Fungal endophyte infection of ryegrass reprograms host metabolism and alters development

New Phytologist

Volumn 208, Issue 4, 2015, Pages 1227-1240

  Dupont, Pierre Yves ^a   Eaton, Carla J ^a   Wargent, Jason J ^a   Fechtner, Susanne ^a   Solomon, Peter ^b   Schmid, Jan ^a   Day, Robert C ^c   Scott, Barry ^a   Cox, Murray P ^a  

^a MASSEY UNIVERSITY   (New Zealand)

^b AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^c UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Endophyte; Metabolism; Mutualism; RNAseq; Ryegrass; Symbiosis

Indexed keywords

ENDOPHYTE; FUNGUS; METABOLISM; MUTUALISM;

FUNGI; HEXAPODA; LOLIUM; LOLIUM PERENNE; POACEAE;

PLANT PROTEIN; PLANT RNA;

ADAPTATION; DROUGHT; ENDOPHYTE; EPICHLOE; GENE EXPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LOLIUM; METABOLISM; MICROBIOLOGY; NUCLEOTIDE SEQUENCE; PLANT DEVELOPMENT; PLANT GENE; SYMBIOSIS;

ADAPTATION, PHYSIOLOGICAL; BASE SEQUENCE; DROUGHTS; ENDOPHYTES; EPICHLOE; GENE EXPRESSION; GENES, PLANT; LOLIUM; PLANT DEVELOPMENT; PLANT PROTEINS; RNA, PLANT; SYMBIOSIS;

EID: 84946078956     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13614     Document Type: Article

References (75)

1. Akiyama K, Hayashi H. 2006. Strigolactones: chemical signals for fungal symbionts and parasitic weeds in plant roots. Annals of Botany 97: 925-931.
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. Journal of Molecular Biology 215: 403-410.
3. Ambrose KV, Belanger FC. 2012. SOLiD-SAGE of endophyte-infected red fescue reveals numerous effects on host transcriptome and an abundance of highly expressed fungal secreted proteins. PLoS ONE 7: e53214.
4. Andrews S. 2010. FastQC A quality control tool for high throughput sequence data. [WWW document] URL http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ [accessed 15 July 2013].
5. Arachevaleta M, Bacon CW, Hoveland CS, Radcliffe DE. 1989. Effect of the tall fescue endophyte on plant-response to environmental-stress. Agronomy Journal 81: 83-90.
6. Bilgin DD, Zavala JA, Zhu J, Clough SJ, Ort DR, DeLucia EH. 2010. Biotic stress globally downregulates photosynthesis genes. Plant, Cell & Environment 33: 1597-1613.
7. Christensen MJ, Bennett RJ, Schmid J. 2002. Growth of Epichloë/Neotyphodium and p-endophytes in leaves of Lolium and Festuca grasses. Mycological Research 106: 93-106.
8. Christensen MJ, Voisey C. 2007. The biology of the endophyte/grass partnership. In: Popay AJ, Thom ER, eds. 6th International symposium on fungal endophytes of grasses grasslands research and practice series. Christchurch, New Zealand: New Zealand Grassland Association, 123-133.
9. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
10. Cox MP, Peterson DA, Biggs PJ. 2010. SolexaQA: at-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinformatics 11: 485.
11. Davies WJ, Zhang JH. 1991. Root signals and the regulation of growth and development of plants in drying soil. Annual Review of Plant Physiology and Plant Molecular Biology 42: 55-76.
12. De Cremer K, Mathys J, Vos C, Froenicke L, Michelmore RW, Cammue BP, De Coninck B. 2013. RNAseq-based transcriptome analysis of Lactuca sativa infected by the fungal necrotroph Botrytis cinerea. Plant, Cell & Environment 36: 1992-2007.
13. Dixon RA, Paiva NL. 1995. Stress-induced phenylpropanoid metabolism. Plant Cell 7: 1085-1097.
14. Djamei A, Schipper K, Rabe F, Ghosh A, Vincon V, Kahnt J, Osorio S, Tohge T, Fernie AR, Feussner I et al. 2011. Metabolic priming by a secreted fungal effector. Nature 478: 395-398.
15. Doehlemann G, Wahl R, Horst RJ, Voll LM, Usadel B, Poree F, Stitt M, Pons-Kühnemann J, Sonnewald U, Kahmann R et al. 2008. Reprogramming a maize plant: transcriptional and metabolic changes induced by the fungal biotroph Ustilago maydis. Plant Journal 56: 181-195.
16. Eaton CJ, Cox MP, Ambrose B, Becker M, Hesse U, Schardl CL, Scott B. 2010. Disruption of signaling in a fungal-grass symbiosis leads to pathogenesis. Plant Physiology 153: 1780-1794.
17. Eaton CJ, Dupont PY, Solomon P, Clayton W, Scott B, Cox MP. 2015. A core gene set describes the molecular basis of mutualism and antagonism in Epichloë spp. Molecular Plant-Microbe Interactions 28: 218-231.
18. van Esse HP, Bolton MD, Stergiopoulos I, de Wit PJ, Thomma BP. 2007. The chitin-binding Cladosporium fulvum effector protein Avr4 is a virulence factor. Molecular Plant Microbe Interactions 20: 1092-1101.
19. Foo E, Ross JJ, Jones WT, Reid JB. 2013. Plant hormones in arbuscular mycorrhizal symbioses: an emerging role for gibberellins. Annals of Botany 111: 769-779.
20. Fu L, Niu B, Zhu Z, Wu S, Li W. 2012. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28: 3150-3152.
21. Gallagher RT, Hawkes AD, Steyn PS, Vleggaar R. 1984. Tremorgenic neurotoxins from perennial ryegrass causing ryegrass staggers disorder of livestock - structure elucidation of lolitrem-B. Journal of the Chemical Society Chemical Communications 9: 614-616.
22. Gomez SK, Javot H, Deewatthanawong P, Torres-Jerez I, Tang Y, Blancaflor EB, Udvardi MK, Harrison MJ. 2009. Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis. BMC Plant Biology 9: 10.
23. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q et al. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology 29: 644-652.
24. Guether M, Balestrini R, Hannah M, He J, Udvardi MK, Bonfante P. 2009. Genome-wide reprogramming of regulatory networks, transport, cell wall and membrane biogenesis during arbuscular mycorrhizal symbiosis in Lotus japonicus. New Phytologist 182: 200-212.
25. Güimil S, Chang HS, Zhu T, Sesma A, Osbourn A, Roux C, Ioannidis V, Oakeley EJ, Docquier M, Descombes P et al. 2005. Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proceedings of the National Academy of Sciences, USA 102: 8066-8070.
26. Hahn H, McManus MT, Warnstorff K, Monahan BJ, Young CA, Davies E, Tapper BA, Scott B. 2008. Neotyphodium fungal endophytes confer physiological protection to perennial ryegrass (Lolium perenne L.) subjected to a water deficit. Environmental and Experimental Botany 63: 183-199.
27. Halket JM, Zaikin VG. 2006. Derivatization in mass spectrometry - 7. On-line derivatisation/degradation. European Journal of Mass Spectrometry 12: 1-13.
28. Hamilton CE, Bauerle TL. 2012. A new currency for mutualism? Fungal endophytes alter antioxidant activity in hosts responding to drought. Fungal Diversity 54: 39-49.
29. Hom EF, Murray AW. 2014. Niche engineering demonstrates a latent capacity for fungal-algal mutualism. Science 345: 94-98.
30. van Hove LWA, Heeres P, Bossen ME. 2002. The annual variation in stomatal ammonia compensation point of rye grass (Lolium perenne L.) leaves in an intensively managed grassland. Atmospheric Environment 36: 2965-2977.
31. Johnson LJ, de Bonth ACM, Briggs LR, Caradus JR, Finch SC, Fleetwood DJ, Fletcher LR, Hume DE, Johnson RD, Popay AJ et al. 2013. The exploitation of epichloae endophytes for agricultural benefit. Fungal Diversity 60: 171-188.
32. de Jonge R, van Esse HP, Kombrink A, Shinya T, Desaki Y, Bours R, van der Krol S, Shibuya N, Joosten MH, Thomma BP. 2010. Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329: 953-955.
33. Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N, Takio K, Minami E, Shibuya N. 2006. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proceedings of the National Academy of Science, USA 103: 11 086-11 091.
34. Kawahara Y, Oono Y, Kanamori H, Matsumoto T, Itoh T, Minami E. 2012. Simultaneous RNA-seq analysis of a mixed transcriptome of rice and blast fungus interaction. PLoS ONE 7: e49423.
35. Koster KL, Lynch DV. 1992. Solute accumulation and compartmentation during the cold acclimation of Puma Rye. Plant Physiology 98: 108-113.
36. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology 10: R25.
37. Latch GCM, Christensen MJ. 1985. Artificial infection of grasses with endophytes. Annals of Applied Biology 107: 17-24.
38. Leuchtmann A, Bacon CW, Schardl CL, White JF Jr, Tadych M. 2014. Nomenclatural realignment of Neotyphodium species with genus Epichoë. Mycologia 106: 202-215.
39. Lohse M, Nagel A, Herter T, May P, Schroda M, Zrenner R, Tohge T, Fernie AR, Stitt M, Usadel B. 2014. Mercator: a fast and simple web server for genome scale functional annotation of plant sequence data. Plant, Cell & Environment 37: 1250-1258.
40. Lowe RGT, Lord M, Rybak K, Trengove RD, Oliver RP, Solomon PS. 2009. Trehalose biosynthesis is involved in sporulation of Stagonospora nodorum. Fungal Genetics and Biology 46: 381-389.
41. Morán-Diez E, Rubio B, Domínguez S, Hermosa R, Monte E, Nicolás C. 2012. Transcriptomic response of Arabidopsis thaliana after 24 h incubation with the biocontrol fungus Trichoderma harzianum. Journal of Plant Physiology 169: 614-620.
42. Pańka D, Piesik D, Jeske M, Baturo-Cieśniewska A. 2013a. Production of phenolics and the emission of volatile organic compounds by perennial ryegrass (Lolium perenne L.)/Neotyphodium lolii association as a response to infection by Fusarium poae. Journal of Plant Physiology 170: 1010-1019.
43. Pańka D, West CP, Guerber CA, Richardson MD. 2013b. Susceptibility of tall fescue to Rhizoctonia zeae infection as affected by endophyte symbiosis. Annals of Applied Biology 163: 257-268.
44. Pelloux J, Rustérucci C, Mellerowicz EJ. 2007. New insights into pectin methylesterase structure and function. Trends in Plant Science 12: 267-277.
45. Perazza D, Vachon G, Herzog M. 1998. Gibberellins promote trichome formation by up-regulating GLABROUS1 in Arabidopsis. Plant Physiology 117: 375-383.
46. Perazzolli M, Moretto M, Fontana P, Ferrarini A, Velasco R, Moser C, Delledonne M, Pertot I. 2012. Downy mildew resistance induced by Trichoderma harzianum T39 in susceptible grapevines partially mimics transcriptional changes of resistant genotypes. BMC Genomics 13: 660.
47. Plett JM, Kemppainen M, Kale SD, Kohler A, Legué V, Brun A, Tyler BM, Pardo AG, Martin F. 2011. A secreted effector protein of Laccaria bicolor is required for symbiosis development. Current Biology 21: 1197-1203.
48. Plett JM, Tisserant E, Brun A, Morin E, Grigoriev IV, Kuo A, Martin F, Kohler A. 2015. The mutualist Laccaria bicolor expresses a core gene regulon during the colonization of diverse host plants and a variable regulon to counteract host-specific defenses. Molecular Plant-Microbe Interactions 28: 261-273.
49. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J et al. 2012. The Pfam protein families database. Nucleic Acids Research 40: D290-D301.
50. Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, Lopez R. 2005. InterProScan: protein domains identifier. Nucleic Acids Research 33: W116-W120.
51. Rowan DD, Dymock JJ, Brimble MA. 1990. Effect of fungal metabolite peramine and analogs on feeding and development of Argentine stem weevil (Listronotus bonariensis). Journal of Chemical Ecology 16: 1683-1695.
52. Rowan DD, Hunt MB, Gaynor DL. 1986. Peramine, a novel insect feeding deterrent from ryegrass infected with the endophyte Acremonium loliae. Journal of the Chemical Society, Chemical Communications 12: 935-936.
53. Schardl CL. 2001. Epichloë festucae and related mutualistic symbionts of grasses. Fungal Genetics and Biology 33: 69-82.
54. Schardl CL, Leuchtmann A, Spiering MJ. 2004. Symbioses of grasses with seedborne fungal endophytes. Annual Review of Plant Biology 55: 315-340.
55. Schardl CL, Young CA, Hesse U, Amyotte SG, Andreeva K, Calie PJ, Fleetwood DJ, Haws DC, Moore N, Oeser B et al. 2013. Plant-symbiotic fungi as chemical engineers: multi-genome analysis of the Clavicipitaceae reveals dynamics of alkaloid loci. PLoS Genetics 9: e1003323.
56. Schauer N, Steinhauser D, Strelkov S, Schomburg D, Allison G, Moritz T, Lundgren K, Roessner-Tunali U, Forbes MG, Willmitzer L et al. 2005. GC-MS libraries for the rapid identification of metabolites in complex biological samples. FEBS Letters 579: 1332-1337.
57. Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9: 671-675.
58. Spiering MJ, Greer DH, Schmid J. 2006. Effects of the fungal endophyte, Neotyphodium lolii, on net photosynthesis and growth rates of perennial ryegrass (Lolium perenne) are independent of in planta endophyte concentration. Annals of Botany 98: 379-387.
59. Storey JD, Tibshirani R. 2003. Statistical significance for genomewide studies. Proceedings of the National Academy of Sciences, USA 100: 9440-9445.
60. 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. Molecular Microbiology 57: 1036-1050.
61. Tanaka S, Brefort T, Neidig N, Djamei A, Kahnt J, Vermerris W, Koenig S, Feussner K, Feussner I, Kahmann R. 2014. A secreted Ustilago maydis effector promotes virulence by targeting anthocyanin biosynthesis in maize. eLife 3: e01355.
62. Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Muller LA, Rhee SY, Stitt M. 2004. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant Journal 37: 914-939.
63. Tian P, Nan ZB, Li CJ, Spangenberg G. 2008. Effect of the endophyte Neotyphodium lolii on susceptibility and host physiological response of perennial ryegrass to fungal pathogens. European Journal of Plant Pathology 122: 593-602.
64. Trejo CL, Davies WJ, Ruiz LDP. 1993. Sensitivity of stomata to abscisic-acid - an effect of the mesophyll. Plant Physiology 102: 497-502.
65. Urbanczyk-Wochniak E, Usadel B, Thimm O, Nunes-Nesi A, Carrari F, Davy M, Bläsing O, Kowalczyk M, Weicht D, Polinceusz A et al. 2006. Conversion of MapMan to allow the analysis of transcript data from Solanaceous species: effects of genetic and environmental alterations in energy metabolism in the leaf. Plant Molecular Biology 60: 773-792.
66. Usadel B, Nagel A, Thimm O, Redestig H, Blaesing OE, Palacios-Rojas N, Selbig J, Hannemann J, Piques MC, Steinhauser D et al. 2005. Extension of the visualization tool MapMan to allow statistical analysis of arrays, display of coresponding genes, and comparison with known responses. Plant Physiology 138: 1195-1204.
67. Usadel B, Poree F, Nagel A, Lohse M, Czedik-Eysenberg A, Stitt M. 2009. A guide to using MapMan to visualize and compare Omics data in plants: a case study in the crop species, Maize. Plant, Cell & Environment 32: 1211-1229.
68. Vincent D, Du Fall LA, Livk A, Mathesius U, Lipscombe RJ, Oliver RP, Friesen TL, Solomon PS. 2012. A functional genomics approach to dissect the mode of action of the Stagonospora nodorum effector protein SnToxA in wheat. Molecular Plant Pathology 13: 467-482.
69. Wang LK, Feng ZX, Wang X, Wang XW, Zhang XG. 2010. DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26: 136-138.
70. 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.
71. Wilkinson S, Davies WJ. 2002. ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant, Cell & Environment 25: 195-210.
72. Young CA, Bryant MK, Christensen MJ, Tapper BA, Bryan GT, Scott B. 2005. Molecular cloning and genetic analysis of a symbiosis-expressed gene cluster for lolitrem biosynthesis from a mutualistic endophyte of perennial ryegrass. Molecular Genetics and Genomics 274: 13-29.
73. Young CA, Hume DE, McCulley RL. 2013. Forages and pastures symposium: fungal endophytes of tall fescue and perennial ryegrass: pasture friend or foe? Journal of Animal Science 91: 2379-2394.
74. Zhang Z, Schwartz S, Wagner L, Miller W. 2000. A greedy algorithm for aligning DNA sequences. Journal of Computational Biology 7: 203-214.
75. Zouari I, Salvioli A, Chialva M, Novero M, Miozzi L, Tenore GC, Bagnaresi P, Bonfante P. 2014. From root to fruit: RNA-Seq analysis shows that arbuscular mycorrhizal symbiosis may affect tomato fruit metabolism. BMC Genomics 15: 221.