Abstract
Despite colonizing nearly every plant on Earth, foliar fungal symbionts have received little attention in studies on the biogeography of host-associated microbes. Evidence from regional scale studies suggests that foliar fungal symbiont distributions are influenced both by plant hosts and environmental variation in climate and soil resources. However, previous surveys have focused on either one plant host across an environmental gradient or one gradient and multiple plant hosts, making it difficult to disentangle the influence of host identity from the influence of the environment on foliar endophyte communities. We used a culture-based approach to survey fungal symbiont composition in the leaves of nine C3 grass species along replicated elevation gradients in grasslands of the Colorado Rocky Mountains. In these ecosystems, the taxonomic richness and composition of foliar fungal symbionts were mostly structured by the taxonomic identity of the plant host rather than by variation in climate. Plant traits related to size (height and leaf length) were the best predictors of foliar fungal symbiont composition and diversity, and composition did not vary predictably with plant evolutionary history. The largest plants had the most diverse and distinctive fungal communities. These results suggest that across the ~ 300 m elevation range that we sampled, foliar fungal symbionts may indirectly experience climate change by tracking the shifting distributions of plant hosts rather than tracking climate directly.
Similar content being viewed by others
References
Higgins KL, Arnold AE, Coley PD, Kursar TA (2014) Communities of fungal endophytes in tropical forest grasses: highly diverse host- and habitat generalists characterized by strong spatial structure. Fungal Ecol 8:1–11
Giauque H, Hawkes CV (2013) Climate affects symbiotic fungal endophyte diversity and performance. Am J Bot 100:1435–1444
Malinowski DP, Belesky DB (2000) Adaptations of endophyte-infected cool season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci 40:923–940
Elmi AA, West CP (1995) Endophyte infection effects on stomatal conductance, osmotic adjustment and drought recovery of tall fescue. New Phytol 131:61–67
Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM (2002) Thermotolerance generated by plant/fungal symbiosis. Science 298:1581
Gange AC, Eschen R, Wearn JA, Thawer A, Sutton BC (2012) Differential effects of foliar endophytic fungi on insect herbivores attacking a herbaceous plant. Oecologia 168:1023–1031
Arnold AE, Mejia LC, Kyllo D, Rojas EI, Maynard Z, Robbins N, Herre EA (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci U S A 100:15649–15654
Hartley SE, Gange AC (2009) Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Annu Rev Entomol 54:323–342
Kivlin SN, Emery SM, Rudgers JA (2013) Fungal symbionts alter plant responses to global change. Am J Bot 100:1445–1457
Arnold AE, Lutzoni F (2007) Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88:541–549
Kivlin SN, Lynn JS, Kazenel MR, Beals KK, Rudgers JA (2017) Biogeography of plant-associated fungal symbionts in mountain ecosystems: a meta-analysis. Divers Distrib 23:1067–1077
Zimmerman NB, Vitousek PM (2012) Fungal endophyte communities reflect environmental structuring across a Hawaiian landscape. Proc Natl Acad Sci U S A 109:13022–13027
Yang T, Weisenhorn P, Gilber JA, Ni Y, Sun R, Shi Y, Chu H (2017) Carbon constrains fungal endophyte assemblages along the timberline. Environ Microbiol 18:2455–2469
Giauque H, Hawkes CV (2016) Historical and current climate drive spatial and temporal patterns in fungal endophyte diversity. Fungal Ecol 20:108–114
Gazis R, Chaverri P (2010) Diversity of fungal endophytes in leaves and stems of wild rubber trees (Hevea brasiliensis) in Peru. Fungal Ecol 3:240–254
Koide RT, Ricks KD, Davis ER (2017) Climate and dispersal influence the structure of leaf fungal endophyte communities of Quercus gambelii in the eastern Great Basin, USA. Fungal Ecol 30:19–28
Christenhusz M, Byng JW (2016) The number of known plant species in the world and its annual increase. Phytotaxa 261:201–217
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavendar-Barres J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas M-L, Niinemets U, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827
Treseder KK, Kivlin SN, Hawkes CV (2011) Evolutionary trade-offs among decomposers determine responses to nitrogen enrichment. Ecol Lett 14:933–938
Martiny AC, Treseder K, Pusch G (2013) Phylogenetic conservation of functional traits in microorganisms. ISME J 7:830–838
Kembel SW, Mueller RC (2014) Plant traits and taxonomy drive host associations in tropical phyllosphere fungal communities. Botany 92:303–311
Van Bael S, Estrada C, Arnold AE (2017) Chapter 6: foliar endophyte communities and leaf traits in tropical trees. In: Dighton J, White JF (eds) The fungal community: its organization and role in the ecosystem. CRC Press, Boca Raton, pp 79–94
Valkama E, Koricheva J, Salminen J-P, Helander M, Saloniemi I, Saikkonen K, Pihlaja K (2005) Leaf surface traits: overlooked determinants of birch resistance to herbivores and foliar micro-fungi? Trees 19:191–197
Giauque H, Connor EW, Hawkes CV (2018) Endophyte traits relevant to stress tolerance, resource use and habitat origin predict effects on host plants. New Phytol. https://doi.org/10.1111/nph.15504
Higgins KL, Arnold AE, Miadlikowska J, Sarvate SD, Lutzoni F (2007) Phylogenetic relationships, host affinity, and geographic structure of boreal and arctic endophytes from three major plant lineages. Mol Phylogenet Evol 42:543–555
Massimo NC, Devan MN, Arendt KR, Wilch MH, Riddle JM, Furr SH, Steen C, U’Ren JM, Sandberg DC, Arnold AE (2015) Fungal endophytes in aboveground tissues of desert plants: infrequent in culture, but highly diverse and distinctive symbionts. Microb Ecol 70:61–76
Del Olmo-Ruiz M, Arnold AE (2014) Interannual variation and host affiliations of endophytic fungi associated with ferns at La Selva, Costa Rica. Mycologia 106:8–21
Suryanarayanan TS, Wittlinger SK, Faeth SH (2005) Endophytic fungi associated with cacti in Arizona. Mycol Res 109:635–639
Kittel TGF, Thornton PE, Royle JA, Chase TN (2002) Climates of the Rocky Mountains: historical and future patterns. In: Baron JS (ed) Rocky Mountain futures: an ecological perspective. Island Press, Covelo, pp 59–82
Dunne JA, Harte J, Taylor KJ (2003) Subalpine meadow flowering phenology responses to climate change: integrating experimental and gradient methods. Ecol Monogr 73:69–86
Pepin N, Losleben M (2002) Climate change in the Colorado Rocky Mountains: free air versus surface temperature trends. Int J Climatol 22(3):311–329
Rangwala I, Miller JR (2012) Climate change in mountains a review of elevation-dependent warming and its possible causes. Clim Chang 114:527–547
Lynn JS, Canfield S, Conover RR, Keene J, Rudgers JA (in press) Pocket gopher (Thomomys talpoides) soil disturbance peaks at mid elevation and is associated with air temperature, forb cover, and plant diversity. Arctic, Antarctic, and Alpine Research.
Shaw RB (2008) Grasses of Colorado. University Press of Colorado, Boulder
USDA NRCS (2018) The PLANTS Database (http://plants.usda.gov, 21 January 2018). National Plant Data Team, Greensboro, NC 27401–4901 USA
Paine CET, Norden N, Chave J, Forget P-M, Fortunel C, Dexter KG, Baraloto C (2012) Phylogenetic density dependence and environmental filtering predict seedling mortality in a tropical forest. Ecol Lett 15:34–41
Vincent JB, Weiblen GD, May G (2016) Host associations and beta diversity of fungal endophyte communities in New Guinea rainforest trees. Mol Ecol 25:825–841
Taylor DL, Booth MG, McFarland JW, Herriott IC, Lennon NJ, Nusbaum C, Marr TG (2008) Increasing ecological inference from high throughput sequencing of fungi in the environmental through a tagging approach. Mol Ecol Resour 8:742–752
Caparaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Gonzalez Pena A, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevensky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336
Glassman SI, Martiny JBH (2018) Broadscale ecological patterns are robust to use of exact sequence variants versus operational taxonomic units. mSphere 3:e00148–e00118
Corradi N, Croll D, Colard A, Kuhn G, Ehinger M, Sanders IR (2007) Gene copy number polymorphisms in an arbuscular mycorrhizal fungal population. Appl Environ Microbiol 73:366–369
Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A, Balestrini R, Charron P, Duensing N, Frei dit Frey N, Gianinazzi-Pearson V, Gilbert LB, Handa Y, Herr JR, Hijri M, Koul R, Kawaguchi M, Krajinski F, Lammers PJ, Masclaux FG, Murat C, Morin E, Nedikumana S, Pagni M, Petitpierre D, Requena N, Rosikiewicz P, Riley R, Saito K, San Clemente H, Shapiro H, van Tuinen D, Becard G, Bonfante P, Paszkowski U, Shachar-Hill YY, Tuskan GA, JPW Y, Sanders IR, Henrissat B, Rensing SA, Grigoriev IV, Corradi N, Roux C, Martin F (2013) Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc Natl Acad Sci U S A 110:20117–20122
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
Thiery O, Vasar M, Jairus T, Davison J, Roux C, Kivistik PA, Metspalu A, Milani L, Saks U, Moora M, Zobel M (2016) Sequence variation in nuclear ribosomal small subunit, internal transcribed spacer and large subunit regions of Rhizophagus irregularis and Gigaspora margarita is high and isolate-dependent. Mol Ecol 25:2816–2832
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Nhuyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Steves MHH, Szoecs E, Wagner H (2017) Vegan: community ecology package. R package version 2.4–5. https://CRAN.R-project.org/package=vegan
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Shannon CE (1948) A mathematical theory of communication. Bell Syst Tech J 27:379–423
Bates S, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Clarke KR, Gorley RN (2009) Primer version 6.1.10 user manual and tutorial. Primer-E, Plymouth
Anderson MJ, Walsh DCI (2013) PERMANOVA, ANOSIM, and the mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing? Ecol Monogr 83:557–574
Roberts DW (2007) Labdsv: ordination and multivariate analysis for ecology. R Package Version 1.8–0
Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14
Ranelli LB, Hendricks WQ, Lynn JS, Kivlin SN, Rudgers JA (2015) Biotic and abiotic predictors of fungal colonization in grasses of the Colorado Rockies. Divers Distrib 21:962–976
Classen AT, Sundqvist MK, Henning JA, Newman GS, Moore JAM, Cregger MA, Moorhead LC, Patterson CM (2015) Direct and indirect effects of climate change on soil microbial-plant interactions: what lies ahead? Ecosphere 6:1–21
Langenheim JH (1962) Vegetation and environmental patterns in the Crested Butte area, Gunnison County, Colorado. Ecol Monogr 32:249–285
Zorio SD, Williams CF, Aho KA (2016) Sixty-five years of change in montane plant communities in Western Colorado, USA. Arct Antarct Alp Res 48:703–722
Rodriguez RJ, White JF, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330
Ravnskov S, Jensen B, Knudsen IMB, Bodker L, Jensen DF, Karlinski L, Larsen J (2006) Soil inoculation with the biocontrol agent Clonostachys rosea and the mycorrhizal fungus Glomus intraradices results in mutual inhibition, plant growth promotion and alteration of soil microbial communities. Soil Biol Biochem 38:3452–3462
Buckley H, Young CA, Charlton ND, Hendricks WQ, Haley B, Nagabhyru P, Rudgers JA (in revision) Leaf endophytes mediate fertilizer effects on plant yield and traits in northern oat grass (Trisetum spicatum). Plant Soil
Mack KML, Rudgers JA (2008) Balancing multiple mutualists: asymmetric interactions among plants, arbuscular mycorrhizal fungi, and fungal endophytes. Oikos 117:310–320
Bond BJ (2000) Age-related changes in photosynthesis of woody plants. Trends Plant Sci 8:349–353
Kivlin SN, Winston GC, Goulden ML, Treseder KK (2014) Environmental filtering affects soil fungal community composition more than dispersal limitation at regional scales. Fungal Ecol 12:14–25
Musick HB, Trujillo SM, Truman CR (1996) Wind-tunnel modeling of the influence of vegetation structure on saltation threshold. Earth Surf Process Landf 21:589–605
Kazenel MR 2016. Altitudinal gradients do not predict plant-symbiont response to experimental warming. http://digitalrepository.unm.edu/biol_etds/124
Acknowledgments
We thank K. Anderson and B. McCormick for help maintaining the foliar endophyte culture collection and A. Chung and J. Bell for assistance with DNA extraction and sequencing.
Funding
This work was supported by National Science Foundation grant number DEB1354972 to Rudgers, Taylor and Kivlin and RMBL fellowships to Kivlin, Rudgers, and Lynn.
Author information
Authors and Affiliations
Corresponding author
Electronic Supplementary Material
ESM 1
(DOCX 192 kb)
Rights and permissions
About this article
Cite this article
Kivlin, S.N., Kazenel, M.R., Lynn, J.S. et al. Plant Identity Influences Foliar Fungal Symbionts More Than Elevation in the Colorado Rocky Mountains. Microb Ecol 78, 688–698 (2019). https://doi.org/10.1007/s00248-019-01336-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-019-01336-4