH range of 5.8 to 6.5, and 
et al., 2013; Pardo-De la Hoz et al., 2016). From work in the intergenic temperature of 25–28°C (Sharma and Kulshrestha, 2015). These 
regions of apn2 and MAT1-2-1 (ApMat) genes, 22 phenotypes favorable conditions stimulate the release of spores from acervuli of 
(Supplementary Table S1) have been identified (Cannon et al., 2012), seeds, leaves, fruits, or trash of hosts. Dispersal of spores may occur 
and four distinct phylogenies (C. fructicola, C. frgariae sensu stricto, through air currents, insects, water splash or other forms of direct 
C. melanocaulon and C. jasmine-sambac) within the complex described transmission (Sharma and Kulshrestha, 2015). After successful 
(Doyle et  al., 2013). Subsequently, another team using the same dispersal, C. gloeosporioides utilizes a hemibiotrophic mode of 
approach confirmed that these four and five potentially novel infection to penetrate, develop and spread within a susceptible host 
Colletotrichum lineages, yet to be  assigned specie names, were plant (Münch et al., 2008). Through this mode, the infection of host 
associated with anthracnose in mango tissues (Sharma et al., 2013). plants usually consists of two stages: penetration and colonization 
Intervention strategies against C. gloeosporioides have been (Marcianò et al., 2021). Melanized appressoria are initially formed to 
explored as molecular knowledge of the pathogenic fungus delves aid in host penetration and harmless formation of primary hyphae in 
deeper. For instance, Yong et al. (2013) showed conclusively that the a biotrophic phase of infection, followed by the secondary formation 
MAPK gene Cgl-SLT2 is required for appressorium formation, of hyphae in a necrotrophic phase that is potentially deleterious to the 
conidiation and pathogenicity in C. gloeosporioides. Subsequently, the host (Münch et al., 2008). This leads to the spread of spores on the 
mutant Cgl-slt2 showed defective hyphae formation and sporulation surface of infected tissues that are subsequently dispersed to repeat the 
compared to the wild type. Other mutagenic studies are exploring transmission and infection cycle of the pathogen (Figure 2). Thus, the 
using T-DNA (transferred-DNA) to yield fewer pathogenic phenotypes. disease moves through a cycle of dissemination of asexual spores 
(conidia), inoculation of spores into susceptible part of the host, 
development of symptoms in fruiting bodies (acervuli), infection of a 
6. Mode of transmission and infection host, further development of disease, reproduction of pathogen, and 
of pathogen survival of pathogen (Paudel et al., 2022). Glomerella cingulata, the 
name typically given to the sexual stage (teleomorph) of the same 
Pathogenic fungi of plants need to align with the seasonal growth pathogen, may induce dark, long-necked perithecia with clavate asci 
stages of the host plant for a successful transmission and infection that are relatively rarely observed (Figure 3).
cycle. For instance, since most plants shed leaves and remain dormant Several C. gloeosporioides genes play critical roles in host defense 
during the autumn and winter seasons, plants’ pathogenic fungi mechanisms during infection. Most of these genes interact with a 
typically adopt corresponding dormancy strategies until spring pH-responsive transcription factor (pacC) that regulates the 
(Marcianò et al., 2021). These strategies include the production of expression of approximately 5% fungal genome involved in transport, 
spores, the development of sclerotia, hiding within the host plant, oxidative damage, and cell wall degradation (Alkan et al., 2013). The 
finding shelter in the ground, or moving to another active host plant expression of pectate lyase by pelB induces the degradation of the 
during adverse conditions (Marcianò et al., 2021). When conditions plant cell wall in a pH-dependent manner under the regulation of 
become favorable, spores may be  transmitted by water, wind, or pacC (Drori et al., 2003; Kramer-Haimovich et al., 2006). A PepCYP 
animals to a susceptible host for infection. product homologous to cytochrome P450 with a heme-containing 
Frontiers in Microbiology 07 frontiersin.org
Dofuor et al. 10.3389/fmicb.2023.1168203
FIGURE 3
Life cycle of Colletotrichum gloeosporioides in Mango (Mangifera indica).
domain involved in host defense mechanisms during pathogen during fungal pathogenesis: pnl-2 is highly expressed in the 
invasion and colonization is also expressed in a ripening–dependent necrotrophic phase of infection, and pnl-1 may be observed in 
manner by C. gloeosporioides (Oh et al., 1999). both necrotrophic and biotrophic phases (Wei et al., 2002).
Several genes also mediate pathogenesis in the fungus. CgRac1 
protein regulates morphogenesis, nuclear division, and 
germination via potential concentration in conidia and hyphal 7. Host range
tips (Nesher et  al., 2011). The expression of cgOPT1 varies in 
resting and germinating spores during mycelia development The pathogen responsible for severe anthracnose infections in 
(Chagué et al., 2009). Several nitrogen-metabolism-related genes Brazil’s southeast was identified, and disease susceptibility among a 
(GDH2, GS1, GLT, and MEP) are differentially expressed to aid in global collection of mango germplasm was assessed, based on a 
the induction of ammonia accumulation and fungal pathogenicity survey. Colletotrichum was the most common pathogen of commercial 
(Miyara et al., 2012). The expression of Bcl-2 protein plays a role mangoes in the region, and the cultivars ‘Ubà,’ ‘Quinzenga,’ 
in cell death and survival of the fungus through processes such as ‘Amarelinha da Sementeira,’ ‘Aroeira,’ and ‘Correjo’ were particularly 
pathogenicity, conidial germination, and mycelium growth vulnerable to C. asianum infections (Vitale et al., 2020). The disease is 
(Barhoom and Sharon, 2007). CgCTR2, a putative vacuolar copper notably less severe on ‘Ourinho’ and ‘Lita’ cultivars but less on ‘Mallika’. 
transporter, is critical in cellular copper balance during the initial None of the accessions tested was resistant, and commercial cultivars 
stages of pathogenesis (Barhoom et al., 2008). The expression of generally cannot deliver appropriate qualitative and quantitative yields 
pel1 and pel2 proteins also plays vital roles in pathogenesis during under humid environmental conditions without regularly applying 
the neurotropic phase of fungal infection (Shih et al., 2000). The fungicide sprays (Arauz, 2000). Mango (‘Palmer,’ ‘Keith,’ and ‘Tommy 
expression of the cgDN3 gene of C. gloeosporioides is stimulated Arkins’) from the orchards of Northeastern Brazil were used to test 
during the early stages of infection to aid in the modulation of a the virulence of five species of Colletotrichum (C. asianum, C. dianesei, 
hypersensitive-like response by a compatible host (Stephenson C. fructicola, C. karstii, and C. tropicale). Neither the ‘Keith’ nor the 
et al., 2000). The chip6 gene plays an essential role in conidial ‘Palmer’ cultivars were affected by C. karstii, suggesting that it is not 
germination and appressorium formation (Kim et  al., 2002). pathogenic to these species (Lima et al., 2015). The Tommy Atkins 
Moreover, two pectin lyase genes are differentially expressed cultivar was more tolerant to infection from all Colletotrichum species 
Frontiers in Microbiology 08 frontiersin.org
Dofuor et al. 10.3389/fmicb.2023.1168203
tested, and the alternate host plants were all susceptible to the asianum is associated with mangoes but has been reported on 
Colletotrichum spp. In Australia, ‘Carrie’, ‘Tommy Atkins’, ‘Saigon’ avocados (Persea americana) in Indonesia (Zhafarina et al., 2021). 
cultivars are resistant to C. gloeosporioides, while ‘Kensington Pride’ Colletotrichum cigarro has been isolated from mango in Colombia and 
shows moderate resistance to the disease (Nelson, 2008; Kankam et al., Italy (Ismail et al., 2015; Pardo-De la Hoz et al., 2016). The species also 
2022). In the Philippines, ‘Palmer’, ‘Siam’, ‘Velei-Colomban’, and ‘Joe occurs in plants, such as Kunzea ericoides in New Zealand (Weir et al., 
Welch’ are resistant cultivars, whereas ‘Fernandin’, ‘Arumanis’, ‘Edward’, 2012), Areca catechu in China (Zhang et al., 2020) and apple (Malus 
‘Gedong’, and Tjenkir’ are fairly resistant to the disease. Moreover, domestica) in Belgium and the USA (Grammen et al., 2019; McCulloch 
‘Paris’, ‘Fairchild’, and ‘Rapoza’ show resistance to C. gloeosporioides in et al., 2020). C. endophyticum is associated with mango fruits and 
Hawai‘I, with only ‘Haden’ showing moderate resistance to the leaves but also occurs in Camellia sinensis (Wang et al., 2016), and 
pathogen. In Florida, the ‘Zill’ shows resistance to C. gloeosporioides. coffee (Coffea arabica and C. robusta) leaves and fruits (Cao et al., 
In addition to mango, other hosts of C. gloeosporioides include 2019). The pathogen is of grave concern in Southeast Asia to tea, 
Musa species, avocado (Persea americana Mill.) and guava (Psidium coffee and mango plantations (Talhinhas and Baroncelli, 2021). 
guajava L.) (Nelson, 2008; Moraes et al., 2013). The pathogen has also C. perseae is associated with MAD (Hofer et al., 2021) and avocado 
been found in apples (Malus domestica Borkh.) (Munir et al., 2016), (Talhinhas and Baroncelli, 2021). C. queenslandicum affects papaya 
papaya (Carica papaya L.) (Maharaj and Rampersad, 2012) and leaves, and avocado in Australia, cashew in Brazil (Veloso et al., 2018), and 
tubers and seeds of yam (Dioscorea alata L.) (Abang et al., 2002). coffee in Fiji (Weir et al., 2012). The pathogen has been found in a 
Besides, capsicum, coffee, eggplant, and tomato are susceptible to variety of other host plants, including Citrus latifolia in the 
MAD. Lima et  al. (2015) suggest alternative host plants (papaya, United States (Kunta et al., 2018), Licania tomentosa in Brazil (Lisboa 
banana, guava and bell pepper) are susceptible to C. asianum, et al., 2018), Litchi chinensis in Australia (Anderson et al., 2013; Shivas 
C. dianesei, C. fructicola, C. karstii and C. tropicale. There are many et al., 2016), Nephelium lappaceum in Puerto Rico (Serrato-Diaz et al., 
strains of the pathogen that can infect non-mango host plants, which 2014; Shivas et al., 2016). C. liaoningense attacks mango in China (Li 
include ornamental lupine (Lupinus hartwegii L.), marsh lupine et  al., 2019). However, the pathogen can also occur in Solanum 
(Lupinus polyphyllus Lindl.), various herbs such as angelica pseudocapsicum (Liu et  al., 2021). In mangoes, larger lesions are 
(Archangelica officinalis Hoffm.), thyme (Thymus vulgaris L.) caraway observed on hosts at temperatures ranging between 25 and 30°C, 
(Carum carvi L.) and elder (Sambucus nigra L.) (Paulitz, 1995). though many species exhibit varying thermal requirements for 
Anthracnose symptoms have been observed in mango cv. R2E2 when maximal pathogenicity in the fruits (Lima et al., 2015). Table 2 lists a 
C. alienum B.S. Weir and P.R. Johnst., C. kahawae subsp. cigarro range of mango cultivars with varying levels of resistance 
B.S. Weir and P.R. Johnst., and C. theobromicola Delacr., were isolated and susceptibility.
from avocados (Grice et al., 2022). In Venezuela, Coffee Berry Borer 
-infested and -uninfested branches and twigs, as well as ripe and green 
berries with indications of anthracnose, were all found to be positive 8. Detection of mango anthracnose
for C. siamense and C. alienum (Castillo et al., 2022). The dragon fruit, 
or Hylocereus undatus, is a species of the Hylocereus that often has a Traditionally, MAD is identified using certain morphological 
white pulp and scarlet or pink skin. One of the most widespread features such as mycelial growth, conidia size, colony color, texture, 
worldwide phytopathogens responsible for postharvest anthracnose and presence and absence of setae (Abera et al., 2016; Ashraful et al., 
in dragon fruits is Colletotrichum spp. (Bordoh et  al., 2020). The 2017). Although these features are still used with other techniques to 
disease infects fruits in the field, during transportation, and during identify and characterize the causative organisms of the disease, the 
cold storage, thereby reducing the shelf life of the fruits. Colletotrichum differences in these physical features are not adequate to separate the 
scovillei causes anthracnose symptoms in bananas, mangoes, wampi different species of Colletotrichum. This was confirmed in a study 
(Clausena lansium, Rutaceae), and onions (Zhou Y. et al., 2017; Qin where it was shown that differences exist between identical specimens 
et al., 2019; Lin et al., 2020; Lopes et al., 2021). grown under different laboratory conditions (Mo et  al., 2018). 
Though C. tamarilloi is associated with tamarillo in Colombia and According to Peres et  al. (2002), there is an overlap between the 
Ecuador, the fungus also attacks mango and onion in Columbia and conidial morphology and cultural characteristics, thus making the use 
Brazil, respectively (Damm et al., 2012; Pardo-De la Hoz et al., 2016; of these features unreliable.
Caicedo et al., 2017; Lopes et al., 2021). In China, C. gigasporum was Biochemical reactions and immunoassays have been used to 
isolated from mango (Li et al., 2019), and the same species attacks distinguish between bacterial, fungal, protozoan, and plant species 
coffee in Mexico and China (Cristóbal-Martínez et al., 2017; Cao et al., based on differences in certain structural features associated with 
2019). In Brazil, C. gigasporum, was recorded as a secondary fungal these organisms. Some of these reactions have been employed to 
disease on Annona spp. (Costa et al., 2019). Colletotrichum alienum separate the different species of MAD causative agents. Honger et al. 
attacks many crops, including Aquilaria sinensis and Camellia sinensis (2014) used the casein hydrolysis method to distinguish between 
in China (Liu et al., 2017, 2020; Ahmad et al., 2021). In Australia, the C. gloeosporioides and C. acutatum in mango isolates from Ghana. 
pathogen has been isolated from Fragaria × ananassa, Grevillea sp., Their study found that C. gloeosporioides and C. acutatum tested 
and Nerium oleander (Liu et al., 2013; Schena et al., 2014; Shivas et al., negative and positive, respectively for the casein hydrolysis method. 
2016). Moreover, in New Zealand, the pathogen has been reported This result further confirmed that the two species are different; hence, 
from Malus domestica (Weir et  al., 2012), Persea americana in they concluded that the main causative species in Ghana was 
Australia, New Zealand and Israel (Weir et al., 2012; Sharma et al., C. gloeosporioides and not C. acutatum.
2017). Colletotrichum cigarro occurs in mango in Colombia and Italy Using indirect ELISA and western blotting techniques, 
(Ismail et  al., 2015; Pardo-De la Hoz et  al., 2016). Colletotrichum Theerthagiri et  al. (2016) could distinguish between the various 
Frontiers in Microbiology 09 frontiersin.org
Dofuor et al. 10.3389/fmicb.2023.1168203
TABLE 2 Mango cultivars susceptibility to the anthracnose disease.
Country Resistant cultivar Resistant level Susceptible cultivars Reference
USA Zill Resistant - Nelson (2008), Ntsoane et al. (2019), Vitale et al. (2020), 
Rapoza Resistant and Kankam et al. (2022)
Haden Moderately resistant
Paris Fairchild Resistant
Philippines Velei-Colomban Resistant Cherakuruasa Nelson (2008), Ntsoane et al. (2019), Vitale et al. (2020), 
Fernandin Moderately resistant Kensington and Kankam et al. (2022)
Joe Welch Resistant Julie
Arumanis Moderately resistant Ah Ping
Palmer Resistant Otts
Siam Resistant Hingurakgoda
Peter Passand
Carrie
Australia Caraboa Florigon Resistant Willard Nelson (2008), Ntsoane et al. (2019), Vitale et al. (2020), 
Carrie Resistant Neelum and Kankam et al. (2022)
Tommy Atkins Resistant Manaranijan
Kensington Pride Moderately resistant
Saigon Resistant
Brazil Ourinho Moderately resistant – Nelson (2008), Ntsoane et al. (2019), Vitale et al. (2020), 
Lita Moderately resistant and Kankam et al. (2022)
causative agents of the disease. For the western blotting results, they multiple gene sequences to differentiate between and within species 
found a 40 kDa molecular weight protein in C. gloeosporioides which (Weir et al., 2012; Dela Cueva et al., 2021). Due to the drawback of using 
was different from other Colletotrichum species. The indirect ELISA ITS, other genes such as actin, β – tubulin, chitin synthase, 
data gave higher titer values of polyclonal antibodies to protein glyceraldehyde-3-phosphate dehydrogenase, calmodulin, and 
extracts of C. gloeosporioides compared to other fungal species, further glutamine synthetase have also been studied to explore the differences 
confirming that it differs from the other Colletotrichum species. among Colletotrichum species (Weir et al., 2012; Lima et al., 2013a,b; 
With technological advancement, molecular techniques have been Dela Cueva et al., 2021). Lima et al. (2013a,b), in their study to identify 
employed to augment morphological and biochemical detection the Colletotrichum species associated with MAD in northeastern Brazil, 
methods. Molecular techniques are accurate, rapid, specific, and sensitive used sets of primers for the glyceraldehyde-3-phosphate, actin, β – 
in detecting the causative organisms of the disease and thus help in tubulin, calmodulin, and glutamine synthetase genes. It was found that 
understanding the mechanism involved in disease pathology and the primers were able to amplify five different species from the 
management (Kamle et  al., 2013). Molecular techniques have been C. gloeosporioides complex namely C. asianum, C. fructicola, C. tropicale, 
developed based on species’ ribosomal DNA (rDNA) differences. The C. karstii, and C. dianesei. A similar result was obtained in mango leaves 
internal transcribed spacer (ITS) regions (ITS 1 and ITS 4) within the in which C. asianum, C. fructicola and C. siamense were identified using 
nuclear ribosomal gene cluster have mainly been found to be a good site glyceraldehyde-3-phosphate dehydrogenase, partial actin, β – tubulin, 
for the design of specific primers for the detection of the causative agents and chitin synthase (Mo et al., 2018). Therefore, the findings suggest 
of the disease (Freeman et al., 2000; Kamle et al., 2013; Zakaria et al., that these genes could be  used to detect different strains within a 
2015). In a study to distinguish between Colletotrichum species, species- species complex.
specific primers MKCgF and MKCgR of amplicon size 380 bp were Current methods focus on designing and developing imaging 
designed. The study showed that the primers could amplify all isolates of processing and algorithms that have aided in automated disease 
C. gloeosporioides but not the other species, such as C. acutatum, detection. Accurate techniques such as camera-assisted image analysis 
C. falcatum and C. capsici. It was therefore suggested that the MKCgF and (Corkidi et al., 2006) and a computer vision system based on ultraviolet 
MKCgR would be a good marker for distinguishing between species- light (Alberto et al., 2022) have been employed in the visual detection 
specific Colletotrichum and hence valuable for developing a rapid and of the disease. However, this is only effective if the symptoms appear 
sensitive a diagnostic PCR assay for early detection and management of on the skin of the fruits hence unable to detect the disease at an early 
the disease (Kamle et al., 2013). In another study from Ghana using stage. A hyperspectral imaging spectrum based on spectroscopy and 
480 bp species-specific primers CgInt and ITS 4, it was observed that the computer vision has been developed for early detection of the disease. 
C. gloeosporioides complex showed amplification products at 480 bp The technique has been shown to provide information about the spatial 
while C. acutatum did not. Phylogenetic analysis also showed that the distribution of components in the mango plant for easy detection and 
C. acutatum clade clustered far away from the C. gloeosporioides complex, classification under different infection levels (Siriptrawan, 2021). 
thus indicating that the two species are different (Honger et al., 2014). Another computer study was done using a Matrix Laboratory 
Although the ITS gene sequence is instrumental in identifying (MATLAB) based disease detection system. The system employs a 
Colletotrichum species, it cannot distinguish between closely related Gray Level Co-occurrence Matrix (GLCM) algorithm, which can 
species (Cannon et al., 2012). This, therefore, has led to the use of extract the features of the disease, and an SVM classifier that classifies 
Frontiers in Microbiology 10 frontiersin.org
Dofuor et al. 10.3389/fmicb.2023.1168203
the disease type based on the extracted features from the GLCM. The were found in ‘Keitt’ fruit during development and storage compared 
study observed that the system yields a 90% accuracy of automated to ‘Zill’ fruit. Additionally, ‘Keitt’ fruit had higher contents of hydrogen 
detection and provides appropriate preventive and curative solutions peroxide and lignin in harvested fruit early during storage (Gong 
(Veling et  al., 2019). Thus, a combination of different detection et  al., 2013). These findings highlight the importance of defense 
methods can ensure efficient and accurate disease detection. enzymes and chemicals in mango fruit’s resistance to MAD. It has 
been proposed that these could be utilized as markers to screen for 
mango cultivars with increased resistance to post-harvest illnesses 
9. Chemical and host plant resistance (Gong et al., 2013).
Resistant varieties vary in their ability to suppress disease 
In Taiwan, systemic fungicides known as Benzimidazoles are used development in the crop. The varieties may have specific biochemical 
to control C. gloeosporioides (Chung et al., 2010). Certain strains of differences which enable them to suppress disease development, and 
this fungus show different levels of resistance to Benzimidazole. There humanity can exploit the suppressive ability to overcome the 
are known C. gloeosporioides isolates from resistant crops, but we still problems of resistant strains. In order to understand these 
need a complete picture of their molecular features (Chung et al., biochemical differences, a study was conducted in India to find the 
2010). Benzimidazole-resistant strains have been found in Japan constitutive antifungal phenolic lipids, phenolics contents, and 
(Tashiro et al., 2012). There appears to be a spectrum of resistance antioxidant activities in a resistant variety of mango known as 
among the species in the C. gloeosporioides Species Complex (CGSC), ‘Kensingtonpride’ and two susceptible varieties known as ‘Badami’ 
as determined by genetic analysis (Yokosawa et al., 2017). It has been and ‘Raspuri’; their resistance and susceptibility were to the MAD 
reported that benomyl-resistant C. gloeosporioides f.sp. malvae was (Supriya et al., 2020). Both the 5-n-pentadecyl resorcinol and total 
isolated from uv-irradiated, actively developing mycelium phenolics levels were measured using phytochemical analysis. 
(Holmström-Ruddick and Mortensen, 1995). Mycoherbicide agents Furthermore, the antioxidant potential of the mango peel methanolic 
for round-leaved mallow can be registered for this plant. Benomyl extracts was evaluated using in vitro DPPH assay. The results 
foliar spray has been shown to be quite effective in preventing the demonstrate that early in fruit growth (at 30DFS), ‘Kensington 
spread of C. gloeosporioides; nevertheless, some strains have become pride,’ as opposed to ‘Badami’ and ‘Raspuri,’ has the highest 
resistant to the spray after repeated administration. The amino acid concentration of 5-n-pentadecyl resorcinol in the mango fruit peel 
sequence at the benzimidazole binding site can change because of a extract. High levels (p ≤ 0.05) of constitutive antifungal 
point mutation in a β-tubulin gene resulting in fungal resistance to 5-n-pentadecyl resorcinol in anthracnose-resistant mango cultivar 
benomyl (Maymon et  al., 2006). Two β-tubulin genes have been (‘Kensington pride’) was endogenously produced and retained 
characterized in some Colletotrichum spp., namely TUB1 and TUB2 during the early stage of fruit development. During plants’ growing, 
(Maymon et al., 2006). maturing, and ripening stages, this molecule confers resistance to 
Colletotrichum gloeosporioides has become a global problem disease, and it may serve as a foundation of the plant’s defense 
causing significant economic damage (Chung et al., 2010) with some mechanism against anthracnose (Supriya et al., 2020).
strains being resistant and difficult to control using specific chemicals. The resistant varieties of mango contain fungi toxic levels of 
The microorganism has been classified taxonomically using antifungal resorcinols, which enable the mangoes to resist infection 
microscopic and morphological characteristics. Resistance strains are (Karunanayake et  al., 2014). In China, it has been shown that by 
microorganisms that do not yield to the expected effect of chemicals. manipulating temperatures and carbendazim concentrations, the 
Some phenolic lipids in living organisms include alkyl phenols, alkyl strains of C. gloesporioides resistant to Benzamidazole can be effectively 
resorcinols, anarcadic acids, and alkyl catechols (Supriya et al., 2020). controlled (Lin et al., 2016). Screening of mango hybrids against the 
Alkylresorcinols impart resistance to plants and other living organisms disease is also a step taken by several research institutes (Bally et al., 
against abiotic and biotic stresses (Supriya et al., 2020). They do not 2010). It is advisable to use fungicides to which the strains are not 
only elicit defensive action in plants grown in biotic stress conditions, resistant. Mancozeb and Copper Oxychloride are two fungicides 
but the alkylresorcinols extracted from rye can inhibit the mycelial currently being used, and the latter is known to increase fruit set 
growth of Fusarium culmorum and Rhizoctonia solani. There are also (Uddin et al., 2018).
reports of resistance by C. gloeosporioides to systemic fungicides 
named Benzimidazoles (Chung et al., 2010). Different strains have 
different levels of pathogenicity to different plants (Sanchez-Arizpe 10. Management of the disease
et al., 2021).
Natural disease resistance in Mango varieties is being exploited as Management plans must be cost-effective, efficient, and safe for 
a control against anthracnose disease in mango fruits (Gong et al., the environment, consumers, and agricultural workers. Pre-harvest, 
2013). Different cultivars show different levels of disease resistance. A postharvest, or, ideally, a mix of both treatments are effective ways to 
study was carried out on the resistance of two mango varieties (‘Keitt’ control anthracnose. A wide range of options are available for dealing 
and ‘Zill’) to anthracnose disease. C. gloeosporioides infection of young with MAD in the field. Fungicide spraying, proper cultural techniques, 
or commercially ripe fruit resulted in reduced lesion diameters on and the choice of cultivars are the primary components.
‘Keitt’ fruit compared to ‘Zill’ fruit (Gong et  al., 2013). When The varied responses of cultivars to the disease in various regions 
non-inoculated fruits were harvested at commercial maturity, “Keitt” have prevented resistance from being consistently employed as a 
showed a lower disease index than ‘Zill’, indicating that ‘Keitt’ was method of controlling MAD. With an appropriate mango variety, 
more disease resistant than ‘Zill’ (Gong et al., 2013). More significant growers can grow a crop with fewer incidences of anthracnose, 
amounts of hydrogen peroxide, total phenolic compounds, and lignin resulting in an increased yield and fruit of superior quality. Resistance 
Frontiers in Microbiology 11 frontiersin.org
Dofuor et al. 10.3389/fmicb.2023.1168203
also reduces the need for fungicides to protect the crop, making it pathogens (Zin and Badaluddin, 2020). They have been reported to 
more cost-effective and sustainable (Leadbeater, 2014). be effective in reducing the incidence of MAD by competing with 
Wet conditions or high relative humidity are necessary for the C. gloeosporioides for nutrients and space. However, there is currently 
disease to flourish (Božič and Kanduč, 2021). Therefore, locating no evidence of this finding’s commercial implementation, although it 
farms in areas with a distinct dry season is ideal, as this promotes appears to be quite promising.
disease-free fruit growth. Additionally, it has been suggested that field Recent studies have also revealed the success of using botanicals 
sanitation procedures incorporate collecting and burning trash from to cure MAD (Alemu et al., 2014). The in vitro mycelial growth of 
fallen trees and fruit (Sosnowski et al., 2009). C. gloeosporioides has been demonstrated to be suppressed by aqueous 
Fungicide use has received the majority of the focus and attention extracts of the leaves of Eucalyptus camaldulensis and Azadirachta 
in the fight against anthracnose. Inflorescence and fruit damage are indica. Anthracnose on mango trees was reduced in both occurrence 
minimized with the administration of fungicides. Different fungicides and severity after foliar application of the extracts, even in field 
may be  utilized depending on where the exported fruit will go. settings (Haider et al., 2020). When applied to mangoes before storage, 
Non-systemic fungicides like zineb, maneb, or captan, applied weekly aqueous extracts of Ruta chalepensis at a concentration of 50 grams of 
during blossoming and then monthly during fruit development, were the powdered plant material in 100 mL of distilled water effectively 
shown in early experiments to be  effective against the disease decreased the incidence of anthracnose disease, maintaining quality, 
(Sardrood and Goltapeh, 2018). Applying copper oxychloride or and making the fruits more marketable (Alemu et al., 2014).
copper oxychloride in conjunction with zineb in pre-harvest The inadequacies and inconsistent efficacy of postharvest 
management is recommended for anthracnose control in South Africa treatments demonstrate the need for an integrated strategy in 
every 14 days in wet conditions and every 28 days in dry conditions managing MAD. Figure 4 provides a schematic illustration of the 
(Akem, 2006). In addition, after the fruit had begun to set, mancozeb various management strategies employed to deal with MAD before 
and copper oxychloride were alternated every month until harvest. and after harvest.
Although copper fungicides are recommended, they are not as 
effective as dithiocarbamates when dealing with high disease pressure 
and hence pose a worry for phytotoxicity on mango blossoms (Thind 11. Conclusion and future prospects
and Hollomon, 2018). Fungicides with an after-infection activity, such 
as benzimidazoles and imidazole prochloraz, are effective against MAD is still a widespread fungal disease that lowers production 
MAD. Scheduled applications of benomyl, sometimes in conjunction and quality worldwide. Colletotrichum is endemic to nearly all places 
with protectant fungicides, have been used to halt the development of where mangoes are grown, posing a significant threat to the industry 
resistance in pathogen populations. Both preventative and curative worldwide. Decay patches from dark brown to black appear on leaves, 
applications of prochloraz have been made (Chiangsin et al., 2016). twigs, flowers, and fruits during the pre-and postharvest stages of the 
Prioritizing the reduction of dormant infections on mangoes disease. The pathogenic fungus that causes MAD tends to infest 
could be a mainstay of postharvest management strategies for unripe mango fruits and become dormant until the fruit ripens. The 
MAD. Anthracnose in ripe fruit has been a target of postharvest extensive use of synthetic fungicides to prevent the occurrences of 
treatments for a long time. It has been shown that hot water dips are MAD can lead to environmental pollution, water pollution, soil 
useful for controlling anthracnose (Mirshekari et  al., 2012). compaction, and ecological problems, which then affect the 
Commercially, latent infection is removed using heat, chemicals, or a sustainability of mango production. Research on the biological 
mix of both approaches. It has been suggested to expose subjects to characteristics and behavior of the pathogen, epidemiology, and 
temperatures between 50 and 55°C for exposure durations ranging management of MAD has recently increased. The availability of 
from 3 to 15 min (Mirshekari et al., 2012). To control anthracnose, a genomic data on C. gloeosporioides has provided a better 
variety of fungicides have been used after harvest. Prochloraz and understanding and knowledge of the host-fungal interaction. This has 
Thiabendazole can be utilized. However, their effectiveness varies with also assisted in developing new methods for rapidly detecting 
the severity of the condition (Shi et  al., 2020). One benefit of C. gloeosporioides.
benzimidazole fungicides like benomyl or thiabendazole is that they Significant progress in MAD management has been made, 
work well to suppress stem-end rot on mangoes brought on by especially concerning fungicides and timing treatments, postharvest 
Lasiodiplodia theobromae (Pat.), which is regarded as the second most treatments, and resistant cultivars. However, improper identification 
significant postharvest disease of mango in tropical regions (Shi et al., of closely related species of the pathogen that causes MAD remains a 
2020). Postharvest techniques, including a controlled environment significant challenge in managing the disease. This has been attributed 
and cold storage, maintain resistance to deterioration by postponing to the similarities in the morphological traits of pathogens and their 
the ripening phase. The potential benefit of this strategy has several symptoms on the host plant. Plant breeding projects for developing 
restrictions. Mangoes suffer damage at temperatures below 10 to 13°C new disease-resistant mango cultivars could benefit from a more 
because they are susceptible to chilling (Patel et al., 2016). Disease in-depth understanding of the disease’s epidemiology. There is little 
naturally develops if the fruit is allowed to ripe in natural settings. known about C. gloeosporioides’ population structure, genetic 
There have been limited and inconsistent attempts at postharvest diversity, or sensitivity to varying fungicide concentrations. Further 
biological control of MAD. Numerous microorganisms have been research on the population, diversity, and fungicides sensitivity of the 
implicated in the cases of MAD as having antagonistic relationships pathogen is vital for developing effective management strategies for 
with the disease’s causal agent (C. gloeosporioides) (Kankam et al., the disease.
2022). For example, Trichoderma spp. Bacillus spp. and Pseudomonas MAD remains the most crucial economic disease worldwide in 
spp. are known for their antagonistic properties against plant almost all mango production areas. It requires pre-harvest and 
Frontiers in Microbiology 12 frontiersin.org
Dofuor et al. 10.3389/fmicb.2023.1168203
FIGURE 4
Schematic diagram for the management of mango anthracnose. Options that have had an influence in at least some field settings are indicated by an 
asterisk (*).
postharvest strategies for effective control because it affects nearly all their defense mechanism against the pathogenic fungus. More targets 
of the plant’s above-ground portions. Timely application of appropriate for the development of innovations or fungicides against 
fungicides in the field, good cultural practices, resistant cultivars, and C. gloeosporioides can be found through a systematic investigation of 
appropriate postharvest treatments, such as dip treatments and the manufacturing and signal transduction pathways of pathogenic 
refrigeration, are only some of the management methods that have fungal hormones.
been called for to lessen the impact of this threat. However, picking Pathogenic fungi also release effector proteins, which serve crucial 
the best control approach requires more information about this functions in plant cells and modify the interaction between pathogens 
condition and public awareness. and their hosts. Little is known about the fungal effectors that cause 
Alternatives to fungicides have been developed in light of rising mango disease. The host-plant relationship, the pathogenic fungus’s 
awareness of the fungicides’ deleterious effects on human health, the pathogenic processes, and host plants’ disease-resistance mechanisms 
presence of fungicide residues in mango fruits, and the contamination may all benefit from functional investigations and comparative 
of the natural environment that results from their widespread use. analyses of the C. gloeosporioides effector protein.
Essential oils, botanicals, and oxalic acid treatments have all been The key motivating factors for creating alternative techniques to 
shown to be  effective alternatives to chemical control, especially reduce MAD include the recent understanding of health dangers, the 
in  locations where the use of synthetic fungicides is prohibited. rising customer preference for healthy agricultural products, and the 
Microbial agents and biological control of the MAD have also environmental pollution connected with fungicide usage. Further 
broadened developmental prospects for establishing environmentally research should be encouraged on host-pathogenic fungal interaction, 
friendly pest management. transmission, and effective control techniques. Shortly, research on 
Furthermore, resistance breeding is vital to the control of MAD should be geared toward developing techniques that address 
MAD. Research on host-pathogen interaction and identification of many environmental factors and pathogenic fungal resistance. Future 
fungal genes underlying virulence, phytotoxins of C. gloeosporioides, research on developing and deploying electronic and disease sensors 
and its pathway genes will improve knowledge of resistance for rapid detection of C. gloeosporioides on-site and entry points of 
mechanisms and management of the disease. Invading fungi usually disease-free regions are recommended to minimize the 
secrete plant growth regulators such as auxin, cytokines, ethylene, spread of MAD.
gibberellic acid, jasmonic acid, and salicylic acid. These growth For instance, smartphone-based fingerprinting of leaf volatiles has 
regulators distract plants’ levels of endogenous hormones, weakening may be to detect the late blight of tomatoes. In addition, a microneedle 
Frontiers in Microbiology 13 frontiersin.org
Dofuor et al. 10.3389/fmicb.2023.1168203
patch coupled with a loop-meditated isothermal amplification-based Acknowledgments
sensor may be developed to detect coinfections of late blight and 
spotted wilt virus in tomatoes. These strategies could be adopted for The authors thank Frederick Leo Sossah for his insightful 
MAD and a more comprehensive and coordinated surveillance and comments and contributions to earlier versions of this manuscript.
monitoring strategies for MAD that includes all stakeholders, 
government, and non-government organizations would help to reduce 
the migration of the disease pathogens. Conflict of interest
Furthermore, research programs that focus on disease surveillance 
through risk modeling, bioinformatics tools, and geospatial analytic The authors declare that the research was conducted in the 
tools for mapping and analyzing data about the pathogen and its host absence of any commercial or financial relationships that could 
must be  deployed to respond to potential anthracnose threats in be construed as a potential conflict of interest.
mango production. Global sharing of data or information by 
researchers and policymakers, and identification of a global hot spot 
for new outbreaks of MAD will be needed to manage the disease. Publisher’s note
There is still more to learn about MAD, its detection, and causal 
organism and management strategies. Future research areas should All claims expressed in this article are solely those of the authors 
include; how climate change affects the spread and management of and do not necessarily represent those of their affiliated organizations, 
MAD, sensors for on-site detection, and the deployment of gene or those of the publisher, the editors and the reviewers. Any product 
editing, nanoparticles, and nanotechnology for managing the diseases. that may be evaluated in this article, or claim that may be made by its 
manufacturer, is not guaranteed or endorsed by the publisher.
Author contributions
Supplementary material
AD and OA: study-conceived and designed, writing–original 
draft, review, and editing. NQ, AO, AA-A, BB, FA, KA, HL, SL, JO-O, The Supplementary material for this article can be found online 
JO, WE, and JH: writing–original draft. KN: review and editing. All at: https://www.frontiersin.org/articles/10.3389/fmicb.2023.1168203/
authors approved the submitted version. full#supplementary-material
References
Abang, M. M., Winter, S., Green, K. R., Hoffmann, P., Mignouna, H. D., and Wolf, G. A. Bally, I. S., Akem, C. N., Dillon, N. L., Grice, C., Lakhesar, D., and Stockdale, K. (2010). 
(2002). Molecular identification of Colletotrichum gloeosporioides causing yam anthracnose Screening and breeding for genetic resistance to anthracnose in mango. In IX 
in Nigeria. Plant Pathol. 51, 63–71. doi: 10.1046/j.0032-0862.2001.00655.x International Mango Symposium 992 (pp. 239–244)
Abera, A., Lemessa, F., and Adunga, G. (2016). Morphological characteristics of Barhoom, S., Kupiec, M., Zhao, X., Xu, J. R., and Sharon, A. (2008). Functional 
Colletotrichum species associated with mango (Mangifera indica L.) in Southwest characterization of CgCTR2, a putative vacuole copper transporter that is involved in 
Ethiopia. Food Sci. Qual. Manag. 48, 106–115. germination and pathogenicity in Colletotrichum gloeosporioides. Eukaryot. Cell 7, 
Ahmad, T., Wang, J., Zheng, Y., Mugizi, A. E., Moosa, A., Nie, C., et al. (2021). First 1098–1108. doi: 10.1128/EC.00109-07
record of Colletotrichum alienum causing postharvest anthracnose disease of mango Barhoom, S., and Sharon, A. (2007). Bcl-2 proteins link programmed cell death 
fruit in China. Plant Dis. 105:1852. doi: 10.1094/PDIS-09-20-2074-PDN with growth and morphogenetic adaptations in the fungal plant pathogen 
Ajitomi, A., Takushi, T., Sato, Y., Arasaki, C., and Ooshiro, A. (2020). First report of Colletotrichum gloeosporioides. Fungal Genet. Biol. 44, 32–43. doi: 10.1016/j.
powdery mildew of mango caused by Erysiphe quercicola in Japan. J. Gen. Plant Pathol. fgb.2006.06.007
86, 316–321. doi: 10.1007/s10327-020-00918-2 Benatar, G. V., Wibowo, A., and Suryanti,  (2021). First report of Colletotrichum 
Akem, C. N. (2006). Mango anthracnose disease: present status and future research asianum associated with mango fruit anthracnose in Indonesia. Crop Prot. 141:105432. 
priorities. Plant Pathol. J. 5, 266–273. doi: 10.3923/ppj.2006.266.273 doi: 10.1016/j.cropro.2020.105432
Alberto, L. R., Ardila, C. E. C., and Ortiz, F. A. P. (2022). A computer vision system Bhagwat, R. G., Mehta, B. P., Patil, V. A., and Sharma, H. (2015). Screening of cultivars/
for early detection of anthracnose in sugar mango (Mangifera indica) based on UV-A varieties against mango anthracnose caused by Colletotrichum gloeosporioides. Int. J. 
illumination. Inf. Process. Agric. 10, 204–215. doi: 10.1016/j.inpa.2022.02.001 Environ. Agric. Res. 1, 21–23.
Alemu, K., Ayalew, A., and Woldetsadik, K. (2014). Antifungal activity of plant Bordoh, P. K., Ali, A., Dickinson, M., Siddiqui, Y., and Romanazzi, G. (2020). A review 
extracts and their applicability in extending the shelf-life of mango fruits. Food Sci. Qual. on the management of postharvest anthracnose in dragon fruits caused by Colletotrichum 
Manag. 33, 47–53. spp. Crop Prot. 130:105067. doi: 10.1016/j.cropro.2019.105067
Alkan, N., Meng, X., Friedlander, G., Reuveni, E., Sukno, S., Sherman, A., et al. (2013). Božič, A., and Kanduč, M. (2021). Relative humidity in droplet and airborne 
Global aspects of pacC regulation of pathogenicity genes in Colletotrichum transmission of disease. J. Biol. Phys. 47, 1–29. doi: 10.1007/s10867-020-09562-5
gloeosporioides as revealed by transcriptome analysis. Mol. Plant-Microbe Interact. 26, Caicedo, J. D., Lalangui, K. P., Pozo, A. N., Cevallos, P. A., Arahana, V. S., and 
1345–1358. doi: 10.1094/MPMI-03-13-0080-R Méndez, K. S. (2017). Multilocus molecular identification and phylogenetic analysis of 
Anderson, J. M., Aitken, E. A. B., Dann, E. K., and Coates, L. M. (2013). Morphological Colletotrichum tamarilloi as the causal agent of Tamarillo (Solanum betaceum) 
and molecular diversity of Colletotrichum spp. causing pepper spot and anthracnose of anthracnose in the Ecuadorian highlands. Europ. J. Plant Pathol. 148, 983–996. doi: 
lychee (Litchi chinensis) in Australia. Plant Pathol. 62, 279–288. doi: 10.1007/s10658-017-1155-3
10.1111/j.1365-3059.2012.02632.x Cannon, P. F., Damm, U., Johnston, P. R., and Weir, B. S. (2012). Colletotrichum: 
Arauz, L. F. (2000). Mango anthracnose: economic impact and current options for current status and future directions. Stud. Mycol. 73, 181–213. doi: 10.3114/
integrated managaement. Plant Dis. 84, 600–611. doi: 10.1094/PDIS.2000.84.6.600 sim0014
Ashraful, A., Sanjoy, K. A., and Mahtalat, A. (2017). Morphological characterization Cao, X. R., Xu, X. M., Che, H. Y., West, J. S., and Luo, D. Q. (2019). Characteristics and 
of Colletotrichum gloeosporioiedes identified from anthracnose of Mangifera indica L. distribution of Colletotrichum species in coffee plantations in Hainan, China. Plant 
Asian J. Plant. Pathol. 11, 102–117. doi: 10.3923/ajppaj.2017.102.117 Pathol. 68, 1146–1156. doi: 10.1111/ppa.13028
Awa, O. C., Samuel, O., Oworu, O. O., and Sosanya, O. (2012). First report of fruit Castillo, S. R. M., Miller, S., and Stewart, J. (2022). Colletotrichum spp. and other fungi 
anthracnose in mango caused by Colletotrichum gloeosporioides in southwestern Nigeria. associated with anthracnose on Coffea arabica L. in Mérida state, Venezuela. Summa 
Int. J. Sci. Technol. Res. 1, 30–34. Phytopathol. 48, 99–111. doi: 10.1590/0100-5405/245876
Frontiers in Microbiology 14 frontiersin.org
Dofuor et al. 10.3389/fmicb.2023.1168203
Chagué, V., Maor, R., and Sharon, A. (2009). CgOpt1, a putative oligopeptide Gautam, C., Prabhu, H. V., and Nargund, V. B. (2017). In vitro evaluation of fungicides, 
transporter from Colletotrichum gloeosporioides that is involved in responses to auxin botanicals and bioagents against Peziotrichum corticolum causing black banded disease 
and pathogenicity. BMC Microbiol. 9, 1–12. doi: 10.1186/1471-2180-9-173 of mango. Int. J. Curr. Microbiol. Appl. Sci. 6, 652–661. doi: 10.20546/ijcmas.2017.603.076
Chala, A., Getahun, M., Alemayehu, S., and Tadesse, M. (2014). Survey of mango Gong, D. Q., Zhu, S. J., Gu, H., Zhang, L. B., Hong, K. Q., and Xie, J. H. (2013). Disease 
anthracnose in southern Ethiopia and in-vitro screening of some essential oils against resistance of ‘Zill’and ‘Keitt’mango fruit to anthracnose in relation to defence enzyme 
Colletotrichum gloeosporioides. Int. J. Fruit Sci. 14, 157–173. doi: 10.1080/15538362.2013.817899 activities and the content of anti-fungal substances. J. Hortic. Sci. Biotechnol. 88, 
Cheng, Y. J., Wu, Y. J., Lee, F. W., Ou, L. Y., Chen, C. N., Chu, Y. Y., et al. (2022). Impact 243–250. doi: 10.1080/14620316.2013.11512962
of storage condition on chemical composition and antifungal activity of pomelo extract Grammen, A., Wenneker, M., Van Campenhout, J., Pham, K. T. K., Van Hemelrijck, W., 
against Colletotrichum gloeosporioides and anthracnose in post-harvest mango. Plan. Bylemans, D., et al. (2019). Identification and pathogenicity assessment of Colletotrichum 
Theory 11:2064. doi: 10.3390/plants11152064 isolates causing bitter rot of apple fruit in Belgium. Eur. J. Plant Pathol. 153, 47–63. doi: 
Chiangsin, R., Wanichkul, K., Guest, D. I., and Sangchote, S. (2016). Reduction of 10.1007/s10658-018-1539-z
anthracnose on ripened mango fruits by chemicals, fruit bagging, and postharvest Grice, K. R. E., Bally, I. S. E., Wright, C. L., Maddox, C., Ali, A., and Dillon, N. L. 
treatments. Australas. Plant Pathol. 45, 629–635. doi: 10.1007/s13313-016-0456-x (2022). Mango germplasm screening for the identification of sources of tolerance to 
anthracnose. Australas. Plant Pathol. 52, 27–41. doi: 10.1007/s13313-022-00899-0
Chowdhury, M. N., and Rahim, M. A. (2009). Integrated crop management to control 
anthracnose (Colletotrichum gloeosporioides) of mango. J. Agric. Ext. Rural Dev., Guevara-Suarez, M., Cárdenas, M., Jiménez, P., Afanador-Kafuri, L., and Restrepo, S. 
115–120. doi: 10.3329/jard.v7i1.4430 (2022). Colletotrichum species complexes associated with crops in northern South 
America: a review. Agronomy 12:548. doi: 10.3390/agronomy12030548
Chung, W. H., Chung, W. C., Peng, M. T., Yang, H. R., and Huang, J. W. (2010). 
Specific detection of benzimidazole resistance in Colletotrichum gloeosporioides from Haider, E., Khan, M. A., Atiq, M., Shahbaz, M., and Yaseen, S. (2020). Phytoextracts 
fruit crops by PCR-RFLP. New Biotechnol. 27, 17–24. doi: 10.1016/j.nbt.2009.10.004 as management tool against fungal diseases of vegetables. Int. J. Biosci. 16, 303–314. doi: 
10.12692/ijb/16.3.303-314
Ciofini, A., Negrini, F., Baroncelli, R., and Baraldi, E. (2022). Management of Post-
Harvest Anthracnose: current approaches and future perspectives. Plan. Theory 11:1856. Hofer, K. M., Braithwaite, M., Braithwaite, L. J., Sorensen, S., Siebert, B., Pather, V., 
doi: 10.3390/plants11141856 et al. (2021). First report of Colletotrichum fructicola, C. perseae, and C. siamense causing 
anthracnose disease of avocado (Persea americana) in New Zealand. Plant Dis. 105:1564. 
Corda, A. C. I. (1831). “Die Pilze Deutschlands” in Deutschlands Flora in Abbildungen doi: 10.1094/PDIS-06-20-1313-PDN
nach der Natur mit Beschreibungen. ed. J. Sturm, vol. 3 (Nürnberg: Sturm), 33–64.
Holmström-Ruddick, B., and Mortensen, K. (1995). Factors affecting pathogenicity 
Corkidi, G., Balderas-Ruíz, K. A., Taboada, B., Serrano-Carreón, L., and Galindo, E. (2006). of a benomyl-resistant strain of Colletotrichum gloeosporioides f. sp. malvae. Mycol. Res. 
Assessing mango anthracnose using a new three-dimensional image-analysis technique to 99, 1108–1112. doi: 10.1016/S0953-7562(09)80780-6
quantify lesions on fruit. Plant Pathol. 55, 250–257. doi: 10.111/j.1365-3059.2005.01321.x
Honger, J. O., Offei, S. K., Oduro, K. A., and Odamtten, G. T. (2015). Nature of mango 
Costa, J. F., Kamei, S. H., Silva, J. R. A., Miranda, A. R. G. D. S., Netto, M. B., da anthracnose in Ghana: implications for the control of the disease. Ghana J. Agric. Sci. 
Silva, S. J. C., et al. (2019). Species diversity of Colletotrichum infecting Annona spp. in 49, 53–67.
Brazil. Europ. J. Plant Pathol. 153, 1119–1130. doi: 10.1007/s10658-018-01630-w
Honger, J. O., Offei, S. K., Oduro, K. A., Odamtten, G. T., and Nyaku, S. T. (2014). 
Cristóbal-Martínez, A. L., de Jesús Yáñez-Morales, M., Solano-Vidal, R., Identification and species status of the mango biotype of Colletotrichum gloeosporioides 
Segura-León, O., and Hernández-Anguiano, A. M. (2017). Diversity of Colletotrichum in Ghana. Eur. J. Plant Pathol. 140, 455–467. doi: 10.1007/s10658-014-0480-z
species in coffee (Coffea arabica) plantations in Mexico. Eur. J. Plant Pathol. 147, 
605–614. doi: 10.1007/s10658-016-1029-0 Hossain, A. A., and Ahmed, A. (1994). A monograph on mango varieties of Bangladesh. 
Dhaka: Bangladesh Agricultural Research Institute.
Damm, U., Cannon, P. F., Woudenberg, J. H. C., and Crous, P. W. (2012). The 
Colletotrichum acutatum species complex. Stud. Mycol. 73, 37–113. doi: 10.3114/ Ismail, A. M., Cirvilleri, G., Yaseen, T., Epifani, F., Perrone, G., and Polizzi, G. (2015). 
sim0010 Characterisation of Colletotrichum species causing anthracnose disease of mango in 
Italy. J. Plant Pathol., 167–171. doi: 10.4454/JPP.V97I1.011
De Jonge, R., Peter van Esse, H., Kombrink, A., Shinya, T., Desaki, Y., Bours, R., et al. 
(2010). Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in Ismail, A. M., and El-Ganainy, S. M. (2022). Characterization of Colletotrichum species 
plants. Science 329, 953–955. doi: 10.1126/science.1190859 associating with anthracnose disease of mango in Egypt. J. Plant Dis. Prot. 129, 449–454. 
doi: 10.1007/s41348-021-00538-8
De Souza, A., Delphino Carboni, R. C., Wickert, E., de Macedo Lemos, E. G., and de 
Goes, A. (2013). Lack of host specificity of Colletotrichum spp. isolates associated with Janamatti, A. T., Kumar, A., Kaur, C., Gogoi, R., Varghese, E., and Kumar, S. (2022). 
anthracnose symptoms on mango in Brazil. Plant Pathol. 62, 1038–1047. doi: 10.1111/ Fumigation by bacterial volatile 2, 5-dimethylpyrazine enhances anthracnose resistance 
ppa.12021 and shelf life of mango. Eur. J. Plant Pathol. 164, 209–227. doi: 10.1007/
s10658-022-02551-5
Dela Cueva, F. M., Laurel, N. R., Dalisay, T. U., and Sison, M. L. J. (2021). Identification 
and characterisation of Colletotrichum fructicola, C. tropicale and C. theobromicola Jenny, F., Sultana, N., Islam, M., Khandaker, M. M., and Bhuiyan, M. A. B. (2019). A 
causing mango anthracnose in the Philippines. Arch. Phytopathol. 54, 1989–2006. doi: review on anthracnose of mango caused by Colletotrichum gloeosporioides. Bangladesh 
10.1080/03235408.2021.1968234 J. Plant Phytopathol. 35, 65–74.
Dembele, D. D., Camara, B., Grechi, I., Rey, J. Y., and Kone, D. (2019). Pre and Kadam, J. A., Shimpi, S. B., Biradar, R. P., and Chate, S. V. (2002). Review on post 
postharvest assessment of mango anthracnose incidence and severity in the north of harvest diseases and management of mango fruits. J. Plant Pathol. Microbiol. 13:1000635.
Côte d’Ivoire. Int. J. Biol. Chem. Sci. 10, 33–43. doi: 10.3923/IJAR.2015.33.43 Kamle, M., and Kumar, P. (2016). Colletotrichum gloeosporioides: pathogen of 
Doyle, V. P., Oudemans, P. V., Rehner, S. A., and Litt, A. (2013). Habitat and host anthracnose disease in mango (Mangifera indica L.). Curr. Trends Plant Dis. Diagn. 
indicate lineage identity in Colletotrichum gloeosporioides sl from wild and agricultural Manag. Pract., 207–219. doi: 10.1007/978-3-319-27312-9_9
landscapes in North America. PLoS One 8:e62394. doi: 10.1371/journal.pone.0062394 Kamle, M., Pandey, B. K., Kumar, P., and Kumar, M. (2013). A species-specific PCR 
Drori, N., Kramer-Haimovich, H., Rollins, J., Dinoor, A., Okon, Y., Pines, O., et al. based assay for rapid detection of mango anthracnose pathogen Colletotrichum 
(2003). External pH and nitrogen source affect secretion of pectate lyase by gloeosporioides Penz. And Sacc. J. Plant Pathol. Microbiol. 4:184. doi: 
Colletotrichum gloeosporioides. Appl. Environ. Microbiol. 69, 3258–3262. doi: 10.1128/ 10.4172/2157-7471.1000184
AEM.69.6.3258-3262.2003 Kankam, F., Larbi-Koranteng, S., Adomako, J., Kwodaga, J. K., Akpatsu, I. B., Danso, Y., 
Evangelista-Martínez, Z., Ek-Cen, A., Torres-Calzada, C., and Uc-Várguez, A. (2022). et al. (2022). “Anthracnose disease of mango: epidemiology, impact and management 
Potential of Streptomyces sp. strain AGS-58  in controlling anthracnose-causing options” in Current and emerging challenges in the diseases of trees (London: IntechOpen)
Colletotrichum siamense from post-harvest mango fruits. J. Plant Pathol. 104, 553–563. Karunanayake, K. O. L. C., Sinniah, G. D., Adikaram, N. K. B., and Abayasekara, C. L. 
doi: 10.1007/s42161-022-01104-3 (2014). Cultivar differences in antifungal activity and the resistance to postharvest 
Feng, G., Zhang, X. S., Zhang, Z. K., Ye, H. C., Liu, Y. Q., Yang, G. Z., et al. (2019). anthracnose and stem-end rot in mango (Mangifera indica L.). Australas. Plant Pathol. 
Fungicidal activities of camptothecin semisynthetic derivatives against Colletotrichum 43, 151–159. doi: 10.1007/s13313-013-0257-4
gloeosporioides in vitro and in mango fruit. Postharvest Biol. Technol. 147, 139–147. doi: Khan, M. S., Uandai, S. B., and Srinivasan, H. (2019). Anthracnose disease diagnosis 
10.1016/j.postharvbio.2018.09.019 by image processing, support vector machine and correlation with pigments. J. Plant 
Freeman, S., Minz, D., Jurkevitch, E., Maymon, M., and Shabi, E. (2000). Molecular Pathol. 101, 749–751. doi: 10.1007/s42161-019-00268-9
analyses of Colletotrichum species from almond and other fruits. Phytopathology 90, Kim, Y. K., Wang, Y., Liu, Z. M., and Kolattukudy, P. E. (2002). Identification of a hard 
608–614. doi: 10.1094/PHYTO.2000.90.6.608 surface contact-induced gene in Colletotrichum gloeosporioides conidia as a sterol 
Fujikawa, T., Sakaguchi, A., Nishizawa, Y., Kouzai, Y., Minami, E., Yano, S., et al. glycosyl transferase, a novel fungal virulence factor. Plant J. 30, 177–187. doi: 10.1046/j.
(2012). Surface α-1, 3-glucan facilitates fungal stealth infection by interfering with 1365-313x.2002.01284.x
innate immunity in plants. PLoS Pathog. 8:e1002882. doi: 10.1371/journal.ppat.1002882 Kramer-Haimovich, H., Servi, E., Katan, T., Rollins, J., Okon, Y., and Prusky, D. 
Gan, P., Ikeda, K., Irieda, H., Narusaka, M., O'Connell, R. J., Narusaka, Y., et al. (2013). (2006). Effect of ammonia production by Colletotrichum gloeosporioides on pelB 
Comparative genomic and transcriptomic analyses reveal the hemibiotrophic stage shift activation, pectate lyase secretion, and fruit pathogenicity. Appl. Environ. Microbiol. 72, 
of Colletotrichum fungi. New Phytol. 197, 1236–1249. doi: 10.1111/nph.12085 1034–1039. doi: 10.1128/AEM.72.2.1034-1039.2006
Frontiers in Microbiology 15 frontiersin.org
Dofuor et al. 10.3389/fmicb.2023.1168203
Kumari, C., Sharma, M., Kumar, V., Sharma, R., Kumar, V., Sharma, P., et al. (2022). Marikar, F. M. M. T., Sivakumar, D., and Wijerathnam, R. W. (2008). Biological control 
Genome editing technology for genetic amelioration of fruits and vegetables for of rambutan post-harvest anthracnose (Colleotrichum gloeosporioides) by combined 
alleviating post-harvest loss. Bioengineering 9:176. doi: 10.3390/bioengineering9040176 treatment of Trichoderma harzianum-TrH40 culture filtrates and calcium salts. Food 
Kumari, P., Singh, R., and Punia, R. (2017). Survival of Colletotrichum gloeosporioides Biotechnol. 22, 326–337. doi: 10.1080/08905430802458412
causing anthracnose of mango at different depths and durations in soil. J. Pharmacogn. Maske, J. M., Masih, S., and Verma, O. P. (2022). A review on morphological and 
Phytochem. 6, 2194–2198. molecular characterization of Colletotrichum species associated with mango anthracnose 
Kunta, M., Park, J. W., Vedasharan, P., da Graça, J. V., and Terry, M. D. (2018). First in Konkan region of Maharashtra state. J. Pharm. Innov. 11, 1577–1581.
report of Colletotrichum queenslandicum on persian lime causing leaf anthracnose in the Maymon, M., Zveibil, A., Pivonia, S., Minz, D., and Freeman, S. (2006). Identification 
United States. Plant Dis. 102:677. doi: 10.1094/PDIS-09-17-1382-PDN and characterization of benomyl-resistant and-sensitive populations of Colletotrichum 
Lai, A. A., and Simon, S. (2013). Post harvest management of anthracnose rot of gloeosporioides from statice (Limonium spp.). Phytopathology 96, 542–548. doi: 10.1094/
mango (Mangifera indica l.). Ann. Plant Prot. Sci. 21, 121–124. PHYTO-96-0542
Leadbeater, A. J. (2014). Plant health management: fungicides and antibiotics, McCulloch, M. J., Gauthier, N. W., and Vaillancourt, L. J. (2020). First report of bitter 
encyclopedia of agriculture and food systems. Biology. doi: 10.1016/ rot of apple caused by a Colletotrichum sp. in the C. kahawae clade in Kentucky. Plant 
B978-0-444-52512-3.00179-0 Dis. 104:289. doi: 10.1094/PDIS-06-19-1247-PDN
Li, Q., Bu, J., Shu, J., Yu, Z., Tang, L., Huang, S., et al. (2019). Colletotrichum species Mirshekari, A., Ding, P., Kadir, J., and Ghazali, H. M. (2012). Effect of hot water dip 
associated with mango in southern China. Sci. Rep. 9:18891. doi: 10.1038/ treatment on postharvest anthracnose of banana var Berangan. Afr. J. Agric. Res. 7, 6–10. 
s41598-019-54809-4 doi: 10.5897/AJAR11.056
Li, Q., Shu, J., Tang, L., Huang, S., Guo, T., Mo, J., et al. (2020). First report of mango Miyara, I., Shnaiderman, C., Meng, X., Vargas, W. A., Diaz-Minguez, J. M., 
leaf anthracnose caused by Colletotrichum asianum in Vietnam. Plant Dis. 104:1558. doi: Sherman, A., et al. (2012). Role of nitrogen-metabolism genes expressed during 
10.1094/PDIS-09-19-1830-PDN pathogenicity of the alkalinizing Colletotrichum gloeosporioides and their differential 
expression in acidifying pathogens. Mol. Plant-Microbe Interact. 25, 1251–1263. doi: 
Liang, Y. S., Fu, J. Y., Chao, S. H., Tzean, Y., Hsiao, C. Y., Yang, Y. Y., et al. (2022). Postharvest 10.1094/MPMI-01-12-0017-R
application of Bacillus amyloliquefaciens PMB04 fermentation broth reduces anthracnose 
occurrence in mango fruit. Agriculture 12:1646. doi: 10.3390/agriculture12101646 Mo, J., Zhao, G., Li, Q., Solangi, G. S., Tang, L., Guo, T., et al. (2018). Identification and 
characterization of Colletotrichum species associated with mango anthracnose in 
Lima, N. B., De Batista, M. V. A., De Morais, M. A., Barbosa, M. A., Michereff, S. J., Guangxi, China. Plant Dis. 102, 1283–1289. doi: 10.1094/PDIS-09-17-1516-RE
Hyde, K. D., et al. (2013a). Five Colletotrichum species are responsible for mango anthracnose 
in northeastern Brazil. Fungal Divers. 61, 75–88. doi: 10.1007/s13225-013-0237-6 Moraes, S. R. G., Tanaka, F. A. O., and Massola Júnior, N. S. (2013). Histopathology 
of Colletotrichum gloeosporioides on guava fruits (Psidium guajava L.). Rev. Bras. Frutic. 
Lima, N. B., Lima, W. G., Tovar-Pedraza, J. M., Michereff, S. J., and Câmara, M. P. 35, 657–664. doi: 10.1590/S0100-29452013000200039
(2015). Comparative epidemiology of Colletotrichum species from mango in 
northeastern Brazil. Eur. J. Plant Pathol. 141, 679–688. doi: 10.1007/s10658-014-0570-y Münch, S., Lingner, U., Floss, D. S., Ludwig, N., Sauer, N., and Deising, H. B. (2008). 
The hemibiotrophic lifestyle of Colletotrichum species. J. Plant Physiol. 165, 41–51. doi: 
Lima, N. B., Marques, M. W., Michereff, S. J., Morais, M. A. Jr., Barbosa, M. A. G., and 10.1016/j.jplph.2007.06.008
Camara, M. P. S. (2013b). First report of mango anthracnose caused by Colletotrichum 
karstii in Brazil. Plant Dis. 97:1248. doi: 10.1094/PDIS-01-13-0002-PDN Munir, M., Amsden, B., Dixon, E., Vaillancourt, L., and Gauthier, N. W. (2016). 
Characterization of Colletotrichum species causing bitter rot of apple in Kentucky 
Lin, C. H., Long, X. P., Li, Z. P., Zhang, Y., He, J. J., Liu, W. B., et al. (2020). First report orchards. Plant Dis. 100, 2194–2203. doi: 10.1094/PDIS-10-15-1144-RE
of anthracnose of Clausena lansium caused by Colletotrichum scovillei in China. Plant 
Dis. 104:1557. doi: 10.1094/PDIS-08-19-1765-PDN Nelson, S. C. (2008). Mango anthracnose (Colletotrichum gloeosporiodes). Plant Dis. 
48, 1–9.
Lin, T., Xu, X. F., Dai, D. J., Shi, H. J., Wang, H. D., and Zhang, C. Q. (2016). 
Differentiation in development of benzimidazole resistance in Colletotrichum Nesher, I., Minz, A., Kokkelink, L., Tudzynski, P., and Sharon, A. (2011). Regulation 
gloeosporioides complex populations from strawberry and grape hosts. Australas. Plant of pathogenic spore germination by CgRac1 in the fungal plant pathogen Colletotrichum 
Pathol. 45, 241–249. doi: 10.1007/s13313-016-0413-8 gloeosporioides. Eukaryot. Cell 10, 1122–1130. doi: 10.1128/EC.00321-10
Lisboa, D. O., Silva, M. A., Pinho, D. B., Pereira, O. L., and Furtado, G. Q. (2018). Ntsoane, M. L., Zude-Sasse, M., Mahajan, P., and Sivakumar, D. (2019). Quality 
Diversity of pathogenic and endophytic Colletotrichum isolates from Licania tomentosa assesment and postharvest technology of mango: A review of its current status and 
in Brazil. For. Pathol. 48:e12448. doi: 10.1111/efp.12448 future perspectives. Sci. Hortic. 249, 77–85. doi: 10.1016/j.scienta.2019.01.033
Liu, Y., An, F., Zhang, Y., Fu, C., and Su, Y. (2021). First report of anthracnose on Oh, B. J., Ko, M. K., Kim, Y. S., Kim, K. S., Kostenyuk, I., and Kee, H. K. (1999). A 
Jerusalem cherry caused by Colletotrichum liaoningense in Shandong, China. Plant Dis. cytochrome P450 gene is differentially expressed in compatible and incompatible 
105:2248. doi: 10.1094/PDIS-01-21-0124-PDN interactions between pepper (Capsicum annuum) and the anthracnose fungus, 
Colletotrichum gloeosporioides. Mol. Plant-Microbe Interact. 12, 1044–1052. doi: 10.1094/
Liu, F., Damm, U., Cai, L., and Crous, P. W. (2013). Species of the Colletotrichum MPMI.1999.12.12.1044
gloeosporioides complex associated with anthracnose diseases of Proteaceae. Fungal 
Divers. 61, 89–105. doi: 10.1007/s13225-013-0249-2 Onyeani, C. A., and Amusa, N. A. (2015). Incidence and severity of anthracnose in 
mango fruits and its control with plant extracts in south West Nigeria. Int. J. Agric. Res. 
Liu, H. N., Liu, J. A., and Zhou, G. Y. (2020). First report of Colletotrichum alienum 10, 33–43. doi: 10.3923/IJAR.2015.33.43
causing anthracnose on Aquilaria sinensis in China. Plant Dis. 104:283. doi: 10.1094/
PDIS-01-19-0155-PDN Pardo-De la Hoz, C. J., Calderón, C., Rincón, A. M., Cárdenas, M., Danies, G., 
López-Kleine, L., et al. (2016). Species from the Colletotrichum acutatum, Colletotrichum 
Liu, L. P., Shu, J., Zhang, L., Hu, R., Chen, C. Q., Yang, L. N., et al. (2017). First report boninense and Colletotrichum gloeosporioides species complexes associated with tree 
of post-harvest anthracnose on mango (Mangifera indica) caused by Colletotrichum tomato and mango crops in Colombia. Plant Pathol. 65, 227–237. doi: 10.1111/
siamense in China. Plant Dis. 101:833. doi: 10.1094/PDIS-08-16-1130-PDN ppa.12410
Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P. M., and Henrissat, B. Patel, B., Tandel, Y. N., Patel, A. H., and Patel, B. L. (2016). Chilling injury in tropical 
(2014). The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. and subtropical fruits: A cold storage problem and its remedies: A review. Int. J. Environ. 
42, D490–D495. doi: 10.1093/nar/gkt1178 Sci. Technol. 5, 1882–1887.
Lopes, L. H. R., Boiteux, L. S., Rossato, M., Aguiar, F. M., Fonseca, M. E., Oliveira, V. R., Patil, R. Y., Gulvani, S., Waghmare, V. B., and Mujawar, I. K. (2022). Image based 
et al. (2021). Diversity of Colletotrichum species causing onion anthracnose in Brazil. anthracnose and red-rust leaf disease detection using deep learning. Telkomnika 20, 
Eur. J. Plant Pathol. 159, 339–357. doi: 10.1007/s10658-020-02166-8 1256–1263. doi: 10.12928/telkomnika.v20i6.24262
Mabbett, T. (2014). Disease management in mango. Int. Pest Control 56:104. Patrice, N. D., Alain, H., Bertrand, M. S., Norbert, K. T., Nourou, K. N., Brice, T. T., 
Maharaj, A., and Rampersad, S. N. (2012). Genetic differentiation of Colletotrichum et al. (2020). First report of red rust disease caused by Cephaleuros virescens on mango 
gloeosporioides and C. truncatum associated with anthracnose disease of papaya (Carica (Mangifera indica) tree in Cameroon. Int. J. Phytopathol. 9, 187–193. doi: 10.33687/
papaya L.) and bell pepper (Capsium annuum L.) based on ITS PCR-RFLP phytopath.009.03.3432
fingerprinting. Mol. Biotechnol. 50, 237–249. doi: 10.1007/s12033-011-9434-2 Paudel, A., Poudel, P., and Yogi, M. (2022). Insights on the mango anthracnose and its 
Malik, M. T., Ammar, M., Ranan, M., Rehman, A., and Bally, I. S. (2014). Chemical management. J Plant Pathol. Res. 4, 81–90. doi: 10.36959/394/629
and cultural management of die back disease of mango in Pakistan. In XXIX Paulitz, T. C. (1995). First report of Colletotrichum gloeosporioides on lupine in 
International Horticultural Congress on Horticulture: Sustaining Lives, Livelihoods and Canada. Plant Dis. 79:319. doi: 10.1094/PD-79-0319D
Landscapes (IHC2014): IV 1111 (pp. 363–368).
Peres, N. A., Kuramae, E. E., Dias, M. S., and De Souza, N. L. (2002). Identification 
Manzano León, A. M., Serra Hernández, W., García Pérez, L., Crespo, K., and and characterization of Colletotrichum spp. affecting fruit after harvest in Brazil. J. 
Guarnaccia, V. (2018). First report of leaf anthracnose caused by Colletotrichum grossum on Phytopathol. 150, 128–134. doi: 10.1046/j.1439-0434.2002.00732.x
mango (Mangifera indica) in Cuba. J. Plant Pathol. 100:329. doi: 10.1007/s42161-018-0040-z
Pérez-Mora, J. L., Mora-Romero, G. A., Beltrán-Peña, H., García-León, E., Lima, N. B., 
Marcianò, D., Mizzotti, C., Maddalena, G., and Toffolatti, S. L. (2021). The dark side Camacho-Tapia, M., et al. (2021). First report of Colletotrichum siamense and C. 
of Fungi: how they cause diseases in plants. Front. Young Minds 9:315. doi: 10.3389/ gloeosporioides causing anthracnose of Citrus spp. in Mexico. Plant Dis. 105:496. doi: 
frym.2021.560315 10.1094/PDIS-08-20-1743-PDN
Frontiers in Microbiology 16 frontiersin.org
Dofuor et al. 10.3389/fmicb.2023.1168203
Prabu, M., and Chelliah, B. J. (2022). Mango leaf disease identification and programmes for plant pathogen eradication. Plant Pathol. 58, 621–635. doi: 
classification using a CNN architecture optimized by crossover-based levy flight 10.1111/j.1365-3059.2009.02042.x
distribution algorithm. Neural Comput. Appl. 34, 7311–7324. doi: 10.1007/
s00521-021-06726-9 Stephenson, S. A., Hatfield, J., Rusu, A. G., Maclean, D. J., and Manners, J. M. (2000). CgDN3: an essential pathogenicity gene of Colletotrichum gloeosporioides necessary to 
Prakash, O., and Srivastava, K. C. (1987). Mango diseases and their management. A avert a hypersensitive-like response in the host Stylosanthes guianensis. Mol. Plant-
world review. Today and Tomorrow's Printers and Publishers: New Delhi. Microbe Interact. 13, 929–941. doi: 10.1094/MPMI.2000.13.9.929
Qin, L. P., Zhang, Y., Su, Q., Chen, Y. L., Nong, Q., Xie, L., et al. (2019). First report of Su, Y. Y., Noireung, P., Liu, F., Hyde, K. D., Moslem, M. A., Bahkali, A. H., et al. (2011). 
anthracnose of Mangifera indica caused by Colletotrichum scovillei in China. Plant Dis. Epitypification of Colletotrichum musae, the causative agent of banana anthracnose. 
103:1043. doi: 10.1094/PDIS-11-18-1980-PDN Mycoscience 52, 376–382. doi: 10.1007/s10267-011-0120-9
Reyes-Perez, J. J., Hernandez-Montiel, L. G., Vero, S., Noa-Carrazana, J. C., Supriya, A., Kumar, A., and Kudachikar, V. B. (2020). A comparison investigation on 
Quiñones-Aguilar, E. E., and Rincón-Enríquez, G. (2019). Postharvest biocontrol of antioxidant activities, constitutive antifungal phenolic lipids and phenolics contents of 
Colletotrichum gloeosporioides on mango using the marine bacterium Stenotrophomonas anthracnose resistant and susceptible mango fruit cultivars. Int. J. Fruit Sci. 20, 692–704. 
rhizophila and its possible mechanisms of action. J. Food Sci. Technol. 56, 4992–4999. doi: 10.1080/15538362.2019.1668332
doi: 10.1007/s13197-019-03971-8 Talhinhas, P., and Baroncelli, R. (2021). Colletotrichum species and complexes: 
Rodriguez-Moreno, L., Ebert, M. K., Bolton, M. D., and Thomma, B. P. (2018). Tools geographic distribution, host range and conservation status. Fungal Divers. 110, 
of the crook-infection strategies of fungal plant pathogens. Plant J. 93, 664–674. doi: 109–198. doi: 10.1007/s13225-021-00491-9
10.1111/tpj.13810 Talhinhas, P., Loureiro, A., and Oliveira, H. (2018). Olive anthracnose: a yield-and oil 
Rosman, N. F., Asli, N. A., Abdullah, S., and Rusop, M. (2019). “Some common disease in quality-degrading disease caused by several species of Colletotrichum that differ in 
mango” in AIP conference proceedings, vol. 2151 (New York: AIP Publishing LLC), 020019. virulence, host preference and geographical distribution. Mol. Plant Pathol. 19, 
Saeed, E. E., Sham, A., AbuZarqa, A., Al Shurafa, K. A., Al Naqbi, T. S., Iratni, R., et al. 1797–1807. doi: 10.1111/mpp.12676
(2017). Detection and management of mango dieback disease in the Tashiro, N., Manabe, K., and Ide, Y. (2012). Emergence and frequency of highly 
United Arab Emirates. Int. J. Mol. Sci. 18:2086. doi: 10.3390/ijms18102086 benzimidazole-resistant Colletotrichum gloeosporioides, pathogen of Japanese pear 
Sanchez-Arizpe, A., Galindo-Cepeda, M. E., Arispe-Vazquez, J. L., anthracnose, after discontinued use of benzimidazole. J. Gen. Plant Pathol. 78, 221–226. 
Genis-Velazquez, R., Vazquez-Badillo, M. E., and Antonio-Bautista, A. (2021). Natural doi: 10.1007/s10327-012-0375-9
resistance of two Mango'mangifera indica'l. commercial cultivars to anthracnose caused Theerthagiri, A., Govindasamy, S., Thiruvengadam, R., and Ramasamy, S. (2016). 
by'Colletotrichum gloeosporioides' Penz. Penz. and Sacc. Aust. J. Crop Sci. 15, Immunoassay-based techniques for early and specific detection of latent postharvest 
1198–1203. doi: 10.21475/ajcs.21.15.08.p3347 anthracnose in mango. J. Phytopathol. 164, 318–329. doi: 10.1111/jph.12459
Sardrood, B. P., and Goltapeh, E. M. (2018). “Effect of agricultural chemicals and Thind, T. S., and Hollomon, D. W. (2018). Thiocarbamate fungicides: reliable tools in 
organic amendments on biological control Fungi” in Sustainable Agriculture Reviews. resistance management and future outlook. Pest Manag. Sci. 74, 1547–1551. doi: 
ed. E. Lichtfouse, vol. 12 (Berlin: Springer), 217–359. 10.1002/ps.4844
Sardsud, U., Sardsud, V., and Singkaew, S. (2003). Postharvest loss assessment of Torres-Calzada, C., Tapia-Tussell, R., Higuera-Ciapara, I., and Perez-Brito, D. (2013). 
mango cv. Nam Dok Mai. Warasan Witthayasat Kaset. Available at: https://agris.fao.org/ Morphological, pathological and genetic diversity of Colletotrichum species responsible 
agris-search/search.do?recordID=TH2005000687 (Accessed February 1, 2023). for anthracnose in papaya (Carica papaya L). Eur. J. Plant Pathol. 135, 67–79. doi: 
Sarkar, A. K. (2016). Anthracnose diseases of some common medicinally important 10.1007/s10658-012-0065-7
fruit plants. J. Med. Plant Res. 4, 233–236. Tovar-Pedraza, J. M., Mora-Aguilera, J. A., Nava-Diaz, C., Lima, N. B., Michereff, S. J., 
Schena, L., Mosca, S., Cacciola, S. O., Faedda, R., Sanzani, S. M., Agosteo, G. E., et al. Sandoval-Islas, J. S., et al. (2020). Distribution and pathogenicity of Colletotrichum 
(2014). Species of the Colletotrichum gloeosporioides and C. boninense complexes species associated with mango anthracnose in Mexico. Plant Dis. 104, 137–146. doi: 
associated with olive anthracnose. Plant Pathol. 63, 437–446. doi: 10.1111/ppa.12110 10.1094/PDIS-01-19-0178-RE
Sefu, G., Satheesh, N., and Berecha, G. (2015). Effect of essential oils treatment on Tucho, A., Lemessa, F., and Berecha, G. (2014). Distribution and occurrence of 
anthracnose (Colletotrichum gloeosporioides) disease development, quality and shelf life mango anthracnose (Colletotrichum gloesporioides penz and sacc) in humid agro-
of mango fruits (Mangifera indica L). Am. Eurasian J. Agric. Environ. Sci. 15, 2160–2169. ecology of Southwest Ethiopia. Plant Pathol. J. 13, 268–277. doi: 10.3923/
doi: 10.5829/idosi.aejaes.2015.15.11.96140 ppj.2014.268.277
Serrato-Diaz, L. M., Rivera-Vargas, L. I., and French-Monar, R. D. (2014). First report of Uddin, M., Shefat, S., Afroz, M., and Moon, N. (2018). Management of anthracnose 
Neofusicoccum mangiferae causing rachis necrosis and inflorescence blight of mango disease of mango caused by Colletotrichum gloeosporioides: A review. Acta Sci. Agric. 2, 
(Mangifera indica) in Puerto Rico. Plant Dis. 98:570. doi: 10.1094/PDIS-08-13-0878-PDN 169–177. doi: 10.35248/2157-7471.22.13.635
Sharma, M., and Kulshrestha, S. (2015). Colletotrichum gloeosporioides: an anthracnose Ullagaddi, S. B., and Raju, S. V. (2017). “Disease recognition in mango crop using 
causing pathogen of fruits and vegetables. Biosci. Biotechnol. Res. Asia 12, 1233–1246. modified rotational kernel transform features” in 2017 4th international conference on 
doi: 10.13005/bbra/1776 advanced computing and communication systems (ICACCS) (New York: IEEE), 1–8.
Sharma, G., Kumar, N., Weir, B. S., Hyde, K. D., and Shenoy, B. D. (2013). The ApMat Veling, P. S., Kalelkar, R. S., Ajgaonkar, L. V., Mestry, N. V., and Gawade, N. N. (2019). 
marker can resolve Colletotrichum species: a case study with Mangifera indica. Fungal Mango disease detection by using image processing. IJRASET 7, 3717–3726. doi: 
Divers. 61, 117–138. doi: 10.1007/s13225-013-0247-4 10.22214/ijraset.2019.4624
Sharma, G., Maymon, M., and Freeman, S. (2017). Epidemiology, pathology and Veloso, J. S., Câmara, M. P., Lima, W. G., Michereff, S. J., and Doyle, V. P. (2018). Why 
identification of Colletotrichum including a novel species associated with avocado (Persea species delimitation matters for fungal ecology: Colletotrichum diversity on wild and 
americana) anthracnose in Israel. Sci. Rep. 7:15839. doi: 10.1038/s41598-017-15946-w cultivated cashew in Brazil. Fungal boil. 122, 677–691. doi: 10.1016/j.funbio.2018.03.005
Sharma, A., and Verma, K. S. (2007). In vitro cross pathogenicity and management of Vilcarromero-Ramos, R. L., Díaz-Valderrama, J. R., Caetano, A. C., Huamán-Pilco, J., 
Colletotrichum gloeosporioides causing anthracnose of mango. Ann. Plant Prot. Sci 15, and Mansilla-Córdova, P. J. (2022). First report of anthracnose caused by Colletotrichum 
186–188. asianum on mango (Mangifera indica) in Peru. Plant Dis. 107:2245. doi: 10.1094/
PDIS-10-22-2357-PDN
Shi, N., Ruan, H., Jie, Y., Chen, F., and Du, Y. (2020). Sensitivity and efficacy of 
fungicides against wet bubble disease of Agaricus bisporus caused by Mycogone Vitale, A., Alfenas, A. C., de Siqueira, D. L., Magistà, D., Perrone, G., and Polizzi, G. 
perniciosa. Eur. J. Plant Pathol. 157, 873–885. doi: 10.1007/s10658-020-02047-0 (2020). Cultivar resistance against Colletotrichum asianum in the world collection of 
mango germplasm in southeastern Brazil. Plan. Theory 9:182. doi: 10.1094/
Shih, J., Wei, Y., and Goodwin, P. H. (2000). A comparison of the pectate lyase genes, PDIS.2000.84.6.600
pel-1 and pel-2, of Colletotrichum gloeosporioides f. sp. malvae and the relationship 
between their expression in culture and during necrotrophic infection. Gene 243, Wang, Y. C., Hao, X. Y., Wang, L., Xiao, B., Wang, X. C., and Yang, Y. J. (2016). Diverse 
139–150. doi: 10.1016/s0378-1119(99)00546-6 Colletotrichum species cause anthracnose of tea plants (Camellia sinensis (L.) O. Kuntze) 
in China. Sci. Rep. 6:35287. doi: 10.1038/srep35287
Shivas, R. G., Tan, Y. P., Edwards, J., Dinh, Q., Maxwell, A., Andjic, V., et al. (2016). 
Colletotrichum species in Australia. Australas. Plant Pathol. 45, 447–464. doi: 10.1007/ Wei, Y., Shih, J., Li, J., and Goodwin, P. H. (2002). Two pectin lyase genes, pnl-1 and 
s13313-016-0443-2 pnl-2, from Colletotrichum gloeosporioides f. sp. malvae differ in a cellulose-binding 
domain and in their expression during infection of Malva pusilla. Microbiol. 148, 
Silué, Y., Nindjin, C., Cissé, M., Kouamé, K. A., Mbéguié-A-Mbéguié, D., 
Lopez-Lauri, F., et al. (2022). Hexanal application reduces postharvest losses of mango 2149–2157. doi: 10.1099/00221287-148-7-2149
(Mangifera indica L. variety" Kent") over cold storage whilst maintaining fruit quality. Weir, B. S., Johnston, P. R., and Damm, U. (2012). The Colletotrichum gloeosporioides 
Postharvest Biol. Technol. 189:111930. doi: 10.1016/j.postharvbio.2022.111930 species complex. Stud. Mycol. 73, 115–180. doi: 10.3114/sim0011
Siriptrawan, U. (2021). Early detection of anthracnose on mango fruit using Wu, Y., Cheng, J. H., and Sun, D. W. (2022). Subcellular damages of Colletotrichum 
hyperspectral imaging. Rep. Grant. Res. Asahi Glass Foundation 90:81. doi: 10.50867/ asianum and inhibition of mango anthracnose by dielectric barrier discharge plasma. 
afreport.2021_081 Food Chem. 381:132197. doi: 10.1016/j.foodchem.2022.132197
Sosnowski, M. R., Fletcher, J. D., Daly, A. M., Rodoni, B. C., and Viljanen-Rollinson, S. L. Wu, J., Ji, Z., Wang, N., Chi, F., Xu, C., Zhou, Z., et al. (2016). Identification of 
H. (2009). Techniques for the treatment, removal and disposal of host material during conidiogenesis-associated genes in Colletotrichum gloeosporioides by Agrobacterium 
Frontiers in Microbiology 17 frontiersin.org
Dofuor et al. 10.3389/fmicb.2023.1168203
tumefaciens-mediated transformation. Curr. Microbiol. 73, 802–810. doi: 10.1007/ region of Yogyakarta, Indonesia. Pak. J. Biol. Sci. PJBS 24, 53–65. doi: 10.3923/
s00284-016-1131-8 pjbs.2021.53.65
Yokosawa, S., Eguchi, N., Kondo, K. I., and Sato, T. (2017). Phylogenetic relationship Zhang, H., Wei, Y., and Shi, H. (2020). First report of anthracnose caused by 
and fungicide sensitivity of members of the Colletotrichum gloeosporioides species Colletotrichum kahawae subsp. ciggaro on Areca in China. Plant Dis. 104:1871. doi: 
complex from apple. J. Gen. Plant Pathol. 83, 291–298. doi: 10.1007/s10327-017-0732-9 10.1094/PDIS-12-19-2628-PDN
Yong, H. Y., Bakar, F. D. A., Illias, R. M., Mahadi, N. M., and Murad, A. A. (2013). Zhou, Y., Huang, J. S., Yang, L. Y., Wang, G. F., and Li, J. Q. (2017). First report of 
Cgl-SLT2 is required for appressorium formation, sporulation and pathogenicity in banana anthracnose caused by Colletotrichum scovillei in China. Plant Dis. 101:381. doi: 
Colletotrichum gloeosporioide. Braz. J. Microbiol. 44, 1241–1250. doi: 10.1590/ 10.1094/PDIS-08-16-1135-PDN
S1517-83822013000400031 Zhou, Z., Wu, J., Wang, M., and Zhang, J. (2017). ABC protein CgABCF2 is required 
Zakaria, L., Juhari, N. Z., Vijaya, S. I., and Anuar, I. S. M. (2015). Molecular for asexual and sexual development, appressorial formation and plant infection in 
characterization of Colletotrichum isolates associated with anthracnose of mango fruit. Colletotrichum gloeosporioides. Microb. Pathog. 110, 85–92. doi: 10.1016/j.
Sains Malays. 44, 651–656. doi: 10.17576/jsm-2015-4405-02 micpath.2017.06.028
Zhafarina, S., Wibowo, A., and Widiastuti, A. (2021). Multi-genetic analysis of Zin, N. A., and Badaluddin, N. A. (2020). Biological functions of Trichoderma spp. for 
Colletotrichum spp. associated with postharvest disease of fruits anthracnose in special agriculture applications. Ann. Agric. Sci. 65, 168–178. doi: 10.1016/j.aoas.2020.09.003
Frontiers in Microbiology 18 frontiersin.org