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Review

Colletotrichum Species Complexes Associated with Crops in Northern South America: A Review

by
Marcela Guevara-Suarez
1,2,
Martha Cárdenas
2,
Pedro Jiménez
3,
Lucía Afanador-Kafuri
4 and
Silvia Restrepo
2,*
1
Applied Genomics Research Group, Vice-Presidency for Research and Creation, Universidad de los Andes, Bogotá 111711, Colombia
2
Laboratorio de Micología y Fitopatología (LAMFU), Facultad de Ingeniería, Universidad de los Andes, Bogotá 111711, Colombia
3
Facultad de Ciencias Básicas y Aplicadas, Universidad Militar Nueva Granada, Cajicá 250247, Colombia
4
Facultad de Ciencias Agrarias, Universidad Nacional de Colombia, Medellín 050034, Colombia
*
Author to whom correspondence should be addressed.
Agronomy 2022, 12(3), 548; https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy12030548
Submission received: 31 December 2021 / Revised: 12 February 2022 / Accepted: 14 February 2022 / Published: 23 February 2022
(This article belongs to the Special Issue Fungal and Oomycete Pathogens in Tropical Crop Plants)
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Abstract

:
Colletotrichum genus comprises a high number of plant pathogens causing anthracnose disease in different tropical and non-tropical crops. We aimed to review northern South American studies in the online SCOPUS database to: create a taxonomically updated list of the species complexes found in the region, describe their most important phytopathological characteristics, revise the methods used in the region to control disease, and discuss the role of fungus as a plant endophyte. A total of 19 Colletotrichum species within five complexes—acutatum, boninense, gigasporum, gloeosporioides, and orbiculare—have been reported in northern South America. Few studies have been conducted, particularly in Peru and Ecuador, despite the diversity of Colletotrichum hosts cultivated in the region. Important information can be extracted from our review: species do not appear to show host specificity, although some isolates show host preferences, certain plant species can host several Colletotrichum species, some studies show the importance of using plant extracts to control the disease, but biological control using microorganisms is certainly an open area of research in the region. In northern South America, only a few hosts have been reported to harbor Colletotrichum as endophyte, and the potential of these endophytes as biological control agents has not yet been explored.

1. Introduction

The genus Colletotrichum (Sordariomycetes, Ascomycota) includes an important number of plant pathogens for vegetables, legumes, cereals, and tropical and non-tropical crops worldwide [1,2]. Many Colletotrichum species have been named after their hosts. Taxonomically, Colletotrichum is a confusing genus that has been subject to various taxonomic revisions in the last few years [3,4,5]. Additionally, numerous species have been described since its first report in 1831 by Corda [6]. According to the Index Fungorum Database, there are a total of 942 records for Colletotrichum. However, recent taxonomic studies and the EPPO-Q-BANK database suggest that there are currently only about 257 accepted species. Colletotrichum species are distributed across 15 major monophyletic clades or species complexes: acutatum, agaves, boninense, caudatum, dematium, destructivum, dracaenophilum, gigasporum, gloeosporioides, graminicola, magnum, orbiculare, orchidearum, spaethianum and truncatum [7,8].
The taxonomy of Colletotrichum has recently changed based on available molecular data and subsequent phylogenetic analyses since phenotypic features alone are not informative. In the last decade, species within this genus have been delineated based on a polyphasic approach that has mainly involved evaluation of morphological characters and multi-locus sequence analyses of molecular markers such as internal transcribed spacer region rDNA (ITS), β-tubulin (TUB), actin (ACT), calmodulin (CAL), chitin synthase I (CHS-1), glyceraldehyde-3-phosphate dehydrogenase (GAPDH), the large subunit of RNA polymerase II (RPB2), and translation elongation factor 1-α (EF1α). Although the ITS region alone cannot identify or differentiate species in the genus, it can be used to separate taxa at the species complex level. In addition, some genes like GAPDH can be useful to preliminarily perform an identification to the species level [9,10].
In the northern South American region (Colombia, Ecuador, Peru, and Venezuela) many tropical crops have been affected by Colletotrichum species [5,8]. Therefore, in each country there is an interest to characterize the pathogen and most studies are focused on its isolation, morphological identification and phytopathological behavior. However, to date there are no papers that integrate this information at the regional level.
Consequently, this review has four goals: (i) to list the species complexes and, when available, the species of Colletotrichum associated with cultivated hosts in Colombia, Ecuador, Peru, and Venezuela; (ii) to review the geographical range of the pathogen in the northern region of South America, as reported in the literature; (iii) to describe their most important phytopathological characteristics: hosts, specificity, and methods of control; and (iv) to review the role of fungi belonging to the genus Colletotrichum as endophytes.

2. Materials and Methods

We reviewed the studies that included isolates of Colletotrichum genus associated with cultivated plants in the northern region of South America, which includes Colombia, Ecuador, Peru, and Venezuela. This search was performed in the online SCOPUS database using the keyword phrases “Colletotrichum AND Colombia,” “Colletotrichum AND Peru,” “Colletotrichum AND Ecuador,” and “Colletotrichum AND Venezuela”. We included papers in English and Spanish published in peer-reviewed research journals.
In addition, in order to list the Colletotrichum species complexes associated with cultivated hosts in Colombia, Ecuador, Peru, and Venezuela we performed a phylogenetic analysis of available sequences retrieved from GenBank that were reported in the studies included in this review. We also included sequences of the type strains of most of the accepted species in the genus. To ensure that we included most of the isolates reported in the studied region, we could only be able to include the molecular marker used in most of the studies reviewed: the ITS region comprising the 5.8S nuclear ribosomal gene. The sequences were aligned using the MAFFT algorithm in the EMBL-EBI Web Services portal and manually adjusted using MEGA v 6.0 [11]. Phylogenetic reconstructions by maximum likelihood (ML) and Bayesian inference (BI) were carried out using MEGA v. 6.0 and MrBayes v. 3.1.2 [12]. For ML, the trees were inferred using the heuristic method Nearest-Neighbor-Interchange, and gaps underwent partial deletion with a 95% site coverage cut-off. Phylogeny support for internal branches was assessed by 1000 ML bootstrapped pseudo-replicates, and the bootstrap support (bs ≥70) was considered significant. The BI analyses were performed using one million Markov chain Monte Carlo (MCMC) generations, with two runs (one cold and three heated chains) and samples were stored every 1000 generations. The 50% majority-rule consensus tree and posterior probability values (pp) were calculated after discarding the first 25% of the samples. A pp value ≥0.95 was considered significant. The best substitution models for each data partition were estimated using the jModelTest v.2.1.3 based on the Akaike criterion [13,14]. The resulting trees were plotted using FigTree v.1.3.1 and edited in Adobe Illustrator CS3.

3. Results and Discussion

A total of 105 research articles on Colletotrichum in northern South America (Ecuador, Venezuela, Peru, and Colombia), were obtained in November 2021. We excluded the articles that focused on host resistance, or reviews of other fungi, and we retained 71 articles (Table S1). Next, we will present the most relevant aspects of our review.

3.1. Species Complexes of Colletotrichum Associated with Crops in Northern South America

We obtained a total of 192 sequences for the ITS region. The aligned dataset was 465 bp long, with 158 variable sites and 114 phylogenetic informative sites. The best substitution model for ML was determined to be T92+G. In general, the topology of the phylogenetic tree showed well-delimitated clades. This analysis showed that the species reported in Colombia, Ecuador, Peru, and Venezuela are mainly distributed across five clades of Colletotrichum (acutatum, boninense, gigasporum, gloeosporioides, and orbiculare), with most of the species observed in the gloeosporioides clade (Figure 1).
The first clade corresponds to species in the C. gloeosporioides complex. Currently, this group comprises 57 species, which are mainly characterized as phytopathogens and sometimes reported to be endophytes [8,9,10]. Most isolates reported for northern South America are clustered in this complex (Figure 2). Although the ITS region is not a good molecular marker for identifying closely related species, we were able to identify seven species in this complex: C. asianum, C. fructicola, C. cigarro (formerly C. kahawae subsp. ciggaro), C. gloesporioides sensu stricto, C. musae, C. siamense, and C. theobromicola. A small number of isolates were located in a closely related group containing species with identical ITS sequences (C. aenigma, C. cobbittiense, C. changpingense, C. tropicale, and C. yulongense). For these species, a multi-locus analysis including the ApMat–Intergenic region of apn2 and MAT1-2-1 genes, which has been proposed to differentiate at the species level within the C. gloeosporioides complex, is necessary [15]. Our analyses suggested that some isolates (n = 15) in this group that are likely mislabeled and need to be revised. On the other hand, we found one ITS sequence deposited in GenBank as C. rhexiae (accession number KJ846800), this sequence was obtained from tree tomato in Colombia, but according to our analyses (Figure 2) and a literature review, this sequence could be mislabeled. To date, C. rhexiae has only been isolates from leaf and stem of Rhexia virginica and from fruits of Vaccinium macrocarpon [8,16]. One of the most reported species was C. kahawae subsp. ciggaro. Recently, the taxonomic status of C. kahawae subsp. ciggaro was updated and it is now considered a species which was named as C. cigarro [17]. All isolates of our search were clustered within C. cigarro. This last determination is important because C. kahawae is a significant pathogen of Coffea arabica, a crop with agricultural importance in the region.
Moreno-Moran and Burbano-Figueroa (2016) reported C. gossypii in cotton ramulosis in Colombia [18]. However, the isolates presented in this study could not be included in our analysis because there are no available ITS sequences. Moreno-Moran and Burbano-Figueroa [18] used TUB and GAPDH sequences to identify isolates, but Weir et al. [9] reported that there are no sequences available for these genes for the ex-type strain, and therefore accurate molecular identification of this species is not possible.
The boninense clade (Figure 3) is one of the largest complexes within the Colletotrichum genus. Species within this complex are considered to be pathogens and endophytes [19,20]. The isolates from northern South America included in our analysis were distributed into four subclades. The first includes C. boninense, C. brassicicola, and C. colombiense, which cannot be identified with certainty using ITS sequences because the sequences of ex-type strains are identical. Colletotrichum colombiense was described by Damm et al. [20] from a leaf of Passiflora edulis in the department of Cundinamarca, Colombia. The authors highlighted that Afanador-Kafuri et al. [21] isolated many other isolates of Colletotrichum from the same host; however, these isolates could not be assigned to the C. colombiense species due to the fact that only their ITS sequences were available. The second subclade includes Colletotrichum sp. GM52-L01 [22]. We reviewed all available sequences of this isolate (data not shown), but we could not perform identification at the species level since no ex-type strain was included in this group, and a BLASTn search (non-redundant (nr) database and default parameters) revealed a low percentage of similarity. The third subclade includes the only species that could be identified, C. karstii. The fourth subclade includes Colletotrichum sp. Q026 [23], which is closely phylogenetically related to C. pryrifolia, a species that was recently described in association with the Pyrus species in China. However, according to the description of this species, C. pryrifolia differs from Colletotrichum sp. Q026 in the size of the conidia and in the ACT and TUB2 sequences. Interestingly, Colletotrichum sp. Q026 and Colletotrichum sp. GM52-L01 could be two new species within the boninense clade.
In the orbiculare and gigasporum clades, only one species was identified in each complex: C. lindemuthianum and C. gigasporum, respectively (Figure 4). Colletotrichum lindemuthianum is one of eight species in the orbiculare clade, and it is restricted to Phaseolus vulgaris and P. coccineus (Fabaceae) [24]. A total of five isolates obtained from P. vulgaris in Colombia were included in our analysis and formed a different clade than those already reported for C. lindemuthianum [24]. The C. gigasporum species complex includes eight species. Among these, C. gigasporum is the most frequently isolated species, and it seems to have a wide host range and geographic distribution. Colletotrichum gigasporum was described by Rakotoniriana et al. [25], including one isolate from Colombia (VEGA 508, FN557349) obtained as an endophytic fungus from Coffea arabica. To our knowledge this would be the first and only report of C. gigasporum in the region.
Finally, in the acutatum clade, we identified two species—C. godetiae and C. tamarilloi—the latter of which is the most reported species in the region (Figure 5). Members of the acutatum clade have been reported in agricultural and natural hosts across the world. This species complex includes approximately 41 species, of which C. acutatum and closely related species are considered pathogens that cause rot in fruit trees [20]. In addition, the complex includes one of the most important pathogens in the region, C. tamarilloi, which is the causal agent of anthracnose in Solanum betaceum (tree tomato, tamarillo), an important fruit crop in northern South America. The species C. tamarilloi was described (culture ex-type CBS 129814) by Damm et al. [20] in strains isolated from S. betaceum in Colombia. Damm et al. [20] also described C. laticiphilum and included additional material isolated from leaf of Hevea brasiliensis which was collected in Meta, Colombia. The isolate of this species was not included in our analysis due to the fact that it is a well characterized species. Besides, our SCOPUS search did not find the paper of Damm et al. [20] as a result.
In addition, C. coccodes is another species reported in Colombia, Ecuador, and Peru [26]. However, there are no sequences available in the GenBank with which to confirm the identity of this species. Colletotrichum coccodes has been categorized as a singleton species in the genus as a result of do not cluster with any complex [8].
In summary, a total of 22 Colletotrichum species distributed within five complexes (acutatum, boninense, gigasporum, gloeosporioides, and orbiculare) have been reported in northern South America (Table 1). However, studies on the molecular identification of Colletotrichum species in Ecuador, Peru, and Venezuela are limited. Even though Colombian researchers have tried to address this issue, more taxonomic work must be performed in the northern South American region to describe the diversity of the genus in this region.

3.2. Geographical Distribution of Colletotrichum Complexes in Northern South America

Of the 71 studies retrieved from the databases, 35 reported Colletotrichum species in the four countries focused upon in this review. Of these, 21 studies reported species in Colombia [18,21,22,23,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43], five reported species in Venezuela [44,45,46,47,48], only three reported species in Peru [49,50,51], and six reported species in Ecuador [52,53,54,55,56,57].
Pathogens were reported in almost all regions of Colombia, from lowlands (i.e., Afanador-Kafuri et al. [21]) to highlands (i.e., Pardo de la Hoz et al. [28]). The department of Antioquia was the most mentioned. Interestingly, two out of the three studies conducted in Peru focused on the Amazonian region [27,50]. Four studies were performed in the western part of Venezuela in the states of Lara [47], Mérida [44], Trujillo [47] and Zulia [45,46,48], also two studies that did not appear in the SCOPUS databases reported the fungus in the central part of the country in the states of Aragua and Miranda [58,59].
In each country, different hosts were sampled. Very few were reported in several countries, and none were reported in all four countries. Some of the same crops were studied in Colombia and Ecuador and in Colombia and Venezuela. All the crops studied in Ecuador (S. betaceum, Musa spp., R. glaucus and P. vulgaris), except Lupinus mutabilis, were also studied in Colombia. The tamarillo or tree tomato (S. betaceum) was the most common crop studied in both Colombia and Ecuador with the same pathogen species complexes [21,28,37,53,54,56]. Only one crop was found in both Venezuela and Colombia: soursop (Annona muricata). Several hosts were found in only one country: the Amazonian fruit camu camu (Myrciaria dubia) was found in Peru [50] as well as pea (Pisum sativum) [51], and lupine (Lupinus mutabilis) was found in Ecuador, while oil palm (Elaeis guineensis) [43] macadamia [60], onion [48] and strawberry (Fragaria × ananassa) [44,47] were found in Venezuela, and in Colombia were found cotton (Gossypium hirsutum) [18], grape vine (Vitis vinifera) [38], gulupa fruit (Passiflora edulis) [29], heliconia (Heliconia spp.) [32], mango (Mangifera indica) [21,28], Passiflora (Passiflora spp.), rubber (Hevea brasiliensis) [42,61] and pepper (Capsicum annun) [35].
Despite the high diversity of the Colletotrichum hosts studied in previous studies, few complexes (the gloeosporioides, acutatum, boninense, gigasporum and orbiculare species complexes) were identified in the four countries. As expected, the diversity of complexes increased with the number of studies, and Colombia was the country with the highest diversity. Several species are ubiquitous, notably C. gloeosporioides, C. acutatum, and C. lindemuthianum. Interestingly, the species C. karstii was found in different studies investigating different hosts [21,23].

3.3. Phytopathological Aspects

3.3.1. Hosts, Diversity and Botanical Families

Colletotrichum is a fungal genus with different pathogenetic, saprophytic, or endophytic relationships with a wide range of hosts (i.e., herbaceous and woody plants) in both agricultural and natural systems within tropical, subtropical and temperate regions [62]. Virtually every crop worldwide is susceptible to one or more Colletotrichum species. All diseases caused by these fungi are characterized by symptoms called anthracnose, including leaf spots, blasts, cankers, postharvest rot, and symptoms in stems, fruits and leaf petioles.
Species belonging to the Colletotrichum genus cause losses of 50%–100% in several economically important crops, particularly fruit trees, vegetables, and ornamentals. Occasionally, the damages caused by Colletotrichum species extend to basic food crops, such as bananas, beans, plantains, yuca (cassava/manioc) and sorghum, which provide livelihoods for a substantial number of farmers in developing countries in tropical and subtropical areas [63]. Colletotrichum species are successful postharvest pathogens because they produce latent infections that start during the preharvest period and are activated once the fruits are stored [64].
In tropical and subtropical countries in the northern South American region, different Colletotrichum species cause diseases in crops of high economic importance. In the reviewed studies, anthracnose and related symptoms were detected in crops from 16 botanical families and 23 species of fruit trees, fodders, ornamentals, leguminous and seasoning plants, and plants intended for industrial use to produce beverages, fibers and oils (Table 2).
In fruit plants, attacks by Colletotrichum species have been reported in tree tomato (Solanum betaceum) [21,28,56,65,66], mango (Mangifera indica) [21,28,67], Passiflora (Passiflora edulis) [21,29], strawberry (Fragaria × ananassa) [44,47], blackberry (Rubus glaucus) [23,30,31,32], plantain (Musa spp.) [36], soursop (Annona muricata) [22,45], avocado (Persea americana) [39,40,43] Tahiti lima (Citrus latifolia) [41,68,69], papaya (Carica papaya) [70], and grape (Vitis vinifera) crops [38].
Regarding leguminous plants, anthracnose has been reported to affect beans (Phaseolus vulgaris) [33,34,71], pea (Pisum sativum) [51], Stylosanthes guianensis [49,72], and lupin (Lupinus mutabilis) [53,73]. Regarding vegetables and tubers, diseases have been reported in yam (Dioscorea spp.) [74], onion (Allium fistulosum) [48] and pepper (Capsicum annuum) plants [75]. Other important plant to consider are ornamental species, such as heliconias [50], seasoning species, such as vanilla (Vanilla planifolia) [76], and plants intended for industrial purposes, such as coffee (Coffea arabica) [25,77], cocoa (Theobroma cacao) [78], cotton (Gossypium hirsutum) [18], and oil palm (Elaeis guineensis) [46], and rubber (Hevea brasiliensis) [42,61].

3.3.2. Virulence and Aggressiveness

Manawasinghe et al. [79] propose definitions of pathogenicity based on a summary of the terms used to describe the level of damage caused by pathogens in plants. In the plant pathology field and related areas, pathogenicity is defined as the capacity of a microorganism to produce a disease or to cause damage to a host, and virulence and aggressiveness describe the relative capacity of a microorganism to cause damage to a host [80]. When the pathogen is host-specific, the term “virulence” is used as a quantitative measure of pathogenicity, and in susceptible hosts without specificity, “aggressiveness” is used to refer to quantitative variations in pathogenicity [81]. Based on these definitions, Manawasinghe et al. [82] propose the term “pathogenicity” as a qualitative way to describe the specific character of a particular organism with the capacity to cause a disease.
In the case of Colletotrichum species, which affect a numerous number of hosts, the most accurate term might be “aggressiveness.” Only in specific cases might the term “virulence” be valid, such as in the case of C. lindemuthianum in beans and C. gloeosporioides in Stylosanthes, which are known to exhibit variability in terms of pathotype and race.
Artificial methods to test the pathogenicity and/or aggressiveness of plant pathogens are an important part of the process of determining the capacity of a fungus, such as Colletotrichum species, to cause diseases in the plant species from which they were originally isolated or to predict genotypic responses to a disease under field conditions [79]. Specifically, an artificial inoculation method that accurately simulates all natural conditions of the infection should be used to extrapolate the obtained results to the disease under natural pressure in field conditions [83]. Ideally, to test pathogenicity, healthy plants from the same species should be inoculated without wounds and to assess virulence, wounds can be used. For the pathogen, aspersion of aqueous suspensions or drops from conidia, or agar plugs with mycelium can be used. These tests can be performed either under controlled conditions in a laboratory or greenhouse or under field conditions. In either case, several environmental factors, temperature, relative humidity, might influence the artificial inoculation process. In addition, the obtained results depend on the size, age and resistance level of the host [83].
Studies have tested the pathogenicity and measured the aggressiveness of Colletotrichum species, which have been reported to be plant pathogens in countries such as Colombia, Ecuador, Peru and Venezuela. These studies used a variety of inoculation methods and obtained a range of different results regarding aggressiveness and virulence from the different species and/or isolates being tested. No consensus was achieved concerning the terminology used to describe the response or behavior of the Colletotrichum species tested, including “pathogenicity.” According to the definition presented above, “pathogenicity” refers to the capacity of the tested species to cause disease in the host from where it was initially isolated, in line with Koch’s postulates [36].
Certain studies clearly describe the difference between “pathogenicity” and “virulence.” For example, Sicard et al. [52] distinguish between a pathogenicity test, which was to be performed in a highly susceptible host, and a test of virulence diversity based on the results obtained for 12 different genotypes of beans with different genetic levels of resistance to anthracnose. The authors identified three groups within the pathogen population based on the isolates’ response to the hosts’ genes.
Rueda-Hernández et al. [30] performed a pathogenicity test (which confirmed Koch’s postulates) of Colletotrichum isolates belonging to the C. gloeosporioides complex and C. acutatum complex that were found in Andean blackberry plants. The term “pathogenicity” is well used according to the description above, and terms such as “latency period” and “incubation period” are introduced in order to establish differences within and between the Colletotrichum species complexes. Therefore, the authors performed a quantitative evaluation of the fungus’s capacity to cause disease depending on o the fungus species and the host genotype.
In the same study [30], the authors evaluate differences in pathogenicity between samples inoculated using different methods (i.e., wound-mediated vs. woundless inoculation). They conclude that certain differences exist in the capacity of the two species complexes to cause infection; the Colletotrichum gloeosporioides species complex has the capacity to cause infection in both wounded and woundless tissues, while the C. acutatum species complex can infect only wounded tissues. These results are interesting considering that most of the isolates from the C. acutatum complex were obtained from stem tissues, which are the first tissues to be affected in the field.
The results of Rueda-Hernández et al. [30] align with those of Afanador-Kafuri et al. [21], who performed a study with Colletotrichum species obtained from blackberry plants in eight productive areas of Colombia and found that the C. acutatum species complex has a lower infection capacity in stems when the wound-mediated inoculation method is used. Afanador-Kafuri et al. [23] concluded that the differences they found between the C. acutatum and C. gloeosporioides species complexes (in terms of their infection capacity in blackberry stems) are due to differences in the colonization strategy applied in different tissues of the plant. Colletotrichum acutatum is found more often in flower and fruit tissues, while C. gloeosporioides seems to prefer stems. Moreover, the authors highlight differences in the kind of blackberry (i.e., spiny, or spineless) from which the species complexes were isolated, which is important to consider because there are several anatomical and structural disparities between the two analyzed ecotypes. In spineless blackberry ecotypes, Afanador-Kafuri et al. [23] observed a prevalence of species within the C. acutatum complex, which are mainly associated with symptoms of inflorescence and fruits while stems are free from disease. In the spiny ecotype, the C. gloeosporioides complex was prevalent. These results support those of López-Vasquez et al. [32], who found that spiny plants had greater susceptibility than spineless plants or genotypes, as the later showed total resistance to artificial inoculation of C. gloeosporioides isolates under field conditions.
These studies illustrate the presence of different infection mechanisms among Colletotrichum species belonging to both the C. gloeosporioides and C. acutatum complexes. Those mechanisms seem to be closely related to the original host genotype and the host’s morphological and anatomical characteristics. In some cases, wounds, even imperceptible ones, are necessary for penetration of the pathogen. Thus, studies of pathogenicity, aggressiveness, and virulence must consider differences in inoculation methods (i.e., wound-mediated or woundless) and in plant tissues, as well as the characterization of the infection cycle.

3.3.3. Host Specificity

The Colletotrichum genus is an important pathogen worldwide due to its capacity to colonize and infect an extensive range of hosts in different families and botanical species. This capacity seems to be closely associated with speciation in this fungal genus, which may be due to changes in its behavior [5,84].
There are significant differences between phytopathogenic fungi in terms of the number and diversity of hosts they can infect and/or colonize. Fungal plant pathogens may be classified as “specialists” if they infect only one plant species or a narrowly related, restricted group or as “generalists” if they can infect a wide range of plants in several environments. However, it is rare to find both fungal categories within the same phylogenetic lineage or fungal genus, as is the case for the Colletotrichum genus. A specialist species found in the northern part of South America is C. lindemuthianum, which has been described only in beans (Phaseolus vulgaris) in Colombia [33,34] and Ecuador [52].
Studies of fruit trees in Colombia, such as the Andean blackberry, grape, tree tomato, and soursop, have demonstrated the coexistence of different Colletotrichum species in the same host, not only those belonging to the C. acutatum complex but also those from the C. gloeosporioides and C. boninense complexes. For instance, in a study aiming to characterize the causal agent of fruit deformation in grape plants, Lopez-Zapata et al. [35] report that two species (C. aenigma and C. siamense in the gloeosporioides clade) were attacking the same host. Similarly, Afanador-Kafuri et al. [23] report that Colletotrichum species belonging to the C. gloeosporioides (C. cigarro (formerly C. kahawae subsp. ciggaro) and C. fruticola), C. acutatum (C. godetiae, and Colletotrichum sp.) and C. boninense (C. brassicicola and I) complexes were attacking the same Andean blackberry host, but in different tissues. Species in the C. acutatum complex show a preference for fruits and flowers, while those in the C. gloesosporioides and I complexes prefer stem tissues. Similar results have been found for soursop, a fruit tree in which disease is caused by species belonging to the C. gloesporioides (C. theobromicola, C. tropicale, C. siamense and Colletotrichum sp.), C. acutatum (Colletotrichum sp.), and C. boninense (C. karstii and Colletotrichum sp.) complexes. These species show differences in their capacity to cause disease; C. tropicale and C. theobromicola were found to be most aggressive.
A study conducted in Ecuador by Falconi et al. [73] shows that isolates belonging to the same Colletotrichum species can have host preferences or differential adaptations. This study focuses on the pathogenetic, molecular, and morphological characterization of C. acutatum isolates that cause anthracnose in tree tomato and lupin plants. The results of this study enable classification of isolates into two populations based on their specificity and strategy for attacking the host (biotrophic vs. necrotrophic) and on phylogenetic analysis of the ITS sequences. One population includes tree tomato isolates and one lupin isolate, and the other population consists of only lupin isolates. The host range assays indicate that each of these two species of plants is attacked by a population of C. acutatum that has adapted to the species. Based on the symptoms and lesion sizes observed in each host, the authors conclude that the isolates were more aggressive in their original hosts but pathogenetic in their alternative hosts, so host adaptation is more likely to be quantitative than qualitative.
Studies of mango and tree tomato crops in Colombia have found that isolates of species belonging to the C. gloeosporioides, C. acutatum, and C. boninense complexes did not exhibit host preference or specificity. Nevertheless, some differences between isolates in terms of their aggressiveness (i.e., ability to cause lesions) and dissemination capacity (i.e., sporulation on the affected tissue) have been observed [65]. This led authors to suggest that the lack of host specificity in these Colletotrichum species may favor the migration of populations from one host to another, which might be a threat to these two crops in Colombia. In addition, considering that the evaluated species exhibited higher sporulation capacity in alternative hosts, their dissemination capacity might be more related to their survival strategy under adverse conditions, which can allow the fungus to generate a larger number of propagules, rather than host adaptation. These findings support the final analyses of Cabrera et al. [65], who state that categorization of Colletotrichum species into generalists and specialists is very simplistic and the reality might be more complex.
Therefore, it is necessary to consider and evaluate other criteria to clarify the mechanisms involved in host preference or specificity within Colletotrichum species. Baroncelli et al. [84] found an association between broad host range and gene content changes in the Colletotrichum genus (C. acutatum and C. gloeosporiodes species complexes). In addition, Liang et al. [85] state that species in the Colletotrichum genus could share new and conserved virulence factors, which are built in a lineage-specific way and allow the pathogen to adapt to a particular host and tissue. The authors suggest that it is critical to identify these virulence factors and their evolution in order to control diseases caused by Colletotrichum species and better understand of the fundamental mechanisms of the plant–pathogen interaction.

3.3.4. Strategies for Controlling Colletotrichum Species in Northern South America

Plant diseases challenge the ability of agriculture to provide adequate amounts of food for an increasing population [86,87]. There are two approaches to address this issue, each of which has advantages and disadvantages. The first is using agrochemicals, which have been questioned recently due to their lateral effects on the environment and animal health [87,88]. The second is to use alternative methods, such as integrated crop management, organic farming, conventional plant breeding, genetic engineering and biocontrol [87,88]. Bacteria and fungi used for biocontrol have been obtained from diverse sources, including compost [89], the rhizosphere [90], seeds [91] and inside plants (endophytes) [92] (for a more thorough review of these topics, see De Silva et al. [88]).
Our literature review revealed several articles that discussed methods of controlling Colletotrichum species. Of these, 17 were conducted in Colombia, three in Venezuela, one in Ecuador, and two in Peru. The Colombian studies mainly performed agrochemicals evaluations [93] or in vitro evaluations of natural products, such as essential oils and metabolites obtained from plants [35,49,94,95,96,97,98] and from microorganisms [42,99,100,101]. In addition, we found an article evaluating the in vitro effect of a bacterium and its cell-free culture filtrate [27], an article evaluating resistance to anthracnose for plant breeding [32], and an article evaluating climatological conditions and the incidence of anthracnose [102]. The Venezuelan studies mostly performed in vitro evaluations of extracts, including tests on detached fruits [47,103] and propolis ethanolic extract [104]. The Ecuadorian article evaluated plants’ resistance to anthracnose [47], and both Peruvian articles examined chemical control [50,51].
The studies conducted in northern South America to examine methods of controlling anthracnose do not have a homogeneous approach, although the main goal is to find new molecules that could eventually substitute the old agrochemical molecules. This is a common approach, and it is probably based on fear that more “biological“ approaches (i.e., those using microorganisms) will be less efficient. The international literature includes many studies of the use of microorganisms for controlling anthracnose induced by Colletotrichum [105,106,107,108], then it is expectable that performing further research in northern South American countries could increase the range of options to control this limiting disease.

3.4. Colletotrichum Species as Endophytes

Recent studies aiming to determine the behaviors of fungi considered fungi isolated from infected tissue to be pathogens, those isolated from healthy tissue to be endophytes, and those isolated from dead vegetable material to be saprophytes. Most Colletotrichum species are important phytopathogens for different crops, although some are endophytes or saprophytes. The endophytic lifestyle of Colletotrichum species has been described in various countries, particularly in relation to tropical trees and grasses [109,110].
In the northern South American region, only a few hosts have been reported to harbor Colletotrichum as an endophyte. In Venezuela, C. gloeosporioides was isolated from the Haden variety of mango (Mangifera indica) in the eastern part of the country [67] and from floral buds of Psidium guajava [111]. Recently, two isolates of C. gloeosporioides s.l. were obtained as endophytes from cacao leaves (Theobroma cacao) in two localities (Naranjal and Balao) in the province of Guayas, Ecuador. They were tested for the capacity to control the growth of Moniliophthora roreri and M. perniciosa, two of the main pathogens affecting cacao crops [78]. In Colombia, three main hosts have been reported for endophyte Colletotrichum species: vanilla, coffee and mango. In a study aiming to identify the fungal endophytes associated with vanilla species, Gamboa-Gaitán [76] reported the presence of C. boninense in the stems of Vanilla planifolia, while C. gloeosporioides was isolated from leaves. In addition, Vega et al. [77] found that Colletotrichum was the dominant genus in a fungal endophytic community of Coffea arabica in Colombia. Indeed, 106 out of a total of 267 endophytic fungal (Colletotrichum) isolates were obtained from the leaves (n = 78), berries (n = 2), crowns (n = 15), peduncles (n = 11), and stems (n = 22) of coffee in one location in Colombia. After molecular characterization based on the ITS region, the isolates were distributed into 25 genotypes, and they showed an unexpected diversity [77]. In a mango cultivar (M. indica cultivar Azucar), Quintero-Mercado et al. [112] reported eight isolates from leaves and just one from a branch. The pathogenic potential of these entophytic isolates in mango fruits was evaluated, and all nine isolates were found to have the capacity to produce lesions. Just the most virulent isolate was identified and corresponded to C. tropicale.
The fact that Colletotrichum can be isolated as an endophyte from different plants may be due to the fact that an endophytic behavior could be confused with the initial phase of the pathogenic cycle involved in a hemibiotrophic lifestyle when the host exhibits no symptoms [108]. In northern South America, more evidence is needed to determine whether Colletotrichum species can behave as latent pathogens, hemibiotrophs, or endophytes and whether these species have a wider host range as endophytes than they do as pathogens, as was reported in Panama [113].

4. Conclusions

This review is not a taxonomic study of the genus Colletotrichum in the northern South American region. The studies reviewed in this manuscript vary in terms of the rigorousness with which formal identification of the isolated samples was conducted. Some studies performed morphological identification, while others used multi-locus phylogeny to identify isolates at the species level. For this reason, we decided to start this review with a robust phylogenetic analysis of the Colletotrichum isolates reported in the region, although limited by the availability of the corresponding sequences. In this way, researchers in the region can realize that many of the isolates could be misidentified or mislabeled. This does not allow us to know what species are really associated with crops in the northern South American region. Our results showed that, to date, five complexes have been reported in northern South American crops.
There was also high variability in terms of inoculation methodologies. Some studies employed wound-mediated inoculation, while others preferred to not damage the plant material. We believe that this is important to consider since wounds hinder identification of the pathogenicity of the isolate and thus no definitive conclusions can be made regarding the host range of the species. Despite this, we conclude that host specificity is not always present in Colletotrichum isolates, but a host preference can sometimes be observed. This is particularly important in countries with high plant biodiversity and in which crops are present in a field all year long and share pathogens.
In addition, we found a disparity in the number of studies conducted in each country and a lack of continuity in the studies. It is worth noting that the studies conducted in Colombia and Ecuador cover a wide range of years, while just one study in Venezuela [48] and one in Peru were conducted recently [51]. For each crop, few studies have been published in each country. In our opinion, more studies should study the diversity and its geographical distribution of the pathogen’s isolates. This information helps to guide the control strategies, for example the deployment of resistant genotypes. More studies are also needed on biological control or other alternative methods of control, as an option to chemical control.

Supplementary Materials

The following supporting information can be downloaded at: https://0-www-mdpi-com.brum.beds.ac.uk/article/10.3390/agronomy12030548/s1. Table S1. Studies reviewed in this manuscript to obtain the data presented [114].

Author Contributions

Conceptualization, S.R. and P.J.; methodology, M.G.-S., M.C. and S.R.; formal analysis, M.G.-S., M.C., P.J., L.A.-K. and S.R.; writing—original draft preparation, M.G.-S., M.C., P.J., L.A.-K. and S.R.; writing—review and editing, M.G.-S., M.C., P.J., L.A.-K. and S.R. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Vice Presidency of Research & Creation’s Publication at Universidad de los Andes for its financial support.

Conflicts of Interest

No conflict of interest is declared.

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Figure 1. An ML tree of the Colletotrichum clades reported in northern South America (Colombia, Ecuador, Peru, and Venezuela). The tree was created based on the alignment of ITS sequences (465 bp) retrieved from GenBank. Branch lengths are proportional to phylogenetic distance. The best substitution model for ML was determined to be T92+G. Bootstrap support values/Bayesian posterior probability scores above 70%/0.95 are indicated on the nodes. The tree was rooted to Monilochaetes infuscans CBS 869.96 (type strain).
Figure 1. An ML tree of the Colletotrichum clades reported in northern South America (Colombia, Ecuador, Peru, and Venezuela). The tree was created based on the alignment of ITS sequences (465 bp) retrieved from GenBank. Branch lengths are proportional to phylogenetic distance. The best substitution model for ML was determined to be T92+G. Bootstrap support values/Bayesian posterior probability scores above 70%/0.95 are indicated on the nodes. The tree was rooted to Monilochaetes infuscans CBS 869.96 (type strain).
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Agronomy 12 00548 g002a 550Agronomy 12 00548 g002b 550
Figure 2. An ML tree of the gloesporioides clade that includes species reported in northern South America (Colombia, Ecuador, Peru, and Venezuela). The tree was created based on the alignment of ITS (434 bp). The GenBank accession numbers of sequences retrieved from the database are given in parentheses. Reference strains are shown in bold. Branch lengths are proportional to phylogenetic distance. The best substitution model for ML was determined to be T92+G. Bootstrap support values/Bayesian posterior probability scores above 70%/0.95 are indicated on the nodes. The tree was rooted to Monilochaetes infuscans CBS 869.96. T = Ex-type strain. ** Isolates are probably mislabeled in GenBank.
Figure 2. An ML tree of the gloesporioides clade that includes species reported in northern South America (Colombia, Ecuador, Peru, and Venezuela). The tree was created based on the alignment of ITS (434 bp). The GenBank accession numbers of sequences retrieved from the database are given in parentheses. Reference strains are shown in bold. Branch lengths are proportional to phylogenetic distance. The best substitution model for ML was determined to be T92+G. Bootstrap support values/Bayesian posterior probability scores above 70%/0.95 are indicated on the nodes. The tree was rooted to Monilochaetes infuscans CBS 869.96. T = Ex-type strain. ** Isolates are probably mislabeled in GenBank.
Agronomy 12 00548 g002aAgronomy 12 00548 g002b
Agronomy 12 00548 g003 550
Figure 3. An ML tree of the boninense clade that includes species reported in northern South America (Colombia, Ecuador, Peru, and Venezuela). The tree was created based on the alignment of ITS (449 bp). The GenBank accession numbers of sequences retrieved from the database are given in parentheses. Reference strains are shown in bold. Branch lengths are proportional to phylogenetic distance. The best substitution model for ML was determined to be T92+G. Bootstrap support values/Bayesian posterior probability scores above 70%/0.95 are indicated on the nodes. The tree was rooted to Monilochaetes infuscans CBS 869.96. T = Ex-type strain. ** Isolates are probably mislabeled in GenBank.
Figure 3. An ML tree of the boninense clade that includes species reported in northern South America (Colombia, Ecuador, Peru, and Venezuela). The tree was created based on the alignment of ITS (449 bp). The GenBank accession numbers of sequences retrieved from the database are given in parentheses. Reference strains are shown in bold. Branch lengths are proportional to phylogenetic distance. The best substitution model for ML was determined to be T92+G. Bootstrap support values/Bayesian posterior probability scores above 70%/0.95 are indicated on the nodes. The tree was rooted to Monilochaetes infuscans CBS 869.96. T = Ex-type strain. ** Isolates are probably mislabeled in GenBank.
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Agronomy 12 00548 g004 550
Figure 4. An ML tree of the orbiculare and gigasporum clades that includes species reported in northern South America (Colombia, Ecuador, Peru, and Venezuela). The tree was created based on the alignment of ITS (436 bp). The GenBank accession numbers of sequences retrieved from the database are given in parentheses. Reference strains are presented in bold. Branch lengths are proportional to phylogenetic distance. The best substitution model for ML was determined to be T92+G. Bootstrap support values/Bayesian posterior probability scores above 70%/0.95 are indicated on the nodes. Clades 1 and 2 of C. lindemuthianum were reported by Damm et al. [19]. The tree was rooted to Monilochaetes infuscans CBS 869.96. T = Ex-type strain.
Figure 4. An ML tree of the orbiculare and gigasporum clades that includes species reported in northern South America (Colombia, Ecuador, Peru, and Venezuela). The tree was created based on the alignment of ITS (436 bp). The GenBank accession numbers of sequences retrieved from the database are given in parentheses. Reference strains are presented in bold. Branch lengths are proportional to phylogenetic distance. The best substitution model for ML was determined to be T92+G. Bootstrap support values/Bayesian posterior probability scores above 70%/0.95 are indicated on the nodes. Clades 1 and 2 of C. lindemuthianum were reported by Damm et al. [19]. The tree was rooted to Monilochaetes infuscans CBS 869.96. T = Ex-type strain.
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Agronomy 12 00548 g005 550
Figure 5. An ML tree of the acutatum clade that includes the species reported in northern South America (Colombia, Ecuador, Peru, and Venezuela). The tree was created based on the alignment of ITS (442 bp). The GenBank accession numbers of sequences retrieved from the database are given in parentheses. Reference strains are presented in bold. Branch lengths are proportional to phylogenetic distance. The best substitution model for ML was determined to be T92. Bootstrap support values/Bayesian posterior probability scores above 70%/0.95 are indicated on the nodes. The tree was rooted to Monilochaetes infuscans CBS 869.96. T = Ex-type strain. ** Isolates are probably mislabeled in GenBank.
Figure 5. An ML tree of the acutatum clade that includes the species reported in northern South America (Colombia, Ecuador, Peru, and Venezuela). The tree was created based on the alignment of ITS (442 bp). The GenBank accession numbers of sequences retrieved from the database are given in parentheses. Reference strains are presented in bold. Branch lengths are proportional to phylogenetic distance. The best substitution model for ML was determined to be T92. Bootstrap support values/Bayesian posterior probability scores above 70%/0.95 are indicated on the nodes. The tree was rooted to Monilochaetes infuscans CBS 869.96. T = Ex-type strain. ** Isolates are probably mislabeled in GenBank.
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Table
Table 1. Colletotrichum species reported in Colombia, Ecuador, Peru, and Venezuela.
Table 1. Colletotrichum species reported in Colombia, Ecuador, Peru, and Venezuela.
ComplexSpeciesCountriesObservations
C. acutatum species
complex		C. acutatumColombia, Ecuador
C. godetiaeColombia
C. laticiphilumColombia
C. tamarilloiColombia, Ecuador
C. boninense species
complex		C. annellatumColombia
C. colombienseColombia
C. boninenseColombia
C. brassicicolaColombia
C. karstiiColombia
C. gigasporum species
complex		C. gigasporumColombiaEndophyte
C. gloeosporioides species complexC. aenigmaColombia
C. asianumColombia
C. cigarroColombiaFormerly labeled C. kahawae
C. fructicolaColombia
C. gloeosporioides ss.Colombia
C. gloeosporioides sl.Colombia, Ecuador
C. gossypiiColombiaUnverified
C. siamenseColombia
C. theobromicolaColombia
C. tropicaleColombia
C. orbiculare species
complex		C. lindemuthianumColombia, PeruPeru
unverified
Singleton speciesC. coccodesColombiaUnverified
ss: sensu stricto. sl: sensu lato.
Table
Table 2. Families and botanical species in Colombia, Ecuador, Peru, and Venezuela reported to have diseases caused by Colletotrichum species complexes.
Table 2. Families and botanical species in Colombia, Ecuador, Peru, and Venezuela reported to have diseases caused by Colletotrichum species complexes.
Family Species Common Name
Anacardiaceae Manguifera indica L. Mango
Annonaceae Annona muricata L. Soursop
Areacaceae Elaeis guinensis Jacq. Oil palm, African palm
CaricaceaeCarica papaya L.Papaya
Euphorbiaceae Hevea brasiliensis Muell. Rubber
Fabaceae Phaseolus vulgaris L. Common bean
Lupinus mutabilis Sweet Tarwi, Lupin, Chocho, Altramuz
Stylosanthes guianensis Aubl. Stylosanthes
Heliconiaceae Heliconia spp. Heliconia, platanillo
Lauraceae Persea americana Mill. Avocado
Malvaceae Theobroma cacao L. Cocoa
Gossypium spp. Cotton
Musaceae Musa AAB Simmonds Platane
Passifloraceae Passiflora edulis f. edulis Sims Gulupa, Poro poro, purple passion fruit
ProteaceaeMacadamia integrifoliaMacadamia
Rosaceae Rubus glaucus Benth. Andean raspberry
Fragaria × ananassaStrawberry
Rubiaceae Coffea arabica L. Coffee
RutaceaeCitrus latifolia TanakaTahiti Lima
Solanaceae Capsicum spp. L. Pepper
Solanum melongena L. Eggplant
Solanum betaceum Cav. Tamarillo, tree tomato
Solanum tuberosumPotato Group Andigena
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Guevara-Suarez, M.; Cárdenas, M.; Jiménez, P.; Afanador-Kafuri, L.; Restrepo, S. Colletotrichum Species Complexes Associated with Crops in Northern South America: A Review. Agronomy 2022, 12, 548. https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy12030548

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Guevara-Suarez M, Cárdenas M, Jiménez P, Afanador-Kafuri L, Restrepo S. Colletotrichum Species Complexes Associated with Crops in Northern South America: A Review. Agronomy. 2022; 12(3):548. https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy12030548

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Guevara-Suarez, Marcela, Martha Cárdenas, Pedro Jiménez, Lucía Afanador-Kafuri, and Silvia Restrepo. 2022. "Colletotrichum Species Complexes Associated with Crops in Northern South America: A Review" Agronomy 12, no. 3: 548. https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy12030548

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