Abstract
Epichloë festucae and its asexual derivative Neotyphodium lolii are mutualistic symbionts that confer on their Festuca and Lolium grass hosts, protection from various biotic and abiotic stresses. The genetic tractability of E. festucae has led to its adoption as a model experimental system to study fungal–grass symbiotic interactions. Growth of E. festucae in Lolium perenne is both epiphytic and endophytic. Endophytic growth is characterized by hyphal tip growth and branching in the meristematic tissues but in the leaves hyphae divide and extend by intercalary growth in synchrony with the same pattern of growth of the leaves. Forward and reverse genetics approaches have shown that the NADPH oxidase (Nox) complex and MAP kinase signaling pathways are crucial for maintaining this restrictive pattern of hyphal growth in the leaves. Disruption of genes that encode components of these signaling complexes leads to proliferative (pathogenic) growth in the host and a breakdown in the symbiosis. This chapter provides an overview of morphogenesis, growth, and development of E. festucae in culture and in planta and an oversight of what is currently known about the fungal signaling mechanisms required for maintaining a balanced symbiosis.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Bacon CW, Hinton DM (1988) Ascosporic iterative germination in Epichloë typhina. Trans Br Mycol Soc 90:563–569
Bai Z, Harvey LM, McNeil B (2001) Use of the chemiluminescent probe lucigenin to monitor the production of the superoxide anion radical in a recombinant Aspergillus niger (B1-D). Biotechnol Bioeng 75:204–211
Bassett SA, Bond JJ, Kwan FY, McCulloch AF, Haynes PA, Johnson RD, Bryan GT, Jordan TW (2009) Proteomic analysis of a filamentous fungal endophyte using EST datasets. Proteomics 9:2295–2300
Belden WJ, Larrondo LF, Froehlich AC, Shi M, Chen CH, Loros JJ, Dunlap JC (2007) The band mutation in Neurospora crassa is a dominant allele of ras-1 implicating RAS signaling in circadian output. Genes Dev 21:1494–1505
Brasell E (2010) Identification of genes regulating the plant-specific expression of the ltmM gene in Epichloë festucae. M.Sc. thesis. Massey University, Palmerston North, New Zealand
Bultman TL, Leuchtmann A (2009) Biology of the Epichloë-Botanophila interaction: an intriguing association between fungi and insects. Fungal Biol Rev 22:131–138
Bultman TL, White JF Jr, Bowdish TI, Welch AM (1998) A new kind of mutualism between fungi and insects. Mycol Res 102:235–238
Cao M, Koulman A, Johnson LJ, Lane GA, Rasmussen S (2008) Advanced data-mining strategies for the analysis of direct-infusion ion trap mass spectrometry data from the association of perennial ryegrass with its endophytic fungus, Neotyphodium lolii. Plant Physiol 146:1501–1514
Christensen MJ, Latch GCM (1991) Variation among isolates of Acremonium endophytes (A. coenophialum and possibly A. typhinum) from tall fescue (Festuca arundinacea). Mycol Res 95:1123–1126
Christensen MJ, Voissey CR (2007) The biology of the endophyte/grass partnership. In: Popay AJ, Thom ER (eds) Proceedings of the 6th international symposium on fungal endophytes of grasses grasslands research and practice series no. 13. New Zealand Grassland Association, Christchurch, pp 123–133
Christensen MJ, Ball OJ-P, Bennett RJ, Schardl CL (1997) Fungal and host genotype effects on compatibility and vascular colonization by Epichloë festucae. Mycol Res 101:493–501
Christensen MJ, Bennett RJ, Schmid J (2001) Vascular bundle colonisation by Neotyphodium endophytes in natural and novel associations with grasses. Mycol Res 105:1239–1245
Christensen MJ, Bennett RJ, Schmid J (2002) Growth of Epichloë/Neotyphodium and p-endophytes in leaves of Lolium and Festuca grasses. Mycol Res 106:93–106
Christensen MJ, Bennett RJ, Ansari HA, Koga H, Johnson RD, Bryan GT, Simpson WR, Koolaard JP, Nickless EM, Voisey CR (2008) Epichloë endophytes grow by intercalary hyphal extension in elongating grass leaves. Fungal Genet Biol 45:84–93
Chung K-R, Schardl CL (1997) Sexual cycle and horizontal transmission of the grass symbiont, Epichloë typina. Mycol Res 101:295–301
Cox MP, Eaton CJ, Scott B (2010) Exploring molecular signaling in plant-fungal symbioses using high throughput RNA sequencing. Plant Signal Behav 5:1353–1358
Delaunay A, Pflieger D, Barrault MB, Vinh J, Toledano MB (2002) A thiol peroxidase is an H2O2 receptor and redox-transducer in gene activation. Cell 111:471–481
DerMardirossian C, Schnelzer A, Bokoch GM (2004) Phosphorylation of RhoGDI by Pak1 mediates dissociation of Rac GTPase. Mol Cell 15:117–127
Dooley CT, Dore TM, Hanson GT, Jackson WC, Remington SJ, Tsien RY (2004) Imaging dynamic redox changes in mammalian cells with green fluorescent protein indicators. J Biol Chem 279:22284–22293
Eaton CJ, Jourdain I, Foster SJ, Hyams JS, Scott B (2008) Functional analysis of a fungal endophyte stress-activated MAP kinase. Curr Genet 53:163–174
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 Physiol 153:1780–1794
Eaton C, Mitic M, Scott B (2011a) Signalling in the Epichloë festucae-perennial ryegrass mutualistic symbiotic interaction. In: Perotto S, Baluska F (eds) Signalling and communication in plant symbiosis (communication and signaling in plants). Springer, Heidelberg
Eaton CJ, Cox MP, Scott B (2011b) What triggers grass endophytes to switch from mutualism to pathogenism? Plant Sci 180:190–195
Egan M, Wang Z-Y, Jones MA, Smirnoff N, Talbot NJ (2007) Generation of reactive oxygen species by fungal NADPH oxidases is required for rice blast disease. Proc Natl Acad Sci USA 104:11772–11777
Fleetwood DJ, Scott B, Lane GA, Tanaka A, Johnson RD (2007) A complex ergovaline gene cluster in epichloë endophytes of grasses. Appl Environ Microbiol 73:2571–2579
Florea S, Andreeva K, Machado C, Mirabito PM, Schardl CL (2009) Elimination of marker genes from transformed filamentous fungi by unselected transient transfection with a Cre-expressing plasmid. Fungal Genet Biol 46:721–730
Giesbert S, Schurg T, Scheele S, Tudzynski P (2008) The NADPH oxidase Cpnox1 is required for full pathogenicity of the ergot fungus Claviceps purpurea. Mol Plant Pathol 9:317–327
Guo M, Chen Y, Du Y, Dong Y, Guo W, Zhai S, Zhang H, Dong S, Zhang Z, Wang Y, Wang P, Zheng X (2011) The bZIP transcription factor MoAP1 mediates the oxidative stress response and is critical for pathogenicity of the rice blast fungus Magnaporthe oryzae. PLoS Pathog 7:e1001302
Haarmann T, Rolke Y, Giesbert S, Tudzynski P (2009) Ergot: from witchcraft to biotechnology. Mol Plant Pathol 10:563–577
Hanson GT, Aggeler R, Oglesbee D, Cannon M, Capaldi RA, Tsien RY, Remington SJ (2004) Investigating mitochondrial redox potential with redox-sensitive green fluorescent protein indicators. J Biol Chem 279:13044–13053
Hinton DM, Bacon CW (1985) The distribution and ultrastructure of the endophyte of toxic tall fescue. Can J Microbiol 63:36–42
Jackson SL, Heath IB (1993) Roles of calcium ions in hyphal tip growth. Microbiol Rev 57:367–382
Kuldau GA, Tsai H-F, Schardl CL (1999) Genome sizes of Epichloë species and anamorphic hybrids. Mycologia 91:776–782
Latch GCM, Christensen MJ (1985) Artificial infection of grasses with endophytes. Ann Appl Biol 107:17–24
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
Leuchtmann A, Schmidt D, Bush LP (2000) Different levels of protective alkaloids in grasses with stroma-forming and seed-transmitted Epichloë/Neotyphodium endophytes. J Chem Ecol 26:1025–1036
Lin CH, Yang SL, Chung KR (2009) The YAP1 homolog-mediated oxidative stress tolerance is crucial for pathogenicity of the necrotrophic fungus Alternaria alternata in citrus. Mol Plant Microbe Interact 22:942–952
Martyn KD, Kim M-J, Quinn MT, Dinauer MC, Knaus UG (2005) p21-activated kinase (Pak) regulates NADPH oxidase activation in human neutrophils. Blood 106:3962–3969
May KJ, Bryant MK, Zhang X, Ambrose B, Scott B (2008) Patterns of expression of a lolitrem biosynthetic gene in the Epichloë festucae-perennial ryegrass symbiosis. Mol Plant Microbe Interact 21:188–197
Meyer AJ, Dick TP (2010) Fluorescent protein-based redox probes. Antioxid Redox Signal 13:1–30
Michalakis Y, Olivieri I, Renaud F, Raymond M (1992) Pleiotropic action of parasites: how to be good for the host. Trends Ecol Evol 7:59–62
Mishina NM, Tyurin-Kuzmin PA, Markvicheva KN, Vorotnikov AV, Tkachuk VA, Laketa V, Schultz C, Lukyanov S, Belousov VV (2011) Does cellular hydrogen peroxide diffuse or act locally? Antioxid Redox Signal 14:1–7
Molina L, Kahmann R (2007) An Ustilago maydis gene involved in H2O2 detoxification is required for virulence. Plant Cell 19:2293–2309
Moon CD, Craven KD, Leuchtmann A, Clement SL, Schardl CL (2004) Prevalence of interspecific hybrids amongst asexual fungal endophytes of grasses. Mol Ecol 13:1455–1467
Moy M, Belanger F, Duncan R, Freehoff A, Leary C, Meyer W, Sullivan R, WJ JF (2000) Identification of epiphyllous mycelial nets on leaves of grasses infected by clavicipitaceous endophytes. Symbiosis 28:291–302
Nathues E, Joshi S, Tenberge KB, von den Driesch M, Oeser B, Baumer N, Mihlan M, Tudzynski P (2004) CPTF1, a CREB-like transcription factor, is involved in the oxidative stress response in the phytopathogen Claviceps purpurea and modulates ROS level in its host Secale cereale. Mol Plant Microbe Interact 17:383–393
Ostergaard H, Henriksen A, Hansen FG, Winther JR (2001) Shedding light on disulfide bond formation: engineering a redox switch in green fluorescent protein. EMBO J 20:5853–5862
Ostergaard H, Tachibana C, Winther JR (2004) Monitoring disulfide bond formation in the eukaryotic cytosol. J Cell Biol 166:337–345
Philipson MN, Christey MC (1986) The relationship of host and endophyte during flowering, seed formation, and germination of Lolium perenne. New Zeal J Bot 24:125–134
Rasmussen S, Parsons AJ, Bassett S, Christensen MJ, Hume DE, Johnson LJ, Johnson RD, Simpson WR, Stacke C, Voisey CR, Xue H, Newman JA (2007) High nitrogen supply and carbohydrate content reduce fungal endophyte and alkaloid concentration in Lolium perenne. New Phytol 173:787–797
Rasmussen S, Parsons AJ, Fraser K, Xue H, Newman JA (2008) Metabolic profiles of Lolium perenne are differentially affected by nitrogen supply, carbohydrate content, and fungal endophyte infection. Plant Physiol 146:1440–1453
Rolke Y, Tudzynski P (2008) The small GTPase Rac and the p21-activated kinase Cla4 in Claviceps purpurea: interaction and impact on polarity, development and pathogenicity. Mol Microbiol 68:405–423
Sampson K (1933) The systemic infection of grasses by Epichloë typhina (Pers.) Tul. Trans Br Mycol Soc 18:30–47
Schardl CL (2001) Epichloë festucae and related mutualistic symbionts of grasses. Fungal Genet Biol 33:69–82
Schardl CL, Leuchtmann A, Tsai H-F, 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, Leuchtmann A, Chung K-R, Penny D, Siegel MR (1997) Coevolution by common descent of fungal symbionts (Epichloë spp.) and grass hosts. Mol Biol Evol 14:133–143
Schardl CL, Scott B, Florea S, Zhang D (2009) Epichloë endophytes: clavicipitaceous symbionts of grasses. In: Deising HB (ed) The mycota volume V – plant relationships. Springer, Berlin, pp 275–306
Scheffer J, Chen C, Heidrich P, Dickman MB, Tudzynski P (2005) A CDC42 homologue in Claviceps purpurea is involved in vegetative differentiation and is essential for pathogenicity. Eukaryot Cell 4:1228–1238
Schiestl FP, Steinebrunner F, Schulz C, Von Reub S, Francke W, Weymuth C, Leuchtmann A (2006) Evolution of ‘pollinator’-attracting signals in fungi. Biol Lett 2:401–404
Schmid J, Spiering MJ, Christensen MJ (2000) Metabolic activity, distribution, and propagation of grass endophytes in planta: investigations using the GUS reporter gene system. In: Bacon CW, White JF Jr (eds) Microbial endophytes. Dekker, New York, pp 295–322
Scott B, Eaton CJ (2008) Role of reactive oxygen species in fungal cellular differentiations. Curr Opin Microbiol 11:488–493
Scott B, Schardl C (1993) Fungal symbionts of grasses: evolutionary insights and agricultural potential. Trends Microbiol 1:196–200
Scott B, Takemoto D, Tanaka A, Young CA, Bryant MK, May KJ (2007) Functional analysis of the Epichloë festucae-perennial ryegrass symbiosis. In: Popay AJ, Thom ER (eds) Proceedings of the 6th international symposium on fungal endophytes of grasses grasslands research and practice series no. 13. New Zealand Grassland Association, Christchurch, pp 433–441
Segmüller N, Kokkelink L, Giesbert S, Odinius D, van Kan J, Tudzynski P (2008) NADPH oxidases are involved in differentiation and pathogenicity in Botrytis cinerea. Mol Plant Microbe Interact 21:808–819
Semighini CP, Harris SD (2008) Regulation of apical dominance in Aspergillus nidulans hyphae by reactive oxygen species. Genetics 179:1919–1932
Slepecky RA, Starmer WT (2009) Phenotypic plasticity in fungi: a review with observations on Aureobasidium pullulans. Mycologia 101:823–832
Soper K, Mitchell KJ (1956) The developmental anatomy of perennial ryegrass (Lolium perenne L.). N Z J Sci Technol 37:484–505
Spanu PD et al (2010) Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330:1543–1546
Steinebrunner F, Schiestl FP, Leuchtmann A (2008a) Ecological role of volatiles produced by Epichloë: differences in antifungal toxicity. FEMS Microbiol Ecol 64:307–316
Steinebrunner F, Schiestl FP, Leuchtmann A (2008b) Variation of insect attracting odor in endophytic Epichloë fungi: phylogenetic constrains versus host influence. J Chem Ecol 34:772–782
Steinebrunner F, Twele R, Francke W, Leuchtmann A, Schiestl FP (2008c) Role of odour compounds in the attraction of gamete vectors in endophytic Epichloë fungi. New Phytol 178:401–411
Takemoto D, Tanaka A, Scott B (2006) A p67Phox-like regulator is recruited to control hyphal branching in a fungal-grass mutualistic symbiosis. Plant Cell 18:2807–2821
Takemoto D, Kamakura S, Saikia S, Becker Y, Wrenn R, Tanaka A, Sumimoto H, Scott B (2011) Polarity proteins Bem1 and Cdc24 are components of the filamentous fungal NADPH oxidase complex. Proc Natl Acad Sci USA 108:2861–2866
Tan YY, Spiering MJ, Scott V, Lane GA, Christensen MJ, Schmid J (2001) In planta regulation of extension of an endophytic fungus and maintenance of high metabolic rates in its mycelium in the absence of apical extension. Appl Environ Microbiol 67:5377–5383
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
Tanaka A, Christensen MJ, Takemoto D, Park P, Scott B (2006) Reactive oxygen species play a role in regulating a fungus-perennial ryegrass mutualistic association. Plant Cell 18:1052–1066
Tanaka A, Wrenn RE, Takemoto D, Scott B (2007) Agrobacterium tumefaciens T-DNA mediated transformation of Epichloë festucae. In: Popay AJ, Thon ER (eds) Proceedings of the 6th international symposium on fungal endophytes of grasses grassland research and practice series no. 13. New Zealand Grassland Association, Christchurch, pp 469–472
Tanaka A, Takemoto D, Hyon GS, Park P, Scott B (2008) NoxA activation by the small GTPase RacA is required to maintain a mutualistic symbiotic association between Epichloë festucae and perennial ryegrass. Mol Microbiol 68:1165–1178
Torralba S, Heath IB (2001) Cytoskeletal and Ca2+ regulation of hyphal tip growth and initiation. Curr Top Dev Biol 51:135–187
Trinci APJ (1978) The duplication cycle and branching in fungi. In: Burnett JH, Trinci APJ (eds) Symposium of the British Mycological Society. Cambridge University Press, Queen Elizabeth College, London, pp 319–357
Tudzynski P, Scheffer J (2004) Claviceps purpurea: molecular aspects of a unique pathogenic lifestyle. Mol Plant Pathol 5:377–388
Veit B (2006) Stem cell signalling networks in plants. Plant Mol Biol 60:793–810
Voisey CR (2010) Intercalary growth in hyphae of filamentous fungi. Fungal Biol Rev 24:123–131
Winterbourn CC, Hampton MB (2008) Thiol chemistry and specificity in redox signaling. Free Radic Biol Med 45:549–561
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. Mol Genet Genomics 274:13–29
Zhang N-X, Zhang S, Borchert S, Richardson K, Schmid J (2011) High levels of a fungal superoxide dismutase and increased concentration of a PR-10 plant protein in associations between the endophytic fungus Neotyphodium lolii and ryegrass. Mol Plant Microbe Interact 24(8):984–992
Acknowledgments
This research was supported by grants from the Tertiary Education Commission (TEC) to the Bio-Protection Research Centre, the Royal Society of New Zealand Marsden Fund (MAU0701), Massey University, and by a Top Achiever Doctoral Scholarship to GC from TEC. We thank Dimitry Sokolov and Doug Hopcroft (Manawatu Microscopy and Imaging Centre, IMBS) for technical assistance with microscopy. We also thank Carla Eaton for comments on the manuscript.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2012 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Scott, B., Becker, Y., Becker, M., Cartwright, G. (2012). Morphogenesis, Growth, and Development of the Grass Symbiont Epichlöe festucae . In: Pérez-Martín, J., Di Pietro, A. (eds) Morphogenesis and Pathogenicity in Fungi. Topics in Current Genetics, vol 22. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-22916-9_12
Download citation
DOI: https://doi.org/10.1007/978-3-642-22916-9_12
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-22915-2
Online ISBN: 978-3-642-22916-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)