Metabolic profiles of Lolium perenne are differentially affected by nitrogen supply, carbohydrate content, and fungal endophyte infection

Plant Physiology

Volumn 146, Issue 3, 2008, Pages 1440-1453

  Rasmussen, Susanne ^a   Parsons, Anthony J ^a   Fraser, Karl ^a   Xue, Hong ^a   Newman, Jonathan A ^b  

^a AGRESEARCH GRASSLANDS   (New Zealand)

^b UNIVERSITY OF GUELPH   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

LOLIUM PERENNE; NEOTYPHODIUM LOLII;

MANNITOL; NITROGEN;

ANIMAL; ARTICLE; ASCOMYCETES; CARBOHYDRATE METABOLISM; GROWTH, DEVELOPMENT AND AGING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LOLIUM; MASS FRAGMENTOGRAPHY; METABOLISM; MICROBIOLOGY; NEAR INFRARED SPECTROSCOPY; PHYSIOLOGY; PRINCIPAL COMPONENT ANALYSIS; SYMBIOSIS;

ANIMALS; CARBOHYDRATE METABOLISM; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; HYPOCREALES; LOLIUM; MANNITOL; NITROGEN; PRINCIPAL COMPONENT ANALYSIS; SPECTROSCOPY, NEAR-INFRARED; SYMBIOSIS;

EID: 48949120152     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.107.111898     Document Type: Article

References (111)

1. Amalric C, Sallanon H, Monnet F, Hitmi A, Coudret A (1999) Gas exchange and chlorophyll fluorescence in symbiotic and non-symbiotic ryegrass under water stress. Photosynthetica 37: 107-112
2. Bacetty AA, Snook ME, Glenn AE, Bacon CW, Nagabhyru P, Schardl CL (2007) Nematotoxic effects of endophyte-infected tall fescue toxins and extracts in an in vitro bioassay using the nematode Pratylenchus scribnery. In AJ Popay, ER Thorn, eds, Proceedings of the 6th International Symposium on Fungal Endophytes of Grasses. Grassland Research and Practice Series No. 13, NZ Grassland Association, Dunedin, New Zealand, pp 357-361
3. Bailly J, Debaud JC, Verner MC, Plassard C, Chalot M, Marmeisse R, Fraissinet-Tachet L (2007) How does a symbiotic fungus modulate expression of its host-plant nitrite reductase? New Phytol 175: 155-165
4. Belesky DP, Devine OJ, Pallas JE, Stringer WC (1987) Photosynthetic activity of tall fescue as influenced by a fungal endophyte. Photosynthetica 21: 82-87
5. Belesky DP, Fedders JM (1996) Does endophyte influence regrowth of tall fescue? Ann Bot (Lond) 78: 499-505
6. Belesky DP, Stringer WC, Hill NS (1989) Influence of endophyte and water regime upon tall fescue accessions. I. Growth characteristics. Ann Bot (Lond) 63: 495-503
7. Belesky DP, Stuedemann JA, Plattner RD, Wilkinson SR (1988) Ergopeptine alkaloids in grazed tall fescue. Agron J 80: 209-212
8. Bianchi G, Gamba A, Limiroli R, Pozzi N, Elster R, Salamini F, Bartels D (1993) The unusual sugar composition in leaves of the resurrection plant Myrothamnus flabellifolia. Physiol Plant 87: 223-226
9. Blee KA, Anderson AJ (2002) Transcripts for genes encoding soluble acid invertase and sucrose synthase accumulate in root tip and cortical cells containing mycorrhizal arbuscules. Plant Mol Biol 50: 197-211
10. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254
11. Bush LP, Wilkinson HH, Schardl CL (1997) Bioprotective alkaloids of grass-fungal endophyte symbioses. Plant Physiol 114: 1-7
12. Cheplick GP (2004) Recovery from drought stress in Lolium perenne (Poaceae): Are fungal endophytes detrimental? Am J Bot 91: 1960-1968
13. Cheplick GP (2007) Costs of fungal endophyte infection in Lolium perenne genotypes from Eurasia and North Africa under extreme resource limitation. Environ Exp Bot 60: 202-210
14. Cheplick GP, Cho R (2003) Interactive effects of fungal endophyte infection and host genotype on growth and storage in Lolium perenne. New Phytol 158: 183-191
15. Cheplick GP, Clay K, Marks S (1989) Interactions between infection by endophytic fungi and nutrient limitation in the grasses Lolium perenne and Festuca arundinacea. New Phytol 111: 89-97
16. Cheplick GP, Perera A, Koulouris K (2000) Effect of drought on the growth of Lolium perenne genotypes with and without fungal endophytes. Funct Ecol 14: 657-667
17. Christensen MJ, Leuchtmann A, Rowan DD, Tapper BA (1993) Taxonomy of Acremonium endophytes of tall fescue (Festuca arundinacea), meadow fescue (Festuca pratensis) and perennial ryegrass (Lolium perenne). Mycol Res 97: 1083-1092
18. 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
19. 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
20. Clay K, Holah J, Rudgers JA (2005) Herbivores cause a rapid increase in hereditary symbiosis and alter plant community composition. Proc Natl Acad Sci USA 102: 12465-12470
21. Clay K, Schardl C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160: S99-S127
22. Corson DC, Waghorn GC, Ulyatt MJ, Lee J (1999) NIRS: forage analysis and livestock feeding. Proc NZ Grassland Assoc 51: 127-132
23. Dixon RA (2001) Natural products and plant disease resistance. Nature 411: 843-847
24. Douds DD, Pfeffer PE, Shachar-Hill Y (2000) Carbon partitioning, cost and metabolism of arbuscular mycorrhizae in arbuscular mycorrhizas: physiology and function. In Y Kapulnick, DD Douds Jr, eds, Arbuscular Mycorrhizas: Molecular Biology and Physiology. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 107-129
25. Edwards GR, Parsons AJ, Rasmussen S, Bryant RH (2008) High sugar ryegrasses for livestock systems in New Zealand. Proc NZ Grassland Assoc 69: 161-172
26. Faeth SH, Fagan WF (2002) Fungal endophytes: common host plant symbionts but uncommon mutualists. Integr Comp Biol 42: 360-368
27. Faeth SH, Hamilton CE (2006) Does an asexual endophyte symbiont alter life stage and long-term survival in a perennial host grass? Microb Ecol 52: 748-755
28. Faeth SH, Helander ML, Saikkonen KT (2004) Asexual Neotyphodium endophytes in a native grass reduce competitive abilities. Ecol Lett 7: 304-313
29. Faeth SH, Sullivan TJ (2003) Mutualistic asexual endophytes in a native grass are usually parasitic. Am Nat 161: 310-325
30. Felton GW, Korth KL, Bi JL, Wesley SV, Huhman DV, Mathews MC, Murphy JB, Lamb C, Dixon RA (1999) Inverse relationship between systemic resistance of plants to microorganisms and to insect herbivory. Curr Biol 9: 317-320
31. Finkes LK, Cady AB, Mulroy JC, Clay K, Rudgers JA (2006) Plant-fungus mutualism affects spider composition in successional fields. Ecol Lett 9: 347-356
32. Gordon AJ, Ryle GJA, Powell CE, Mitchell DF (1980) Export, mobilization and respiration of assimilates in uniculm barley during light and darkness. J Exp Bot 31: 461-473
33. Govindarajulu M, Pfeffer PE, Jin H, Abubaker J, Douds DD, Allen JW, Bücking H, Lammers PJ, Shachar-Hill Y (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435: 819-823
34. Graefe H, Gütschow B, Gehring H, Dibbelt L (2003) Sensitive and specific photometric determination ofmannitol in human serum. Clin Chem Lab Med 41: 1049-1055
35. Graham JH (2000) Assessing costs of arbuscular mycorrhizal symbiosis agroecosystems fungi. In GK Podila, DD Douds Jr, eds, Current Advances in Mycorrhizae Research. APS Press, St. Paul, MN, pp 127-140
36. Hair JF, Anderson RE, Tatham RL, Black WC (1998) Multivariate Data Analysis, Ed 5. Prentice Hall, Upper Saddle River, NJ
37. Harris PM, Lobley GE (1991) Amino acid metabolism in peripheral tissues. In T Tsuda, Y Sasaki, R Kawashima, eds, Physiological Aspects of Digestion and Metabolism in Ruminants. Proceedings of the Seventh International Symposium on Ruminant Physiology. Academic Press, San Diego, pp 201-230
38. Harrison MJ, Dixon RA (1993) Isoflavonoid accumulation and expression of defense gene transcripts during the establishment of vesiculararbuscular mycorrhizal associations in roots of Medicago truncatula. Mol Plant Microbe Interact 6: 643-654
39. Harwood VD (1954) Analytical studies on the carbohydrates of grasses and clover. VII. The isolation of D-mannitol from perennial ryegrass (Lolium perenne L.). J Sci Food Agric 5: 453-455
40. Herrmann KM (1995) The shikimate pathway: early steps in the biosynthesis of aromatic compounds. Plant Cell 7: 907-919
41. Herrmann KM, Weaver LM (1999) The shikimate pathway. Annu Rev Plant Physiol Plant Mol Biol 50: 473-503
42. Hesse U, Hahn H, Andreeva K, Förster K, Warnstorff K, Schöberlein W, Diepenbrock W (2004) Investigations on the influence of Neotyphodium endophytes on plant growth and seed yield of Lolium perenne genotypes. Crop Sci 44: 1689-1695
43. Hesse U, Schöberlein W, Wittenmayer L, Förster K, Warnstorff K, Diepenbrock W, Merbach W (2003) Effects of Neotyphodium endophytes on growth, reproduction and drought-stress tolerance of three Lolium perenne L. genotypes. Grass For Sci 58: 407-415
44. Hesse U, Schöberlein W, Wittenmayer L, Förster K, Warnstorff K, Diepenbrock W, Merbach W (2005) Influence of water supply and endophyte infection (Neotyphodium spp.) on vegetative and reproductive growth of two Lolium perenne L. genotypes. Eur J Agron 22: 45-54
45. Hohnjec N, Vieweg MF, Pühler A, Becker A, Küster H (2005) Overlaps in the transcriptional profiles of Medicago truncatula roots inoculated with two different Glomus fungi provide insights into the genetic program activated during arbuscular mycorrhiza. Plant Physiol 137: 1283-1301
46. 2, nitrogen and fungal endophyte-infection on Lolium perenne L. growth, chemical composition and alkaloid production. Plant Cell Environ 28: 1345-1354
47. Koshino H, Tekada SI, Yoshihara T, Sakamura S, Shimanuki T, Sato T, Tajimi A (1988) Three phenolic acid derivatives from stromata of Epichloë typhina on Phleum pratense. Phytochemistry 27: 1333-1338
48. Krauss J, Harri SA, Bush L, Husi R, Bigler L, Power SA, Müller CB (2007) Effects of fertilizer, fungal endophytes and plant cultivar on the performance of insect herbivores and their natural enemies. Funct Ecol 21: 107-116
49. Lam H-M, Coschigano KT, Oliveira IC, Melo-Oliveira R, Coruzzi GM (1996) The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Annu Rev Plant Physiol 47: 569-593
50. Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48: 251-275
51. Leuchtmann A (1993) Systematics, distribution, and host specificity of grass endophytes. Nat Toxins 1: 150-162
52. Lewis DH, Smith DC (1967) Sugar alcohols (polyols) in fungi and green plants. New Phytol 66: 143-184
53. Lyons PC, Evans JJ, Bacon CW (1990) Effects of the fungal endophyte Acremonium coenophialum on nitrogen accumulation and metabolism in tall fescue. Plant Physiol 92: 726-732
54. Malinowski DP, Alloush GA, Belesky DP (1998a) Evidence for chemical changes on the root surface of tall fescue in response to infection with the fungal endophyte Neotyphodium coenophialum. Plant Soil 205: 1-12
55. 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: 923-940
56. Malinowski DP, Belesky DP (2006) Ecological importance of Neotyphodium spp. grass endophytes in agroecosystems. Grassl Sci 52: 1-14
57. Malinowski DP, Belesky DP, Hill NS, Baligar VC, Fedders JM (1998b) Influence of phosphorus on the growth and ergot alkaloid content of Neotyphodium coenophialum-infected tall fescue (Festuca arundinacea Schreb.). Plant Soil 198: 53-61
58. Marks S, Clay K (1996) Physiological responses of Festuca arundinacea to fungal endophyte infection. New Phytol 133: 727-733
59. Martinoia E, Rentsch D (1994) Malate compartmentation-responses to a complex metabolism. Annu Rev Plant Physiol 45: 447-467
60. McGarigal K, Cushman S, Stafford S (2000) Multivariate Statistics for Wildlife and Ecology Research. Springer Verlag, New York
61. Meister B, Krauss J, Haerri SA, Schneider MV, Müller CB (2006) Fungal endosymbionts affect aphid population size by reduction of adult life span and fecundity. Basic Appl Ecol 7: 244-252
62. Miller RG (1981) Simultaneous Statistical Inference, Ed 2. Springer Verlag, New York
63. Morot-Gaudry JF, Job D, Lea PJ (2001) Amino acid metabolism. In PJ Lea, JF Morot-Gaudry, eds, Plant N. Springer Verlag, Berlin, pp 167-211
64. Morse LJ, Day TA, Faeth SH (2002) Effect of Neotyphodium endophyte infection on growth and leaf gas exchange of Arizona fescue under contrasting water availability regimes. Environ Exp Bot 48: 257-268
65. Müller CB, Krauss J (2005) Symbiosis between grasses and asexual fungal endophytes. Curr Opin Plant Biol 8: 450-456
66. 2, nitrogen and fungal endophyte-infection on tall fescue: growth, photosynthesis, chemical composition and digestibility. Glob Change Biol 9: 425-437
67. Noctor G, Novitskaya L, Lea PJ, Foyer CH (2002) Co-ordination of leaf minor amino acid contents in crop species: significance and interpretation. J Exp Bot 53: 939-945
68. Omacini M, Chaneton EJ, Ghersa CM, Müller CB (2001) Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature 409: 78-81
69. Ouborg NJ, Vriezen WH (2007) An ecologist's guide to ecogenomics. J Ecol 95: 8-16
70. Pavis N, Chatterton NJ, Harrison PA, Baumgartner S, Praznik W, Boucaud J, Prud'homme MP (2001) Structure of fructans in roots and leaf tissues of Lolium perenne. New Phytol 150: 83-95
71. Pellegrini L, Rohfritsch O, Fritig B, Legrand M (1994) Phenylalanine ammonia-lyase in tobacco. Molecular cloning and gene expression during the hypersensitive reaction to tobacco mosaic virus and the response to fungal elicitor. Plant Physiol 106: 877-886
72. Pfeffer PE, Bago B, Shachar-Hill Y (2001) Exploring mycorrhizal function with NMR spectroscopy. New Phytol 150: 543-553
73. Pfeffer PE, Douds DD, Bécard G, Shachar-Hill Y (1999) Carbon uptake and the metabolism and transport of lipids in an arbuscular mycorrhiza. Plant Physiol 120: 587-598
74. Pollock CJ, Jones T (1979) Seasonal patterns of fructan metabolism in forage grasses. New Phytol 83: 9-15
75. Prud'homme MP, Gonzalez B, Billard JP, Boucaud J (1992) Carbohydrate content, fructan and sucrose enzyme activities in roots, stubble and leaves of ryegrass (Lolium perenne L.) as affected by source/sink modification after cutting. J Plant Physiol 140: 282-291
76. Rasmussen S, Parsons AJ, Bassett S, Christensen MJ, Hume DE, Johnson LJ, Johnson RD, Simpson WR, Stacke C, Voisey CR, et al (2007) High nitrogen supply and carbohydrate content reduce fungal endophyte and alkaloid concentration in Lolium perenne. New Phytol 173: 787-797
77. Reverter M, Lundh T, Lindberg JE (1997) Determination of free amino acids in pig plasma by precolumn derivatization with 6-N-aminoquinolyl-N- hydroxysuccinimidyl carbamate and high performance liquid chromatography. J Chromatogr B Biomed Sci Appl 696: 1-8
78. Richardson MD, Chapman GW Jr, Hoveland CS, Bacon CW (1992) Sugar alcohols in endophyte-infected tall fescue under drought. Crop Sci 32: 1060-1061
79. Roessner U, Luedemann A, Brust D, Fiehn O, Linke T, Willmitzer L, Fernie AR (2001) Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell 13: 11-29
80. Roessner U, Wagner C, Kopka J, Tretheway RN, Willmitzer L (2000) Simultaneous analysis of metabolites in potato tuber by gas chromatography-mass spectrometry. Plant J 23: 131-142
81. Rowan DD, Hunt MB, Gaynor DL (1986) Peramine, a novel insect feeding deterrent from ryegrass infected with the endophyte Acremonium loliae. J Chem Soc Chem Commun 1986: 935-936
82. Rudgers JA, Mattingly WB, Koslow JM (2005) Mutualistic fungus promotes plant invasion into diverse communities. Oecologia 144: 463-471
83. Ruijter GJG, Bax J, van de Vondervoort PJI, de Vries RP, vanKuyk PA, Visser J (2003) Mannitol is required for stress tolerance in Aspergillus niger conidiospores. Eukaryot Cell 2: 690-698
84. Saikkonen K, Lehtonen P, Helander M, Koricheva J, Faeth SH (2007) Model systems in ecology: dissecting the endophyte-grass literature. Trends Plant Sci 11: 428-433
85. Saikkonen K, Wäli P, Helander M, Faeth SH (2004) Evolution of endophyte-plant symbiosis. Trends Plant Sci 9: 275-280
86. Sarosh BR, Sivaramakrishnan S, Shetty HS (2005) Elicitation of defense related enzymes and resistance by L-methionine in pearl millet against downy mildew disease caused by Sclerospora graminicola. Plant Physiol Biochem 43: 808-815
87. Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 55: 315-340
88. Schingoethe DJ (1996) Balancing the amino acid needs of the dairy cow. Anim Feed Sci Technol 60: 153-160
89. Schliemann W, Ammer C, Strack D (2008) Metabolite profiling of mycorrhizal roots of Medicago truncatula. Phytochemistry 69: 112-146
90. Singh SB, Bais BS, Singh DR (1972) Effect of different carbon and nitrogen sources on the growth and sporulation of claviceps microcephala (Wallr.) Tul. Mycopathol Mycol Appl 46: 373-378
91. Smith AM, Stitt M (2007) Coordination of carbon supply and plant growth. Plant Cell Environ 30: 1126-1149
92. Smith SE, Dickson S, Smith FA (2001) Nutrient transfer in arbuscular mycorrhizas: How are fungal and plant processes integrated? Aust J Plant Physiol 28: 683-694
93. Snoeren TA, de Jong PW, Dicke M (2007) Ecogenomic approach to the role of herbivore-induced plant volatiles in community ecology. J Ecol 95: 17-26
94. Solaiman MDZ, Saito M (1997) Use of sugars by intraradical hyphae of arbuscular mycorrhizal fungi revealed by radiorespirometry. New Phytol 136: 533-538
95. Solomon PS, Waters ODC, Jörgens CI, Lowe RGT, Rechberger J, Trengove RD, Oliver RP (2006) Mannitol is required for asexual sporulation in the wheat pathogen Stagonospora nodorum (glume blotch). Biochem J 399: 231-239
96. Solomon PS, Waters ODC, Oliver RP (2007) Decoding the mannitol enigma in filamentous fungi. Trends Microbiol 15: 257-262
97. Spiering MJ, Greer DH, Schmid J (2006) Effects of fungal endophyte, Neotyphodium lolii, on net photosynthesis and growth rates of perennial ryegrass (Lolium perenne) are independent of in planta endophyte concentration. Ann Bot (Lond) 98: 379-387
98. Stitt M, Müller C, Matt P, Gibon Y, Carillo P, Morcuende R, Scheible WR, Krapp A (2002) Steps towards an integrated view of nitrogen metabolism. J Exp Bot 53: 959-970
99. Südekum KH, Wolffram S, Ader P, Robert JC (2004) Bioavailability of three ruminally protected methionine sources in cattle. Anim Feed Sci Technol 113: 17-25
100. 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
101. Tanaka A, Christensen MJ, Takemoto D, Park P, Scott B (2006) Reactive oxygen species play a role in regulating a fungus-perennial ryegrass mutualistic interaction. Plant Cell 18: 1052-1066
102. Taper ML, Lele SR (2004) The Nature of Scientific Evidence: Statistical, Philosophical and Empirical Considerations. University Chicago Press, Chicago
103. van der Heijden MGA, Streitwolf-Engel R, Riedl R, Siegrist S, Neudecker A, Ineichen K, Boller T, Wiemken A, Sanders IR (2006) The mycorrhizal contribution to plant productivity, plant nutrition and soil structure in experimental grassland. New Phytol 172: 739-752
104. Vogelsang KM, Reynolds HL, Bever JD (2006) Mycorrhizal fungal identity and richness determine the diversity and productivity of a tallgrass prairie system. New Phytol 172: 554-562
105. Volpin H, Elkind Y, Okon Y, Kapulnik Y (1994) A vesicular arbuscular mycorrhizal fungus (Glomus intraradix) induces a defense response in alfalfa roots. Plant Physiol 104: 683-689
106. Wingler A, Guttenberger M, Hampp R (1993) Determination of mannitol in ectomycorrhizal fungi and ectomycorrhizas by enzymatic microassays. Mycorrhiza 3: 69-73
107. Wright DP, Read DJ, Scholes JD (1998) Mycorrhizal sink strength influences whole plant carbon balance of Trifolium repens L. Plant Cell Environ 21: 881-891
108. Wynn JP, bin Abdul Hamid A, Ratledge C (1999) The role of malic enzyme in the regulation of lipid accumulation in filamentous fungi. Microbiology 145: 1911-1917
109. Wynn JP, Ratledge C (1997) Malic enzyme is a major source of NADPH for lipid accumulation by Aspergillus nidulans. Microbiology 143: 253-257
110. Zabalgogeazcoa Í, Ciudad AG, de Aldana BRV, Criado BG (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
111. Zhang Y, Adams IP, Ratledge C (2007) Malic enzyme: the controlling activity for lipid production? Overexpression of malic enzyme in Mucor circinelloides leads to a 2.5-fold increase in lipid accumulation. Microbiology 153: 2013-2025