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Fungal endophyte mediated occurrence of seminiferous and pseudoviviparous panicles in Festuca rubra

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Abstract

Fungal endophytes are suggested to manipulate host grass reproduction. Using different grass-endophyte combinations in a four year common garden experiment, we show that endophyte can retain control over the reproductive functions of the host. Plants were collected as seeds from two different environments, meadows and riverbanks. Natural endophyte infection (E+) increased reproductive effort of plants; 13 and 15 % higher proportion of E+ plants produced panicles compared to naturally uninfected (E-) and manipulatively endophyte-infected (ME+) plants, respectively. Meadow-origin E+ plants produced also higher number of panicles compared to E- in the last two years, and both meadow- and riverbank-origin ME+ plants produced higher number of panicles compared to ME- plants in most of the years. Pseudovivipary was recorded in 5 % of the plants each year. Pollen limitation appears not to induce pseudovivipary. Both E+ and ME+ plants produced higher number of seminiferous panicles compared to E- and ME- plants. The higher proportion of pseudoviviparism in ME+ plants compared to E+, E- and ME- plants from meadows suggests specific genotype-genotype cross-talk between endophyte and grass. Pseudovivipary was affected by year and primarily explained by plant reproductive effort since most vigorous plants produced more pseudoviviparous panicles. We propose that endophytes can promote host grass reproduction in a habitat-specific manner and depending on genetic compatibility between partners. However, reproductive behavior depended on maternal habitat and the annual environmental conditions highlighting the importance of long-term experiments to estimate the effects of endophytes on host plant ecology.

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References

  • Ahlholm JU, Helander M, Lehtimäki S, Wäli P, Saikkonen K (2002) Vertically transmitted fungal endophytes: different responses of host-parasite systems to environmental conditions. Oikos 99:173–183

    Article  Google Scholar 

  • Aiken SG, Lefkovitch LP, Darbyshire SJ, Armstrong KC (1988) Vegetative proliferation in inflorescences of red fescue (Festuca rubra s.l, Poaceae). Can J Bot 66(1):1–10

    Article  Google Scholar 

  • Barton C (2012) MuMIn: Multi-model inference.

  • Bates D, Maechler M, Bolker B (2011) lme4: Linear mixed-effects models using s4 classes.

  • Bazely DR, Ball JP, Vicari M, Tanentzap AJ, Bérenger M, Rakocevic T, Koh S (2007) Broad-scale geographic patterns in the distribution of vertically-transmitted, asexual endophytes in four naturally-occurring grasses in Sweden. Ecography 30:367–374

    Article  Google Scholar 

  • Beetle AA (1980) Vivipary, proliferation, and phyllody in grasses. J Range Manag 33(4):256–261

    Article  Google Scholar 

  • Brochmann C, Brysting AK, Alasos IG, Borgen L, Grundt HH, Scheen A-C, Elven R (2004) Polyploidy in arctic plants. Biol J Linn Soc 82:521–536

    Article  Google Scholar 

  • Burnham KP, Anderson DR, Huyvaert KP (2011) AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol 65:23–35

    Article  Google Scholar 

  • Chiurugwi T, Beaumont MA, Wilkinson MJ, Battey NH (2011) Adaptive divergence and speciation among sexual and pseudoviviparous populations of Festuca. Heredity 106:854–861

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Clay K (1986) Induced vivipary in the sedge Cyperus virens and the transmission of the fungus Balansia cyperi (Clavicipitaceae). Can J Bot 64:2984–2988

    Article  Google Scholar 

  • Clay K, Schardl CL (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160:S99–S127

    Article  PubMed  Google Scholar 

  • Dirihan S, Terho P, Helander M, Saikkonen K (2013) Efficient analysis of ploidy levels in plant evolutionary ecology. Caryologia. Int J Cytol Cytosystematics and Cytogenetics 66(3):251–256

    Google Scholar 

  • Elmqvist T, Cox PA (1996) The evolution of vivipary in flowering plants. Oikos 77(1):3–9

    Article  Google Scholar 

  • Faeth SH, Sullivan TJ (2003) Mutualistic, asexual endophytes in a native grass are usually parasitic. Am Nat 161:310–325

    Article  PubMed  Google Scholar 

  • Faeth SH (2002) Are endophytic fungi generally plant mutualists? Oikos 98:25–36

    Article  Google Scholar 

  • Gorischek AM, Afkhami ME, Seifert EK, Rudgers JA (2013) Fungal symbionts as manipulators of plant reproductive biology. Am Nat 181:562–570

    Article  PubMed  Google Scholar 

  • Granath G, Vicari M, Bazely DR, Ball JP, Puentes A, Rakocevic T (2007) Variation in the abundance of fungal endophytes in fescue grasses along altitudinal and grazing gradients. Ecography 30:422–430

    Article  Google Scholar 

  • Gundel PE, Omacini M, Sadras VO, Ghersa CM (2010) The interplay between the effectiveness of the grass-endophyte mutualism and the genetic variability of the host plant in an agronomic context. Evol Appl 3(5–6):538–546

    Article  PubMed Central  Google Scholar 

  • Gundel PE, Zabalgogeazcoa I, Vázquez de Aldana BR (2011) Interaction between plant genotype and the symbiosis with Epichloë fungal endophytes in seeds of red fescue (Festuca rubra). Crop and Pasture Sci 62:1010–1016

    Article  CAS  Google Scholar 

  • Gundel PE, Helander M, Casas C, Hamilton CE, Faeth SH, Saikkonen K (2013a) Neotyphodium fungal endophyte in tall fescue (Schedonorus phoenix): A comparison of three Northern European wild populations and the cultivar Kentucky-31. Fungal Divers 60(1):15–24

    Article  Google Scholar 

  • Gundel PE, Garibaldi LA, Helander M, Saikkonen K (2013b) Symbiotic interactions as drivers of trade-offs in plants: effects of fungal endophytes on tall fescue. Fungal Divers 60(1):5–14

    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

    Article  Google Scholar 

  • Harberd DJ (1961) Observations on population structure and longevity of Festuca rubra L. New Phytol 60:184–192

    Article  Google Scholar 

  • Harmer R, Lee JA (1978a) The growth and nutrient content of Festuca vivipara (L.) SM. Plantlets. New Phytol 80(1):99–106

    Article  CAS  Google Scholar 

  • Harmer R, Lee JA (1978b) The germination and viability of Festuca vivipara (L.) SM. Plantlets. New Phytol 81:745–751

    Article  Google Scholar 

  • Harper JL (1977) Population biology of plants. Academic, London

    Google Scholar 

  • Heide OM (1988) Environmental modification of flowering and viviparous proliferation in Festuca vivipara and F. ovina. Oikos 51(2):171–178

    Article  Google Scholar 

  • Heide OM (1989) Control of fowering and viviparous proliferation in seminiferous and viviparous Arctic populations of two Poa species. Arct Alp Res 21(3):305–315

    Article  Google Scholar 

  • Heide OM (1990) Primary and secondary induction requirements for flowering of Festuca rubra. Physiol Plant 79(1):51–56

    Article  Google Scholar 

  • Heide OM (1994) Control of flowering and reproduction in temperate grasses. New Phytol 128(2):347–362

    Article  CAS  Google Scholar 

  • Huff DR, Palazzo AJ (1998) Fine fescue species determination by laser flow cytometry. Crop Sci 38:445–450

    Article  Google Scholar 

  • Jauhar PP (1993) Cytogenetics of the Festuca-Lolium complex. Relevance to breeding. In: Frankel R, Grossman M, Maliga P (eds.), Monograph on Theoretical and Applied Genetics, vol. 18. Springer–Verlag, Berlin.

  • Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108

    Article  PubMed  Google Scholar 

  • Leuchtmann A, Schardl CL, Siegel MR (1994) Sexual compatibility and taxonomy of a new species of Epichloë symbiotic with fine fescue grasses. Mycologia 86:802–812

    Article  Google Scholar 

  • Latch GCM, Christensen MJ (1985) Artificial infection of grasses with endophytes. Ann Appl Biol 107:17–24

    Article  Google Scholar 

  • Lee JA, Harmer R (1980) Vivipary, a reproductive strategy in response to environmental stress? Oikos 35(2):254–265

    Article  Google Scholar 

  • Molau U (1993) Relationships between flowering phenology and life history strategies in Tundra plants. Arct Alp Res 25(4):391–402

    Article  Google Scholar 

  • Moore DM, Doggett MC (1976) Pseudo-vivipary in Fuegian and Falkland islands grasses. Brit Antarct Surv Bull 43:103–110

    Google Scholar 

  • Mosseau TA, Fox CW (eds) (1998) Maternal effects as adaptations. Oxford Univ. Press, New York, p 369

    Google Scholar 

  • Obeso JR (2002) The costs of reproduction in plants. New Phytol 155:321–348

    Article  Google Scholar 

  • Pierce S, Stirling CM, Baxter R (2003) Pseudoviviparous reproduction of Poa alpina var. vivipara L. (Poaceae) during long‐term exposure to elevated atmospheric CO2. Ann Bot 91(6):613–622

    Article  PubMed  Google Scholar 

  • Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012) Biomass allocation to leaves, stems and roots: meta analyses of interspecific variation and environmental control. New Phytol 193(1):30–50

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team. 2011. R: A language and environment for statistical computing.

  • Richards SA (2005) Testing ecological theory using the information-theoretic approach: examples and cautionary results. Ecology 86:2805–2814

    Article  Google Scholar 

  • Saha DC, Jackson MA, Johonson-Cicalese JM (1988) A rapid staining method for detection of endophytic fungi in turf and forage grasses. Phytopathology 78:237–239

    Article  CAS  Google Scholar 

  • Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Evol Syst 29:319–343

    Article  Google Scholar 

  • Saikkonen K, Ahlholm J, Helander M, Lehtimäki S, Niemeläinen O (2000) Endophytic fungi in wild and cultivated grasses in Finland. Ecography 23:360–366

    Article  Google Scholar 

  • Saikkonen K, Ion D, Gyllenberg M (2002) The persistence of vertically transmitted fungi in grass metapopulations. Proc R Soc B 269:1397–1403

    Article  PubMed Central  PubMed  Google Scholar 

  • Saikkonen K, Wäli P, Helander M, Faeth SH (2004) Evolution of endophyte–plant symbioses. Trends Plant Sci 9(6):275–280

    Article  CAS  PubMed  Google Scholar 

  • Saikkonen K, Wäli PR, Helander M (2010) Genetic compatibility determines endophyte-grass combinations. PLoS ONE 5:e11395. doi:10.1371/journal.pone.0011395

    Article  PubMed Central  PubMed  Google Scholar 

  • Saikkonen K, Ruokolainen K, Huitu O, Gundel PE, Piltti T, Hamilton CE, Helander M (2013a) Fungal endophytes help prevent weed invasions. Agric Ecosyst Environ 165(15):1–5

    Article  Google Scholar 

  • Saikkonen K, Gundel PE, Helander M (2013b) Chemical ecology mediated by fungal endophytes in grasses. J Chem Ecol 39:962–968

    Article  CAS  PubMed  Google Scholar 

  • Sarapul’tsev IE (2001) The phenomenon of pseudoviviparity in alpine and arctomontane grasses (deschampsia beauv., Festuca L., and Poa L.). Russ J Ecol 32(3):170–178

    Article  Google Scholar 

  • Schardl CL (2001) Epichloë festucae and related mutualistic symbionts of grasses. Fungal Genet Biol 33:69–82

    Article  CAS  PubMed  Google Scholar 

  • Tadych M, Ambrose KV, Bergen MS, Belanger FC, White JF Jr (2012) Taxonomic placement of Epichloë poae sp. nov. and horizontal dissemination to seedlings via conidia. Fungal Divers 54(1):117–131

    Article  Google Scholar 

  • Tredway LP, White JF Jr, Gaut BS, Reddy PV, Richardson MD, Clarke BB (1999) Phylogenetic relationships within and between Epichloë and Neotyphodium endophytes as estimated by AFLP markers and rDNA sequences. Mycol Res 103(12):1593–1603

    Article  CAS  Google Scholar 

  • Tuomi J, Hakala T, Haukioja E (1983) Alternative concepts of reproductive effort, cost of reproduction, and selection in life-history evolution. Am Zool 23:25–34

    Google Scholar 

  • Vega AS, Rúgolo de Agrasar ZE (2006) Vivipary and pseudovivipary in the Poaceae, including the first record of pseudovivipary in digitaria (panicoideae: paniceae). S Afr J Bot 72:559–564

    Article  Google Scholar 

  • Vila-Aiub MM, Gundel PE, Ghersa CM (2005) Fungal endophyte infection changes growth attributes in Lolium multiflorum Lam. Aust Ecol 30:49–57

    Article  Google Scholar 

  • Wäli PR, Ahlholm JU, Helander M, Saikkonen K (2007) Occurrence and genetic structure of the systemic grass endophyte Epichloë festucae in fine fescue populations. Microb Ecol 53:20–29

    Article  PubMed  Google Scholar 

  • Wäli PR, Helander M, Nissinen O, Lehtonen P, Saikkonen K (2008) Endophyte infection, nutrient status of the soil and duration of snow cover influence the performance of meadow fescue in sub-arctic conditions. Grass Forage Sci 63:324–330

    Article  Google Scholar 

  • Williams MJ, Backman PA, Clark EM, White JF Jr (1984) Seed treatments for control of the tall fescue endophyte Acremonium coenophialum. Plant Dis 68:49–52

    Article  Google Scholar 

  • Zabalgogeazcoa I, García Ciudad A, Vázquez de Aldana B, García Criado B (2006) Effects of the infection by the fungal endophyte Epichloë festucae in the growth and nutrient content of Festuca rubra. Eur J Agron 24:374–384

    Article  CAS  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R first. Springer, New York

    Book  Google Scholar 

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Authors and Affiliations

  1. MTT Agrifood Research Finland, Department of Plant Production, Jokioinen, Finland

    P. E. Gundel & K. Saikkonen

  2. IFEVA–CONICET–Faculty of Agronomy, Buenos Aires University (UBA), Buenos Aires, Argentina

    P. E. Gundel

  3. Sede Andina, Universidad Nacional de Río Negro (UNRN) and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Mitre 630, CP 8,400, San Carlos de Bariloche, Río Negro, Argentina

    L. A. Garibaldi

  4. Department of Biology, University of Oulu, Oulu, Finland

    P. R. Wäli

  5. Section of Ecology, Department of Biology, University of Turku, Turku, Finland

    M. Helander & S. Dirihan

  6. MTT Agrifood Research Finland, Plant Production Research, 31600, Jokioinen, Finland

    P. E. Gundel

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  1. P. E. Gundel
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  2. L. A. Garibaldi
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  3. P. R. Wäli
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  4. M. Helander
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Correspondence to P. E. Gundel.

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Gundel, P.E., Garibaldi, L.A., Wäli, P.R. et al. Fungal endophyte mediated occurrence of seminiferous and pseudoviviparous panicles in Festuca rubra . Fungal Diversity 66, 69–76 (2014). https://doi.org/10.1007/s13225-014-0290-9

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