The composition of phyllosphere fungal assemblages of European beech (fagus sylvatica) varies significantly along an elevation gradient

New Phytologist

Volumn 196, Issue 2, 2012, Pages 510-519

  Cordier, Tristan ^a,b   Robin, Cécile ^a,b   Capdevielle, Xavier ^a,b   Fabreguettes, Olivier ^a,b   Desprez Loustau, Marie Laure ^a,b   Vacher, Corinne ^a,b  

^a UMR 1202 BIOGECO   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

454 pyrosequencing; Climate change; Community structure; Elevation gradient; Fagus sylvatica; Fungi; Pathogens; Phyllosphere

Indexed keywords

CLIMATE CHANGE; COMMUNITY STRUCTURE; DECIDUOUS TREE; ELEVATION; FUNGAL DISEASE; FUNGUS; PATHOGENICITY; PLANT COMMUNITY; RELATIVE ABUNDANCE; TEMPERATURE GRADIENT;

ALTITUDE; ARTICLE; BEECH; CLIMATE; ECOSYSTEM; FRANCE; FUNGUS; MICROBIOLOGY; MOLECULAR GENETICS; MULTIVARIATE ANALYSIS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PLANT LEAF; STATISTICAL MODEL; WEATHER;

ALTITUDE; CLIMATE; ECOSYSTEM; FAGUS; FRANCE; FUNGI; LINEAR MODELS; MOLECULAR SEQUENCE DATA; MULTIVARIATE ANALYSIS; PLANT LEAVES; WEATHER;

FRANCE; PYRENEES;

FAGUS; FAGUS SYLVATICA; FUNGI; MYCOSPHAERELLA PUNCTIFORMIS;

EID: 84866410010     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2012.04284.x     Document Type: Article

References (76)

1. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25: 3389-3402.
2. Amend AS, Seifert KA, Bruns Thomas D. 2010. Quantifying microbial communities with 454 pyrosequencing: does read abundance count? Molecular Ecology 19: 5555-5565.
3. Anderson MJ. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26: 32-46.
4. Arnold AE, Mejia LC, Kyllo D, Rojas EI, Maynard Z, Robbins N, Herre EA. 2003. Fungal endophytes limit pathogen damage in a tropical tree. Proceedings of the National Academy of Sciences, USA 100: 15649-15654.
5. Aryal B, Neuner G. 2010. Leaf wettability decreases along an extreme altitudinal gradient. Oecologia 162: 1-9.
6. Bahnweg G, Heller W, Stich S, Knappe C, Betz G, Heerdt C, Kehr RD, Ernst D, Langebartels C, Nunn AJ et al. 2005. Beech leaf colonization by the endophyte Apiognomonia errabunda dramatically depends on light exposure and climatic conditions. Plant Biology 7: 659-669.
7. Bahram M, Põlme S, Kõljalg U, Zarre S, Tedersoo L. 2011. Regional and local patterns of ectomycorrhizal fungal diversity and community structure along an altitudinal gradient in the Hyrcanian forests of northern Iran. New Phytologist 193: 465-473.
8. Bailey JK, Hendry AP, Kinnison MT, Post DM, Palkovacs EP, Pelletier F, Harmon LJ, Schweitzer JA. 2009. From genes to ecosystems: an emerging synthesis of eco-evolutionary dynamics. New Phytologist 184: 746-749.
9. Bateman BL, VanDerWal J, Johnson CN. 2012. Nice weather for bettongs: using weather events, not climate means, in species distribution models. Ecography 35: 306-314.
10. Begerow D, Nilsson H, Unterseher M, Maier W. 2010. Current state and perspectives of fungal DNA barcoding and rapid identification procedures. Applied Microbiology and Biotechnology 87: 99-108.
11. Benichou P, Le Breton O. 1987. Prise en compte de la topographie pour la cartographie de champs pluviométriques statistiques. La Météorologie 19: 23-24.
12. Bradley DJ, Gilbert GS, Martiny JBH. 2008. Pathogens promote plant diversity through a compensatory response. Ecology Letters 11: 461-469.
13. 2 partial pressures. Annals of Forest Science 66: 505.
14. Bresson CC, Vitasse Y, Kremer A, Delzon S. 2011. To what extent is altitudinal variation of functional traits driven by genetic adaptation in European oak and beech? Tree Physiology 31: 1164-1174.
15. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7: 335-336.
16. Clarke KR, Ainsworth M. 1993. A method of linking multivariate community structure to environmental variables. Marine Ecology Progress Series 92: 205-219.
17. Clay K, Holah J. 1999. Fungal endophyte symbiosis and plant diversity in successional fields. Science 285: 1742-1744.
18. Cordier T, Robin C, Capdevielle X, Desprez-Loustau M-L, Vacher C. 2012. Spatial variability of phyllosphere fungal assemblages: genetic distance predominates over geographic distance in a European beech stand (Fagus sylvatica). Fungal Ecology 5: 509-520.
19. Devictor V, Julliard R, Jiguet F, Couvet D. 2008. Birds are tracking climate warming, but not fast enough. Proceedings of the Royal Society of London B 275: 2743-2748.
20. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461.
21. Edgar RC. 2011. Usearch: software and documentation. Version 5.1. [WWW document] URL http://drive5.com/usearch [accessed 20 May 2012].
22. Fauth JE, Bernardo J, Camara M, Resetarits WJ Jr, Buskirk JV, McCollum SA. 1996. Simplifying the jargon of community ecology: a conceptual approach. The American Naturalist 147: 282-286.
23. Filteau M, Lagace L, Lapointe G, Roy D. 2011. Correlation of maple sap composition with bacterial and fungal communities determined by multiplex automated ribosomal intergenic spacer analysis (MARISA). Food Microbiology 28: 980-989.
24. Gange AC, Gange EG, Sparks TH, Boddy L. 2007. Rapid and recent changes in fungal fruiting patterns. Science 316: 71.
25. Gardes M, Bruns TD. 1993. Its primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts. Molecular Ecology 2: 113-118.
26. Gilbert GS. 2002. Evolutionary ecology of plant diseases in natural ecosystems. Annual Review of Phytopathology 40: 13-43.
27. Hashizume Y, Sahashi N, Fukuda K. 2008. The influence of altitude on endophytic mycobiota in Quercus acuta leaves collected in two areas 1000 km apart. Forest Pathology 38: 218-226.
28. Helander M, Ahlholm J, Sieber TN, Hinneri S, Saikkonen K. 2007. Fragmented environment affects birch leaf endophytes. New Phytologist 175: 547-553.
29. Inácio J, Pereira P, Carvalho M, Fonseca Á, Amaral-Collaço MT, Spencer-Martins I. 2002. Estimation and diversity of phylloplane mycobiota on selected plants in a mediterranean-type ecosystem in Portugal. Microbial Ecology 44: 344-353.
30. Inacio J, Rodrigues MG, Sobral P, Fonseca A. 2004. Characterisation and classification of phylloplane yeasts from Portugal related to the genus Taphrina and description of five novel Lalaria species. FEMS Yeast Research 4: 541-555.
31. IPCC 2007. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL, eds. Climate change 2007: the physical science basis. Contribution of Working Group I to the fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge, UK and New York, NY, USA: Cambridge University Press.
32. Jones HG. 1992. Plants and microclimate: a quantitative approach to environmental plant physiology. Cambridge, UK: Cambridge University Press.
33. Jump AS, Hunt JM, Penuelas J. 2007. Climate relationships of growth and establishment across the altitudinal range of Fagus sylvatica in the Montseny Mountains, northeast Spain. Ecoscience 14: 507-518.
34. Jumpponen A, Jones KL. 2009. Massively parallel 454 sequencing indicates hyperdiverse fungal communities in temperate Quercus macrocarpa phyllosphere. New Phytologist 184: 438-448.
35. Jumpponen A, Jones KL. 2010. Seasonally dynamic fungal communities in the Quercus macrocarpa phyllosphere differ between urban and nonurban environments. New Phytologist 186: 496-513.
36. Körner C. 2007. The use of "altitude" in ecological research. Trends in Ecology & Evolution 22: 569-574.
37. Lenoir J, Gégout JC, Marquet PA, de Ruffray P, Brisse H. 2008. A significant upward shift in plant species optimum elevation during the 20th century. Science 320: 1768-1771.
38. Levetin E, Dorsey K. 2006. Contribution of leaf surface fungi to the air spora. Aerobiologia 22: 3-12.
39. Lindow SE, Brandl MT. 2003. Microbiology of the phyllosphere. Applied and Environmental Microbiology 69: 1875-1883.
40. Löchelt S, Franke A. 1995. Genetic constitution of beech stands (Fagus sylvatica L.) along an altitudinal transect from Freiburg to the top of "Mount Schauinsland". Silvae Genetica 44: 312-318.
41. Marchisio VF, Airaudi D, Barchi C. 1997. One-year monitoring of the airborne fungal community in a suburb of Turin (Italy) and assessment of its functional relations with the environment. Mycological Research 101: 821-828.
42. Meier CL, Rapp J, Bowers Robert M, Silman M, Fierer N. 2010. Fungal growth on a common wood substrate across a tropical elevation gradient: temperature sensitivity, community composition, and potential for above-ground decomposition. Soil Biology and Biochemistry 42: 1083-1090.
43. Moody SA, Newsham Kevin K, Ayres PG, Paul ND. 1999. Variation in the responses of litter and phylloplane fungi to UV-B radiation. Mycological Research 103: 1469-1477.
44. Newsham KK, Low MNR, McLeod AR, Greenslade PD, Emmett BA. 1997. Ultraviolet-b radiation influences the abundance and distribution of phylloplane fungi on pedunculate oak (Quercus robur). New Phytologist 136: 287-297.
45. Newton AC, Fitt BDL, Atkins SD, Walters DR, Daniell TJ. 2010. Pathogenesis, parasitism and mutualism in the trophic space of microbe-plant interactions. Trends in Microbiology 18: 365-373.
46. Nilsson RH, Kristiansson E, Ryberg M, Hallenberg N, Larsson KH. 2008. Intraspecific ITS variability in the kingdom fungi as expressed in the international sequence databases and its implications for molecular species identification. Evolutionary Bioinformatics Online 4: 193-201.
47. Nilsson RH, Ryberg M, Abarenkov K, Sjokvist E, Kristiansson E. 2009. The ITS region as a target for characterization of fungal communities using emerging sequencing technologies. FEMS Microbiology Letters 296: 97-101.
48. Nilsson RH, Veldre V, Hartmann M, Unterseher M, Amend A, Bergsten J, Kristiansson E, Ryberg M, Jumpponen A, Abarenkov K. 2010. An open source software package for automated extraction of ITS1 and ITS2 from fungal ITS sequences for use in high-throughput community assays and molecular ecology. Fungal Ecology 3: 284-287.
49. Ohsawa T, Ide Y. 2008. Global patterns of genetic variation in plant species along vertical and horizontal gradients on mountains. Global Ecology and Biogeography 17: 152-163.
50. Oksanen JF, Blanchet G, Kindt R, Legendre P, O'Hara RB, Simpson GL, Solymos P, Stevens MHM, Wagner H. 2010. vegan:community ecology package. R package version 1.17-4. http://CRAN.R-project.org/package=vegan.
51. Omacini M, Chaneton EJ, Ghersa CM, Muller CB. 2001. Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature 409: 78-81.
52. Osono T. 2006. Role of phyllosphere fungi of forest trees in the development of decomposer fungal communities and decomposition processes of leaf litter. Canadian Journal of Microbiology 52: 701-716.
53. Parmesan C. 2006. Ecological and evolutionary responses to recent climate change. Annual Review of Ecology, Evolution, and Systematics 37: 637-669.
54. Peñuelas J, Boada M. 2003. A global change-induced biome shift in the Montseny mountains (NE Spain). Global Change Biology 9: 131-140.
55. Quince C, Lanzen A, Curtis TP, Davenport RJ, Hall N, Head IM, Read LF, Sloan WT. 2009. Accurate determination of microbial diversity from 454 pyrosequencing data. Nature Methods 6: 639-641.
56. R Development Core Team. 2011. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
57. Redford AJ, Bowers RM, Knight R, Linhart Y, Fierer N. 2010. The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves. Environmental Microbiology 12: 2885-2893.
58. Redman RS, Sheehan KB, Stout RG, Rodriguez Russell J, Henson JM. 2002. Thermotolerance generated by plant/fungal symbiosis. Science 298: 1581.
59. Rodriguez RJ, White JF Jr, Arnold AE, Redman RS. 2009. Fungal endophytes: diversity and functional roles. New Phytologist 182: 314-330.
60. Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA. 2003. Fingerprints of global warming on wild animals and plants. Nature 421: 57-60.
61. Sander T, König S, Rothe GM, Janßen A, Weisgerber H. 2000. Genetic variation of European beech (Fagus sylvatica L.) along an altitudinal transect at mount Vogelsberg in Hesse, Germany. Molecular Ecology 9: 1349-1361.
62. SAS Institute Inc. 1997. SAS/STAT1 software. Release 8.1. Cary, NC: SAS Institute Inc.
63. Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, André Levesque C, Chen W, Fungal Barcoding Consortium. 2012. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. PNAS 109: 6241-6246.
64. Seifert KA. 2009. Progress towards DNA barcoding of fungi. Molecular Ecology Resources 9(Suppl 1): 83-89.
65. Sheik CS, Beasley WH, Elshahed MS, Zhou X, Luo Y, Krumholz LR. 2011. Effect of warming and drought on grassland microbial communities. ISME Journal 5: 1692-1700.
66. Shendure J, Ji H. 2008. Next-generation DNA sequencing. Nature Biotechnology 26: 1135-1145.
67. Suda W, Nagasaki A, Shishido M. 2009. Powdery mildew-infection changes bacterial community composition in the phyllosphere. Microbes and Environments 24: 217-223.
68. Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ, Collingham YC, Erasmus BFN, de Siqueira MF, Grainger A, Hannah L et al. 2004. Extinction risk from climate change. Nature 427: 145-148.
69. Tylianakis JM, Didham RK, Bascompte J, Wardle DA. 2008. Global change and species interactions in terrestrial ecosystems. Ecology Letters 11: 1351-1363.
70. Unterseher M, Jumpponen A, Opik M, Tedersoo L, Moora M, Dormann CF, Schnittler M. 2011. Species abundance distributions and richness estimations in fungal metagenomics - lessons learned from community ecology. Molecular Ecology 20: 275-285.
71. Unterseher M, Schnittler M. 2009. Dilution-to-extinction cultivation of leaf-inhabiting endophytic fungi in beech (Fagus sylvatica L.) - different cultivation techniques influence fungal biodiversity assessment. Mycological Research 113: 645-654.
72. Unterseher M, Schnittler M. 2010. Species richness analysis and ITS rDNA phylogeny revealed the majority of cultivable foliar endophytes from beech (Fagus sylvatica). Fungal Ecology 3: 366-378.
73. Verkley GJM, Crous PW, Groenewald JZ, Braun U, Aptroot A. 2004. Mycosphaerella punctiformis revisited: morphology, phylogeny, and epitypitication of the type species of the genus Mycosphaerella (Dothideales, Ascomycota). Mycological Research 108: 1271-1282.
74. White TJ, Bruns T, Lee S, Taylor JW. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MH, Gelfand DH, Sninsky JJ, White TJ, eds. PCR protocols: a guide to methods and applications. New York, NY, USA: Academic Press, Inc., 315-322.
75. Wilkinson HH, Siegel MR, Blankenship JD, Mallory AC, Bush LP, Schardl CL. 2000. Contribution of fungal loline alkaloids to protection from aphids in a grass-endophyte mutualism. Molecular Plant-Microbe Interactions 13: 1027-1033.
76. Yuste JC, Peñuelas J, Estiarte M, Garcia-Mas J, Mattana S, Ogaya R, Pujol M, Sardans J. 2011. Drought-resistant fungi control soil organic matter decomposition and its response to temperature. Global Change Biology 17: 1475-1486.