Skip to main content
SpringerLink
Log in

Does a foliar endophyte improve plant fitness under flooding?

  • Published:
Plant Ecology Aims and scope Submit manuscript

Abstract

Although endophytic fungi are ubiquitous in plants, their full range of ecological effects has yet to be characterized, particularly in non-agronomic systems. In this study, we compared the responses of two congeneric bluegrass species to flooding. Both plant species co-occur in subalpine zones of the Rocky Mountains. Marsh bluegrass (Poa leptocoma) commonly hosts a vertically transmitted fungal endophyte (Epichloë sp.) and naturally grows in wetter conditions than does nodding bluegrass (Poa reflexa), which lacks an epichloid endophyte. We investigated the novel hypothesis that endophyte symbiosis promotes host fitness under flooded conditions, contributing to niche differentiation between the two bluegrass species. We used a factorial greenhouse experiment to test whether endophyte presence improved survival, growth, or reproduction of P. leptocoma under flooded versus non-flooded edaphic conditions by experimentally removing the endophyte from half of the plants. We compared P. leptocoma responses to those of the endophyte-free congener. In contrast to expectations generated from the natural distributions of the two plant species, endophyte presence was more beneficial to P. leptocoma under ambient soil moisture than under flooding. Increased benefits of symbiosis in drier soils are consistent with studies of other grass endophytes. Flooded soils also unexpectedly improved the growth of P. reflexa more than that of the wet habitat specialist, P. leptocoma. While our results demonstrate an overall benefit of fungal symbiosis in this system, ecological factors other than flooding per se likely underlie the observed geographical distributions of these congeneric grasses in nature.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Afkhami ME, McIntyre PJ, Strauss SY (2014) Mutualist-mediated effects on species’ range limits across large geographic scales. Ecol Lett 17:1265–1273. doi:10.1111/Ele.12332

    Article  PubMed  Google Scholar 

  • Anderton LK, Barkworth ME (2009) Grasses of the intermountain region. Utah State University, Logan

    Google Scholar 

  • Arachevaleta M, Bacon CW, Hoveland CS, Radcliffe DE (1989) Effect of the tall fescue endophyte on plant response to environmental stress. Agron J 81:83–90

    Article  Google Scholar 

  • Arnold AE, Mejía 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 100:15649–15654. doi:10.1073/pnas.2533483100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bacon CW, White JF Jr (1994) Stains, media, and procedures for analyzing endophytes. In: Bacon CW, White JF Jr (eds) Biotechnology of endophytic fungi of grasses. CRC Press, Boca Raton

    Google Scholar 

  • Barkworth ME, Capels KM, Long S, Anderton LK, Piep MB (eds) (2007) Flora of North America volume 24: North of Mexico: Magnoliophyta: Commelinidae (in part): Poaceae, part 1. Oxford University Press, New York

  • Cheplick GP, Faeth SH (2009) Ecology and evolution of the grass-endophyte symbiosis. Oxford University Press, Oxford

    Book  Google Scholar 

  • Chung YY, Miller TEX, Rudgers JA (2015) Fungal symbionts maintain a rare host plant population but demographic advantage drives the dominance of a common host. J Ecol 103:967–977. doi:10.1111/1365-2745.12406

    Article  Google Scholar 

  • Compant S, van der Heijden MGA, Sessitsch A (2010) Climate change effects on beneficial plant-microorganism interactions. FEMS Microbiol Ecol 73:197–214. doi:10.1111/j.1574-6941.2010.00900.x

    CAS  PubMed  Google Scholar 

  • Davitt AJ, Chen C, Rudgers JA (2011) Understanding context-dependency in plant-microbe symbiosis: the influence of abiotic and biotic contexts on host fitness and the rate of symbiont transmission. Environ Exp Bot 71:137–145. doi:10.1016/j.envexpbot.2010.11.004

    Article  CAS  Google Scholar 

  • Deepika S, Kothamasi D (2015) Soil moisture—a regulator of arbuscular mycorrhizal fungal community assembly and symbiotic phosphorus uptake. Mycorrhiza 25:67–75. doi:10.1007/s00572-014-0596-1

    Article  CAS  PubMed  Google Scholar 

  • Elias M, Gompert Z, Jiggins C, Willmott K (2008) Mutualistic interactions drive ecological niche convergence in a diverse butterfly community. PLoS Biol 6:2642–2649. doi:10.1371/journal.pbio.0060300

    Article  CAS  PubMed  Google Scholar 

  • Emery SM, Bell-Dereske L, Rudgers JA (2015) Fungal symbiosis and precipitation alter traits and dune building by the ecosystem engineer, Ammophila breviligulata. Ecology 96:927–935. doi:10.1890/14-1121.1

    Article  PubMed  Google Scholar 

  • Forister M, Gompert A, Nice C, Forister G, Fordyce J (2011) Ant association facilitates the evolution of diet breadth in a lycaenid butterfly. Proc R Soc B 278:1539–1547. doi:10.1098/rspb.2010.1959

    Article  PubMed  Google Scholar 

  • Gibert A, Hazard L (2011) Endophyte infection of Festuca eskia enhances seedling survival to drought and cutting at the expense of clonal expansion. J Plant Ecol 4:201–208

    Article  Google Scholar 

  • Gillespie LJ, Soreng RJ (2005) A phylogenetic analysis of the bluegrass genus Poa based on cpDNA restriction site data. Syst Bot 30:84–105

    Article  Google Scholar 

  • Giussani LM, Gillespie LJ, Scataglini MA, Negritto MA, Anton AM, Soreng RJ (2016) Breeding system diversification and evolution in American Poa supersect. Homalopoa (Poaceae: Poeae: Poinae). Ann Bot 118:281–303

    Article  PubMed  PubMed Central  Google Scholar 

  • Gundel PE, Garibaldi LA, Martínez-Ghersa MA, Ghersa CM (2012) Trade-off between seed number and weight: influence of a grass–endophyte symbiosis. Basic Appl Ecol 13:32–39. doi:10.1016/j.baae.2011.10.008

    Article  Google Scholar 

  • Hajiboland R, Aliasgharzad N, Barzeghar R (2009) Phosphorus mobilization and uptake in mycorrhizal rice (Oryza sativa L.) plants under flooded and non-flooded conditions. Acta Agric Slov 93:153–161. doi:10.2478/v10014-009-0010-4

    Article  Google Scholar 

  • Hamilton CE, Gundel PE, Helander M, Saikkonen K (2012) Endophytic mediation of reactive oxygen species and antioxidant activity in plants: a review. Fungal Divers 54:1–10. doi:10.1007/s13225-012-0158-9

    Article  Google Scholar 

  • Herbert TD, Lawrence KT, Tzanova A, Peterson LC, Caballero-Gill R, Kelly CS (2016) Late Miocene global cooling and the rise of modern ecosystems. Nat Geosci 9:843–847. doi:10.1038/NGEO2813

    Article  CAS  Google Scholar 

  • Hesse U, Schöberlein W, Wittenmayer L, Förster K, Warnstorff K, Diepenbrock W, Merbach W (2005) Influence of water supply and endophyte infection (Neotyphodium spp.) on vegetative and reproductive growth of two Lolium perenne L. genotypes. Eur J Agron 22:45–54. doi:10.1016/j.eja.2003.12.002

    Article  Google Scholar 

  • Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabinski C, Bever JD, Moore JC, Wilson GWT, Klironomos JN, Umbanhowar J (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407. doi:10.1111/j.1461-0248.2009.01430.x

    Article  PubMed  Google Scholar 

  • Joy JB (2013) Symbiosis catalyses niche expansion and diversification. Proc R Soc B 280:1–7. doi:10.1098/Rspb.2012.2820

    Article  Google Scholar 

  • Kane KH (2011) Effects of endophyte infection on drought stress tolerance of Lolium perenne accessions from the Mediterranean region. Environ Exp Bot 71:337–344. doi:10.1016/j.envexpbot.2011.01.002

    Google Scholar 

  • Kannadan S, Rudgers J (2008) Endophyte symbiosis benefits a rare grass under low water availability. Funct Ecol 22:706–713

    Article  Google Scholar 

  • Kazenel MR, Debban CL, Ranelli L, Hendricks WQ, Chung YA, Pendergast TH, Charlton ND, Young CA, Rudgers JA (2015) A mutualistic endophyte alters the niche dimensions of its host plant. AoB Plants. doi:10.1093/aobpla/plv005

  • Kivlin SN, Emery SM, Rudgers JA (2013) Fungal symbionts alter plant responses to global change. Am J Bot 100:1445–1457. doi:10.3732/ajb.1200558

    Article  PubMed  Google Scholar 

  • Kozlowski TT (2012) Flooding and plant growth. Academic Press, Orlando

    Google Scholar 

  • Leuchtmann A (1992) Systematics, distribution, and host specificity of grass endophytes. Nat Toxins 1:150–162

    Article  CAS  PubMed  Google Scholar 

  • Lewis G (2004) Effects of biotic and abiotic stress on the growth of three genotypes of Lolium perenne with and without infection by the fungal endophyte Neotyphodium lolii. Ann Appl Biol 144:53–63

    Article  Google Scholar 

  • Malinowski DP, Belesky DP (1999) Neotyphodium coenophialum-endophyte infection affects the ability of tall fescue to use sparingly available phosphorus. J Plant Nutr 22:835–853. doi:10.1080/01904169909365675

    Article  CAS  Google Scholar 

  • Malinowski DP, Belesky DP (2000) Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci 40:923–940

    Article  CAS  Google Scholar 

  • Morse L, Day T, Faeth S (2002) Effect of Neotyphodium endophyte infection on growth and leaf gas exchange of Arizona fescue under contrasting water availability regimes. Environ Exp Bot 48:257–268

    Article  Google Scholar 

  • Müller C, Godfray H (1999) Predators and mutualists influence the exclusion of aphid species from natural communities. Oecologia 119:120–125

    Article  PubMed  Google Scholar 

  • Nagabhyru P, Dinkins RD, Wood CL, Bacon CW, Schardl CL (2013) Tall fescue endophyte effects on tolerance to water-deficit stress. BMC Plant Biol 13:1–17. doi:10.1186/1471-2229-13-127

    Article  Google Scholar 

  • Newsham KK (2011) A meta-analysis of plant responses to dark septate root endophytes. New Phytol 190:783–793. doi:10.1111/j.1469-8137.2010.03611.x

    Article  CAS  PubMed  Google Scholar 

  • Niones JT, Takemoto D (2014) An isolate of Epichloe festucae, an endophytic fungus of temperate grasses, has growth inhibitory activity against selected grass pathogens. J Gen Plant Pathol 80:337–347. doi:10.1007/s10327-014-0521-7

    Article  CAS  Google Scholar 

  • Oberhofer M, Güsewell S, Leuchtmann A (2014) Effects of natural hybrid and non-hybrid Epichloë endophytes on the response of Hordelymus europaeus to drought stress. New Phytol 201:242–253

    Article  PubMed  Google Scholar 

  • Orchard S, Standish RJ, Nicol D, Gupta VVSR, Ryan MH (2016) The response of fine root endophyte (Glomus tenue) to waterlogging is dependent on host plant species and soil type. Plant Soil 403:305–315. doi:10.1007/s11104-016-2804-6

    Article  CAS  Google Scholar 

  • Rahman M, Saiga S (2005) Endophytic fungi (Neotyphodium coenophialum) affect the growth and mineral uptake, transport and efficiency ratios in tall fescue (Festuca arundinacea). Plant Soil 272:163–171

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Reddy KR, Patrick WH, Broadbent FE (1984) Nitrogen transformations and loss in flooded soils and sediments. CRC Crit Rev Environ Control 13:273–309. doi:10.1080/10643388409381709

    Article  CAS  Google Scholar 

  • Ren A, Wei M, Yin L, Wu L, Zhou Y, Li X, Gao Y (2014) Benefits of a fungal endophyte in Leymus chinensis depend more on water than on nutrient availability. Environ Exp Bot 108:71–78

    Article  CAS  Google Scholar 

  • Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim YO, Redman RS (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2:404–416. doi:10.1038/ismej.2007.106

    Article  PubMed  Google Scholar 

  • Rodriguez RJ, White JF, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330. doi:10.1111/j.1469-8137.2009.02773.x

    Article  CAS  PubMed  Google Scholar 

  • Rudgers JA, Swafford AL (2009) Benefits of a fungal endophyte in Elymus virginicus decline under drought stress. Basic Appl Ecol 10:43–51

    Article  Google Scholar 

  • Rudgers JA, Miller TEX, Ziegler SM, Craven KD (2012) There are many ways to be a mutualist: endophytic fungus reduces plant survival but increases population growth. Ecology 93:565–574

    Article  PubMed  Google Scholar 

  • Saona NM, Albrectsen BR, Ericson L, Bazely DR (2010) Environmental stresses mediate endophyte–grass interactions in a boreal archipelago. J Ecol 98:470–479

    Article  Google Scholar 

  • Schardl CL (2010) The epichloae, symbionts of the grass subfamily Poöideae. Ann Mo Bot Gard 97:646–665

    Article  Google Scholar 

  • Schardl CL, Grossman RB, Nagabhyru P, Faulkner JR, Mallik UP (2007) Loline alkaloids: currencies of mutualism. Phytochemistry 68:980–996. doi:10.1016/j.phytochem.2007.01.010

    Article  CAS  PubMed  Google Scholar 

  • Schardl CL, Florea S, Pan J, Nagabhyru P, Bec S, Calie PJ (2013) The epichloae: alkaloid diversity and roles in symbiosis with grasses. Curr Opin Plant Biol 16:480–488. doi:10.1016/j.pbi.2013.06.012

    Article  CAS  PubMed  Google Scholar 

  • Song M, Li X, Saikkonen K, Li C, Nan Z (2015) An asexual Epichloë endophyte enhances waterlogging tolerance of Hordeum brevisubulatum. Fungal Ecol 13:44–52

    Article  Google Scholar 

  • Soreng RJ, Bull RD, Gillespie LJ (2010) Phylogeny and reticulation in Poa based on plastid trnTLF and nrITS sequences with attention to diploids. In: Seberg O, Petersen G, Barfod A, Davis JI (eds) Diversity, phylogeny, and evolution in the monocotyledons. Aarhus University Press, Denmark

    Google Scholar 

  • Tanaka A, Tapper BA, Popay A, Parker EJ, Scott B (2005) A symbiosis expressed non-ribosomal peptide synthetase from a mutualistic fungal endophyte of perennial ryegrass confers protection to the symbiotum from insect herbivory. Mol Microbiol 57:1036–1050

    Article  CAS  PubMed  Google Scholar 

  • Tikvic I, Seletkovic Z, Ugarkovic D, Rosavec R (2007) Growth of pedunculate oak seedlings inoculated with ectomycorrhiza Laccaria bicolor in excessively humid substrate conditions. Period Biol 109:47–53

    Google Scholar 

  • Torres MS, White JF Jr, Zhang X, Hinton DM, Bacon CW (2012) Endophyte-mediated adjustments in host morphology and physiology and effects on host fitness traits in grasses. Fungal Ecol 5:322–330. doi:10.1016/j.funeco.2011.05.006

    Article  Google Scholar 

  • Tuo X-Q, Li S, Wu Q-S, Zou Y-N (2015) Alleviation of waterlogged stress in peach seedlings inoculated with Funneliformis mosseae: changes in chlorophyll and proline metabolism. Sci Hortic 197:130–134. doi:10.1016/j.scienta.2015.09.022

    Article  CAS  Google Scholar 

  • Van der Putten WH (2012) Climate change, aboveground-belowground interactions, and species’ range shifts. Annu Rev Ecol Evol Syst 43:365–383. doi:10.1146/annurev-ecolsys-110411-160423

    Article  Google Scholar 

  • Worchel ER, Giauque HE, Kivlin SN (2013) Fungal symbionts alter plant drought response. Microb Ecol 65:671–678. doi:10.1007/s00248-012-0151-6

    Article  CAS  PubMed  Google Scholar 

  • Wu Q-S, Zou Y-N, Huang Y-M (2013) The arbuscular mycorrhizal fungus Diversispora spurca ameliorates effects of waterlogging on growth, root system architecture, and antioxidant enzyme activities of citrus seedlings. Fungal Ecol 6:37–43. doi:10.1016/j.funeco.2012.09.002

    Article  Google Scholar 

  • Zhang Y-P, Nan Z-B (2007) Growth and antioxidative systems changes in Elymus dahuricus is affected by Neotyphodium endophyte under contrasting water availability. J Agron Crop Sci 193:377–386. doi:10.1155/2014/923610

    Article  CAS  Google Scholar 

  • Zhang X-X, Li C-J, Nan Z-B (2011) Effects of salt and drought stress on alkaloid production in endophyte-infected drunken horse grass (Achnatherum inebrians). Biochem Syst Ecol 39:471–476. doi:10.1016/j.bse.2011.06.016

    Article  Google Scholar 

  • Zou YN, Srivastava AK, Wu QS, Huang YM (2014) Increased tolerance of trifoliate orange (Poncirus trifoliata) seedlings to waterlogging after inoculation with arbuscular mycorrhizal fungi. J Anim Plant Sci 24:1415–1420

    Google Scholar 

Download references

Acknowledgements

We thank Joy Avritt and Bethany Haley for assisting with plant care and harvesting. Funding was provided by the University of New Mexico, National Science Foundation DEB#1354972 and #1145588 to JAR, and the Rocky Mountain Biological Laboratory (National Science Foundation Grants DBI-0753774 and OIA-0963529).

Author information

Authors and Affiliations

  1. Department of Biology, University of New Mexico, Albuquerque, NM, 87131, USA

    Amy E. Adams, Melanie R. Kazenel & Jennifer A. Rudgers

  2. Department of Biology, University of Oklahoma, Norman, OK, 73019, USA

    Amy E. Adams

Authors
  1. Amy E. Adams
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Melanie R. Kazenel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jennifer A. Rudgers
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jennifer A. Rudgers.

Additional information

Communicated by Peter Minchin.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 15 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Adams, A.E., Kazenel, M.R. & Rudgers, J.A. Does a foliar endophyte improve plant fitness under flooding?. Plant Ecol 218, 711–723 (2017). https://doi.org/10.1007/s11258-017-0723-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11258-017-0723-0

Keywords

Search

Navigation