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Colletotrichum sublineola (wrongly named for many years as Colletotrichum sublineolum), is the causal agent of sorghum anthracnose, which is one of the most important diseases in sorghum and can cause losses up to 25%.

Taxonomic History/Systematics
The history of the taxonomy and systematics of C. sublineola and related species is highlighted below.

Important Developments in Classification - Taxonomy

1790 – Tode ''et. al''. first reported the genus Vermicularia.

1831 - Corda (22) introduced the genus Colletotrichum, the name that is most commonly used in modern taxonomy.

1904 - C. sublineola was first published as C. sublineola Henn. in Kaba´t and Buba´k (1904). However, the MycoBank and Index Fungorum consider this name as invalid. Article 32.1(d) of the ICBN code stipulates the prerequisite of a description in order for the taxon to be validly published. Index Fungorum argues that the author did not follow Article 32.1(d) (61). However, Crouch (61) speculated that “the label to Kaba´t’s and Buba´k’s Fungi Imperfecti Exsiccati No. 186 includes a detailed Latin description of C. sublineola, in compliance with Article 32.1 requirements of the nomenclatural code for pre-1953 taxa”, thus the name published in 1904 should be accepted.

1909 – The first Colletotrichum species from a pooid grass was formally reported and described (20).

1913 – C. sublineola was formally described as Colletotrichum sublineola Henn. ex Sacc. & Trotter, Sylloge Fungorum 22: 1206 (1913). This is the name adopted by MycoBank and Index Fungorum and in recent publications.

1914 – It was proposed that anthracnose diseases in cereals and grasses were caused by different Colletotrichum species. Each species was proposed based on host specificity and morphological features. The Colletotrichum species and their hosts proposed are the following: C. sublineola was found to be pathogenic to Sorghum spp.; C. caudatum was pathogenic to several C4 grasses, such as indiangrass and big bluestem; and C. falcatum was found to cause red rot in sugarcane (14). C. graminicola (Ces.) G.W. Wilson, in contrast, was believed to infect a wide range of hosts such as corn (Zea mays L.), wheat (Triticum aestivum L.), oats (Avena sativa L.), and several species from Poaceae subfamily Pooideae, such as forage, turf, and amenity grasses (14).

1957 - C. sublineola was considered by Arx ''et. al., along with C. falcatum and C. caudatum, as synonyms of C. graminicola'' (11). Arx reduced the 750 Colletotrichum names that had been published up to that point to just eleven. Arx’s monograph was groundbreaking in Colletotrichum taxonomy.

1980 – Sutton ''et. al''. proposed the application of the name C. graminicola to any Colletotrichum spp. From graminicolous hosts other than corn (15).

1980 – Sutton re-established C. sublineola as a distinct taxon based on appressorial characters (15).

1990 - The University of Bath, UK, held the first International Workshop on Colletotrichum, where the taxonomy of the Colletotrichum was discussed.

1992 - Mills et al. (41) and Sreenivasaprasad et al. (47) published the first papers using DNA sequence data to distinguish Colletotrichum species.

1994 - Sherriff et al. (44) used ITS2 and LSU sequences of 27 Colletotrichum strains and built the first bootstrapped NJ trees for Colletotrichum. The author found that those 27 strains belonged to 13 different species.

1996 - A second phylogenetic study of the genus was published by Sreenivasaprasad et al. (48) using parsimony analysis of ITS 1 and 2 sequences from 18 species of Colletotrichum, and the authors were able to identify six infrageneric groups.

1999 - Another study proposed an association between isolates from turf grasses and those from corn (16). None was mentioned about isolates from sorghum.

1999 - Results from Browning ''et. al''. supported a separate lineage of turfgrass pathogens and corn. Now, sorghum isolates was also included and the result showed that all the isolates shared a single ancestor (18).

2002 - First multilocus phylogenetic analyses of Colletotrichum species were published by Talhinhas et al. (52), using ITS, TUB2 and HIS4 sequences. C. sublineola was not included in this work.

2004 - Molecular data using RAPD marker profiles were used to suggest a close connection between C. sublineola and isolates of Colletotrichum causing anthracnose in annual bluegrass turf. (16, 17).

2006 – Despite morphological similarity, molecular techniques using ITS region were able to differentiate C. cereale, C. graminicola and C. sublineola (31).

2008 - Crouch et. al suggested that Colletotrichum spp. from grass hosts arose only once in the genus.

2009 –A list of Colletotrichum names in current use was published in which 66 species were accepted and 20 species names were considered doubtful (36).

2009 – The name C. sublineolum changed to C. sublineola. The Index Fungorum accepted the hypothesis that the sublineolum was an incorrect variation from the original name sublineola (62, 63).

2012 - Whole-genome sequences of C. graminicola and C. higginsianum have been completed (9) which will help researchers to understand the host-parasite interactions and relationship between species in Colletotrichum.

After several changes on the systematics of the genera Colletotrichum, C. sublineola was placed in the following classification:

› KINGDOM - Fungi

› SUBKINGDOM - Dikarya

› PHYLUM - Ascomycota

› SUBPHYLUM - Pezizomycotina

› CLASS – Sordariomycetes

Distinguishing morphological features
In order to identify Colletotrichum species, criteria based on morphology, such as conidial shape and size have been used. Additionally, host identity and type of damage caused by the pathogen has been important in determining the causal agent.

Crouch (60) described C. sublineola as very similar to C. eremochloae J.A. Crouch & Tomaso- Peterson sp. nov. FIGS. 1–3 MycoBank MB563346. Both species, however, are distinct based on fixed nucleotide differences at nuclear internal transcribed spacer region, Apn2, Apn2/Mat1 and Sod2 (60).. Crouch (60) described colonies of C. eremochloae on PDA as follows: “Colonies on PDA raised, aerial mycelium light to dark gray without visible conidial masses, with agar surrounding colony bright yellow. Conidia one-celled, falcate sometimes fusiform with acute or rounded apices, smooth, hyaline, (19.2–)22.5–24.3(–25.1) 3 (3.4–)5.1–6.2(–7.4) mm (mean 5 23.4 3 5.6, S.D. 1.0, 1.0, n 5 50). Setae and sclerotia absent. Hyphal appressoria abundant in culture, medium to dark brown, globose, ovoid, oboviod or clavate, lobate or multilobate, apices obtuse, edges entire, (8.1–)9.8–14.5 3 7.2– 10.4(–13.2) mm (mean 5 12.4 3 8.9, S.D. 0.9, 0.8, n 5 50).”.

Typical lesions of C. sublineola in sorghum plants have red margins and centers that turns ashy gray as the tissue dies. Lesions on the stem have a gray center and are circular with a red to black border. This fungus produces dark cup-shaped acervuli surrounded by several setae in the center of the lesions. The lesion also shows a dark textured surface, due to the dense setae. Acervuli contain creamy colored conidial masses (8) and conidia are colorless and crescent-shaped. Only falcate conidia are produced on solid media, whereas the conidia are mostly oval and variable in size in liquid media (1).

Phylogenetic Affinities and Modern Phylogenetic Research
Morphological and cultural criteria have been used effectively for identification of some species; however, this methodology has many limitations. However, molecular techniques based on multi-gene analysis and barcoding have been successfully used to delimit species boundaries. These new approaches are useful for characterizing and identifying taxa within Colletotrichum (23). Traditional and modern methodologies for Colletotrichum taxon identification are also applicable to C. sublineola. A number of conflicting hypotheses have been proposed concerning the phylogenetic affinities of C. sublineola and other species of Colletotrichum (see above “Important Developments in Classification - Taxonomy”). Recent papers, using molecular approaches, have proposed a close relationship among C. sublineola, C. cereale, C. graminicola and C. eremochloae. Although C. cereale, C. graminicola and C. sublineola share similar morphological features, sequence analyses of 1229 bp from three loci (ITS1/5.8S/ITS2, MAT1-2, and SOD2) were able to differentiate these three species. However, the work done by Crouch ''et. al''. (31) did not resolve the relationships among these taxa.

Until 2009, papers published in molecular phylogenetic assumed that 1229 bp from three loci were sufficient to distinguish C. sublineola from its morphologically similar grass pathogens, such as C. cereale and C. graminicola. However, this 1229 bp dataset was unable to distinguish these taxa at a fine-scale resolution. In order to overcome this issue, in 2009, Crouch ''et. al''. (65) used four nuclear genes from ITS1/5.8S/ITS2, MAT1-2, Apn1, and SOD2, and generated a total of 3031 bp of sequence data. In this work, Crouch, ''et. al''. found that the lineages that come from C3 plants, C. cereale, occur on a wide range of host species divided into 10 different populations according to ecosystem and/or host plant. One single generalist population was found to be spread across numerous habitat types. The author also reported that host specialization predominates in graminicolous (C4) Colletotrichum such as C. graminicola, C. sublineola, C. falcatum, C. eleusines and C. caudatum. However, it still unclear whether Colletotrichum species really exhibit host specificity, due to the fact that a number of Colletotrichum species have endophytic behavior, and most of work done has incomplete sampling.

In 2012, Crouch published another paper proposing that the new species C. eremochloae, responsible for centipedegrass anthracnose disease, is closely related to C. sublineola. The author used sequence data from C. eremochloae (Apn2, Apn2/Mat1, Sod2, ITS) and compared with data from C. sublineola to determine that C. eremochloae is the sister taxon of C. sublineola, and used genealogical concordance phylogenetic species recognition to define species boundaries.

A list of principal phylogenetic research papers on Colletotrichum species based on DNA sequence data was published in 2012 by Cannon (9). This list includes the clade, host taxa, geographical limits and loci used in each publication. This is a nice source of information for phylogenetic studies with C. sublineola and other species of Colletotrichum. The same publication cites the molecular markers used as authentic sequences for accepted Colletotrichum species and where to find the GenBank accession numbers.

Ecology
Host Distribution

The genus Colletotrichum is one of the most numerous with around 600 species that infect over 3200 species of monocot and dicot plants (66). However, the host range of C. sublineola is poorly defined. This is due to a number of reasons that includes incomplete sampling, lack of knowledge of pathogenic effects, incorrect assignment of sequences on GenBank, and the fact that several species of Colletotrichum exist as endophytes and therefore additional isolates of C. sublineola may remain unsampled.

Koch's postulate has not been properly used to define host specificity in many species of Colletotrichum. The current methodology for definition of host range, based simply on isolation from living plant tissue, is not sufficient to verify if a species is a latent pathogen with a hemibiotrophic/biotrophic phase or an endophyte.

Hyde (64) cites molecular work done by Crouch (unpubl. data) in which only Sorghum bicolor and S. halepense were confirmed as hosts (Crouch, unpubl. data). As described previously (see above “Phylogenetic Affinities and Modern Phylogenetic Research”) morphological observations of C. sublineola from other host may be erroneous, as the morphology of this fungus is indistinguishable from several other graminicolous Colletotrichum species (65).

Geographic Distribution

Since the nomenclature and classification of C. sublineola is complex, and may be incorrect in several publications, it is challenging to find out the actual geographic distribution of this pathogen. The USDA host-fungus database (69) mentions several countries in which this species was reported; these countries includes: Togo, Myanmar, Brazil, Ethiopia, Germany, India, Japan, South Africa, Zambia, China, Sudan. Colletotrichum sublineola is reported by USDA host-fungus database to be distributed in several states in the United States, including North Carolina, Texas, Virginia, Indiana, Arkansas and Minnesota. Sorghum anthracnose has been reported as an important disease in different states in the United States, such as Florida, Arkansas, Alabama, Texas, Missouri and Georgia (71, 72, 73, 74, 75, 76). However, most of the extension publications in this area refer to C. graminicola and not C. sublineola as the causal agent of this disease.

Reproductive Biology
Lifecycle/Sexual/Sexual/Asexual Reproduction

Similar to many other fungi, the Colletotrichum asexual morph is more commonly associated with disease symptoms; whereas the sexual morph, Glomerella, tends to develop on moribund or dead host tissues (51). Connection of historical asexual-sexual marphs in Colletotrichum is very problematic because many of the claimed links are not based on authentic material; most are based on little more than association with diseased plant samples (9). In most cases the sexual names are not typified according to modern practice. Many asexual-sexual connections need further study.

In a number of Colletotrichum species, sexual reproduction has been documented only in laboratory crosses, but it is unclear if sexual recombination occurs in natural populations (34, 32). The first description of a Colletotrichum sexual morph was done by Stoneman (49) in the genus Gnomoniopsis Stoneman. The teleomorph of C. sublineola was identified by Vaillancourt and Hanau in 1992, but never was formally described or named. Cannon ''et. al''. provides a complete list of Colletotrichum species with reported Glomerella sexual morphs (9).

Based on genetics and morphological comparisons of Glomerella isolates from maize and from sorghum, Vaillancourt proposed in 2000 that C. falcatum and C. graminicola are essentially homothallic, while C. sublineola may be strictly heterothallic (67, 68).

Dispersal Mechanisms
It is not very well understood how C. sublineola is dispersed. Cannon ''et. al''. state that Colletotrichum is spread via air transmission of ascospores and water-splash dispersal of conidia from infected plants. Menezes ''et. al''. (60) speculates that the conidial mucilage may act as a protectant, permitting wind dispersal of conidial masses (60). These dispersal mechanisms may apply to C. sublineola, but in depth studies need to be done to learn and understand how this species is dispersed.

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