Advertisement

Fungal Diversity

, Volume 61, Issue 1, pp 117–138 | Cite as

The ApMat marker can resolve Colletotrichum species: a case study with Mangifera indica

  • Gunjan Sharma
  • Navinder Kumar
  • Bevan S. Weir
  • Kevin D. Hyde
  • Belle Damodara Shenoy
Article

Abstract

Anthracnose disease caused by the Colletotrichum gloeosporioides species complex is a major problem worldwide. In this study, we investigated the phylogenetic diversity of 207 Indian Colletotrichum isolates, associated with symptomatic and asymptomatic tissues of mango, belonging to this species complex. Phylogenetic analyses were performed based on a 6-gene dataset (act, cal, chs1, gapdh, ITS and tub2), followed by ApMat sequence-analysis. The ApMat-based phylogeny was found to be superior as it provided finer resolution in most of the species-level clades. Importantly, the ApMat marker identified seven lineages within C. siamense sensu lato, including C. jasmini-sambac, C. hymenocallidis, C. melanocaulon, C. siamense sensu stricto and three undesignated, potentially novel lineages. In this study, C. fragariae sensu stricto, C. fructicola, C. jasmini-sambac, C. melanocaulon and five undesignated, potentially novel lineages were found to be associated with mango tissues. There is a need to develop a consensus among mycologists as to which genes should be used to define and delimit a Colletotrichum species and in the mean time mycologists should voluntarily restrain from describing new species based on inadequate datasets.

Keywords

Anthracnose Identification Phylogeny Polyphasic taxonomy Secondary barcode Systematics 

Notes

Acknowledgments

We thank Institute of Microbial Technology (CSIR-IMTECH) for the financial support. We thank Dr. Eric McKenzie from International Collection of Microorganisms from Plants, New Zealand and Dr. Makoto Kawase from National Institute Agrobiological Sciences Japan for providing some Colletotrichum type strains as gifts. Dr. D. Ananthapadmanaban, Deepak Bhatt, Amandeep Kaur, Deepinder Kaur and Yamini Agrawal from CSIR-IMTECH are thanked for their encouragement. Drs. Lei Cai and Roger Shivas are thanked for the inspiration and useful discussions on Colletotrichum taxonomy. We also thank Dr. Rakesh Pandey and Mr. Ashwin Nannaware (CSIR-NBRI, Lucknow, Uttar Pradesh), Mr. Pradip Kumar Singh (Banaras, Uttar Pradesh), Mr. Chittarjeet Singh (CSIR-CSIO, Chandigarh), Mr. Jignesh Patel (Gujrat), Mr. Srinivas Kamath (Maharashtra), Dr. S. Siddharthan (Chennai, Tamil Nadu), Ms. Sonika Verma (Patna, Bihar); Mr. Arun Prabhu and Pai (Goa) for their help in sample collections from the respective states. We acknowledge the help of Dr. V. Shanmugham, CSIR-IHBT, Palampur, India in performing the pathogenicity testing. Gavin Blyth, Landcare Research, New Zealand provided some sequences. This work was supported by CSIR-IMTECH-OLP0071 project and CSIR-SRF fellowship awarded to GS and UGC-SRF fellowship to NK. K.D. Hyde thanks the National Research Council of Thailand for the award of grant No. 54201020003 and a grant from the National Plan of Science and Technology, King Abdulaziz City of Science and Technology, Riyadh, Saudi Arabia, project No. 10-Bio-965-02 to study Colletotrichum.

Supplementary material

13225_2013_247_MOESM1_ESM.doc (436 kb)
Supplementary Table 1 List of Colletotrichum isolates associated with Mangifera indica included in this study with information on taxon, substrate, variety, geographic location, collector’s name and GenBank accession number for the 5 ′tef 1 gene sequenced (DOC 436 kb)
13225_2013_247_MOESM2_ESM.doc (54 kb)
Supplementary Table 2 List of the Colletotrichum type strains included in this study with information on taxon, host, geographic location and GenBank accession number for the 5′tef1 gene sequence (GenBank accession numbers highlighted in bold have been generated in this study, * = Type strain) (DOC 54 kb)

References

  1. Bailey JA, Jeger MJ (eds) (1992) Colletotrichum: Biology, pathology and control. CAB Int, WallingfordGoogle Scholar
  2. Cai L, Hyde KD, Taylor PWJ, Weir BS, Waller J, Abang MM, Zhang JZ, Yang YL, Phoulivong S, Liu ZY, Prihastuti H, Shivas RG, McKenzie EHC, Johnston PR (2009) A polyphasic approach for studying Colletotrichum. Fungal Divers 39:183–204Google Scholar
  3. Cai L, Giraud T, Zhang N, Begerow D, Cai G, Shivas RG (2011) The evolution of species concepts and species recognition criteria in plant pathogenic fungi. Fungal Divers 50:121–133CrossRefGoogle Scholar
  4. Cannon PF, Buddie AG, Bridge PD (2008) The typification of Colletotrichum gloeosporioides. Mycotaxon 104:189–204Google Scholar
  5. Cannon PF, Damm U, Johnston PR, Weir BS (2012) Colletotrichum – current status and future directions. Stud Mycol 73:181–213PubMedCrossRefGoogle Scholar
  6. Chadha KL (2009) Handbook of Horticulture. Directorate of Information and Publication of Agriculture. ICAR, Krishi Anusandhan Bhavan (PUSA), New Delhi. pp 239–245Google Scholar
  7. Crouch JA, Clarke BB, Hillman BI (2009) What is the value of ITS sequence data in Colletotrichum systematics and species diagnosis? A case study using the falcate-spored graminicolous Colletotrichum group. Mycologia 101:648–656PubMedCrossRefGoogle Scholar
  8. Damm U, Wouldenberg JHC, Cannon PF, Crous PW (2009) Colletotrichum species with curved conidia from herbaceous hosts. Fungal Divers 39:45–87Google Scholar
  9. Damm U, Baroncelli R, Cai L, Kubo Y, O’Connell R, Weir B, Yoshino K, Cannon PF (2010) Colletotrichum: species, ecology and interactions. IMA Fungus 1:161–165PubMedCrossRefGoogle Scholar
  10. DCGIS Annual Report (2012) Agriculture and Processed food products Export Development Authority (APEDA), Ministry of Commerce and Industry, Government of India, information accessed online on 23rd April, 2013 from http://agriexchange.apeda.gov.in/product_profile/exp_f_india.aspx?categorycode=0204
  11. Doyle VP, Oudemans PV, Rehner SA, Litt A (2013) Habitat and host indicate lineage identity in Colletotrichum gloeosporioides s. l. from wild and agricultural landscapes in North America. PLoS One 8:e62394PubMedCrossRefGoogle Scholar
  12. Farr DF, Rossman AY (2013) Fungal Databases, Systematic Mycology and Microbiology Laboratory, ARS, USDA. Retrieved April 4, 2013, from http://nt.ars-grin.gov/fungaldatabases/
  13. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evol 39:783–791CrossRefGoogle Scholar
  14. Ferrier P, Petersen E, Landes M (2012) Specialty crop access to US markets: A case study of Indian mangoes. US Department of Agriculture, Economic Research ServiceGoogle Scholar
  15. Freeman S, Katan T, Shabi E (1998) Characterization of Colletotrichum species responsible for anthracnose diseases of various fruits. Plant Dis 82:596–605CrossRefGoogle Scholar
  16. Gräfenhan T, Schroers HJ, Nirenberg HI, Seifert KA (2011) An overview of the taxonomy, phylogeny and typification of nectriaceous fungi in Cosmospora, Acremonium, Fusarium, Stilbella and Volutella. Stud Mycol 68:79–113PubMedCrossRefGoogle Scholar
  17. Gupta VK, Pandey A, Kumar P, Pandey BK, Gaur RK, Bajpai V, Sharma N, Sharma S (2010) Genetic characterization of mango anthracnose pathogen Colletotrichum gloeosporioides Penz. by random amplified polymorphic DNA analysis. Afr J Biotechnol 9:4009–4013Google Scholar
  18. Hibbett DS, Taylor JW (2013) Fungal systematics: is a new age of enlightenment at hand? Nat Rev Microbiol 11:129–133PubMedCrossRefGoogle Scholar
  19. Hunter GC, Crous PW, Carnegie AJ, Burgess TI, Wingfield MJ (2011) Mycosphaerella and Teratosphaeria diseases of Eucalyptus; easily confused and with serious consequences. Fungal Divers 50:145–166CrossRefGoogle Scholar
  20. Hyde KD, Cai L, McKenzie EHC, Yang YL, Zhang JZ, Prihastuti H (2009a) Colletotrichum: a catalogue of confusion. Fungal Divers 39:1–17Google Scholar
  21. Hyde KD, Cai L, Cannon PF, Crouch JA, Crous PW, Damm U, Goodwin PH, Chen H, Johnston PR, Jones EBG, Liu ZY, McKenzie EHC, Moriwaki J, Noireung P, Pennycook SR, Pfenning LH, Prihastuti H, Sato T, Shivas RG, Tan YP, Taylor PWJ, Weir BS, Yang YL, Zhang JZ (2009b) Colletotrichum – names in current use. Fungal Divers 39:147–182Google Scholar
  22. Kishino H, Hasewaga M (1989) Evaluation of maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order of Hominoidea. J Mol Evol 29:170–179PubMedCrossRefGoogle Scholar
  23. Ko Ko TW, McKenzie EHC, Bahkali AH et al (2011) The need for re-inventory of Thai phytopathogens. Chiang Mai J Sci 38:625–638Google Scholar
  24. Kumar AS, Reddy NPE, Reddy KH, Devi MC (2007) Evaluation of fungicidal resistance among Colletotrichum gloeosporioides isolates causing mango anthracnose in Agri Export Zone of Andhra Pradesh, India. Plant Pathol Bull 16:157–160Google Scholar
  25. Kumar B, Mistry NC, Singh B, Gandhi CP (2011) Indian Horticulture Databse-2011. National Horticulture Board, Ministry of Agriculture, Government of India, New DelhiGoogle Scholar
  26. Laxmi BKM, Reddy PN, Prasad RD (2011) Cross infection potential of Colletotrichum gloeosporioides Penz. isolates causing anthracnose in subtropical fruit crops. Trop Agric Res 22:183–193Google Scholar
  27. Liu JK, Phookamsak R, Doilom M, Wikee S, Li YM, Ariyawansha H, Boonmee S et al (2012) Towards a natural classification of Botryosphaeriales. Fungal Divers 57:149–210CrossRefGoogle Scholar
  28. Page RDM (1996) TREEVIEW: an application of display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358PubMedGoogle Scholar
  29. Pavlic D, Slippers B, Coutinho TA, Wingfield MJ (2009) Multiple gene genealogies and phenotypic data reveal cryptic species of the Botryosphaeriaceae: a case study on the Neofusicoccum parvum/N. ribis complex. Mol Phylogenet Evol 51:259–268PubMedCrossRefGoogle Scholar
  30. Peng LJ, Yang Y, Hyde KD, Bahkali AH, Liu Z (2012) Colletotrichum species on Citrus leaves in Guizhou and Yunnan provinces, China. Cryptogam Mycol 33:267–283Google Scholar
  31. 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 54:29–41CrossRefGoogle Scholar
  32. Penzig AGO (1882) Fungi agrumicoli. Contribuzione allo studio dei funghi parassiti degli agrumi. Michelia 2:385–508Google Scholar
  33. Phoulivong S, Cai L, Chen H, McKenzie EHC, Abdelsalam K, Chukeatirote E, Hyde KD (2010) Colletotrichum gloeosporioides is not a common pathogen on tropical fruits. Fungal Divers 44:33–43CrossRefGoogle Scholar
  34. Prihastuti H, Cai L, Chan H, McKenzie EHC, Hyde KD (2009) Characterization of Colletotrichum species associated with coffee berries in northern Thailand. Fungal Divers 39:89–109Google Scholar
  35. Rojas EI, Rehner SA, Samuels GJ (2010) Colletotrichum gloeosporioides s. l. associated with Theobroma cacao and other plants in Panama: multilocus phylogenies distinguish host-associated pathogens from asymptomatic endophytes. Mycologia 102:1318–1338PubMedCrossRefGoogle Scholar
  36. Saitou N, Nei M (1987) The neighbor joining method: a new method for re-constructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  37. Sangeetha CG, Rawal RD (2009) Temperature requirements of different isolates of Colletotrichum gloeosporioides isolated from mango. American-Eurasian J Sci Res 4:20–25Google Scholar
  38. Sarkiyayi S, Mohammed M, Yakubu A (2013) Comparative analysis of nutritional and anti nutritional contents of some varieties of mango (Mangifera indica) in Kaduna Metropolis-Nigeria. Res J Appl Sci Eng Technol 5:387–391Google Scholar
  39. Schoch CL, Crous PW, Groenewald JZ, Boehm EWA, Burgess TI, De Gruyter J, De Hoog GS et al (2009) A class-wide phylogenetic assessment of Dothideomycetes. Stud Mycol 64:1–15PubMedCrossRefGoogle Scholar
  40. Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, André Levesque C, Chen W et al (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci (USA) 109:6241–6246CrossRefGoogle Scholar
  41. Silva DN, Talhinas P, Várzea V, Cai L, Paulo OS, Batista D (2012a) Application of the Apn2/MAT locus to improve the systematics of the Colletotrichum gloeosporioides complex: an example from coffee (Coffea spp.) hosts. Mycologia 104:396–409PubMedCrossRefGoogle Scholar
  42. Silva DN, Talhinhas P, Cai L, Manuel L, Gichuru EK, Loureiro A, Várzea V, Paulo OS, Batista D (2012b) Host-jump drives rapid and recent ecological speciation of the emergent fungal pathogen Colletotrichum kahawae. Mol Ecol 21:2655–2670PubMedCrossRefGoogle Scholar
  43. Singh V, Mishra RK, Mathew AJ, Pandey BK (2013) Molecular characterization of mango anthracnose pathogen Colletotrichum gloeosporioides sensu lato. Gene. doi: 10.1016/j.gene.2013.05.010 Google Scholar
  44. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol 57:758–771PubMedCrossRefGoogle Scholar
  45. Summerell BA, Leslie JF (2011) Fifty years of Fusarium : how could nine species have ever been enough? Fungal Divers 50:135–144CrossRefGoogle Scholar
  46. Summerell BA, Leslie JF, Liew ECY, Laurence MH, Bullock S, Petrovic T, Bentley AR, Howard CG, Peterson SA, Walsh JL (2011) Fusarium species associated with plants in Australia. Fungal Divers 46:1–27CrossRefGoogle Scholar
  47. Swamy JS (2012) Anthracnose - a devastating pre and post-harvest disease in mango. Int J Plant Prot 5:429–437Google Scholar
  48. Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, SunderlandGoogle Scholar
  49. Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci (USA) 101:11030–11035CrossRefGoogle Scholar
  50. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCrossRefGoogle Scholar
  51. Udayanga D, Liu XX, McKenzie EHC, Chukeatirote E, Bahkali AH, Hyde KD (2011) The genus Phomopsis: biology, applications, species concepts and names of common phytopathogens. Fungal Divers 50:189–225CrossRefGoogle Scholar
  52. Udayanga D, Liu XX, Crous PW, McKenzie EHC, Chukeatirote E, Hyde KD (2012) A multi-locus phylogenetic evaluation of Diaporthe (Phomopsis). Fungal Divers 56:157–171CrossRefGoogle Scholar
  53. Vaidya G, Lohman DJ, Meier R (2011) SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 27:171–180CrossRefGoogle Scholar
  54. Waller JM (1992) Colletotrichum diseases of perennial and other cash crops. In: Bailey JA, Jeger MJ (eds) Colletotrichum: Biology, pathology and control. CAB International, Wallingford, pp 131–142Google Scholar
  55. Weir BS, Johnston PR, Damm U (2012) The Colletotrichum gloeosporioides species complex. Stud Mycol 73:115–180PubMedCrossRefGoogle Scholar
  56. 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 Divers 46:171–182CrossRefGoogle Scholar
  57. Yang YL, Liu ZY, Cai L, Hyde KD, Yu ZN, McKenzie EHC (2009) Colletotrichum anthracnose of Amaryllidaceae. Fungal Divers 39:123–146Google Scholar

Copyright information

© Mushroom Research Foundation 2013

Authors and Affiliations

  • Gunjan Sharma
    • 1
  • Navinder Kumar
    • 1
  • Bevan S. Weir
    • 2
  • Kevin D. Hyde
    • 3
  • Belle Damodara Shenoy
    • 4
  1. 1.Microbial Type Culture Collection and Gene BankCSIR-Institute of Microbial TechnologyChandigarhIndia
  2. 2.Landcare ResearchAucklandNew Zealand
  3. 3.Institute of Excellence in Fungal Research and School of ScienceMae Fah Luang UniversityChiang RaiThailand
  4. 4.CSIR-National Institute of OceanographyDona PaulaIndia

Personalised recommendations