Skip to main content
Log in

Colletotrichum species associated with cultivated citrus in China

  • Published:
Fungal Diversity Aims and scope Submit manuscript

Abstract

There have been considerable advances in the understanding of species concepts in the genus Colletotrichum. This has lead to the need to carry out fresh surveys of Colletotrichum species associated with important hosts. Colletotrichum species are associated with Citrus plants as saprobes, important pre-harvest and post-harvest pathogens, as well as endophytes. In this study, a total of 312 Colletotrichum strains were isolated from leaves, shoots and fruits of cultivated Citrus and Fortunella species with or without disease symptoms across the main citrus production areas in China. The morphology of all strains were studied and multilocus (ACT, TUB2, CAL, GAPDH, GS, ITS) phylogeny established. Strains were from four important species complexes of Colletotrichum, namely C. gloeosporioides species complex, C. boninense species complex, C. acutatum species complex and a final group including C. truncatum, which was rare on Citrus species. The species belonging to the C. gloeosporioides species complex comprised C. gloeosporioides and C. fructicola, the C. boninense complex comprised C. karstii and a new species C. citricola and the C. acutatum complex included a new species, C. citri. The ability of strains to cause anthracnose on citrus fruits was tested by inoculation and strains of Colletotrichum gloeosporioides, C. fructicola and C. truncatum were pathogenic.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Cai L, Hyde KD, Taylor PWJ, Weir B, Waller J, Abang MM, Zhang JZ, Yang YL, Phoulivong S, Liu ZY (2009) A polyphasic approach for studying Colletotrichum. Fungal Diversity 39:183–204

    Google Scholar 

  • Cannon PF, Buddie AG, Bridge PD (2008) The typification of Colletotrichum gloeosporioides. Mycotaxon 104:189–204

    Google Scholar 

  • Cannon PF, Damm U, Johnston PR, Weir BS (2012) Colletotrichum-current status and future directions. Stud Mycol 73:181–213

    Article  PubMed  CAS  Google Scholar 

  • Carbone I, Kohn LM (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91:553–556

    Google Scholar 

  • Chinese Research Institute of Pomology and Citrus (1994) The records of Chinese fruit trees’ diseases and pests (second edition) (in Chinese). China agriculture press

  • Chomnunti P, Schoch CL, Aguirre-Hudson B, Ko-Ko TW, Hongsanan S, Jones EBG, Kodsueb R, Phookamsak R, Chukeatirote E, Bahkali AH (2011) Capnodiaceae. Fungal Diversity 1–32

  • Crouch JA, Beirn LA, Cortese LM, Bonos SA, Clarke BB (2009a) Anthracnose disease of switchgrass caused by the novel fungal species Colletotrichum navitas. Mycol Res 113(12):1411–1421

    Article  PubMed  CAS  Google Scholar 

  • Crouch JA, Clarke BB, Hillman BI (2006) Unraveling evolutionary relationships among the divergent lineages of Colletotrichum causing anthracnose disease in turfgrass and corn. Phytopathology 96(1):46–60

    Article  PubMed  CAS  Google Scholar 

  • Crouch JA, Clarke BB, White JF Jr, Hillman BI (2009b) Systematic analysis of the falcate-spored graminicolous Colletotrichum and a description of six new species from warm-season grasses. Mycologia 101(5):717–732

    Article  PubMed  Google Scholar 

  • Crouch JA, Tomaso-Peterson M (2012) Anthracnose disease of centipede grass turf caused by Colletotrichum eremochloae, a new fungal species closely related to Colletotrichum sublineola. Mycologia 104(5):1085–1096

    Article  PubMed  Google Scholar 

  • Damm U, Cannon PF, Woudenberg JHC, Crous PW (2012a) The Colletotrichum acutatum species complex. Stud Mycol 73:37–113

    Article  PubMed  CAS  Google Scholar 

  • Damm U, Cannon PF, Woudenberg JHC, Johnston PR, Weir BS, Tan YP, Shivas RG, Crous PW (2012b) The Colletotrichum boninense species complex. Stud Mycol 73:1–36

    Article  PubMed  CAS  Google Scholar 

  • Damm U, Woudenberg J, Cannon P, Crous P (2009) Colletotrichum species with curved conidia from herbaceous hosts. Fungal Diversity 39:45–87

    Google Scholar 

  • Du M, Schardl CL, Nuckles EM, Vaillancourt LJ (2005) Using mating-type gene sequences for improved phylogenetic resolution of Collectotrichum species complexes. Mycologia 97(3):641–658

    Article  PubMed  CAS  Google Scholar 

  • Farr DF, Aime MC, Rossman AY, Palm ME (2006) Species of Colletotrichum on Agavaceae. Mycological Research 110(12):1395–1408

    Google Scholar 

  • Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Applied and Environmental Microbiology 61(4):1323–1330

    Google Scholar 

  • Hyde KD, Cai L, Cannon PF, Crouch JA, Crous PW, Damm U, Goodwin PH, Chen H, Johnston PR, Jones EBG (2009a) Colletotrichum-names in current use. Fungal Diversity 39:147

    Google Scholar 

  • Hyde KD, Cai L, McKenzie EHC, Yang YL, Zhang JZ, Prihastuti H (2009b) Colletotrichum: a catalogue of confusion. Fungal Diversity 39:1–17

    Google Scholar 

  • Inc. SI (2002–2004) SAS 9.1.3 Help and documentation. Cary, NC: SAS Institute Inc

  • Johnson DA, Carris LM, Rogers JD (1997) Morphological and molecular characterization of Colletotrichum nymphaeae and C. nupharicola sp. nov. on water-lilies (Nymphaea and Nuphar). Mycol Res 101(6):641–649

    Article  CAS  Google Scholar 

  • Johnston PR, Jones D (1997) Relationships among Colletotrichum isolates from fruit-rots assessed using rDNA sequences. Mycologia :420–430

  • Ko Ko TW, McKenzie EHC, Bahkali AH, To-anun C, Chukeatirote E, Promputtha I, Abd-Elsalam KA, Soytong K, Wulandari NF, Sanoamuang N (2011a) The need for re-inventory of Thai phytopathogens. Chiang Mai Journal of Science 38:625–638

    Google Scholar 

  • Ko Ko TW, Stephenson SL, Bahkali AH, Hyde KD (2011b) From morphology to molecular biology: can we use sequence data to identify fungal endophytes? Fungal Diversity 50(1):113–120

    Article  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947–2948

    Article  PubMed  CAS  Google Scholar 

  • Lima WG, Spósito MB, Amorim L, Gonçalves FP, de Filho PAM (2011) Colletotrichum gloeosporioides, a new causal agent of citrus post-bloom fruit drop. Eur J Plant Pathol 131(1):157–165

    Article  Google Scholar 

  • Liu F, Hyde KD, Cai L (2011) Neotypification of Colletotrichum coccodes, the causal agent of potato black dot disease and tomato anthracnose. Mycology 2(4):248–254

    Google Scholar 

  • MacKenzie SJ, Peres NA, Barquero MP, Arauz LF, Timmer LW (2009) Host range and genetic relatedness of Colletotrichum acutatum isolates from fruit crops and leatherleaf fern in Florida. Phytopathology 99(5):620–631

    Article  PubMed  CAS  Google Scholar 

  • Marcelino J, Giordano R, Gouli S, Gouli V, Parker BL, Skinner M, TeBeest D, Cesnik R (2008) Colletotrichum acutatum var. fioriniae (teleomorph: Glomerella acutata var. fioriniae var. nov.) infection of a scale insect. Mycologia 100(3):353–374

    Article  PubMed  CAS  Google Scholar 

  • McGovern RJ, Seijo TE, Hendricks K, Roberts PD (2012) New report of Colletotrichum gloeosporioides causing postbloom fruit drop on citrus in Bermuda. Canadian Journal of Plant Pathology 34(2):187–194

    Article  Google Scholar 

  • Moriwaki J, Sato T, Tsukiboshi T (2003) Morphological and molecular characterization of Colletotrichum boninense sp. nov. from Japan. Mycoscience 44(1):47–53

    Article  CAS  Google Scholar 

  • Noireung P, Phoulivong S, Liu F, Cai L, Mckenzie EH, Chukeatirote E, Jones E, Bahkali AH, Hyde KD (2012) Novel species of Colletotrichum revealed by morphology and molecular analysis. Cryptogam Mycol 33(3):347–362

    Article  Google Scholar 

  • O’Donnell K, Nirenberg HI, Aoki T, Cigelnik E (2000) A multigene phylogeny of the Gibberella fujikuroi species complex: Detection of additional phylogenetically distinct species. Mycoscience 41(1):61–78

    Google Scholar 

  • Pai HS (1970) Life cycle of Colletotrichum heveae inciting spot anthracnose of phyllanthus acidus. Mycopathologia 42(1):65–72

    Google Scholar 

  • Peng LJ, Sun T, Yang YL, Cai L, Hyde KD, Bahkali AH, Liu ZY (2013) Colletotrichum species on grape in Guizhou and Yunnan provinces, China. Mycoscience 54(1):29–41

    Article  Google Scholar 

  • Peng LJ, Yang YL, Hyde KD, Bahkali AH, Liu ZY (2012) Colletotrichum species on Citrus leaves in Guizhou and Yunnan provinces, China. Cryptogam Mycol 33(3):267–283

    Article  Google Scholar 

  • Peres N, MacKenzie S, Peever T, Timmer L (2008) Postbloom fruit drop of citrus and key lime anthracnose are caused by distinct phylogenetic lineages of Colletotrichum acutatum. Phytopathology 98(3):345–352

    Article  PubMed  CAS  Google Scholar 

  • Phoulivong S (2011) Colletotrichum, naming, control, resistance, biocontrol of weeds and current challenges. Current Research in Environmental Applied Mycology 1(1):53–73

    Google Scholar 

  • Phoulivong S, Cai L, Chen H, McKenzie EHC, Abdelsalam K, Chukeatirote E, Hyde KD (2010a) Colletotrichum gloeosporioides is not a common pathogen on tropical fruits. Fungal Diversity 44(1):33–43

    Article  Google Scholar 

  • Phoulivong S, Cai L, Parinn N, Chen H, Abd-Elsalam KA, Chukeatirote E, Hyde KD (2010b) A new species of Colletotrichum from Cordyline fruticosa and Eugenia javanica causing anthracnose disease. Mycotaxon 114(1):247–257

    Article  Google Scholar 

  • Prihastuti H, Cai L, Chen H, McKenzie EHC, Hyde KD (2009) Characterization of Colletotrichum species associated with coffee berries in northern Thailand. Fungal Diversity 39:89–109

    Google Scholar 

  • Prihastuti H, Cai L, Crouch JA, Phoulivong S, Moslem MA, McKenzie EHC, Hyde KD (2010) Neotypification of Colletotrichum falcatum, the causative agent of red-rot disease in sugarcane. Sydowia 62:283–293

    Google Scholar 

  • Rambaut A, Drummond A (2010) FigTree v1. 3.1. Institute of evolutionary biology, University of Edinburgh

  • Rojas EI, Rehner SA, Samuels GJ, Van Bael SA, Herre EA, Cannon P, Chen R, Pang J, Wang R, Zhang Y (2010) Colletotrichum gloeosporioides sl associated with Theobroma cacao and other plants in Panamá: multilocus phylogenies distinguish host-associated pathogens from asymptomatic endophytes. Mycologia 102(6):1318–1338

  • Shivas R, Yu Y (2009) A taxonomic re-assessment of Colletotrichum acutatum, introducing C. fioriniae comb. et stat. nov. and C. simmondsii sp. nov. Fungal Diversity 39:111

    Google Scholar 

  • Stephenson SA, Green JR, Manners JM, Maclean DJ (1997) Cloning and characterisation of glutamine synthetase from Colletotrichum gloeosporioides and demonstration of elevated expression during pathogenesis on Stylosanthes guianensis. Current Genetics 31(5):447–454

    Google Scholar 

  • Su YY, Noireung P, Liu F, Hyde KD, Moslem MA, Bahkali AH, Abd-Elsalam KA, Cai L (2011) Epitypification of Colletotrichum musae, the causative agent of banana anthracnose. Mycoscience :1–7

  • Sutton BC (1980) The Coelomycetes, Fungi Imperfecti with acervuli, pycnidia and stromata. Commonwealth Mycological Institute, Kew

    Google Scholar 

  • Sutton BC (1992) The genus Glomerella and its anamorph Colletotrichum. In: Bailey JA, Jeger MJ (eds) Colletotrichum: Biology, pathology and control. CAB international, Wallingford, pp 1–26

    Google Scholar 

  • Swofford DL (2003) PAUP*: Phylogenetic analysis using parsimony, version 4.0 b10

  • Templeton MD, Rikkerink EH, Solon SL, Crowhurst RN (1992) Cloning and molecular characterization of the glyceraldehyde-3-phosphate dehydrogenase-encoding gene and cDNA from the plant pathogenic fungus Glomerella cingulata. Gene 122(1):225–230

    Google Scholar 

  • Timmer LW, Agostini JP, Zitko S, Zulfiqar M (1994) Postbloom fruit drop, an increasingly prevalent disease of citrus in the Americas. Plant Dis 78(4):329–334

    Article  Google Scholar 

  • Timmer LW, Garnsey SM, Graham JH (2000) Compendium of Citrus Diseases(secong edition). The American Phytopathological Society 28–29:44–45

    Google Scholar 

  • Van der Aa HA (1978) A leaf spot disease of Nymphaea alba in the Netherlands. Eur J Plant Pathol 84(3):109–115

    Google Scholar 

  • Wang XH, Chen GQ, Huang F, Zhang JZ, Hyde KD, Li HY (2012) Phyllosticta species associated with citrus diseases in China. Fungal Diversity 52(1):209–224

    Article  Google Scholar 

  • Weir BS, Johnston PR, Damm U (2012) The Colletotrichum gloeosporioides species complex. Stud Mycol 73:115–180

    Article  PubMed  CAS  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR protocols A guide to methods and applications 315–322

  • Wikee S, Cai L, Pairin N, McKenzie EHC, Su YY, Chukeatirote E, Thi HN, Bahkali AH, Moslem MA, Abdelsalam K, Hyde KD (2011) Colletotrichum species from Jasmine (Jasminum sambac). Fungal Diversity 46(1):171–182

    Article  Google Scholar 

  • Yang YL, Cai L, Yu ZN, Liu ZY, Hyde K (2011) Colletotrichum species on Orchidaceae in southwest China. Cryptogam Mycol 32(3):229–253

    Article  Google Scholar 

  • Yang YL, Liu ZY, Cai L, Hyde KD, Yu ZN, McKenzie EHC (2009) Colletotrichum anthracnose of Amaryllidaceae. Fungal Diversity 39:123–146

    Google Scholar 

Download references

Acknowledgment

This work was supported by the China Agriculture Research System (CARS-27). L. Cai acknowledges grants KSCX2-YW-Z-1026 ⁄ NSFC31070020. Fang Liu is thanked for technical advices in the phylogenetic analyses. K.D. Hyde thanks the National Research Council of Thailand, Colletotrichum grant number 54201020003 for financial support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to H. Y. Li.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 67.3 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Huang, F., Chen, G.Q., Hou, X. et al. Colletotrichum species associated with cultivated citrus in China. Fungal Diversity 61, 61–74 (2013). https://doi.org/10.1007/s13225-013-0232-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13225-013-0232-y

Keywords

Navigation