Diversity and phylogenetic affinities of foliar fungal endophytes in loblolly pine inferred by culturing and environmental PCR

Mycologia

Volumn 99, Issue 2, 2007, Pages 185-206

  Arnold, A Elizabeth ^a,b   Henk, Daniel A ^a   Eells, Rebecca L ^a   Lutzoni, François ^a   Vilgalys, Rytas ^a  

^a DUKE UNIVERSITY   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

Ascomycota; Backbone constraint; Basidiomycota; Diversity; Environmental PCR; Fungal endophytes; ITS; LSUrDNA; Phylogenetic diversity; Symbiosis

Indexed keywords

FUNGAL DNA; RIBOSOMAL SPACER DNA; RIBOSOME DNA;

COMMUNITY COMPOSITION; CONIFEROUS TREE; ENDOPHYTE; FUNGUS; GENOTYPE; PHYLOGENETICS; POLYMERASE CHAIN REACTION; SPECIES DIVERSITY; SPECIES RICHNESS; SYMBIOSIS; TAXONOMY;

ARTICLE; BIODIVERSITY; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; FUNGUS; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; LOBLOLLY PINE; MICROBIOLOGY; PHYLOGENY; PLANT LEAF; POLYMERASE CHAIN REACTION; SYMBIOSIS; UNITED STATES;

BIODIVERSITY; DNA, FUNGAL; DNA, RIBOSOMAL; DNA, RIBOSOMAL SPACER; FUNGI; NORTH CAROLINA; PHYLOGENY; PINUS TAEDA; PLANT LEAVES; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SYMBIOSIS;

NORTH AMERICA; NORTH CAROLINA; UNITED STATES;

ASCOMYCOTA; BASIDIOMYCOTA; FUNGI; LEOTIOMYCETES; PINUS TAEDA; SORDARIOMYCETES;

EID: 34547197374     PISSN: 00275514     EISSN: 15572536     Source Type: Journal    
DOI: 10.3852/mycologia.99.2.185     Document Type: Article

References (79)

1. Alexopoulos CJ, Mims CW, Blackwell M. 1996. Introductory Mycology. New York: Wiley & Sons.
2. Allen TR, Millar T, Berch SM, Berbee ML. 2003. Culturing and direct DNA extraction find different fungi from the same ericoid mycorrhizal roots. New Phytol 160:255-272.
3. Arnold AE. 2002. Neotropical fungal endophytes: diversity and ecology [Doctoral dissertation]. Tucson: University of Arizona. 337 p.
4. _, Maynard Z, Gilbert GS, Coley PD, Kursar TA. 2000. Are tropical fungal endophytes hyperdiverse? Ecol Lett 3:267-274.
5. _, 2001. Fungal endophytes in dicotyledonous neotropical trees: patterns of abundance and diversity. Mycol Res 105:1502-1507.
6. _, Mejía LC, Kyllo D, Rojas E, Maynard Z, Robbins NA, Herre EA. 2003. Fungal endophytes limit pathogen damage in a tropical tree. Proc Nat Acad Sci USA 100:15649-15654.
7. _, Lewis LC. 2005. Ecology and evolution of fungal endophytes, and their role against insects. In: Vega R, Blackwell M, eds. Ecological and Evolutionary Advances in Insect-Fungus Associations. Oxford, UK: Oxford University Press. p 74-96.
8. Berbee ML. 2001. The phylogeny of plant and animal pathogens in the Ascomycota. Physiol Mol Plant Path 59:165-187.
9. Cannone JJ, Subramanian S, Schnare MN, Collett JR, R'Souza LM, Du Y, Feng B, Lin N, Madabusi LV, Müller KM, Pande N, Shang Z, Yu N, Guttell RR. 2002. The Comparative RNA Web (CRW) Site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BioMed Cent Bioinformat 3:15.
10. Carey WA, Kelly WD. 1994. Interaction of ozone exposure and Fusarium subglutinans inoculation on growth and disease development of loblolly pine seedlings. Environ Pollut 84:35-43.
11. Carroll GC. 1986. The biology of endophytism in plants with particular reference to woody perennials. In: Fokkema NJ, van den Huevel J, eds. Microbiology of the Phyllosphere. Cambridge, UK: Cambridge University Press. p 205-222.
12. _. 1995. Forest endophytes - pattern and process. Can J Bot 73:S1316-S1324.
13. _, Carroll FE. 1978. Studies on the incidence of coniferous needle endophytes in the Pacific Northwest. Can J Bot 56:3034-3043.
14. Deckert RJ, Peterson RL. 2000. Distribution of foliar fungal endophytes of Pinus strobus between and within host trees. Can J For Res 30:1436-1442.
15. Dobranic JK, Johnson JA, Alikhan QR. 1995. Isolation of endophytic fungi from eastern larch (Larix laricina) leaves from New Brunswick, Canada. Can J Microbiol 41:194-198.
16. Ewing B, Hillier L, Wendl LC, Green P. 1998. Base-calling of automated sequencer traces using Phred. I. Accuracy assessment. Genome Res 8:186-194.
17. Faith DP. 1992. Conservation evaluation and phylogenetic diversity. Biolog Conserv 61:1-10.
18. Felsenstein J. 1981. A likelihood approach to character weighting and what it tells us about parsimony and compatibility. Biolog J Linnaean Soc 16:183-196.
19. Fröhlich J, Hyde KD. 1999. Biodiversity of palm fungi in the tropics: are global fungal diversity estimates realistic? Biodivers Conser 8:977-1004.
20. Gamboa MA, Bayman P. 2001. Communities of endophytic fungi in leaves of a tropical timber tree (Guarea guidonia: Meliaceae). Biotropica 33:352-360.
21. Gardes M, Bruns TD. 1993. ITS primers with enhanced specificity of basidiomycetes: application to the identification of mycorrhizae and rusts. Mol Ecol 2:113-118.
22. Gilbert GS. 2003. Evolutionary ecology of plant diseases in natural systems. Ann Rev Phytopathol 40:13-43.
23. Guo LD, Hyde KD, Liew ECY. 2000. Identification of endophytic fungi from Livistona chinensis based on morphology and rDNA sequences. New Phytolog 147:617-630.
24. _, 2001. Detection and taxonomic placement of endophytic fungi within frond tissues of Livistona chinensis based on rDNA sequences. Mol Phylogenet Evol 20:1-13.
25. _, Huang GR, Wang Y, He WH, Zheng WH, Hyde KD. 2003. Molecular identification of white morphotype strains of endophytic fungi from Pinus tabulaeformis. Mycol Res 107:680-688.
26. Hamamoto M, Nagahama T, Tamura M. 2002. Systematic study of basidiomycetous yeasts - evaluation of the ITS regions of rDNA to delimit species of the genus Rhodosporidium. FEMS Yeast Res 2:409-413.
27. Hata K, Futai K. 1996. Variation in fungal endophyte populations in needles of the genus Pinus. Can J Bot 74:103-114.
28. Hawksworth DL. 1991. The fungal dimension of biodiversity: magnitude, significance and conservation. Mycol Res 95:641-655.
29. _. 1994. Ascomycete systematics: problems and perspectives in the nineties. New York: Plenum Press.
30. _. 2001. The magnitude of fungal diversity: the 1.5 million species estimate revisited. Mycol Res 105:1422-1432.
31. Humphries CJ, Williams PH, Vane-Wright RI. 1995. Measuring biodiversity value for conservation. Ann Rev Ecol Syst 26:93-111.
32. Jacobs KA, Rehner SA. 1998. Comparison of cultural and morphological characters and ITS sequences in anamorphs of Botryosphaeria and related taxa. Mycologia 90:601-610.
33. Kim SH, Breuil K. 2002. Common nuclear ribosomal internal transcribed spacer sequences occur in the sibling species Ophiostoma piceae and O. quercus. Mycol Res 105:331-337.
34. Kirk PM, Cannon PF, David JC, Stalpers JA. 2001. Dictionary of the Fungi. 9th ed. Wallingford, UK: CABI Publishing.
35. Kriel WM, Swart WJ, Crous PW. 2000. Foliar endophytes and their interactions with host plants, with specific reference to the gymnospermae. Advance Bot Res 33:1-34.
36. Lacap DC, Hyde KD, Liew ECY. 2003. An evaluation of the fungal 'morphotype' concept based on ribosomal DNA sequences. Fung Divers 12:53-66.
37. Legault D, Dessureault M, Laflamme G. 1989. Mycoflora of the needles of Pinus banksiana and Pinus resinosa 1. Endophytic fungi. Can J Bot 67:2052-2060.
38. Lieckfeldt E, Seifert KA. 2000. An evaluation of the use of ITS sequences in the taxonomy of the Hypocreales. Stud Mycol 45:35-44.
39. Liu YJ, Hall BD. 2004. Body plan evolution of ascomycetes, as inferred from an RNA polymerase II subunit. Mol Biol Evol 16:1799-1808.
40. Lodge DJ, Fisher BJ, Sutton BC. 1996. Endophytic fungi of Manilkara bidentata leaves in Puerto Rico. Mycologia 88:733-738.
41. Lumbsch HT, Wirtz N, Lindemuth R, Schmitt I. 2002. Higher level phylogenetic relationships of euascomycetes (Pezizomycotina) inferred from a combined analysis of nuclear and mitochondrial sequence data. Mycol Prog 1:57-70.
42. Lutzoni F, Pagel M, Reeb V. 2001. Major fungal lineages are derived from lichen symbiotic ancestors. Nature 411:937-940.
43. _, Kauff F, Cox C, McLaughlin D, Celio G, Dentiger B, PAdamsee M, Hibbett D, James TY, Baloch E, Grube M, Reeb V, Hofstetter V, Schoch C, Arnold AE, Miadlikowska J, Spatafora J, Johnson D, Hambleton S, Crockett M, Shoemaker R, Sung G-H, Lucking R, Lumbsch T, O'Donnell K, Binder M, Diederich P, Ertz D, Gueidan C, Hansen K, Harris RC, Hosaka K, Lim YW, Matheny B, Nishida H, Pfister D, Rogers J, Rossman A, Schmitt I, Sipman H, Stone J, Sugiyama J, Yahr R, Vilgalys R. 2004. Assembling the Fungal Tree of Life: progress, classification and the evolution of subcellular traits. Am J Bot 91:1446-1480.
44. Maddison DR, Maddison WP. 2003. MacClade: analysis of phylogeny and character evolution, Version 4.06. Sunderland, MA: Sinauer Associates.
45. McLenon T, Moncalvo J-M. 2004. The basidiomycete community in a hemlock-dominated plot in a southern Ontario temperate forest. Inoculum 54:35.
46. Miadlikowska J, Lutzoni F, Goward T, Zoller S, Posada D. 2003. New approach to an old problem: incorporating signal from gap-rich regions of ITS and nrDNA large subunit into phylogenetic analyses to resolve the Peltigera canina complex. Mycologia 95:1181-1203.
47. Mihelcic N, Hanula JL, Debarr GL. 2003. Pathogenic microorganisms associated with the southern pine coneworm (Lepidoptera: Pyralidae) attacking loblolly pine. Florida Entomol 86:1-7.
48. Moritz C, Faith DP. 1998. Comparative phylogeography and the identification of genetically divergent areas for conservation. Mol Ecol 7:419-430.
49. Müller MM, Valjakka R, Suokko A, Hantula J. 2001. Diversity of endophytic fungi of single Norway spruce needles and their role as pioneer decomposers. Mol Ecol 10:1801-1810.
50. Petrini O. 1986. Taxonomy of endophytic fungi of aerial plant tissues. In: Fokkema NJ, van den Huevel J, eds. Microbiology of the Phyllosphere. Cambridge, UK: Cambridge University Press. p 175-187.
51. _. 1991. Fungal endophytes of tree leaves. In: Andrews JH, Hirano SS, eds. Microbial Ecology of Leaves. New York: Springer-Verlag. p 179-197.
52. _, Carroll G. 1981. Endophytic fungi in foliage of some Cupressaceae in Oregon. Can J Bot 59:629-636.
53. _, Müller E. 1979. Pilzliche Endophyten am Beispiel von Juniperus communis L. Sydowia 32:224-251.
54. Reeb V, Lutzoni F, Roux C. 2004. Contribution of RPB2 to multilocus phylogenetic studies of the Pezizomycotina (euascomycetes, Fungi) with special emphasis on the lichen-forming Acarosporaceae and evolution of polyspory. Mol Phylogenet Evol 32:1036-1060.
55. Rice P, Longden I, Bleasby O. 2000. EMBOSS: the European molecular biology open software suite. Trend Genet 16:276-277.
56. Rollinger JL, Langenheim JH. 1993. Geographic survey of fungal endophyte community composition in leaves of coastal redwood. Mycologia 85:149-156.
57. Rossman AY. 1994. A strategy for an all-taxa inventory of fungal biodiversity. In: Peng CI, ed. Biodiversity and Terrestrial Ecosystems. Bulletin of the Academy Sinica Institute of Botany; online, at http://www.ars.usda.gov/ services/docs.htm?docid=9426.
58. Sall J, Lehman A. 1996. JMP Start Statistics. Cary, NC: SAS Institute.
59. Shaw AJ, Cox CJ, Boles SB. 2003. Global patterns in peat moss biodiversity. Mol Ecol 12:2553-2570.
60. Sherwood-Pike M, Stone J, Carroll GC. 1986. Rhabdocline parkeri, a ubiquitous foliar endophyte of Douglas-fir. Can J Bot 64:1849-1855.
61. Sluder ER. 1993. Results at age 15 years from a half-diallel cross among 10 loblolly pines selected for resistance to fusiform rust (Cronartium quercuum f-sp. fusiforme). Sylvae Genet 42:223-230.
62. Stanosz GR, Smith DR, Guthmiller MA, Stanosz JC. 1997. Persistence of Sphaeropsis sapinea on or in asymptomatic shoots of red and jack pines. Mycologia 89:525-530.
63. Stone JK. 1985. Foliar endophytes of Pseudotsuga menziesii (Mirb.) Franco. Cytology and physiology of the hostendophyte relationship [Doctoral dissertation]. Eugene: University of Oregon.
64. _. 1987. Initiation and development of latent infections by Rhabdocline parkeri on Douglas-fir. Can J Bot 65:2614-2621.
65. _, Bacon CW, White JR. 2000. An overview of endophytic microbes: endophytism defined. In: Bacon CW, White JF, eds. Microbial Endophytes. New York: Marcel Dekker. p 3-29.
66. Sung SJS, White LM, Marx DH, Otrosina WJ. 1995. Seasonal ectomycorrhizal fungal biomass development on loblolly pine (Pinus taeda L.) seedlings. Mycorrhiza 5:439-447.
67. Swofford DL. 2001. PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4b8. Sunderland, MA: Sinauer Associates.
68. _. 2004. PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4b10. Sunderland, MA: Sinauer Associates.
69. Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser DM, Hibbett DS, Fisher MC. 2000. Phylogenetic species recognition and species concepts in fungi. Fung Genet Biol 31:21-32.
70. Tehler A, Little DP, Farris JS. 2003. The full-length phylogenetic tree from 1551 ribosomal sequences of chitinous fungi, Fungi. Mycol Res 107:901-916.
71. _, Farris JS, Lipscomb DL, Källersjo M. 2000. Phylogenetic analyses of the fungi based on large rDNA datasets. Mycologia 92:459-474.
72. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The Clustal X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acid Res 24:4876-4882.
73. Vane-Wright RI, Humphries CJ, Williams PH. 1991. What to protect? systematics and the agony of choice. Biol Conserv 55:235-254.
74. Vilgalys R, Hester M. 1990. Rapid genetic identification and mapping enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238-4246.
75. _, Sun BL. 1994. Ancient and recent patterns of geographic speciation in the oyster mushroom Pleurotus revealed by phylogenetic analysis of ribosomal DNA sequences. Proc Nat Acad Sci USA 91:4599-4603.
76. West L, Jones RH. 2000. Responses of understory tree seedlings to alteration of the soil fungal community in mid- and late-successional forests. For Ecol Manage 134:125-135.
77. Wheeler WC. 1990. Combinatorial weights in phylogenetic analysis: a statistical parsimony procedure. Cladistics 6:269-275.
78. White TJ, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. Chapter 38. In: Innis M, Gelfand D, Sninsky J, White T, eds. PCR Protocols: a guide to methods and applications. Orlando, Florida: Academic Press. p 315-322.
79. Williams PH, Gaston KJ, Humphries CJ. 1994. Do conservationists and molecular biologists value differences between organisms in the same way? Biodivers Lett 2:67-78.