1,544
Views
5
CrossRef citations to date
0
Altmetric
Genetics/Molecular Biology

Mycelial biomass and concentration of loline alkaloids driven by complex population structure in Epichloë uncinata and meadow fescue (Schedonorus pratensis)

ORCID Icon, , ORCID Icon, , ORCID Icon & ORCID Icon
Pages 474-490 | Received 08 Aug 2019, Accepted 20 Mar 2020, Published online: 15 May 2020

LITERATURE CITED

  • Agee CS, Hill NS. 1994. Ergovaline variability in Acremonium-infected tall fescue due to environment and plant genotype. Crop Science 34:221–226, doi:10.2135/cropsci1994.0011183X003400010040x
  • Andrews S. 2016. FASTQC. A quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/
  • Ashraf BH, Byrne S, Fé D, Czaban A, Asp T, Pedersen MG, Lenk I, Roulund N, Didion T, Jensen CS, Jensen J, Janss LL. 2016. Estimating genomic heritabilities at the level of family-pool samples of perennial ryegrass using genotyping-by-sequencing. Theoretical and Applied Genetics 129:45–52, doi:10.1007/s00122-015-2607-9
  • Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, Selker EU, Cresko WA, Johnson EA. 2008. Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE 3:e3376, doi:10.1371/journal.pone.0003376
  • Baldauf MW, Mace WJ, Richmond DS. 2011. Endophyte-mediated resistance to black cutworm as a function of plant cultivar and endophyte strain in tall fescue. Environmental Entomology 40:639–647, doi:10.1603/EN09227
  • Ball OJP, Tapper BA. 1999. The production of loline alkaloids in artificial and natural grass/endophyte association. In: O’Callaghan M, ed. Proceedings of the NZ Plant Protection Conference, Auckland, New Zealand, August 9–12, 1999. The New Zealand Plant Protection Society. p. 52:264–269.
  • Barker GM, Patchett BJ, Cameron NE. 2015a. Epichloë uncinata infection and loline content protect Festulolium grasses from crickets (Orthoptera: Gryllidae). Journal of Economic Entomology 108:789–797, doi:10.1093/jee/tou058
  • Barker GM, Patchett BJ, Gillanders TJ, Brown GS, Montel SJY, Cameron NE. 2015b. Feeding and oviposition by Argentine stem weevil on Epichloë uncinata-infected, loline-containing Festulolium. New Zealand Plant Protection 68:212–217.
  • Blanco‐Pastor JL, Manel S, Barre P, Roschanski AM, Willner E, Dehmer KJ, Hegarty M, Muylle H, Ruttink T, Roldán‐Ruiz I, Ledauphin T, Escobar‐Gutiérrez A, Sampoux J. 2019. Pleistocene climate changes, and not agricultural spread, accounts for range expansion and admixture in the dominant grassland species Lolium perenne L. Journal of Biogeography 46:1451–1465, doi:10.1111/jbi.13587
  • Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics 30:2114–2120.
  • Brazauskas G, Lenk I, Greve Pedersen M, Studer B, Lübberstedt T. 2011. Genetic variation, population structure, and linkage disequilibrium in European elite germplasm of perennial ryegrass. Plant Science 181:412–420.
  • Cagnano G, Roulund N, Jensen CS, Forte FP, Asp T, Leuchtmann A. 2019. Large scale screening of Epichloë endophytes infecting Schedonorus pratensis and other forage grasses reveals a relation between microsatellite-based haplotypes and loline alkaloid levels. Frontiers in Plant Science 10:765, doi:10.3389/fpls.2019.00765
  • Catchen J, Bassham S, Wilson T, Currey M, O’Brien C, Yeates Q, Cresko WA. 2013. The population structure and recent colonization history of Oregon threespine stickleback determined using restriction-site associated DNA-sequencing. Molecular Ecology 22:2864–2883, doi:10.1111/mec.12330
  • Charlton ND, Craven KD, Mittal S, Hopkins AA, Young CA. 2012. Epichloë canadensis, a new interspecific epichloid hybrid symbiotic with Canada wildrye (Elymus canadensis). Mycologia 104:1187–1199, doi:10.3852/11-403
  • Clay K, Schardl C. 2002. Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. American Naturalist 160:99–127, doi:10.1086/342161
  • Clayton W, Eaton CJ, Dupont P-Y, Gillanders T, Cameron N, Saikia S, Scott B. 2017. Analysis of simple sequence repeat (SSR) structure and sequence within Epichloë endophyte genomes reveals impacts on gene structure and insights into ancestral hybridization events. PLoS ONE 12:e0183748, doi:10.1371/journal.pone.0183748
  • Corander J, Majander KK, Cheng L, Merilä J. 2013. High degree of cryptic population differentiation in the Baltic Sea herring Clupea harengus. Molecular Ecology 22:2931–2940, doi:10.1111/mec.12174
  • Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, McVean G, Durbin R, 1000 Genomes Project Analysis Group 1000. 2011. The variant call format and VCFtools. Bioinformatics 27: 2156–2158, doi:10.1093/bioinformatics/btr330
  • Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML. 2011. Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nature Reviews Genetics 12:499–510, doi:10.1038/nrg3012
  • Deschamps S, Llaca V, May GD. 2012. Genotyping-by-sequencing in plants. Biology 1:460–483, doi:10.3390/biology1030460
  • Ekanayake PN, Hand ML, Spangenberg GC, Forster JW, Guthridge KM. 2012. Genetic diversity and host specificity of fungal endophyte taxa in fescue pasture grasses. Crop Science 52:2243–2252, doi:10.2135/cropsci2011.12.0664
  • Ekanayake PN, Rabinovich M, Guthridge KM, Spangenberg GC, Forster JW, Sawbridge TI. 2013. Phylogenomics of fescue grass-derived fungal endophytes based on selected nuclear genes and the mitochondrial gene complement. BMC Evolutionary Biology 13:270, doi:10.1186/1471-2148-13-270
  • Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE. 2011. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6:e19379, doi:10.1371/journal.pone.0019379
  • Faville MJ, Briggs L, Cao M, Koulman A, Jahufer MZZ, Koolaard J, Hume DE. 2015. A QTL analysis of host plant effects on fungal endophyte biomass and alkaloid expression in perennial ryegrass. Molecular Breeding 35:161, doi:10.1007/s11032-015-0350-1
  • Fjellheim S, Pašakinskiené I, Grønnerød S, Paplauskiené V, Rognli OA. 2009. Genetic structure of local populations and cultivars of meadow fescue from the Nordic and Baltic regions. Crop Science 49:200–210, doi:10.2135/cropsci2007.08.0422
  • Fjellheim S, Rognli OA, Fosnes K, Brochmann C. 2006. Phylogeographical history of the widespread meadow fescue (Festuca pratensis Huds.) inferred from chloroplast DNA sequences. Journal of Biogeography 33:1470–1478, doi:10.1111/j.1365-2699.2006.01521.x
  • Freitas P. 2017. Crossing the species barrier: investigating vertical transmission of a fungal endophyte from tall fescue within a novel ryegrass association [PhD dissertation]. Lincoln, UK: University of Lincoln. 27–33.
  • Gagic M, Faville MJ, Zhang W, Forester NT, Rolston MP, Johnson RD, Ganesh S, Koolaard JP, Easton HS, Hudson D, Johnson LJ, Moon CD, Voisey CR. 2018. Seed transmission of Epichloë endophytes in Lolium perenne is heavily influenced by host genetics. Frontiers in Plant Science 9:1580, doi:10.3389/fpls.2018.01580
  • Galili T. 2015. dendextend: an R package for visualizing, adjusting and comparing trees of hierarchical clustering. Bioinformatics 31:3718–3720, doi:10.1093/bioinformatics/btv428
  • Hill NS, Belesky DP, Stringer WC. 1991. Competitiveness of tall fescue as influenced by Acremonium coenophialum. Crop Science 31:185–190, doi:10.2135/cropsci1991.0011183X003100010042x
  • Hill NS, Bouton JH, Thompson FN, Hawkins L, Hoveland CS, McCann MA. 2002. Performance of tall fescue germplasms bred for high- and low-ergot alkaloids. Crop Science 42:518–523, doi:10.2135/cropsci2002.0518
  • Johnson LJ, Bonth ACM De, Briggs LR, Caradus JR, Finch SC, Fleetwood DJ, Fletcher LR, Hume DE, Johnson RD, Popay AJ, Tapper BA, Simpson WR, Voisey CR, Card SD. 2013. The exploitation of Epichloë endophytes for agricultural benefit. Fungal Diversity 60:171–188, doi:10.1007/s13225-013-0239-4
  • Jombart T. 2008. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405, doi:10.1093/bioinformatics/btn129
  • Jombart T, Devillard S, Balloux F. 2010. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genetics 11:94, doi:10.1186/1471-2156-11-94
  • Jones JC, Fan S, Franchini P, Schartl M, Meyer A. 2013. The evolutionary history of Xiphophorus fish and their sexually selected sword: a genome-wide approach using restriction site-associated DNA sequencing. Molecular Ecology 22:2986–3001, doi:10.1111/mec.12269
  • Joshi NA, Fass JN. 2011. Sickle: a sliding-window, adaptive, quality-based trimming tool for FastQ files (Version 1.33). https://github.com/najoshi/sickle
  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Molecular Biology and Evolution 35:1547–1549, doi:10.1093/molbev/msy096
  • Kutil BL, Greenwald C, Liu G, Spiering MJ, Schardl CL, Wilkinson HH. 2007. Comparison of loline alkaloid gene clusters across fungal endophytes: predicting the co-regulatory sequence motifs and the evolutionary history. Fungal Genetics and Biology 44:1002–1010, doi:10.1016/j.fgb.2007.04.003
  • Le Cocq K, Gurr SJ, Hirsch PR, Mauchline TH. 2017. Exploitation of endophytes for sustainable agricultural intensification. Molecular Plant Pathology 18:469–473, doi:10.1111/mpp.12483
  • Lee T-H, Guo H, Wang X, Kim C, Paterson AH. 2014. SNPhylo: a pipeline to construct a phylogenetic tree from huge SNP data. BMC Genomics 15:162, doi:10.1186/1471-2164-15-162
  • Lepais O, Weir JT. 2014. SimRAD: an R package for simulation-based prediction of the number of loci expected in RADseq and similar genotyping by sequencing approaches. Molecular Ecology Resources 14:1314–1321, doi:10.1111/1755-0998.12273
  • Leuchtmann A. 1992. Systematics, distribution, and host specificity of grass endophytes. Natural Toxins 1:150–162, doi:10.1002/nt.2620010303
  • Leuchtmann A. 1994. Isozyme relationships of Acremonium endophytes from twelve Festuca species. Mycological Research 98:25–33, doi:10.1016/S0953-7562(09)80331-6
  • Leuchtmann A, Schardl CL. 1998. Mating compatibility and phylogenetic relationships among two new species of Epichloë and other congeneric European species. Mycological Research 102:1169–1182, doi:10.1017/S0953756298006236
  • 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:10.1080/00275514.1994.12026487
  • Linck E, Battey CJ. 2017. Minor allele frequency thresholds dramatically affect population structure inference with genomic datasets. Biorxiv, doi:https://doi.org/10.1101/188623
  • Lundqvist A. 2009. The nature of the two-loci incompatibility system in grasses. Hereditas 48:169–181, doi:10.1111/j.1601-5223.1962.tb01805.x
  • McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA. 2010. The genome analysis toolkit: a mapreduce framework for analyzing next-generation DNA sequencing data. Genome Research 20:1297–1303, doi:10.1101/gr.107524.110
  • Moon CD, Craven KD, Leuchtmann A, Clement SL, Schardl CL. 2004. Prevalence of interspecific hybrids amongst asexual fungal endophytes of grasses. Molecular Ecology 13:1455–1467, doi:10.1111/j.1365-294X.2004.02138.x
  • Moon CD, Guillaumin J-J, Ravel C, Li C, Craven KD, Schardl CL. 2007. New Neotyphodium endophyte species from the grass tribes Stipeae and Meliceae. Mycologia 99:895–905, doi:10.1080/15572536.2007.11832521
  • Moon CD, Tapper B, Scott B. 1999. Identification of Epichloë endophytes in planta by a microsatellite-based PCR fingerprinting assay with automated analysis. Applied and Environmental Microbiology 65:1268–1279.
  • Narum SR, Buerkle CA, Davey JW, Miller MR, Hohenlohe PA. 2013. Genotyping-by-sequencing in ecological and conservation genomics. Molecular Ecology 22:2841–2847, doi:10.1111/mec.12350
  • Pan J, Bhardwaj M, Nagabhyru P, Grossman RB, Schardl CL. 2014. Enzymes from fungal and plant origin required for chemical diversification of insecticidal loline alkaloids in grass-Epichloë symbiota. PLoS ONE 9:e115590, doi:10.1371/journal.pone.0115590
  • Panaccione DG, Beaulieu WT, Cook D. 2014. Bioactive alkaloids in vertically transmitted fungal endophytes. Functional Ecology 28:299–314, doi:10.1111/1365-2435.12076
  • Patchett BJ, Chapman RB, Fletcher LR, Gooneratne SR. 2008. Root loline concentration in endophyte-infected meadow fescue (Festuca pratensis) is increased by grass grub (Costelytra zealandica) attack. New Zealand Plant Protection 61:210–214.
  • Pembleton LW, Cogan NOI, Forster JW. 2013. StAMPP: an R package for calculation of genetic differentiation and structure of mixed-ploidy level populations. Molecular Ecology Resources 13:946–952, doi:10.1111/1755-0998.12129
  • Peterson G, Dong Y, Horbach C, Fu Y-B. 2014. Genotyping-by-sequencing for plant genetic diversity analysis: a lab guide for SNP genotyping. Diversity 6:665–680, doi:10.3390/d6040665
  • Pina‐Martins F, Baptista J, Pappas G, Paulo OS. 2019. New insights into adaptation and population structure of cork oak using genotyping by sequencing. Global Change Biology 25:337–350, doi:10.1111/gcb.14497
  • Popay AJ, Hume DE. 2011. Endophytes improve ryegrass persistence by controlling insects. Pasture Persistence—Grassland Research and Practice Series 15:149–156.
  • Rafiei V, Banihashemi Z, Jiménez-Díaz RM, Navas-Cortés JA, Landa BB, Jiménez-Gasco MM, Turgeon BG, Milgroom MG. 2018. Comparison of genotyping by sequencing and microsatellite markers for unravelling population structure in the clonal fungus Verticillium dahliae. Plant Pathology 67:76–86, doi:10.1111/ppa.12713
  • Raj A, Stephens M, Pritchard JK. 2014. fastSTRUCTURE: variational inference of population structure in large SNP data sets. Genetics 197:573–589, doi:10.1534/genetics.114.164350
  • Roylance JT, Hill NS, Agee CS. 1994. Ergovaline and peramine production in endophyte-infected tall fescue: independent regulation and effects of plant and endophyte genotype. Journal of Chemical Ecology 20:2171–2183, doi:10.1007/BF02033195
  • Saikkonen K, Wäli PR, Helander M. 2010. Genetic compatibility determines endophyte-grass combinations. PLoS ONE 5:e11395, doi:10.1371/journal.pone.0011395
  • Sawler J, Stout JM, Gardner KM, Hudson D, Vidmar J, Butler L, Page JE, Myles S. 2015. The genetic structure of marijuana and hemp. PLoS ONE 10:e0133292, doi:10.1371/journal.pone.0133292
  • 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
  • Schardl CL, Leuchtmann A, Spiering MJ. 2004. Symbioses of grasses with seedborne fungal endophytes. Annual Review of Plant Biology 55:315–340, doi:10.1146/annurev.arplant.55.031903.141735
  • Schardl CL, Leuchtmann A, Tsai HF, Collett MA, Watt DM, Scott DB. 1994. Origin of a fungal symbiont of perennial ryegrass by interspecific hybridization of a mutualist with the ryegrass choke pathogen, Epichloë typhina. Genetics 136:1307–1317.
  • Schardl CL, Young CA, Hesse U, Amyotte SG, Andreeva K, Calie PJ, Fleetwood DJ, Haws DC, Moore N, Oeser B, Panaccione DG, Schweri KK, Voisey CR, Farman ML, Jaromczyk JJW, Roe BA, O’Sullivan DM, Scott B, Tudzynski P, An Z, Arnaoudova EG, Bullock CT, Charlton ND, Chen L, Cox M, Dinkins RD, Florea S, Glenn AE, Gordon A, Güldener U, Harris DR, Hollin W, Jaromczyk J, Johnson RD, Khan AK,Leistner E, Leuchtmann A, Li C, Liu J, Liu J, Liu M, Mace W, Machado C, Nagabhyru P, Pan J, Schmid J, Sugawara K, Steiner U, Takach JE, Tanaka E, Webb JS, Wilson EV, Wiseman JL, Yoshida R, Zeng Z. 2013. Plant-symbiotic fungi as chemical engineers: multi-genome analysis of the Clavicipitaceae reveals dynamics of alkaloid loci. PLoS Genetics 9:e1003323, doi:10.1371/journal.pgen.1003323
  • Schirrmann MK, Zoller S, Croll D, Stukenbrock EH, Leuchtmann A, Fior S. 2018. Genomewide signatures of selection in Epichloë reveal candidate genes for host specialization. Molecular Ecology 27:3070–3086, doi:10.1111/mec.14585
  • Selosse M-A, Schardl CL. 2007. Fungal endophytes of grasses: hybrids rescued by vertical transmission? An evolutionary perspective. New Phytologist 173:452–458, doi:10.1111/j.1469-8137.2007.01978.x
  • Shi C, An S, Yao Z, Young CA, Panaccione DG, Lee ST, Schardl CL, Li C. 2017. Toxin-producing Epichloë bromicola strains symbiotic with the forage grass Elymus dahuricus in China. Mycologia 109:847–859, doi:10.1080/00275514.2018.1426941
  • Shoji JY, Charlton ND, Yi M, Young CA, Craven KD. 2015. Vegetative hyphal fusion and subsequent nuclear behavior in Epichloë grass endophytes. PLoS ONE 10:e0121875, doi:10.1371/journal.pone.0121875
  • Siadjeu C, Mayland-Quellhorst E, Albach DC. 2018. Genetic diversity and population structure of trifoliate yam (Dioscorea dumetorum Kunth) in Cameroon revealed by genotyping-by-sequencing (GBS). BMC Plant Biology 18:359, doi:10.1186/s12870-018-1593-x
  • Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJBirol I. 2009. ABySS: a parallel assembler for short read sequence data. Genome Research 19:1117–1123.
  • Tadych M, Bergen M, Dugan FM, White JF. 2007. Evaluation of the potential role of water in spread of conidia of the Neotyphodium endophyte of Poa ampla. Mycological Research 111:466–472, doi:10.1016/j.mycres.2007.02.002
  • Tadych M, Bergen MS, White JF. 2014. Epichloë spp. associated with grasses: new insights on life cycles, dissemination and evolution. Mycologia 106:181–201, doi:10.3852/106.2.181
  • Takach JE, Young CA. 2014. Alkaloid genotype diversity of tall fescue endophytes. Crop Science 54:667–678, doi:10.2135/cropsci2013.06.0423
  • Tredway LP, White JF, 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. Mycological Research 103:1593–1603, doi:10.1017/S0953756299008874
  • West CP, Izekor E, Turner KE, Elmi AA. 1993. Endophyte effects on growth and persistence of tall fescue along a water-supply gradient. Agronomy Journal 85:264–270, doi:10.2134/agronj1993.00021962008500020019x
  • Winter DJ, Ganley ARD, Young CA, Liachko I, Schardl CL, Dupont P-Y, Berry D, Ram A, Scott B, Cox MP. 2018. Repeat elements organise 3D genome structure and mediate transcription in the filamentous fungus Epichloë festucae. PLoS Genetics 14:e1007467, doi:10.1371/journal.pgen.1007467