Re-identification of Colletotrichum gloeosporioides Species Complex Isolates in Korea and Their Host Plants

Article information

Plant Pathol J. 2024;40(1):16-29
Publication date (electronic) : 2024 February 1
doi : https://doi.org/10.5423/PPJ.OA.09.2023.0133
1Korean Agricultural Culture Collection, Agricultural Microbiology Division, National Institute of Agricultural Sciences, Rural Development Administration, Wanju 55365, Korea
2Plant Pathology and Phyto-immunology, Plant Protection Research Institute, Duc Thang, Bac Tu Liem, Ha Noi 143315, Vietnam
3Division of Environmental Science and Ecological Engineering, Korea University, Seoul 02841, Korea
4Crop Protection Division, National Institute of Agricultural Sciences, Rural Development Administration, Wanju 55365, Korea
5Department of Agricultural Biology, Jeonbuk National University, Jeonju 54896, Korea
*Co-corresponding authors. S.-B. Hong, E-mail) funguy@korea.kr, Phone) +82-63-238-3025, FAX) +82-63-238-3845. H.-J. Ju, E-mail) juhojong@jbnu.ac.kr, Phone) +82-63-270-2519, FAX) +82-63-270-2531
Handling Editor : Sook-Young Park
Received 2023 September 27; Revised 2023 November 16; Accepted 2023 December 3.

Abstract

The Colletotrichum gloeosporioides species complex includes many phytopathogenic species, causing anthracnose disease on a wide range of host plants and appearing to be globally distributed. Seventy-one Colletotrichum isolates in the complex from different plants and geographic regions in Korea were preserved in the Korean Agricultural Culture Collection (KACC). Most of them had been identified based on hosts and morphological features, this could lead to inaccurate species names. Therefore, the KACC isolates were re-identified using DNA sequence analyses of six loci, comprising internal transcribed spacer, gapdh, chs-1, his3, act, and tub2 in this study. Based on the combined phylogenetic analysis, KACC strains were assigned to 12 known species and three new species candidates. The detected species are C. siamense (n = 20), C. fructicola (n = 19), C. gloeosporioides (n = 9), C. aenigma (n = 5), C. camelliae (n = 3), C. temperatum (n = 3), C. musae (n = 2), C. theobromicola (n = 2), C. viniferum (n = 2), C. alatae (n = 1), C. jiangxiense (n = 1), and C. yulongense (n = 1). Of these, C. jiangxiense, C. temperatum, C. theobromicola and C. yulongense are unrecorded species in Korea. Host plant comparisons showed that 27 fungus-host associations are newly reported in the country. However, plant-fungus interactions need to be investigated by pathogenicity tests.

The Colletotrichum gloeosporioides species complex is the most diverse group in the genus Colletotrichum, causing anthracnose disease in many economically important crops worldwide and also occurring as asymptomatic endophytes in a broad range of host plants (Hyde et al., 2009; Liu et al., 2022; Lu et al., 2004). In Korea, the species in this complex have been reported as destructive diseases on widely cultivated crops such as C. siamense and C. fructicola on apple (Kim et al., 2018a; Park et al., 2018), peach (Lee et al., 2020a, 2020b) and strawberry (Nam et al., 2013, 2022), and C. gloeosporioides on citrus, apple, grape, persimmon and strawberry (Korean Society of Plant Pathology, 2022).

C. gloeosporioides was first introduced by Penzig (1882), and then became a common phytopathogenic fungus with a global distribution. Prior to the availability of DNA sequence data, C. gloeosporioides and other taxa in the genus Colletotrichum were identified based on host species and morphological characteristics. However, micro-morphological features such as the size and shape of conidia, appressoria and setae or teleomorph characters overlapped in many species and these features could change under different growing conditions (Weir et al., 2012). For instance, cylindrical conidia with round ends were typical characteristics of species of the C. gloeosporioides species complex, but these characteristics were also observed in many members in the C. dracaenophilum, C. magnum, and C. orchidearum species complexes, or in some singleton species (Damm et al., 2019; Liu et al., 2022). Cultural characteristics of different strains of a species in the C. gloeosporioides species complex were often significant variations (Weir et al., 2012). On the other hand, most members of the C. gloeosporioides species complex have a broad host range and a plant could be associated with more than one Colletotrichum species (Jayawardena et al., 2021; Johnston, 2000; Johnston et al., 2005). Therefore, the host reference and morphology are insufficient to distinguish species members in this species complex.

A large number of Colletotrichum species have been re-identified based on DNA sequence analyses of multiple loci such as the nuclear ribosomal internal transcribed spacer (ITS) region, glyceraldehyde-3-phosphate dehydrogenase (gapdh), chitin synthase 1 (chs-1), histone-3 (his3), actin (act), and beta-tubulin 2 (tub2) (Cannon et al., 2012; Jayawardena et al., 2016; Liu et al., 2022; Weir et al., 2012). To date, at least 61 accepted species have been introduced in the C. gloeosporioides species complex (Liu et al., 2022; Zhang et al., 2023; Zheng et al., 2022). They shared high similarity of ITS sequences but could separate using multi-locus analyses of informative loci, especially gapdh and tub2 genes (Weir et al., 2012).

Isolates of the C. gloeosporioides species complex have been collected in Korea since the 1990s and stored in the Korean Agricultural Culture Collection (KACC), National Institute of Agricultural Sciences. However, these isolates had been identified based mainly on the host species and morphological characteristics by depositors. Hence, this study aims to (1) reassess the identification of the C. gloeosporioides species complex isolates in KACC using multi-locus analyses of six loci (ITS, gapdh, chs-1, his3, act, and tub2); (2) re-arrange the combination between host plants and fungal species.

Materials and Methods

Fungal isolates

Seventy-one isolates in the C. gloeosporioides species complex that originated in Korea and stored in KACC were used in this study. Details of the isolates are listed in Table 1. The living cultures preserved in liquid nitrogen were retrieved on potato dextrose agar (PDA; Difco Laboratories, Detroit, MI, USA) and were used for DNA extraction and phylogenetic analyses.

Isolates of the Colletotrichum gloeosporioides species complex used in this study

DNA extraction, polymerase chain reaction amplification, and sequencing

The mycelium of each isolate was taken from a 5-day-old culture on a PDA medium. Genomic DNA extraction was performed with the DNeasy plant mini kit (Qiagen, Hilden, Germany), following the manufacturer’s instructions. Six loci of Colletotrichum isolates, including ITS, gapdh, chs-1, his3, act, and tub2 were amplified with the primer pairs ITS1/ITS4 (White et al., 1990), GDF1/GDR1 (Guerber et al., 2003), CHS-79F/CHS-345R (Carbone and Kohn, 1999), CYLH3F/CYLH3R (Crous et al., 2004), ACT-512F/ACT-783R (Carbone and Kohn, 1999), and T1/BT2b (Glass and Donaldson, 1995; O’Donnell and Cigelnik, 1997), respectively. Each polymerase chain reaction (PCR) was performed in a volume of 25 μl containing 12.5 μl PCR Master Mix (2×), 8.5 μl nuclease-free water, 1 μl (4.5 pMol) of each primer, and 2 μl DNA template (100 ng/μl). PCR conditions of six loci were set up as described by Thao et al. (2023). PCR amplifications were carried out using a MJ Research PTC-200 Thermal Cycler (MJ Research, Ramsey, MN, USA). PCR products were purified with the QIAquick PCR Purification Kit (Qiagen) and checked by gel electrophoresis before being sent to the Macrogen Company (Seoul, Korea) for sequencing with the amplification primers.

Phylogenetic analysis

Raw sequences generated from forward and reverse primers in this study were trimmed and paired by MEGA 11 (Tamura et al., 2021). Assemble sequences were deposited to RDA-GeneBank (http://genebank.rda.go.kr) with accession numbers in Table 1. The closest reference sequences in GenBank were obtained by BLASTN search and were used for phylogenetic analyses with sequences from 71 KACC isolates and a species in the different species complex as an outgroup. The dataset of each locus was separately aligned using the multiple alignment program MAFFT version 7 (https://mafft.cbrc.jp/alignment/server/) with the G-INS-1 option. The poor alignments at both ends were cut and the alignments were improved by visual inspection in MEGA 11 and concatenated afterward in this software. A maximum likelihood (ML) phylogenetic tree was inferred based on the combined six datasets (ITS, gapdh, chs-1, his3, act, and tub2), using IQ-TREE with the best-fit model “TN+F+G4” and 1,000 ultrafast bootstrap replicates. The substitution model options were auto-evaluated according to the provided alignment files. The phylogenetic trees were viewed in MEGA11 and depicted in Adobe Illustrator.

Results

The phylogenetic analysis included 71 KACC isolates that originated in Korea (Table 1), 58 reference strains from 56 previously accepted species and C. arecacearum (MH0003) as the outgroup (Supplementary Table 1). The concatenated dataset alignment consisted of 2,504 characters (1,419 constant, 1,002 variable, and 502 parsimony-informative characters), including gaps. Of these, 565 characters were from ITS, 282 characters from gapdh, 251 characters from chs-1, 376 characters from his3, 264 characters from act, and 766 characters from tub2.

The multi-locus phylogenetic analysis resolved all KACC isolates into 15 clades. Each of the 12 clades was well clustered with an ex-type or holotype strain of the previously described species, supported by 86% to 100% ML bootstrap values (Fig. 1). Of which, 20 isolates clustered with C. siamense, 19 isolates with C. fructicola, nine isolates with C. gloeosporioides sensu stricto, five isolates with C. aenigma, three isolates with C. camelliae, three isolates with C. temperatum, two isolates with C. musae, two isolates with C. theobromicola, two isolates with C. viniferum, one isolate with C. alatae, one isolate with C. jiangxiense and one isolate with C. yulongense. The isolate KACC 47776 formed a sister clade to C. makassarense and C. tropicale. However, this isolate was distinguished from C. makassarense at gapdh (93.97% identity), act (98.76% identity), chs-1 (98.8% identity), and ITS (98.97% identity), and differentiated from C. tropicale by gapdh (94.03% identity), act (98.77% identity), and chs-1 (97.61% identity). The isolate KACC 47035 was phylogenetically related to C. endophyticum and C. artocarpicola, but shared low sequence similarity at gapdh (92.13% and 90.75%, respectively), act (97.93% and 98.35%), his3 (97.2% with C. endophyticum), chs-1 (98.01% with both species), and tub2 (98.34% with both species). Exception of ITS, all other loci of KAC 48700 shared low sequence similarity with the most closely related species, consisting of gapdh (91.3% identity shared with C. siamense), his3 (92.2% identity with C. siamense), act (95.45% identity with C. conoides, C. aenigma and C. siamense), tub2 (95,71% identity with C. endophyticum), and chs-1 (97.61% identity with C. siamense). According to phylogenetic analysis and BLASTN search results, each of the isolates, KACC 47776, KACC 47035, and KACC 48700, were genetically distinct from the other taxa.

Fig. 1

Maximum likelihood tree based on multi-locus sequences of ITS, tub2, his3, gapdh, chs-1, and act. Species names are followed by strain accession numbers and their hosts (blue). Isolates in this study are in bold and listed by the original names. Bootstrap values below 70% are not present. Ex-type strains are emphasised by asterisks (*). The tree is rooted to Colletotrichum arecacearum (MH003).

Host plants of fungal species in this study

Twenty combinations between hosts and accepted fungal species found in this study have not been reported in any countries. However, the fungi were just isolated from the hosts and their pathogenicity was not confirmed. They are C. aenigma on Ampelopsis glandulosa f. citrulloides, Boehmeria japonica, Ilex rotunda, Laurus nobilis, and Zanthoxylum schinifolium; C. alatae on Dioscorea polystachya; C. camelliae on Cayratia japonica; C. fructicola on Pinus koraiensis, Pinus strobus, and Nepeta tenuifolia; C. gloeosporioides on Amaranthus hybridus, Boehmeria japonica, and Rhododendron micranthum; C. jiangxiense on Atractylodes ovata; C. siamense on Limonium sinuatum and Malus coronaria; C. temperatum on Malus domestica and Tricyrtis macropoda; C. theobromicola on Actinidia arguta; and C. yulongense on Camellia japonica. Seven other combinations, including C. fructicola on Capsicum annuum, Castanea sp., and Limonium sinuatum; C. gloeosporioides on Euonymus japonicus, Morus alba, and Portulaca oleracea; and C. siamense on Vitis vinifera are first reported in Korea (Table 2).

Comparison of host plants of KACC isolates and previous reports

Discussion

Based on DNA sequence analyses of six loci, 43 KACC isolates were renamed, three isolates were newly identified at the species level, 21 strains remained as original names and three isolates were considered as three new species candidates. Nineteen isolates in this study had previously been identified as C. gloeosporioides sensu lato by Kim et al. (2006) and one isolate had been identified as C. acutatum by Lee et al. (2007) using morphological features, ITS and tub2 sequence analyses. However, these isolates were resolved by Kim et al. (2020) and by the present study into four different species, C. siamense (n = 10), C. fructicola (n = 7), C. theobromicola (n = 2), and C. temperatum (n = 1), based on multi-locus analyses of ITS, gapdh, chs-1, tub2 and (his3, act) or (cal and ApMat). The results of this study also revealed four fungal species, C. jiangxiense, C. temperatum, C. theobromicola, and C. yulongense, were first recorded in Korea.

C. siamense (n = 20), C. fructicola (n = 19), and C. gloeosporioides sensu stricto (n = 9) are the most dominant species among KACC isolates in the C. gloeosporioides species complex. According to previous studies and this work, C. gloeosporioides, C. siamense, C. fructicola, C. aenigma, C. jiangxiense, C. theobromicola, C. viniferum, and C. temperatum have a wide range of hosts, whereas C. musae has a narrow host range, on Musa spp. and Mangifera indica, and C. alatae is a host-specific fungus, on the genus Dioscorea (Farr and Rossman, 2021; Jayawardena et al., 2021; Li et al., 2019; Liu et al., 2022; Weir et al., 2012; Zhang et al., 2023). In addition, C. yulongense was originally described by Wang et al. (2019a) on Vaccinium dunalianum (Ericaceae family) and this fungus was found on Camellia japonica (Theaceae family) in this study as the second host plant. Another species, C. camelliae was also reported only on the genus Camellia of the family Theaceae (Liu et al., 2022), but this fungal species was herein from the different family Vitaceae (Cayratia japonica).

C. aenigma was introduced by Weir et al. (2012) and this fungus later became a very popular species, causing anthracnose on the grapevine, Asian pear, and walnut in China (Fu et al., 2019; Wang et al., 2021; Yan et al., 2015), on dragon fruits in Thailand (Meetum et al., 2015), on avocado in Israel (Sharma et al., 2017), on miracle in Japan (Truong et al., 2018), on grape and orange stonecrop in Korea (Choi et al., 2017; Kim et al., 2021). In our study, this fungus was isolated from five new hosts (Ampelopsis glandulosa f. citrulloides, Boehmeria japonica, Ilex rotunda, Laurus nobilis, and Zanthoxylum schinifolium) belonging to the five different families.

Apple (Malus domestica) is one of the most economically important crops in Korea. Kim et al. (2006) and Lee et al. (2007) implicated that C. gloeosporioides and C. acutatum were serious pathogens causing bitter rots of apple fruits in Korea. However, the identified species were unreliable as mentioned above. Later, causal agents of apple bitter rot disease in the country were authentically identified as C. siamense, C. fructicola, C. nymphaeae, C. fioriniae, C. gloeosporioides, and C. aenigma based on multi-locus sequence analyses (Cheon et al., 2016; Kim et al., 2020; Lee et al., 2021; Oo et al., 2018). The Colletotrichum isolates from apple in this work and in our earlier study (Thao et al., 2023) have been collected since 1997 from many different geographic locations in Korea, and the most prevalent species on apple were C. siamense (10 isolates), followed by C. fructicola (seven), C. nymphaeae (five) and C. fioriniae (four), while only one isolate of C. gloeosporioides sensu stricto was from apple and no C. acutatum sensu stricto isolates were found in KACC. Additionally, a fungal species C. temperatum, originally described by Doyle et al. (2013) on Vaccinium macrocarpon, was first detected on apple in this study.

Grape (Vitis vinifera) is an extensively cultivated crop worldwide and in Korea. The crop was seriously damaged by the infection of C. acutatum and C. gloeosporioides (Hong et al., 2008), C. viniferum (Oo and Oh, 2017), and C. aenigma (Kim et al., 2021). In this study, two isolates on grape (Vitis sp.) were identified as C. viniferum, whereas the other two isolates on Vitis vinifera were identified as C. siamense.

Kiwiberry (Actinidia spp.) has been widely cultivated in the country and worldwide (Kim et al., 2017; Latocha, 2017). The anthracnose symptoms caused by C. nymphaeae on kiwiberry fruits were observed in Jeonnam province (Kim et al., 2018b). Many other Colletotrichum species also infected kiwi plants worldwide such as C. aenigma on Actinidia arguta in China (Wang et al., 2019b), C. fioriniae, C. karsti, C. gloeosporioides, C. fructicola, and C. siamense on Actinidia spp. in Japan (Poti et al., 2023). A new combination of kiwiberry and C. theobromicola was found in this study.

The main causal fungi of chili pepper (Capsicum annuum) anthracnose in Korea were known as C. gloeosporioides sensu lato, C. acutatum s. lat., C. dematium s. lat., and C. trucatum s. lat. (Oo and Oh, 2016, 2020; Oo et al., 2017; Park and Kim, 1992). However, only one strain of C. fructicola in the C. gloeosporioides species complex from chili pepper is stored in KACC. While 16 strains of the C. acutatum species complex from chili pepper are preserved in KACC (Thao et al., 2023). It suggests that C. gloeosporioides s.c. is not a main causal fungus on chili pepper anthracnose in Korea.

Machilus thunbergii is a medicinal plant and it was widely distributed in the west-southern islands of Korea and some other Asian countries (Park et al., 1990). Only Glomerella cingulate and C. fructicola were formerly known as pathogens on this plant in Japan (Kobayashi, 2007) and China (Liu et al., 2022), respectively. A new species candidate (KACC47776) from Machilus thunbergii in Jeju, Korea was identified in this study. The second new species candidate (KACC48700) was from Paederia foetida, this host was also infected by many different Colletotrichum species (Liu et al., 2022). The third new species candidate (KACC47035) was the first report of a Colletotrichum fungus on coastal hogfennel (Peucedanum japonicum), an edible wild vegetable and medicinal resource.

A reassessment of members of the C. gloeosporioides species complex in Korea revealed new records of four Colletotrichum species and 27 combinations between plants and fungi in Korea. Of which, new findings of C. fructicola on pepper, C. siamense on grape, C. temperatum on apple, and C. theobromicola on kiwiberry could play an important role in the agricultural sciences and practices of Korea. However, the new combinations found in this study need to be clarified by pathogenicity tests in further studies.

Notes

Conflicts of Interest

No potential conflict of interest relevant to this work was reported.

Acknowledgments

This study was supported by a grant (PJ017286) from the National Institute of Agricultural Sciences and was a part of the “2023 KoRAA Long-term Training Program”, Rural Development Administration, Republic of Korea.

Electronic Supplementary Material

Supplementary materials are available at The Plant Pathology Journal website (http://www.ppjonline.org/).

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Article information Continued

Fig. 1

Maximum likelihood tree based on multi-locus sequences of ITS, tub2, his3, gapdh, chs-1, and act. Species names are followed by strain accession numbers and their hosts (blue). Isolates in this study are in bold and listed by the original names. Bootstrap values below 70% are not present. Ex-type strains are emphasised by asterisks (*). The tree is rooted to Colletotrichum arecacearum (MH003).

Table 1

Isolates of the Colletotrichum gloeosporioides species complex used in this study

Species (this study) Isolate no. Location Collection date Hosta Previous identifications by depositors Re-identifications in previous studies RDA-GeneBank accession no.

ITS gapdh chs-1 his3 act tub2
C. aenigma KACC 48663 Wando 2018 Laurus nobilis C. siamense - RDA0062101 RDA0062486 RDA0067036 RDA0067150 RDA0066965 RDA0062292
KACC 48701 Seogwipo 2018 Ampelopsis glandulosa f. citrulloides C. aenigma - RDA0062110 RDA0062500 RDA0067035 RDA0067151 RDA0066966 RDA0062306
KACC 48698 Jeju 2018 Boehmeria japonica C. aenigma - RDA0062108 RDA0062498 RDA0067038 RDA0067148 RDA0066964 RDA0062304
KACC 48896 Yeosu 2019 Zanthoxylum schinifolium C. fructicola - RDA0062113 RDA0062504 RDA0067039 RDA0067147 RDA0066944 RDA0062309
KACC 48654 Wando 2018 Ilex rotunda C. siamense - RDA0062099 RDA0062484 RDA0067037 RDA0067149 RDA0066987 RDA0062290
C. alatae KACC 47605 Gongju 2013 Dioscorea polystachya Colletotrichum sp. - RDA0062083 RDA0062456 RDA0067092 RDA0067176 RDA0067034 RDA0062252
C. camelliae KACC 43131 Boseong 2006 Camellia sinensis C. gloeosporioides - RDA0062064 RDA0062421 RDA0067095 RDA0067180 RDA0067025 RDA0062216
KACC 48695 Jeju 2018 Camellia japonica C. camelliae - RDA0062105 - RDA0067100 RDA0067182 RDA0067024 RDA0062301
KACC 48694 Jeju 2018 Cayratia japonica C. camelliae - RDA0062104 RDA0062495 RDA0067099 RDA0067183 RDA0067027 RDA0062300
C. fructicola KACC 43014 Daejeon 2006 Pinus koraiensis C. gloeosporioides - RDA0062063 RDA0062408 - - RDA0067015 RDA0062202
KACC 40003 Daejeon 1993 Capsicum annuum C. gloeosporioides C. gloeosporioides (Kim et al., 2006) RDA0062019 RDA0062330 - - RDA0067017 RDA0062123
KACC 42251 Daejeon Unknown Pinus strobus C. gloeosporioides - RDA0062049 RDA0062377 RDA0067062 RDA0067117 RDA0067012 RDA0062173
KACC 47033 Eumseong 2012 Nepeta tenuifolia C. fructicola - RDA0062078 RDA0062449 RDA0067073 RDA0067111 RDA0067009 RDA0062244
KACC 42502 Seoul 2006 Malus domestica C. acutatum C. acutatum (Lee et al., 2007) RDA0062057 RDA0062396 RDA0067066 RDA0067115 RDA0067011 RDA0062191
KACC 46566 Gyeryong 2009 Fragaria sp. C. fructicola - RDA0062072 RDA0062439 RDA0067057 RDA0067119 RDA0067020 RDA0062232
KACC 40695 Geochang 1999 Fragaria × ananassa C. gloeosporioides C. gloeosporioides (Kim et al., 2006 ) RDA0060939 RDA0062351 RDA0067045 RDA0067143 RDA0067021 RDA0062142
KACC 40812 Damyang 1998 Fragaria × ananassa C. gloeosporioides C. gloeosporioides (Kim et al., 2006) RDA0062041 RDA0062364 - - RDA0067016 RDA0062162
KACC 40692 Namwon 1998 Limonium sinuatum C. gloeosporioides C. gloeosporioides (Kim et al., 2006) RDA0060934 RDA0062349 RDA0067058 RDA0067118 RDA0067013 RDA0062141
KACC 42507 Jeongeup 2006 Malus domestica C. gloeosporioides C. gloeosporioides (Lee et al., 2007) RDA0062061 RDA0062401 RDA0067053 RDA0067121 RDA0067014 RDA0062196
KACC 49840 Sangju 2020 Atractylodes ovata C. fructicola - RDA0062116 RDA0062511 RDA0067048 RDA0067122 RDA0067018 RDA0062315
KACC 47034 Cheongyang 2012 Lycium sp. C. fructicola - RDA0062079 RDA0062450 RDA0067074 RDA0067110 RDA0067008 RDA0062245
KACC 49923 Yeongdong 2016 Malus domestica C. gloeosporioides - RDA0062121 RDA0062521 RDA0067046 RDA0067142 RDA0067019 RDA0062325
KACC 47512 Gongju 2013 Castanea sp. C. gloeosporioides - RDA0062082 RDA0062455 RDA0067054 RDA0067120 RDA0066989 RDA0062251
KACC 46964 Gunwi 2012 Malus domestica C. gloeosporioides - RDA0062076 RDA0062444 RDA0067072 RDA0067112 RDA0066988 RDA0062239
KACC 47685 Gunwi 2013 Malus domestica C. gloeosporioides - RDA0062084 RDA0062458 RDA0067043 RDA0067144 RDA0066990 RDA0062263
KACC 47827 Iksan 2014 Mangifera indica C. fructicola - RDA0062088 RDA0062465 RDA0067063 RDA0067116 RDA0066991 RDA0062271
KACC 46963 Gimcheon 2012 Malus domestica C. gloeosporioides - RDA0062075 RDA0062443 RDA0067070 RDA0067113 RDA0067010 RDA0062238
KACC 42499 Cheongsong 2006 Malus domestica C. gloeosporioides C. gloeosporioides (Lee et al., 2007) RDA0062055 RDA0062393 RDA0067068 RDA0067114 RDA0067022 RDA0062188
C. gloeosporioides KACC 40892 Jeju Unknown Cactus sp. C. gloeosporioides C. gloeosporioides (Kim et al., 2006) RDA0062042 RDA0062367 RDA0067081 RDA0067101 RDA0067003 RDA0062163
KACC 47686 Mungyeong 2013 Malus domestica C. gloeosporioides - RDA0062085 RDA0067187 RDA0067085 RDA0067103 RDA0066997 -
KACC 42354 Namyangju 2006 Euonymus japonica Colletotrichum sp. - RDA0062050 RDA0062380 RDA0067083 RDA0067104 RDA0066999 RDA0062176
KACC 48637 Goesan 2017 Rhododendron micranthum C. gloeosporioides - RDA0062097 RDA0062482 - - RDA0067001 RDA0062288
KACC 40961 Sancheong 2001 Portulaca oleracea Glomerella cingulata G. cingulata (Kim et al., 2006) RDA0062047 RDA0062373 RDA0067086 RDA0067102 RDA0066996 RDA0062169
KACC 48696 Jeju 2018 Boehmeria japonica C. gloeosporioides - RDA0062106 RDA0062496 RDA0067079 RDA0067108 RDA0067004 RDA0062302
KACC 49841 Mungyeong 2020 Atractylodes ovata C. gloeosporioides - RDA0062117 RDA0062512 RDA0067080 RDA0067107 RDA0067002 RDA0062316
KACC 49597 Jangseong 2019 Morus alba C. gloeosporioides - RDA0062114 RDA0062506 RDA0067084 RDA0067109 RDA0066998 RDA0062311
KACC 48691 Okcheon 2018 Amaranthus hybridus C. gloeosporioides - RDA0062103 RDA0062493 RDA0067082 RDA0067105 RDA0067000 RDA0062298
C. jiangxiense KACC 49842 Sangju Atractylodes ovata C. kahawae - RDA0062118 RDA0062513 RDA0067093 RDA0067179 RDA0067028 RDA0062317
C. musae KACC 49894 Wanju 2021 Musa × paradisiaca C. musae - RDA0062120 RDA0062515 RDA0067078 RDA0067171 RDA0067005 RDA0062319
KACC 40947 Daejeon 2001 Musa × paradisiaca C. musae - RDA0062046 RDA0062372 RDA0067077 RDA0067172 RDA0067006 RDA0062168
C. siamense KACC 49924 Yeongju 2016 Malus domestica C. gloeosporioides - RDA0062122 RDA0062522 RDA0067047 RDA0067166 RDA0066969 RDA0062326
KACC 40897 Suwon Unknown Malus domestica C. gloeosporioides C. gloeosporioides (Kim et al., 2006) RDA0062045 RDA0062370 RDA0067044 RDA0067167 RDA0066970 RDA0062166
KACC 46988 Chungju 2011 Juglans regia C. gloeosporioides - RDA0062077 RDA0062445 RDA0067050 RDA0067164 RDA0066981 RDA0062240
KACC 48478 Sangju 2015 Unknown C. siamense - RDA0062096 RDA0062479 RDA0067060 RDA0067159 RDA0066986 RDA0062285
KACC 48106 Chuncheon 2015 Malus domestica Colletotrichum sp. - RDA0062092 RDA0062474 RDA0067067 RDA0067155 RDA0066963 RDA0062279
KACC 48402 Hwaseong 2017 Vitis vinifera C. fructicola - RDA0062095 RDA0062477 RDA0067056 RDA0067161 RDA0066976 RDA0062283
KACC 40696 Miryang 1999 Fragaria × ananassa C. gloeosporioides C. gloeosporioides (Kim et al., 2006) RDA0060941 RDA0062352 RDA0067052 RDA0067169 RDA0066979 RDA0062151
KACC 42506 Paju 2005 Malus domestica C. gloeosporioides C. gloeosporioides (Lee et al., 2007) RDA0062060 RDA0062400 RDA0067075 - RDA0067007 RDA0062195
KACC 42390 Sangju 2004 Malus domestica C. gloeosporioides C. gloeosporioides (Lee et al., 2007) RDA0062051 RDA0062381 RDA0067076 - RDA0066980 RDA0062177
KACC 49782 Miryang 2020 Carya sp. C. siamense - RDA0062115 RDA0062508 RDA0067049 RDA0067165 RDA0066982 RDA0062312
KACC 49844 Mungyeong 2020 Atractylodes ovata C. siamense - RDA0062119 RDA0062514 RDA0067071 RDA0067153 RDA0066971 RDA0062318
KACC 40896 Yeongi 2000 Prunus persica C. gloeosporioides - RDA0062044 RDA0062369 RDA0067064 RDA0067157 RDA0066974 RDA0062165
KACC 40694 Suwon 1998 Limonium sinuatum C. gloeosporioides C. gloeosporioides (Kim et al., 2006) RDA0060936 RDA0062350 RDA0067042 RDA0067168 RDA0066978 RDA0066985
KACC 40299 Uiseong 1997 Malus domestica Glomerella cingulata G. cingulata (Kim et al., 2006) RDA0062028 RDA0062344 RDA0067091 RDA0067152 RDA0066943 RDA0062136
KACC 40300 Gunwi 1997 Malus domestica Glomerella cingulata G. cingulata (Kim et al., 2006) RDA0062029 RDA0062345 RDA0067051 RDA0067163 RDA0066968 RDA0062137
KACC 42497 Gunwi 2006 Malus domestica C. gloeosporioides C. gloeosporioides (Lee et al., 2007); C. siamense (Kim et al., 2020) RDA0062053 RDA0062391 RDA0067059 RDA0067160 RDA0066967 RDA0062186
KACC 42498 Yeongju 2006 Malus domestica C. gloeosporioides C. gloeosporioides (Lee et al., 2007); C. siamense (Kim et al., 2020) RDA0062054 RDA0062392 RDA0067069 RDA0067154 RDA0066972 RDA0062187
KACC 42494 Cheongsong 2006 Malus domestica C. gloeosporioides C. gloeosporioides (Lee et al., 2007); C. siamense (Kim et al., 2020) RDA0062052 RDA0066942 RDA0067055 RDA0067162 RDA0066977 RDA0066983
KACC 45482 Jinju 2010 Malus coronaria C. gloeosporioides - RDA0062069 RDA0062434 RDA0067065 RDA0067156 RDA0066973 RDA0062227
KACC 43520 Cheongju 2006 Vitis vinifera C. gloeosporioides - RDA0062067 RDA0062424 RDA0067061 RDA0067158 RDA0066975 RDA0062219
C. temperatum KACC 42503 Yeongju 2004 Malus domestica C. gloeosporioides C. gloeosporioides (Lee et al., 2007) RDA0062058 RDA0062397 RDA0067096 RDA0067178 RDA0067023 RDA0062192
KACC 46405 Osan 2011 Tricyrtis macropoda C. tricyrtii - RDA0062071 RDA0062438 RDA0067097 RDA0067177 RDA0067030 RDA0062231
KACC 46374 Gapyeong 2011 Tricyrtis macropoda C. tricyrtii - RDA0062070 RDA0062437 RDA0067094 RDA0067181 RDA0067026 RDA0062230
C. theobromicola KACC 40698 Muan 1998 Actinidia arguta C. gloeosporioides C. gloeosporioides (Kim et al., 2006) RDA0060942 RDA0062353 RDA0067089 RDA0067185 RDA0067032 RDA0062152
KACC 40699 Muan 1998 Actinidia arguta C. gloeosporioides C. gloeosporioides (Kim et al., 2006) RDA0060943 RDA0062354 RDA0067088 RDA0067186 RDA0067033 RDA0062153
C. viniferum KACC 43519 Cheonan 2006 Vitis sp. C. gloeosporioides - RDA0062066 RDA0062423 - - RDA0066993 RDA0062218
KACC 43132 Cheonan 2006 Vitis sp. C. gloeosporioides - RDA0062065 RDA0062422 RDA0067040 RDA0067146 RDA0066994 RDA0062217
C. yulongense KACC 48651 Wando 2018 Camellia japonica C. siamense - RDA0062098 RDA0062483 RDA0067098 RDA0067184 RDA0067029 RDA0062289
Colletotrichum sp. KACC 47776 Jeju 2014 Machilus thunbergii Colletotrichum sp. - RDA0062087 RDA0066941 RDA0067041 RDA0067170 RDA0066992 RDA0066984
Colletotrichum sp. KACC 47035 Eumseong 2012 Peucedanum japonicum Colletotrichum sp. - RDA0062080 RDA0062451 RDA0067087 RDA0067173 RDA0066995 RDA0062246
Colletotrichum sp. KACC 48700 Jeju 2018 Paederia foetida Colletotrichum sp. - RDA0062109 RDA0062499 RDA0067090 RDA0067175 RDA0067031 RDA0062305

ITS, internal transcribed spacer; gapdh, glyceraldehyde-3-phosphate dehydrogenase; chs-1, chitin synthase 1; his3, histone-3; act, actin; tub2, beta-tubulin 2; RDA, Rural Development Administration; KACC, Korean Agricultural Culture Collection.

a

The pathogenicity on host was not confirmed. The fungus was just isolated from the host.

Table 2

Comparison of host plants of KACC isolates and previous reports

Species Hosta

KACC The List of Plant Diseases in Korea Previous reports in Korea Global reports References
C. aenigma Ampelopsis glandulosa f. citrulloides* - - - -
Boehmeria japonica* - - - -
Ilex rotunda* - - - -
Laurus nobilis* - - - -
Zanthoxylum schinifolium* - - - -
C. alatae Dioscorea polystachya* - - - -
C. camelliae Camellia sinensis Camellia sinensis Camellia sinensis Camellia sinensis Hassan et al. (2023)
Camellia japonica Camellia japonica Camellia japonica Camellia japonica Korean Society of Plant Pathology (2022)
Cayratia japonica* - - - -
C. fructicola Atractylodes ovata - Atractylodes ovata Atractylodes ovata Hassan et al. (2022)
Capsicum annuum - - Capsicum annuum Liu et al. (2016)
Castanea sp. - - Castanea sp. Jiang et al. (2021)
Fragaria × ananassa - Fragaria × ananassa Fragaria × ananassa Nam et al. (2013)
Limonium sinuatum - - Limonium sinuatum Zhang et al. (2023)
Lycium sp. - Lycium chinense Lycium chinense Paul et al. (2014)
Malus domestica Malus domestica Malus domestica Malus domestica Kim et al. (2018a)
Mangifera indica Mangifera indica Mangifera indica Mangifera indica Joa et al. (2016)
Pinus koraiensis* - - - -
Pinus strobus* - - - -
Nepeta tenuifolia* - - - -
C. gloeosporioides Amaranthus hybridus* - - - -
Atractylodes ovata Atractylodes ovata Atractylodes ovata Atractylodes ovata Hassan et al. (2022)
Boehmeria japonica* - - - -
Cactus sp. - Cactus sp. Cactus sp. Kim et al. (2000)
Euonymus japonicus - - Euonymus japonicus Huang et al. (2016)
Malus domestica (syn. M. pumila) Malus pumila Malus pumila Malus pumila Cheon et al. (2016)
Morus alba - - Morus alba Sharma et al. (2013)
Portulaca oleracea - - Portulaca oleracea Simmonds (1966)
Rhododendron micranthum* - - - -
C. jiangxiense Atractylodes ovata* - - - -
C. musae Musa × paradisiaca Musa × paradisiaca Musa × paradisiaca Musa × paradisiaca Lim et al. (2002)
C. siamense Atractylodes ovata - Atractylodes ovata Atractylodes ovata Hassan et al. (2022)
Carya sp. - Carya sp. Carya sp. Oh et al. (2021)
Fragaria × ananassa - Fragaria × ananassa Fragaria × ananassa Nam et al. (2022)
Juglans regia Juglans regia Juglans regia Cho et al. (2023)
Limonium sinuatum* - - - -
Malus coronaria* - - - -
Malus domestica (syn. M. pumila) Malus pumila Malus pumila Malus pumila Park et al. (2018)
Prunus persica Prunus persica Prunus persica Prunus persica Lee et al. (2020a)
Vitis vinifera - - Vitis vinifera Zhang et al. (2023)
C. temperatum Malus domestica* - - - -
Tricyrtis macropoda* - - - -
C. theobromicola Actinidia arguta* - - - -
C. viniferum Vitis sp. Vitis vinifera Vitis vinifera Vitis vinifera Oo and Oh (2017)
C. yulongense Camellia japonica* - - - -
Colletotrichum sp. (KACC 47776, new species candidate) Machilus thunbergii* - - - -
Colletotrichum sp. (KACC 47035, new species candidate) Peucedanum japonicum* - - - -
Colletotrichum sp. (KACC 48700, new species candidate) Paederia foetida* - - - -

Hosts in “bold” and “*” are unreported in Korea and in the world, respectively.

KACC, Korean Agricultural Culture Collection.

a

The pathogenicity on host was not confirmed. The fungus was just isolated from the host.