Relocation, high-latitude warming and host genetic identity shape the foliar fungal microbiome of poplars

Molecular Ecology

Volumn 24, Issue 1, 2015, Pages 235-248

  Bálint, Miklõs ^a   Bartha, Lászlõ ^b   O'Hara, Robert B ^a   Olson, Matthew S ^c,d   Otte, Jürgen ^a   Pfenninger, Markus ^a,e   Robertson, Amanda L ^d,f   Tiffin, Peter ^g   Schmitt, Imke ^a,e  

^a BIODIVERSITY AND CLIMATE RESEARCH CENTRE BIK F   (Germany)

^b BABE BOLYAI UNIVERSITY   (Romania)

^c TEXAS TECH UNIVERSITY   (United States)

^d UNIVERSITY OF ALASKA FAIRBANKS   (United States)

^e GOETHE UNIVERSITY   (Germany)

^f U S FISH AND WILDLIFE SERVICE   (United States)

^g UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Climate change; Community genetics; Enemy release; Metabarcoding; micro organism biogeography; plant fungal interactions

Indexed keywords

ANIMALIA; POPULUS; POPULUS BALSAMIFERA;

BIODIVERSITY; CANADA; CLASSIFICATION; ENDOPHYTE; FUNGUS; GREENHOUSE EFFECT; MICROBIOLOGY; MICROFLORA; PLANT LEAF; POPULUS; STATISTICAL MODEL; TREE;

BIODIVERSITY; CANADA; ENDOPHYTES; FUNGI; GLOBAL WARMING; LINEAR MODELS; MICROBIOTA; PLANT LEAVES; POPULUS; TREES;

EID: 84920771605     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.13018     Document Type: Article

References (89)

1. Abarenkov K, Henrik Nilsson R, Larsson K-H, et al,. (2010) The UNITE database for molecular identification of fungi-recent updates and future perspectives. New Phytologist, 186, 281-285.
2. Ahlholm JU, Helander M, Henriksson J, Metzler M, Saikkonen K, (2002) Environmental conditions and host genotype direct genetic diversity of Venturia ditricha, a fungal endophyte of birch trees. Evolution; International Journal of Organic Evolution, 56, 1566-1573.
3. Alsos IG, Ehrich D, Thuiller W, et al,. (2012) Genetic consequences of climate change for northern plants. Proceedings of the Royal Society B: Biological Sciences, 279, 2042-2051.
4. Altschul SF, Madden TL, Schäffer AA, et al,. (1997) Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Research, 25, 3389-3402.
5. Anders S, Huber W, (2010) Differential expression analysis for sequence count data. Genome Biology, 11, R106.
6. Anderson MJ, (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26, 32-46.
7. Anderson MJ, Walsh DCI, (2013) permanova, anosim, and the Mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing? Ecological Monographs, 83, 557-574.
8. Arnold AE, Herre EA, (2003) Canopy cover and leaf age affect colonization by tropical fungal endophytes: ecological pattern and process in Theobroma cacao (Malvaceae). Mycologia, 95, 388-398.
9. Arnold AE, Lutzoni F, (2007) Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology, 88, 541-549.
10. Arnold AE, Mejía LC, Kyllo D, et al,. (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proceedings of the National Academy of Sciences, 100, 15649-15654.
11. Bálint M, Domisch S, Engelhardt CHM, et al,. (2011) Cryptic biodiversity loss linked to global climate change. Nature Climate Change, 1, 313-318.
12. Bálint M, Tiffin P, Hallström B, et al,. (2013) Host genotype shapes the foliar fungal microbiome of Balsam poplar (Populus balsamifera). PLoS ONE, 8, e53987.
13. Bálint M, Schmidt P-A, Sharma R, Thines M, Schmitt I, (2014) An Illumina metabarcoding pipeline for fungi. Ecology and Evolution, 4, 2642-2653.
14. Bebber DP, Ramotowski MAT, Gurr SJ, (2013) Crop pests and pathogens move polewards in a warming world. Nature Climate Change, 3, 985-988.
15. Bellard C, Bertelsmeier C, Leadley P, Thuiller W, Courchamp F, (2012) Impacts of climate change on the future of biodiversity. Ecology Letters, 15, 365-377.
16. Benson AK, Kelly SA, Legge R, et al,. (2010) Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proceedings of the National Academy of Sciences, 107, 18933-18938.
17. Bergelson J, Purrington CB, (1996) Surveying patterns in the cost of resistance in plants. The American Naturalist, 148, 536-558.
18. Bray JR, Curtis JT, (1957) An ordination of the upland forest communities of Southern Wisconsin. Ecological Monographs, 27, 325-349.
19. Bulgarelli D, Rott M, Schlaeppi K, et al,. (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature, 488, 91-95.
20. Busby PE, Zimmerman N, Weston DJ, et al,. (2013) Leaf endophytes and Populus genotype affect severity of damage from the necrotrophic leaf pathogen, Drepanopeziza populi. Ecosphere, 4, art125.
21. Callaway RM, Brooker RW, Choler P, et al,. (2002) Positive interactions among alpine plants increase with stress. Nature, 417, 844-848.
22. Carroll GC, (1986) The biology of endophytism in plants with particular reference to woody perennials. In: Microbiology of the Phyllosphere (eds, Fokkema NJ, Van den Heuvel J,), pp. 205-222. Cambridge University Press, Cambridge, UK.
23. Chen I-C, Hill JK, Ohlemüller R, Roy DB, Thomas CD, (2011) Rapid range shifts of species associated with high levels of climate warming. Science, 333, 1024-1026.
24. Compant S, Van Der Heijden MGA, Sessitsch A, (2010) Climate change effects on beneficial plant-microorganism interactions. FEMS Microbiology Ecology, 73, 197-214.
25. 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.
26. Crous PW, (2009) Taxonomy and phylogeny of the genus Mycosphaerella and its anamorphs. Fungal Diversity, 38, 1-24.
27. Crous PW, Summerell BA, Mostert L, Groenewald JZ, (2008) Host specificity and speciation of Mycosphaerella and Teratosphaeria species associated with leaf spots of Proteaceae. Persoonia, 20, 59-86.
28. Davis MB, Shaw RG, (2001) Range shifts and adaptive responses to Quaternary climate change. Science, 292, 673-679.
29. Davis MB, Shaw RG, Etterson JR, (2005) Evolutionary responses to changing climate. Ecology, 86, 1704-1714.
30. Dethlefsen L, McFall-Ngai M, Relman DA, (2007) An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature, 449, 811-818.
31. Dodds PN, Rathjen JP, (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nature Reviews Genetics, 11, 539-548.
32. Edgar RC, (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics, 26, 2460-2461.
33. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R, (2011) uchime improves sensitivity and speed of chimera detection. Bioinformatics, 27, 2194-2200.
34. Fujimura KE, Egger KN, Henry GHR, (2007) The effect of experimental warming on the root-associated fungal community of Salix arctica. The ISME Journal, 2, 105-114.
35. Gaudet DA, Wang Y, Frick M, et al,. (2011) Low temperature induced defence gene expression in winter wheat in relation to resistance to snow moulds and other wheat diseases. Plant Science: An International Journal of Experimental Plant Biology, 180, 99-110.
36. Gloor GB, Hummelen R, Macklaim JM, et al,. (2010) Microbiome profiling by Illumina sequencing of combinatorial sequence-tagged PCR products. PLoS One, 5, e15406.
37. Grice EA, Segre JA, (2012) The human microbiome: our second genome. Annual Review of Genomics and Human Genetics, 13, 151-170.
38. Hill MO, (1973) Diversity and Evenness: a unifying notation and its consequences. Ecology, 54, 427-432.
39. Hoegh-Guldberg O, Hughes L, McIntyre S, et al,. (2008) Assisted colonization and rapid climate change. Science, 321, 345-346.
40. Holm S, (1979) A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics, 6, 65-70.
41. Hughes JB, Hellmann JJ, (2005) The application of rarefaction techniques to molecular inventories of microbial diversity. Methods in Enzymology, 397, 292-308.
42. Huson DH, Mitra S, Ruscheweyh H-J, Weber N, Schuster SC, (2011) Integrative analysis of environmental sequences using MEGAN4. Genome Research, 21, 1552-1560.
43. IPCC (2013) Climate Change 2013: The Physical Science Basis. Cambridge University Press, Cambridge, UK.
44. Keller SR, Olson MS, Silim S, Schroeder W, Tiffin P, (2010) Genomic diversity, population structure, and migration following rapid range expansion in the Balsam poplar, Populus balsamifera. Molecular Ecology, 19, 1212-1226.
45. Keller SR, Soolanayakanahally RY, Guy RD, et al,. (2011) Climate-driven local adaptation of ecophysiology and phenology in balsam poplar, Populus balsamifera L. (Salicaceae). American Journal of Botany, 98, 99-108.
46. Keller SR, Levsen N, Olson MS, Tiffin P, (2012) Local adaptation in the flowering-time gene network of Balsam poplar, Populus balsamifera L. Molecular Biology and Evolution, 29, 3143-3152.
47. Klironomos JN, (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature, 417, 67-70.
48. Krabel D, Morgenstern K, Herzog S, (2013) Endophytes in changing environments-do we need new concepts in forest management? iForest-Biogeosciences and Forestry, 6, 109-112.
49. Lamit LJ, Lau MK, Sthultz CM, et al,. (2014) Tree genotype and genetically based growth traits structure twig endophyte communities. American Journal of Botany, 101, 467-478.
50. Long SR, (1989) Rhizobium-legume nodulation: Life together in the underground. Cell, 56, 203-214.
51. Lundberg DS, Lebeis SL, Paredes SH, et al,. (2012) Defining the core Arabidopsis thaliana root microbiome. Nature, 488, 86-90.
52. Masella A, Bartram A, Truszkowski J, Brown D, Neufeld J, (2012) pandaseq: paired-end assembler for Illumina sequences. BMC Bioinformatics, 13, 31.
53. McMurdie PJ, Holmes S, (2014) Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Computational Biology, 10, e1003531.
54. Meiser A, Bálint M, Schmitt I, (2014) Meta-analysis of deep-sequenced fungal communities indicates limited taxon sharing between studies and the presence of biogeographic patterns. New Phytologist, 201, 623-635.
55. Mendes R, Kruijt M, de Bruijn I, et al,. (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science, 332, 1097-1100.
56. Müller MM, Sievänen R, Beuker E, et al,. (2014) Predicting the activity of Heterobasidion parviporum on Norway spruce in warming climate from its respiration rate at different temperatures. Forest Pathology, 44, 325-336.
57. Muscatine L, Porter JW, (1977) Reef Corals: mutualistic symbioses adapted to nutrient-poor environments. BioScience, 27, 454-460.
58. Nilsson RH, Veldre V, Hartmann M, et al,. (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.
59. Oksanen J, Blanchet FG, Kindt R, et al,. (2013) vegan v2.1-10: Community Ecology Package (http://cran.r-project.org/web/packages/vegan/index.html, accessed 01.12.2013).
60. Olson MS, Levsen N, Soolanayakanahally RY, et al,. (2013) The adaptive potential of Populus balsamifera L. to phenology requirements in a warmer global climate. Molecular Ecology, 22, 1214-1230.
61. Parfitt D, Hunt J, Dockrell D, Rogers HJ, Boddy L, (2010) Do all trees carry the seeds of their own destruction? PCR reveals numerous wood decay fungi latently present in sapwood of a wide range of angiosperm trees. Fungal Ecology, 3, 338-346.
62. Pauls SU, Nowak C, Bálint M, Pfenninger M, (2013) The impact of global climate change on genetic diversity within populations and species. Molecular Ecology, 22, 925-946.
63. Paulson JN, Stine OC, Bravo HC, Pop M, (2013) Differential abundance analysis for microbial marker-gene surveys. Nature Methods, 10, 1200-1202.
64. Pedranzani H, Sierra-de-Grado R, Vigliocco A, Miersch O, Abdala G, (2007) Cold and water stresses produce changes in endogenous jasmonates in two populations of Pinus pinaster Ait. Plant Growth Regulation, 52, 111-116.
65. R Core Team (2013) R: A Language and Environment for Statistical Computing. R Core Team, Vienna, Austria (http://cran.r-project.org/, accessed 01.11.2013).
66. Raghavendra AKH, Newcombe G, (2013) The contribution of foliar endophytes to quantitative resistance to Melampsora rust. New Phytologist, 197, 909-918.
67. Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM, (2002) Thermotolerance generated by plant/fungal symbiosis. Science, 298, 376-378.
68. Remy W, Taylor TN, Hass H, Kerp H, (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proceedings of the National Academy of Sciences, 91, 11841-11843.
69. Robertson AL, (2012) Acclimation and Migration Potential of a Boreal Forest Tree, Balsam Poplar (Populus balsamifera L.). Biology & Wildlife Department, University of Alaska Fairbanks, Fairbanks, Alaska.
70. Robinson MD, McCarthy DJ, Smyth GK, (2010) edger: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics (Oxford, England), 26, 139-140.
71. Rodriguez RJ, White Jr JF, Arnold AE, Redman RS, (2009) Fungal endophytes: diversity and functional roles. New Phytologist, 182, 314-330.
72. Rowntree JK, Shuker DM, Preziosi RF, (2011) Forward from the crossroads of ecology and evolution. Philosophical Transactions of the Royal Society B: Biological Sciences, 366, 1322-1328.
73. Saikkonen K, (2007) Forest structure and fungal endophytes. Fungal Biology Reviews, 21, 67-74.
74. Schmidt P-A, Bálint M, Greshake B, et al,. (2013) Illumina metabarcoding of a soil fungal community. Soil Biology and Biochemistry, 65, 128-132.
75. Schmieder R, Edwards R, (2011) Quality control and preprocessing of metagenomic datasets. Bioinformatics, 27, 863-864.
76. Scholtysik A, Unterseher M, Otto P, Wirth C, (2013) Spatio-temporal dynamics of endophyte diversity in the canopy of European ash (Fraxinus excelsior). Mycological Progress, 12, 291-304.
77. Sheik CS, Beasley WH, Elshahed MS, et al,. (2011) Effect of warming and drought on grassland microbial communities. The ISME Journal, 5, 1692-1700.
78. Soolanayakanahally RY, Guy RD, Silim SN, Drewes EC, Schroeder WR, (2009) Enhanced assimilation rate and water use efficiency with latitude through increased photosynthetic capacity and internal conductance in balsam poplar (Populus balsamifera L.). Plant, Cell & Environment, 32, 1821-1832.
79. Spor A, Koren O, Ley R, (2011) Unravelling the effects of the environment and host genotype on the gut microbiome. Nature Reviews Microbiology, 9, 279-290.
80. Svensson JR, Lindegarth M, Jonsson PR, Pavia H, (2012) Disturbance-diversity models: what do they really predict and how are they tested? Proceedings of the Royal Society B: Biological Sciences, 279, 2163-2170.
81. Tedersoo L, Bahram M, Toots M, et al,. (2012) Towards global patterns in the diversity and community structure of ectomycorrhizal fungi. Molecular Ecology, 21, 4160-4170.
82. Van der Putten WH, (2012) Climate change, aboveground-belowground interactions, and species' range shifts. Annual Review of Ecology, Evolution, and Systematics, 43, 365-383.
83. Van Grunsven RHA, Van Der Putten WH, Martijn Bezemer T, Berendse F, Veenendaal EM, (2010) Plant-soil interactions in the expansion and native range of a poleward shifting plant species. Global Change Biology, 16, 380-385.
84. Walther G-R, Post E, Convey P, et al,. (2002) Ecological responses to recent climate change. Nature, 416, 389-395.
85. Wang Y, Naumann U, Wright ST, Warton DI, (2012) mvabund-an R package for model-based analysis of multivariate abundance data. Methods in Ecology and Evolution, 3, 471-474.
86. Warton DI, Wright ST, Wang Y, (2012) Distance-based multivariate analyses confound location and dispersion effects. Methods in Ecology and Evolution, 3, 89-101.
87. White T, Bruns T, Lee S, Taylor J, (1990) PCR protocols a guide to methods and applications. In: PCR Protocols: A Guide to Methods and Applications (eds, Innis M, Gelfand D, Shinsky J, White T,), pp. 315-322. Academic Press, San Diego.
88. Wood SN, (2011) Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. Journal of the Royal Statistical Society: Series B (Statistical Methodology), 73, 3-36.
89. Zimmerman NB, Vitousek PM, (2012) Fungal endophyte communities reflect environmental structuring across a Hawaiian landscape. Proceedings of the National Academy of Sciences, 109, 13022-13027.