Hidden diversity of endophytic fungi in an invasive plant

American Journal of Botany

Volumn 95, Issue 9, 2008, Pages 1096-1108

  Shipunov, Alexey ^a   Newcombe, George ^a   Raghavendra, Anil K H ^a   Anderson, Cort L ^a  

^a UNIVERSITY OF IDAHO   (United States)

Author keywords

Asteraceae; Botrytis phylogeny; Centaurea stoebe; Diversity; Endophytes; Geographic origins of fungi; Native and invaded ranges; Spotted knapweed

Indexed keywords

COMMUNITY STRUCTURE; ENDOPHYTE; FUNGUS; HOST-PARASITE INTERACTION; INVASIVE SPECIES; PATHOGEN; PHYLOGENY; PLANT; SPECIES DIVERSITY;

ALTERNARIA ALTERNATA; ASTERACEAE; BOTRYTIS; CENTAUREA; CENTAUREA STOEBE; FUNGI;

EID: 51349166778     PISSN: 00029122     EISSN: None     Source Type: Journal    
DOI: 10.3732/ajb.0800024     Document Type: Article

References (74)

1. AHLHOLM, J. U., M. HELANDER, J. HENRIKSSON, M. METZLER, AND K. SAIKKONEN. 2002. Environmental conditions and host genotype direct genetic diversity of Venturia detricha, a fungal endophyte of birch trees. Evolution 56: 1566-1573.
2. ARNOLD, A. E., D. A. HENK, R. L. EELLS, F. LUTZONI, AND R. VILGALYS. 2007. Diversity and phylogenetic affinities of foliar fungal endophytes in loblolly pine inferred by culturing and environmental PCR. Mycologia 99: 185-206.
3. ARNOLD, A. E., AND F. LUTZONI. 2007. Diversity and host range of foliar fungal endophytes: Are tropical leaves biodiversity hotspots? Ecology 88: 541-549.
4. ARNOLD, A. E., Z. MAYNARD, AND G. S. GILBERT. 2001. Fungal endophytes in dicotyledonous neotropical trees: Patterns of abundance and diversity. Mycological Research 105: 1502-1507.
5. BAILEY, B. A., H. BAE, M. D. STREM, D. P. ROBERTS, S. E. THOMAS, J. CROZIER, G. J. SAMUELS, I. CHOI, AND K. A. HOLMES. 2006. Fungal and plant gene expression during the colonization of cacao seedlings by endophytic isolates of four Trichoderma species. Planta 224: 1449-1464.
6. BAIS, H. P., R. VEPACHEDU, S. GILROY, R. M. CALLAWAY, AND J. M. VIVANCO. 2003. Allelopathy and exotic plant invasion: From molecules and genes to species interactions. Science 301: 1377-1380.
7. BRASIER, C. M., AND K. W. BUCK. 2001. Rapid evolutionary changes in a globally invading fungal pathogen (Dutch elm disease). Biological Invasions 3: 223-233.
8. BROENNIMANN, O., U. A. TREIER, H. MÜLLER- SCHÄRER, W. THUILLER , A. T. PETERSON, AND A. GUISAN. 2007. Evidence of climatic niche shift during biological invasion. Ecology Letters 10: 701-709.
9. CALLAWAY, R. M., AND W. M. RIDENOUR. 2004. Novel weapons: Invasive success and the evolution of increased competitive ability. Frontiers of Ecology and the Environment 2: 436-443.
10. CANNON, P. F. 1997. Strategies for rapid assessment of fungal diversity. Biodiversity and Conservation 6: 669-680.
11. CAPPUCCINO, N., AND J. T. ARNASON. 2006. Novel chemistry of invasive exotic plants. Biology Letters 2: 189-193.
12. CARROLL, G. 1988. Fungal endophytes in stems and leaves: From latent pathogen to mutualistic symbiont. Ecology 69: 2-9.
13. CHAO, A., R. L. CHAZDON, R. K. COLWELL, AND T. A. SHEN. 2005. A new statistical approach for assessing similarity of species composition with incidence and abundance data. Ecology Letters 8: 148-159.
14. CLAY, K., AND J. HOLAH. 1999. Fungal endophyte symbiosis and plant diversity in successional fields. Science 285: 1742-1744.
15. COLWELL, R. K. 2006. EstimateS: Statistical estimation of species richness and shared species from samples, version 8.0. Website http://viceroy.eeb.uconn.edu/EstimateS.
16. COX, G. W. 2004. Alien species and evolution. Island Press, Washington, D.C., USA.
17. CZEREPANOV, S. K. 1994. Vasilek - Centaurea L. In A. A. Fedorov [ed.], Flora of European part of USSR, vol. 7, 260-288 [in Russian]. Nauka, St. Petersburg, Russia.
18. DAHLBERG, K. R., AND J. L. VAN ETTEN. 1982. Physiology and biochemistry of fungal sporulation. Annual Review of Phytopathology 20: 281-301.
19. DE HOOG, G. S., E. GOETTLICH, G. PLATAS, O. GENILLOUD, G. LEOTTA, AND J. VAN BRUMMELEN. 2005. Evolution, taxonomy and ecology of the genus Thelebolus in Antarctica. Studies in Mycology 51: 33-76.
20. DITOMASO, J., AND E. HEALY. 2006. Weeds of California and other western states. University of California Department of Agriculture and Natural Resources, Berkeley, California, USA.
21. DUGAN, F. M., AND S. L. LUPIEN. 2002. Filamentous fungi quiescent in seeds and culm nodes of weedy and forage grass species endemic to the Palouse region of Washington and Idaho. Mycopathologia 156: 31-40.
22. ERNST, M., K. W. MENDGEN, AND S. G. R. WIRSEL. 2003. Endophytic fungal mutualists: Seed-borne Stagonospora spp. enhance reed biomass production in axenic microcosms. Molecular Plant-Microbe Interactions 16: 580-587.
23. FARR, D. F., A. Y. ROSSMAN, M. E. PALM, AND E. B. MCCRAY. Fungal databases. Systematic Mycology and Microbiology Laboratory, Agricultural Research Service, United States Department of Agriculture. Website http://nt.ars-grin.gov/fungaldatabases/ [accessed 6 March 2008].
24. GANLEY, R. J., S. J. BRUNSFELD, AND G. NEWCOMBE. 2004. A community of unknown, endophytic fungi in western white pine. Proceedings of the National Academy of Sciences, USA 101: 10107-10112.
25. GANLEY, R. J., AND G. NEWCOMBE. 2006. Fungal endophytes in seeds and needles of Pinus monticola. Mycological Research 110: 318-332.
26. GAO, X., H. ZHOU, D. XU, C. YU, Y. CHEN, AND L. QU. 2005. High diversity of endophytic fungi from the pharmaceutical plant, Heterosmilax japonica Kunth revealed by cultivation-independent approach. FEMS Microbiology Letters 249: 255-266.
27. GLADIEUX, P., X.-G. ZHANG, D. AFOUFA- BASTIEN, R.-M. VALDEBENITO SANHUEZA, M. SBAGHI, AND B. LE CAM. 2008. On the origin and spread of the scab disease of apple: Out of central Asia. PLoS ONE 3:e1455. 1-14.
28. GOVAERTS, R. 2001. How many species of seed plants are there? Taxon 50: 1085-1090.
29. GRÄSER, Y., J. FRÖHLICH, W. PRESBER, AND S. DE HOOG. 2007. Microsatellite markers reveal geographic population differentiation in Trichophyton rubrum. Journal of Medical Microbiology 56: 1058-1065.
30. HAWKSWORTH, D. L. 1991. The fungal dimension of biodiversity: Magnitude, significance and conservation. Mycological Research 95: 641-655.
31. HAWKSWORTH, D. L. 2001. The magnitude of fungal diversity: The 1.5 million species estimate revisited. Mycological Research 105: 1422-1432.
32. HIBBETT, D. S., M. BINDER, J. F. BISCHOFF, M. BLACKWELL, P. F. CANNON, O. E. ERIKSSON, S. HUHNDORF, ET AL. 2007. A higher-level phylogenetic classification of the Fungi. Mycological Research 111: 509-547.
33. HIGGINS, K. L., A. E. ARNOLD, J. MIADLIKOWSKA, S. D. SARVATE, AND F. LUTZONI. 2007. Phylogenetic relationships, host affinity, and geographic structure of boreal and arctic endophytes from three major plant lineages. Molecular Phylogenetics and Evolution 42: 543-555.
34. HONG, S. G., R. A. CRAMER, C. B. LAWRENCE, AND B. M. PRYOR. 2005. Alt a 1 allergen homologs from Alternaria and related taxa: Analysis of phylogenetic content and secondary structure. Fungal Genetics and Biology 42: 119-129.
35. HYDE, K. D., B. BUSSABAN, B. PAULUS, P. W. CROUS, S. LEE, E. H. C. MCKENZIE, W. PHOTITA, AND S. LUMYONG. 2007. Diversity of saprobic microfungi. Biodiversity and Conservation 16: 7-35.
36. INDERJIT, S. [ed.]. 2005. Invasive plants: Ecological and agricultural aspects. Birkhauser Verlag, Basel, Switzerland.
37. KAUSERUD, H., I. B. SVEGARDEN, G.-P. SAETRE, H. KNUDSEN, O. STENSRUD, O. SCHMIDT, S. DOI, T. SUGIYAMA, AND N. HOGBERG. 2007. Asian origin and rapid global spread of the destructive dry rot fungus Serpula lacrymans. Molecular Ecology 16: 3350-3360.
38. KLIRONOMOS, J. N. 2002. Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417: 67-70.
39. KLOKOV, M. V. 1963. Vasilek - Centaurea L., subgenus Acrolophus (Cass.) Dobrocz. In V. L. Komarov [ed.], Flora USSR, vol. 28, 512-538 (in Russian). Izdatel'stvo Akademii Nauk SSSR, Moscow-Leningrad, USSR.
40. MADDISON, D. R., AND W. P. MADDISON. 2000. MacClade, version 4.06b. Sinauer, Sunderland, Massachusetts, USA.
41. MÁRQUEZ, L. M., R. S. REDMAN, R. J. RODRIGUEZ, AND M. J. ROOSSINCK. 2007. A virus in a fungus in a plant: Three-way symbiosis required for thermal tolerance. Science 315: 513-517.
42. NENTWIG, W. [ed.]. 2007. Biological invasions. Springer, Heidelberg, Germany.
43. NYLANDER, J. A. A. 2004. MrModeltest v2. Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden. Computer program distributed by the author, website http://www.abc.se/~nylander/mrmodeltest2/mrmodeltest2.html.
44. OCHSMANN, J. 2000. Morphologische und molekularsystematische Untersuchungen an der Centaurea stoebe L.-Gruppe (Asteraceae-Cardueae) in Europa. Dissertationes Botanicae 324: 1-242.
45. OCHSMANN, J. 2001. On the taxonomy of spotted knapweed (Centaurea stoebe L.). In Proceedings of 1st international knapweed symposium of the 21st century, Coeur d'Alene, Idaho, USA, 2001, 33-41. U. S. Department of Agriculture, Agricultural Research Service, Albany, California, USA.
46. OKSANEN, J., R. KINDT, P. LEGENDRE, B. O'HARA, AND M. H. H. STEVENS. 2007. Vegan: Community ecology package. R package, version 1.8-8. Website http://r-forge.r-project.org/ projects/vegan/.
47. OMACINI, M., E. J. CHANETON, C. M. GHERSA, AND C. B. MUELLER. 2001. Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature 409: 78-81.
48. OTERO, J. T., J. D. ACKERMAN, AND P. BAYMAN. 2002. Diversity and host specificity of endophytic Rhizoctonia-like fungi from tropical orchids. American Journal of Botany 89: 1852-1858.
49. OTERO, J. T., N. S. FLANAGAN, E. A. HERRE, J. D. ACKERMAN, AND P. BAYMAN. 2007. Widespread mycorrhizal specificity correlates to mycorrhizal function in the neotropical, epiphytic orchid Ionopsis utricularioides (Orchidaceae). American Journal of Botany 94: 1944-1950.
50. PIMENTEL, D., L. LACH, R. ZUNIGA, AND D. MORRISON. 2000. Environmental and economic costs of nonindigenous species in the United States. Bioscience 50: 53-65.
51. PRYOR, B. M., AND R. L. GILBERTSON. 2000. Molecular phylogenetic relationships amongst Alternaria species and related fungi based upon analysis of nuclear ITS and mt SSU rDNA sequences. Mycological Research 104: 1312-1321.
52. R DEVELOPMENT CORE TEAM. 2007. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Website http://www.R-project.org.
53. REDMAN, R. S., K. B. SEEHAN, R. G. STOUT, R. J. RODRIQUEZ, AND J. M. HENSON. 2002. Thermotolerance generated by plant/fungal symbiosis. Science 298: 1581.
54. REINHART, K. O., AND R. CALLAWAY. 2006. Soil biota and invasive plants. New Phytologist 170: 445-457.
55. RICHARDSON, D. M., N. ALLSOPP, C. M. D'ANTONIO, S. J. MILTON, AND M. REJMÁNEK. 2000. Plant invasions - The role of mutualisms. Biological Reviews of the Cambridge Philosophical Society 75: 65-93.
56. RODRIGUEZ, R. J., R. S. REDMAN, AND J. M. HENSON. 2004. The role of fungal symbioses in the adaptation of plants to high stress environments. Mitigation and Adaptation Strategies for Global Change 9: 261-272.
57. SAHASHI, N., T. KUBONO, Y. MIYASAWA, AND S. ITO. 1999. Temporal variations in isolation frequency of endophytic fungi of Japanese beech. Canadian Journal of Botany 77: 197-202.
58. SAIKKONEN, K., S. H. FAETH, M. HELANDER, AND T. J. SULLIVAN. 1998. Fungal endophytes: A continuum of interactions with host plants. Annual Review of Ecology and Systematics 29: 319-343.
59. SCHMIT, J. P., AND G. M. MUELLER. 2007. An estimate of the lower limit of global fungal diversity. Biodiversity and Conservation 16: 99-111.
60. SCHUBERT, K., J. Z. GROENEWALD, U. BRAUN, J. DIJKSTERHUIS, M. STARINK, C. F. HILL, P. ZALAR, G. S. DE HOOG, AND P. W. CROUS. 2007. Biodiversity in the Cladosporium herbarum complex (Davidiellaceae, Capnodiales), with standardization of methods for Cladosporium taxonomy and diagnostics. Studies in Mycology 58: 105-166.
61. SCHULZ, B., U. WANKE, S. DRAEGER, AND H. AUST. 1993. Endophytes from herbaceous plants and shrubs: Effectiveness of surface sterilization methods. Mycological Research 97: 1447-1450.
62. STAATS, M., P. VAN BAARLEN, AND J. A. L. VAN KAN. 2005. Molecular phylogeny of the plant pathogenic genus Botrytis and the evolution of host specificity. Molecular Biology and Evolution 22: 333-346.
63. STORY, J. M., N. W. CALLAN, J. G. CORN, AND L. J. WHITE. 2006. Decline of spotted knapweed density at two sites in western Montana with large populations of the introduced root weevil, Cyphocleonus achates (Fahraeus). Biological Control 38: 227-232.
64. SWOFFORD, D. L. 2003. PAUP*: Phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer, Sunderland, Massachusetts, USA.
65. TAYLOR, J. W., E. TURNER, J. P. TOWNSEND, J. R. DETTMAN, AND D. JACOBSON. 2006. Eukaryotic microbes, species recognition and the geographic limits of species: Examples from the kingdom Fungi. Philosophical Transactions of the Royal Society of London, B, Biological Sciences 361: 1947-1963.
66. TEDERSOO, L., T. SUVI, K. BEAVER, AND U. KOLJALG. 2007. Ectomycorrhizal fungi of the Seychelles: Diversity patterns and host shifts from the native Vateriopsis seychellarum (Dipterocarpaceae) and Intsia bijuga (Caesalpiniaceae) to the introduced Eucalyptus robusta (Myrtaceae), but not Pinus caribea (Pinaceae). New Phytologist 175: 321-333.
67. THOMPSON, J. D., T. J. GIBSON, F. PLEWNIAK, F. JEANMOUGIN, AND D. G. HIGGINS. 1997. The CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25: 4876-4882.
68. THORNE, R. F. 2002. How many species of seed plants are there? Taxon 51: 511-512.
69. UNTERSEHER, M., M. SCHNITTLER, C. DORMANN, AND A. SICKERT. 2008. Application of species richness estimators for the assessment of fungal diversity. FEMS Microbiology Letters 282: 205-213.
70. VAN BAEL, S. A., Z. MAYNARD, N. ROBBINS, J. BISCHOFF, A. E. ARNOLD, E. ROJAS, L. C. MEJIA, D. A. KYLLO, AND E. A. HERRE. 2005. Emerging perspectives on the ecological roles of endophytic fungi in tropical plants. In J. Dighton, P. Oudemans, and J. White [eds.], The fungal community: Its organization and role in the ecosystem, 181-191. CRC Press, Boca Raton, Florida, USA.
71. WEBB, C. O., D. D. ACKERLY, AND S. W. KEMBEL. 2007. Phylocom: Software for the analysis of community phylogenetic structure and character evolution, version 3.41. Website http://www.phylodiversity.net/ phylocom/.
72. WELDON, C., L. H. DU PREEZ, A. D. HYATT, R. MULLER, AND R. SPEARE. 2004. Origin of the amphibian chytrid fungus. Emerging Infectious Diseases 10: 2100-2105.
73. WHITE, I. R., AND D. BACKHOUSE. 2007. Comparison of fungal endophyte communities in the invasive panicoid grass Hyparrhenia hirta and native grass Bothriochloa macra. Australian Journal of Botany 55: 178-185.
74. WHITE, T. J., T. D. BRUNS, S. B. LEE, AND J. W. TAYLOR. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, and T. J. White [eds.], PCR protocols: A guide to methods and applications, 315-332. Academic Press, London, UK.