Co-occurring patterns of endophyte infection and genetic structure in the alpine grass, Festuca eskia: implications for seed sourcing in ecological restoration

Gonzalo-Turpin, H.; Barre, P.; Gibert, A.; Grisard, A.; West, C. P.; Hazard, L.

doi:10.1007/s10592-009-9927-8

Research Article
Published: 28 April 2009

Co-occurring patterns of endophyte infection and genetic structure in the alpine grass, Festuca eskia: implications for seed sourcing in ecological restoration

H. Gonzalo-Turpin¹,
P. Barre²,
A. Gibert¹,
A. Grisard¹,
C. P. West³ &
L. Hazard¹

Conservation Genetics volume 11, pages 877–887 (2010)Cite this article

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Abstract

Choosing the provenance of seed used in ecological restoration could entail its success. An alternative approach to examine local adaptation in seed sourcing is the assessment of genetic structure and diversity based on molecular markers. These types of analyses focus on the genetics of the target plant itself and eliminate the genetic influence of associated organisms, such as Epichloë/Neotyphodium endophytes in grasses. By impacting the fitness of their host, such symbionts may influence population genetic structure and diversity. Therefore, seed sourcing for grasses must consider the influence of their endophytes to increase seed translocation success and minimize the risks associated with this practice. To delineate seed zones for restoration of the alpine fescue Festuca eskia Ramond ex. DC. (Poaceae), we assessed population genetic differentiation and diversity patterns in the species including endophyte occurrence along altitudinal and longitudinal gradients in the Pyrenees Mountains. Twenty-three populations were analysed for endophyte status, and three STS and one SSR marker were used to examine genetic differentiation and diversity patterns. Results showed that F. eskia hosts an asexual form of Epichloë and infection frequency within populations decreased from East to West (100 vs. 8–25%). Molecular markers separated F. eskia into two East and West groups, and endophyte infection and genetic patterns were congruent with molecular data. Little evidence for genetic differentiation or difference in endophyte occurrence associated with altitude was detected. Little variation was found in within population diversity, regardless of provenance altitude and site, and/or endophyte infection frequency. The results of this study suggested the establishment of two distinct management units for F. eskia seed sourcing restoration.

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References

Baudière A, Geslot A, Chiglione C et al (1973) La pelouse à Festuca eskia en Pyrénées centrales et orientales: esquisse taxinomique et écologique. Acta Biol Acad Sci Hung 19:23–35
Google Scholar
Belkhir K, Borsa P, Chikhi L (2001) GENETIX 4.03, logiciel sous Windows™ pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université Montpellier II, Montpellier
Google Scholar
Bottin L, Verhaegen D, Tassin J et al (2005) Genetic diversity and population structure of an insular tree, Santalum austrocaledonicum in New Caledonian archipelago. Mol Ecol 14:1979–1989. doi:10.1111/j.1365-294X.2005.02576.x
Article CAS PubMed Google Scholar
Byars SG, Papst W, Hoffmann AA (2007) Local adaptation and cogradient selection in the alpine plant, Poa hiemata, along a narrow altitudinal gradient. Evol Int J Org Evol 61:2925–2941. doi:10.1111/j.1558-5646.2007.00248.x
Google Scholar
Cavalli-Sforza L, Edwards A (1967) Phylogenetic analysis: models and estimation procedures. Evol Int J Org Evol 32:550–570. doi:10.2307/2406616
Google Scholar
Cheplick GP (2007) Costs of endophyte infection in Lolium perenne genotypes from Eurasia and North Africa under extreme resource limitation. Environ Exp Bot 60:202–210. doi:10.1016/j.envexpbot.2006.10.001
Article Google Scholar
Clay K, Holah J (1999) Fungal endophyte symbiosis and plant diversity in successional fields. Science 285:1742. doi:10.1126/science.285.5434.1742
Article CAS PubMed Google Scholar
Craven KD, Hsiau PTW, Leuchtmann A et al (2001) Multigene phylogeny of Epichloë species, fungal symbionts of grasses. Ann Mo Bot Gard 88:14–34. doi:10.2307/2666129
Article Google Scholar
El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theor Appl Genet 92:832–839. doi:10.1007/BF00221895
Article Google Scholar
Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50
CAS PubMed Google Scholar
Faeth SH, Fagan WF (2002) Fungal endophytes: common host plant symbionts but uncommon mutualists. Integr Comp Biol 42:360–368. doi:10.1093/icb/42.2.360
Article Google Scholar
Felsenstein J (1993) PHYLIP: phylogenetic inference package. University of Washington, Seattle
Google Scholar
Goudet J (1995) FSTAT: a computer program to calculate F-statistics. J Hered 6:1123–1132
Google Scholar
Hiatt EE, Hill NS, Bouton JH et al (1999) Tall fescue endophyte detection: commercial immunoblot test kit compared with microscopic analysis. Crop Sci 39:796–799
Google Scholar
Hufford KM, Mazer S (2003) Plant ecotypes: genetic differentiation in the age of ecological restoration. Trends Ecol Evol 18:147–155. doi:10.1016/S0169-5347(03)00002-8
Article Google Scholar
Iwata H, Kamijo T, Tsumura Y (2006) Assessment of genetic diversity of native species in Izu Islands for a discriminate choice of source populations: implications for revegetation of volcanically devastated sites. Conserv Genet 7:399–413. doi:10.1007/s10592-005-9050-4
Article Google Scholar
Jensen LB, Muylle H, Arens P et al (2005) Development and mapping of a public reference set of SSR markers in Lolium perenne L. Mol Ecol Notes 5:951–957. doi:10.1111/j.1471-8286.2005.01043.x
Article CAS Google Scholar
Jones ES, Dupal MP, Kollier R, Drayton MC, Forster JW (2001) Development and characterization of simple sequence repeat (SSR) markers for perennial ryegrass (Lolium perenne L.). Theor Appl Genet 102:405–415
Article CAS Google Scholar
Keller M, Kollman J, Edwards PJ (2000) Genetic introgression from distant provenances reduces fitness in local weed populations. J Appl Ecol 37:647–659. doi:10.1046/j.1365-2664.2000.00517.x
Article Google Scholar
Knapp EE, Rice KJ (1996) Genetic structure and gene flow in Elymus glaucus (blue wildrye): implications for native grassland restoration. Restor Ecol 4:1–10. doi:10.1111/j.1526-100X.1996.tb00101.x
Article Google Scholar
Koh S, Hik D (2007) Herbivory mediates grass–endophyte relationships. Ecology 88:2752–2757. doi:10.1890/06-1958.1
Article PubMed Google Scholar
Körner C (2007) The use of ‘altitude’ in ecological research. Trends Ecol Evol 22:569–574. doi:10.1016/j.tree.2007.09.006
Article PubMed Google Scholar
Kubik C, Sawkins M, Meyer WA, Gaut BS (2001) Genetic diversity in seven perennial ryegrass (Lolium perenne L.) cultivars based on SSR markers. Crop Sci 41(5):1565–1572
CAS Google Scholar
Lauvergeat V, Barre P, Bonnet M et al (2005) Sixty simple sequence repeat markers for use in the Festuca–Lolium complex of grasses. Mol Ecol Notes 5:401–405. doi:10.1111/j.1471-8286.2005.00941.x
Article CAS Google Scholar
Lem P, Lallemand J (2003) Grass consensus STS markers: an efficient approach for detecting polymorphism in Lolium. Theor Appl Genet 107:1113–1122. doi:10.1007/s00122-003-1308-y
Article CAS PubMed Google Scholar
Lesica P, Allendorf FW (1999) Ecological genetics and restoration of plant communities: mix or match? Restor Ecol 7:42–50. doi:10.1046/j.1526-100X.1999.07105.x
Article Google Scholar
Leuchtmann A (1992) Systematics, distribution and host specificity of grass endophytes. Nat Toxins 1:185–204
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. doi:10.2307/3760595
Article Google Scholar
Leyronas C, Raynal G (2001) Presence of Neotyphodium-like endophytes in European grasses. Ann Appl Biol 139:119–127. doi:10.1111/j.1744-7348.2001.tb00136.x
Article 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 40:929–940
Article Google Scholar
Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220
CAS PubMed Google Scholar
Meijer G, Leuchtmann A (2001) Fungal genotype controls mutualism and sex in Brachypodium sylvaticum infected by Epichloe sylvatica. Acta Biol Hung 52:249–263. doi:10.1556/ABiol.52.2001.2-3.9
Article CAS PubMed Google Scholar
Météorologie Nationale Bessemoulin J (1989) Atlas Climatique de la France. Imprimerie de la Météorologie Nationale, Paris
Google Scholar
Montalvo A, Ellstrand NC (2001) Nonlocal transplantation and outbreeding depression in the subshrub Lotus scoparius (Fabaceae). Am J Bot 88:258–269. doi:10.2307/2657017
Article PubMed Google Scholar
Montalvo A, Williams SL, Rice KJ et al (1997) Restoration biology: a population biology perspective. Restor Ecol 5:277–290. doi:10.1046/j.1526-100X.1997.00542.x
Article Google Scholar
Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590
PubMed CAS Google Scholar
Nieberding CM, Olivieri I (2007) Parasites: proxies for host genealogy and ecology? Trends Ecol Evol 22:156–165. doi:10.1016/j.tree.2006.11.012
Article PubMed Google Scholar
Page RDM (1996) Treeview: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358
CAS PubMed Google Scholar
Raymond M, Rousset F (1995) Genepop (version-1.2)—population-genetics software for exact tests and ecumenicism. J Hered 86:248–249
Google Scholar
Rice W (1989) Analysing tables of statistical tests. Evol Int J Org Evol 43:223–225. doi:10.2307/2409177
Google Scholar
Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228
CAS PubMed Google Scholar
Sachs JL, Simms EL (2006) Pathways to mutualism breakdown. Trends Ecol Evol 21:585–592. doi:10.1016/j.tree.2006.06.018
Article PubMed Google Scholar
Saikkonen K, Faeth SH, Helander M et al (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343. doi:10.1146/annurev.ecolsys.29.1.319
Article Google Scholar
Saikkonen K, Wali P, Helander M et al (2004) Evolution of endophyte-plant symbioses. Trends Plant Sci 9:275–280. doi:10.1016/j.tplants.2004.04.005
Article CAS PubMed Google Scholar
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
CAS PubMed Google Scholar
Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 55:315–340. doi:10.1146/annurev.arplant.55.031903.141735
Article CAS PubMed Google Scholar
Schonswetter P, Stehlik I, Holderegger R et al (2005) Molecular evidence for glacial refugia of mountain plants in the European Alps. Mol Ecol 14:3547–3555. doi:10.1111/j.1365-294X.2005.02683.x
Article CAS PubMed Google Scholar
Segarra-Moragues JG, Palop-Esteban M, Gonzalez-Candelas F et al (2007) Nunatak survival vs. tabula rasa in the Central Pyrenees: a study on the endemic plant species Borderea pyrenaica (Dioscoreaceae). J Biogeogr 34:1893–1906. doi:10.1111/j.1365-2699.2007.01740.x
Article Google Scholar
Sullivan TJ, Faeth H (2004) Gene flow in the endophyte Neotyphodium and implications for coevolution with Festuca arizonica. Mol Ecol 13(3):649–656. doi:10.1046/j.1365-294X.2004.02091.x
Article CAS PubMed Google Scholar
Thompson JN (1994) The coevolutionary process. University of Chicago press, Chicago
Google Scholar
Torrecilla P, Catalan P (2002) Phylogeny of broad-leaved and fine-leaved Festuca lineage (Poaceae) based on nuclear ITS sequences. Syst Bot 27:241–251
Google Scholar
Turner B, Cairns AJ, Armstead IP et al (2006) Dissecting the regulation of fructan metabolism in perennial ryegrass (Lolium perenne) with locus mapping. New Phytol 169:45–58. doi:10.1111/j.1469-8137.2005.01575.x
Article CAS PubMed Google Scholar
Vargas P (2003) Molecular evidence for multiple diversification patterns of alpine plants in Mediterranean Europe. Taxon 52:463–476. doi:10.2307/3647446
Article Google Scholar
Weir B, Cockerham C (1984) Estimating F-statistics for the analysis of population structure. Evol Int J Org Evol 38:1358–1370. doi:10.2307/2408641
Google Scholar
Wesche K, Hensen I, Undrakh R (2006) Genetic structure of Galitzkya macrocarpa and G. potaninii, two closely related endemics of central Asian Mountains Ranges. Ann Bot (Lond) 98:1025–1034. doi:10.1093/aob/mcl182
Article CAS Google Scholar
Williams SL (2001) Reduced genetic diversity in eelgrass transplantations affects both population growth and individual fitness. Ecol Appl 11:1472–1488. doi:10.1890/1051-0761(2001)011[1472:RGDIET]2.0.CO;2
Article Google Scholar
Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354
Google Scholar
Zhao QF, Wang GAN, Li QX et al (2006) Genetic diversity of five Kobresia species along the eastern Qinghai–Tibet plateau in China. Hereditas 143:33–40. doi:10.1111/j.2006.0018-0661.01924.x
Article PubMed Google Scholar

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Acknowledgments

We would like to thank A. Leuchtmann for examining F. eskia endophyte, P. Laurent who collected samples and conducted endophyte laboratory work, P. Cormenier, C. Gibelin and C. Talon for the genetic laboratory work, I. Till-Bottraud for helpful comments on the manuscript and, A. Ashworth for improving the English text. These results are part of H.G.-T. PhD thesis. This work was funded by Ecovars2 project and INRA-SAD. Ecovars2 is funded by The European Union, the French state and Régions Midi-Pyrénées, Aquitaine and Languedoc-Roussillon.

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Authors and Affiliations

INRA, UMR 1248 AGIR, BP 52627, 31326, Castanet-Tolosan cedex, France
H. Gonzalo-Turpin, A. Gibert, A. Grisard & L. Hazard
INRA, UR GAPF, Route de Saintes, BP 6, 86600, Lusignan, France
P. Barre
University of Arkansas, 1366 W. Altheimer Drive, Fayetteville, AR, 72704-6898, USA
C. P. West

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H. Gonzalo-Turpin
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P. Barre
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A. Gibert
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A. Grisard
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C. P. West
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L. Hazard
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Correspondence to L. Hazard.

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Gonzalo-Turpin, H., Barre, P., Gibert, A. et al. Co-occurring patterns of endophyte infection and genetic structure in the alpine grass, Festuca eskia: implications for seed sourcing in ecological restoration. Conserv Genet 11, 877–887 (2010). https://doi.org/10.1007/s10592-009-9927-8

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Received: 11 March 2008
Accepted: 06 April 2009
Published: 28 April 2009
Issue Date: June 2010
DOI: https://doi.org/10.1007/s10592-009-9927-8

Keywords

Epichloë
Endophyte
Festuca eskia
Population genetic structure
Gene flow
STS
SSR
Restoration
Seed sourcing