How well do ITS rDNA sequences differentiate species of true morels (Morchella)?

Mycologia

Volumn 104, Issue 6, 2012, Pages 1351-1368

  Du, Xi Hui ^a,b   Zhao, Qi ^a,b   Yang, Zhu L ^a,b   Hansen, Karen ^c   Taşkin, Hatira ^d   Büyükalaca, Saadet ^d   Dewsbury, Damon ^e   Moncalvo, Jean Marc ^e   Douhan, Greg W ^f   Robert, Vincent A R G ^g   Crous, Pedro W ^g   Rehner, Stephen A ^h   Rooney, Alejandro P ⁱ   Sink, Stacy ⁱ   O'Donnell, Kerry ⁱ  

^a KUNMING INSTITUTE OF BOTANY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c SWEDISH MUSEUM OF NATURAL HISTORY   (Sweden)

^d CUKUROVA UNIVERSITY   (Turkey)

^e UNIVERSITY OF TORONTO   (Canada)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g CBS KNAW FUNGAL BIODIVERSITY CENTRE   (Netherlands)

^h AGRICULTURAL RESEARCH SERVICE   (United States)

ⁱ NATIONAL CENTER FOR AGRICULTURAL UTILIZATION RESEARCH   (United States)

Author keywords

Ascomycota; Biodiversity; Biogeography; Emerencia; GCPSR; Genbank; Phylogeny; Species limits

Indexed keywords

FUNGAL DNA; RIBOSOMAL SPACER DNA;

BIOGEOGRAPHY; COMMERCIAL SPECIES; DATABASE; EXPLOITATION; FRUITING; GENETIC ANALYSIS; IDENTIFICATION METHOD; MANAGEMENT PRACTICE; MUSHROOM; PHYLOGENY; SPECIES CONSERVATION; SPECIES DIVERSITY; TAXONOMY;

ARTICLE; ASCOMYCETES; BIODIVERSITY; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGICAL EXAMINATION; MOLECULAR GENETICS; NUCLEIC ACID DATABASE; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYLOGEOGRAPHY;

ASCOMYCOTA; BASE SEQUENCE; BIODIVERSITY; DATABASES, NUCLEIC ACID; DNA, FUNGAL; DNA, RIBOSOMAL SPACER; MOLECULAR SEQUENCE DATA; MYCOLOGICAL TYPING TECHNIQUES; PHYLOGENY; PHYLOGEOGRAPHY; SEQUENCE ANALYSIS, DNA;

ASCOMYCOTA; FUNGI; MORCHELLA; MORCHELLA ESCULENTA;

EID: 84871728295     PISSN: 00275514     EISSN: 15572536     Source Type: Journal    
DOI: 10.3852/12-056     Document Type: Article

References (73)

1. Abeyrathne PD, Nazar RN. 2005. Parallels in rRNA processing: conserved features in the processing of the internal transcribed spacer I in the pre-rRNA from Schizosaccharomyces pombe. Biochemistry 44:16977- 16987
2. Agerer R, Ammirati J, Blanz P, Courtecuisse R, Desjardin DE, Gams W, Hallenberg N, Halling R, Hawksworth DL, Horak E, Korf RP, Mueller GM, Oberwinkler F, Rambold G, Summerbell RC, Triebel D, Watling R. 2000. Always deposit vouchers. Mycol Res 104:642-644.
3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol 215: 403-410.
4. Baynes M, Newcombe G, Dixon L, Castlebury L, O'Donnell K. 2012. A novel plant-fungal mutualism associated with fire. Fungal Biol 116:113-144
5. Bidartondo MI, Bruns TD, Blackwell M. 2008. Preserving accuracy in GenBank. Science 319:1616
6. Bonito GM, Gryganskyi AP, Trappe JM, Vilgalys R. 2010. A global meta-analysis of Tuber ITS rDNA sequences: species diversity, host association and long-distance dispersal. Mol Ecol 19:4994-5008
7. Bridge PD, Roberts PJ, Spooner BM, Panchal G. 2003. On the unreliability of published DNA sequences. New Phytol 160:43-48
8. 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: 648-656
9. Dahlstrom JL, Smith JE, Weber NS. 2000. Mycorrhiza-like interaction by Morchella with species of the Pinaceae in pure culture synthesis. Mycorrhiza 9:279-285
10. Degreef J, Fischer E, Sharp C, Raspé O. 2009. African Morchella crassipes (Ascomycota, Pezizales) revealed by analysis of nrDNA ITS. Nova Hedwigia 88:11-22
11. Dettman JR, Jacobson DJ, Taylor JW. 2003. A multilocus genealogical approach to phylogenetic species recognition in the model eukaryote Neurospora. Evolution 57:2703-2720.
12. Du X-H, Zhao Q, O'Donnell K, Rooney AP, Yang ZL. 2012. Multigene molecular phylogenetics reveals true morels (Morchella) are especially species-rich in China. Fungal Genet Biol 49:455-469
13. Edgar RC. 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinform 5:1-19
14. Feibelman T, Bayman P, Cibula WG. 1994. Length variation in the internal transcribed spacer of ribosomal DNA in chanterelles. Mycol Res 98:614-618
15. Gardes M, Bruns TD. 1993. ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol 2:113-118
16. Geiser DM, Jiménez-Gasco MdM, Kang S, Makalowska I, Veeraraghavan N, Ward TJ, Zhang N, Kuldau GA, O'Donnell K. 2004.FUSARIUM-IDv. 1.0:ADNA sequence database for identifying Fusarium. Eur J Plant Pathol 110: 473-479
17. Gower JC. 1971. A general coefficient of similarity and some of its properties. Biometrics 27:857-874
18. Hansen K, Laessøe T, Pfister DH. 2002. Phylogenetic diversity in the core group of Peziza inferred from ITS sequences and morphology. Mycol Res 106:879- 902
19. Hansen K, Pfister DH. 2006. Systematics of the Pezizomycetes- the operculate discomycetes. Mycologia 98: 1029-1040
20. Hausner G, Wang X. 2005. Unusual compact rDNA gene arrangements within some members of the Ascomycota: evidence for molecular co-evolution between ITS1 and ITS2. Genome 48:648-660
21. Hawksworth DL. 2004. Fungal diversity and its implications for genetic resource collections. Stud Mycol 50:9-18.
22. Horton TR, Bruns TD. 2001. The molecular revolution in ectomycorrhizal ecology: peeking into the black box. Mol Ecol 10:1855-1871
23. Jacquetant E. 1984. Les Morilles. Paris: La Bibliothe'que des Arts. p 7-114.
24. Jacquetant E., Bon M. 1984. Typifications et mises au point nomenclaturales dans l'ouvrage "Les Morilles"(de E. Jacquetant), Nature-Piantanida 1984. Doc Mycol 14:1.
25. James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J, Lumbsch HT, Rauhut A, Reeb V, Arnold AE, Amtoft A, Stajich JE, Hosaka K, Sung GH, Johnson D, O'Rourke B, Crockett M, Binder M, Curtis JM, Slot JC, Wang Z, Wilson AW, Schussler A, Longcore JE, O'Donnell K, Mozley-Standridge S, Porter D, Letcher PM, Powell MJ, Taylor JW, White MM, Griffith GW, Davies DR, Humber RA, Morton JB, Sugiyama J, Rossman AY, Rogers JD, Pfister DH, Hewitt D, Hansen K, Hambleton S, Shoemaker RA, Kohlmeyer J, Volkmann-Kohlmeyer B, Spotts RA, Serdani M, Crous PW, Hughes KW, Matsuura K, Langer E, Langer G, Untereiner WA, Lü cking R, Budel B, Geiser DM, Aptroot A, Diederich P, Schmitt I, Schultz M, Yahr R, Hibbett DS, Lutzoni F, McLaughlin DJ, Spatafora JW, Vilgalys R. 2006. Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443:818-822
26. Kang S, Mansfield MA, Park B, Geiser DM, Ivors KL, Coffey MD, Grünwald NJ, Martin FN, Lévesque CA, Blair JE. 2010. The promise and pitfalls of sequence-based identification of plant-pathogenic fungi and oomycetes. Phytopathology 100:732-737
27. Kanwal HK, Acharya K, Ramesh G, Reddy MS. 2011. Molecular characterization of Morchella species from the western Himalayan region of India. Curr Microbiol 62:1245-1252
28. Katoh K, Toh H. 2008. Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9:286-298
29. Kellner H, Renker C, Buscot F. 2005. Species diversity within the Morchella esculenta group (Ascomycota: Morchellaceae) in Germany and France. Org Diver Evol 5:101-107
30. Kraus F, Miyamoto MM. 1991. Cladogenesis among the pecoran ruminants: evidence from mitochondrial DNA sequences. Syst Zool 40:117-130
31. Kuo M, Dewsbury DR, O'Donnell K, Carter MC, Rehner SA, Moore JD, Moncalvo J-M, Canfield SA, Methven AS, Volk TJ. 2012. A taxonomic revision of true morels (Morchella) in Canada and the United States. Mycologia 104:1159-1177
32. Lindner DL, Banik MT. 2011. Intragenomic variation in the ITS rDNA region obscures phylogenetic relationships and inflates estimates of operational taxonomic units in genus Laetiporus. Mycologia 103:731-740
33. Lopez-Giraldez F, Wang Z, Townsend JP. 2011. Assessing phylogenetic information content in fungal genomes with PhyDesign, a Web application for smart marker selection. Inoculum 62:30.
34. Masaphy S, Zabari L, Goldberg D, Jander-Shgag G. 2010. The complexity of Morchella systematics: a case of the yellow morel in Israel. Fungi 3:14-18.
35. Matheny PB. 2005. Improving phylogenetic inference of mushrooms with RPB1 and RPB2 nucleotide sequences (Inocybe; Agaricales). Mol Phylogenet Evol 35:1-20
36. Nei M. 1996. Phylogenetic analysis in molecular evolutionary genetics. Annu Rev Genet 30:371-403
37. Nilsson RH, Kristiansson E, Ryberg M, Hallenberg N. 2008. Intraspecific ITS variability in the kingdom Fungi as expressed in the international sequence databases and its implications for molecular species identification. Evol Bioinform 4:193-201.
38. Nilsson RH, Kristiansson E, Ryberg M, Abarenkov K, Larsson K-H, Köljalg U. 2006. Taxonomic reliability of DNA sequences in public sequence databases: a fungal perspective. PLoS One 1, e59
39. Nilsson RH, Kristiansson E, Ryberg M, Larsson K-H. 2005. Approaching the taxonomic affiliation of unidentified sequences in public databases-an example from the mycorrhizal fungi. BMC Bioinform 6:178
40. O'Donnell K. 2000. Molecular phylogeny of the Nectria haematococca-Fusarium solani species complex. Mycologia 92:919-938
41. O'Donnell K., Cigelnik E. 1997. Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Mol Phylogeneti Evol 7:103-116
42. O'Donnell K., Cigelnik E., Weber NS, Trappe JM. 1997. Phylogenetic relationships among ascomycetous truffles and the true and false morels inferred from 18S and 28S ribosomal DNA sequence analysis. Mycologia 89:48-65
43. O'Donnell K., Rooney AP, Mills GL, Kuo M, Weber NS, Rehner SA. 2011. Phylogeny and historical biogeography of true morels (Morchella) reveals an early Cretaceous origin and high continental endemism and provincialism in the Holarctic. Fungal Genet Biol 48:252-265
44. O'Donnell K., Sutton DA, Fothergill A, McCarthy D, Rinaldi MG, Brandt ME, Zhang N, Geiser DM. 2008. Molecular phylogenetic diversity, multilocus haplotype nomenclature and in vitro antifungal resistance within the Fusarium solani species complex. J Clin Microbiol 46: 2477-2490
45. O'Donnell K., Weber NS, Hains JH, Mills GL. 1993. Molecular systematics and phylogenetics of the Morchellaceae. Inoculum 44:52.
46. Ower R, Mills GL, Malachowski JA. 1986. Cultivation of Morchella. US patent 4594809.
47. Pagliaccia D, Douhan GW, Douhan L, Peever TL, Carris LM, Kerrigan JL. 2011. Development of molecular markers and preliminary investigation of the population structure and mating system in one lineage of black morel (Morchella elata) in the Pacific Northwestern USA. Mycologia 103:969-982
48. Peay KG, Kennedy PG, Bruns TD. 2008. Fungal community ecology: a hybrid beast with a molecular master. BioScience 58:799-810
49. Pilz D, McLain R, Alexander S, Villarreal-Ruiz L, Berch S, Wurtz TL, Parks CG, McFarlane E, Baker B, Molina R, Smith JE. 2007. Ecology and Management of Morels Harvested from the Forests of Western North America. Corvallis, OR: PNW-GTR-710. USDA Forest Service.
50. Reeb V, Lutzoni F, Roux C. 2004. Contribution of RPB2 to multilocus phylogenetic studies of the euascomycetes (Pezizomycotina, Fungi) with species emphasis on the lichen-forming Acarosporaceae and evolution of polyspory. Mol Phylogenet Evol 32:1036-1060
51. Robert V, Szoke S, Jabas J, Vu D, Chouchen O, Blom E, Cardinali G. 2011. BioloMICS software, biological data management, identification, classification and statistics. Open Appl Informatics J 5:87-98
52. Roe AD, Rice AV, Bromilow SE, Cooke JEK, Sperling FAH. 2010. Multilocus species identification and fungal DNA barcoding: insights from blue stain fungal symbionts of the mountain pine beetle. Mol Ecol Res 10:946-959
53. Ryberg M, Nilsson RH, Kristiansson E, Töpel M, Jacobsson S, Larsson E. 2008. Mining metadata from unidentified ITS sequences in GenBank: a case study in Inocybe (Basidiomycota). BMC Evol Biol
54. Saitou N, Kristiansson E, Sjökvist E, Nilsson RH. 2009. An outlook on the fungal internal transcribed spacer sequences in GenBank and the introduction of a Web-based tool for the exploration of fungal diversity. New Phytol 181: 471-477
55. Saitou N, Nei N. 1987. The neighbor joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 14:406-425.
56. Simon UK, Weiß M. 2008. Intragenomic variation of fungal ribosomal genes is higher than previously thought. Mol Biol Evol 25:2251-2254
57. Stark C, Babik W, DurkaW. 2009. Fungi from the roots of the common terrestrial orchid Gymnadenia conopsea. Mycol Res 113:952-959
58. Stefani FOP, Sokolski S, Wurtz TL, Piché Y, Hamelin RC, Fortin JA, Bérubé JA. 2010. Morchella tomentosa: a unique belowground structure and a new clade of morels. Mycologia 102:1082-1088
59. Swofford DL. 2002. PAUP* 4.0b10: phylogenetic analysis using parsimony (*and other methods). Sunderland, Massachusetts: Sinauer Associates.
60. Taşkin H, Büyükalaca S, Dogan HH, Rehner SA, O'Donnell K. 2010. A multigene molecular phylogenetic assessment of true morels (Morchella) in Turkey. Fungal Genet Biol 47:672-682
61. Taşkin H, Büyükalaca S, Hansen K, O'Donnell K. 2012. Multilocus phylogenetic analysis of true morels (Morchella) reveals high levels of endemics in Turkey relative to other regions of Europe. Mycologia 104, 446-461.
62. Taylor DL, BoothMG,McFarland JW,Herriott IC, Lennon NJ, Nusbaum C, Marr TG. 2008. Increasing ecological inference from high throughput sequencing of fungi in the environment through a tagging approach. Mol Ecol Resour 8:742-752
63. Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser DM, Hibbett DS, Fischer MC. 2000. Phylogenetic species recognition and species concepts in fungi. Fungal Genet Biol 31:21-32
64. Hibbett DS, Turner E, Townsend JP, Dettman JR, Jacobson D. 2006. Eukaryotic microbes, species recognition and the geographic limits of species: examples from the kingdom Fungi. Phil Trans R Soc B 361:1947-1963
65. Thompson JD, Higgins DG, Gibson TJ. 1994. Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weightmatrix choice. Nucleic Acids Res 22:4673-4680
66. Trappe MJ, Trappe JM, Bonito GM. 2010. Kalapuya brunnea gen. and sp. nov. and its relationship to the other sequestrate genera in Morchellaceae. Mycologia 102: 1058-1065
67. van Nues RW, Rientjes JMJ, Morré SA, Mollee E, Planta RJ, Venema J, Raué HA. 1995. Evolutionary conserved structural elements are critical for processing on internal transcribed spacer 2 from Saccharomyces cerevisiae precursor ribosomal RNA. J Mol Biol 250: 24-26
68. Vellinga EC, Wolfe BE, Pringle A. 2009. Global patterns of ectomycorrhizal introductions. New Phytol 181:960- 973
69. Vilgalys R. 2003. Taxonomic misidentification in public DNA databases. New Phytol 160:4-5
70. White TJ, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand HH, Sninsky JJ, White TJ, eds. PCR protocols: a guide to methods and applications. San Diego: Academic Press. p 315- 322.
71. Will KW, Mishler BD, Wheller QD. 2005. The perils of DNA barcoding and the need for integrative taxonomy. Syst Biol 56:844-851
72. Zhang N, O'Donnell K, Sutton DA, Nalim FA, Summerbell RC, Padhye AA, Geiser DA. 2006. Members of the Fusarium solani species complex that cause infections in both humans and plants are common in the environment. J Clin Microbiol 44:2186-2190
73. Zhao Q, Xu ZZ, Cheng YH, Qi SW, Hou ZJ. 2009. Artificial cultivation of Morchella conica. Southwest China J Agric Sci 22:1690-1693 (in Chinese).