A new currency for mutualism? Fungal endophytes alter antioxidant activity in hosts responding to drought

Fungal Diversity

Volumn 54, Issue , 2012, Pages 39-49

  Hamilton, Cyd E ^a,b   Bauerle, Taryn L ^b  

^a PLANT PRODUCTION RESEARCH   (Finland)

^b Department of Molecular Biology and Genetics   (United States)

Author keywords

Epichloe; Neotyphodium; Reactive oxygen species; Stress; Stress tolerance; Symbiont

Indexed keywords

EPICHLOE; FUNGI; NEOTYPHODIUM;

EID: 84860782173     PISSN: 15602745     EISSN: 18789129     Source Type: Journal    
DOI: 10.1007/s13225-012-0156-y     Document Type: Article

References (95)

1. Aebi H (1984) Catalase in vitro. In: Lester P (ed.) Methods enzymology, Academic Press, pp 121-126
2. S Agarwal 2007 Increased antioxidant activity in Cassia seedlings under UV-B radiation Biol Plant 51 157 160 10.1007/s10535-007-0030-z 1:CAS:528:DC%2BD2sXksVegu7g%3D (Pubitemid 46464802)
3. M Alvarez D Huygens C Fernandez Y Gacitúa E Olivares I Saavedra M Alberdi E Valenzuela 2009 Effect of ectomycorrhizal colonization and drought on reactive oxygen species metabolism of Nothofagus dombeyi roots Tree Phys 29 1047 1057 10.1093/treephys/tpp038 1:CAS:528:DC%2BD1MXhtVGis7rF
4. DF Andrews D Pregibon 1978 Finding the outliers that matter J Royal Stat Soc Series B 40 85 93
5. K Apel H Hirt 2004 Reactive oxygen species: metabolism, oxidative stress, and signal transduction Annu Rev Pl Biol 55 373 399 10.1146/annurev.arplant.55. 031903.141701 1:CAS:528:DC%2BD2cXlvFeisL0%3D (Pubitemid 38940937)
6. Arnold AE (2008) Endophytic fungi: hidden components of tropical community ecology. In: Schnitzer S, Carson W eds. Tropical forest community ecology blackwell scientific, Oxford University Press, pp 254-271
7. K Asada 1992 Ascorbate peroxidase - a hydrogen peroxide-scavenging enzyme in plants Physiologia Plant 85 235 241 10.1111/j.1399-3054.1992.tb04728.x 1:CAS:528:DyaK38XkvVKlsb4%3D
8. Bacon CW, White JF Jr (1993) Biotechnology of endophytic fungi of grasses. CRC Press, Boca Raton, Florida
9. Bae H, Sicher RC, Moon SK, Kim S-H, Strem MD, Melnick RL, Bailey BA (2009) The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in Theobroma cacao. Exp Bot 60:3279-3295
10. H Baltruschat J Fodor BD Harrach E Niemczk B Barna G Gullner A Janeczko K-H Kogel P Schäfer I Schwarczinger A Zuccaro A Skoczowski 2008 Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants New Phytol 180 501 510 18681935 10.1111/j.1469-8137.2008.02583.x 1:CAS:528:DC%2BD1cXhtlKru73E
11. P Baptista A Martins MS Pais RM Tavares T Lino-Neto 2007 Involvement of reactive oxygen species during early stages of ectomycorrhiza establishment between Castanea sativa and Pisolithus tinctorius Mycorrhiza 17 185 193 17216276 10.1007/s00572-006-0091-4 1:CAS:528:DC%2BD2sXktlOhurg%3D (Pubitemid 46632435)
12. JD Bever IA Dickie E Facelli JM Facelli J Klironomos M Moora MC Rillig W Stock M Zobel 2010 Rooting theories of plant community ecology in microbial interactions Trends Ecol Evol 25 468 478 20557974 10.1016/j.tree.2010.05.004
13. AA Calderón JM Zapata R Muñoz MA Pedreño AR Barceló 1993 Resveratrol production as part of the hypersensitive-like response of grapevine cells to an elicitor from Trichoderma viride New Phytol 124 455 463 10.1111/j.1469-8137.1993.tb03836.x
14. C Castillo-Chavez K Cooke W Huang SA Levin 1989 Results on the dynamics for modeling sexual transmission of the human immunodeficiency virus App Math Let 2 327 331 10.1016/0893-9659(89)90080-3
15. GP Cheplick A Perera K Koulouris 2000 Effect of drought on the growth of Lolium perenne genotypes with and without fungal endophytes Funct Ecol 14 657 667 10.1046/j.1365-2435.2000.00466.x (Pubitemid 32044989)
16. K Clay 1993 The ecology and evolution of endophytes Ag Ecosys Environ 44 39 64 10.1016/0167-8809(93)90038-Q (Pubitemid 24410634)
17. K Clay CL Schardl 2002 Evolutionary origins and ecological consequences of endophyte symbiosis with grasses Am Nat 160 S99 S127 18707456 10.1086/342161
18. K Clay S Marks GP Cheplick 1993 Effects of insect herbivory and fungal endophyte infection on competitive interactions among grasses Ecology 74 1767 1777 10.2307/1939935 (Pubitemid 24407743)
19. EP Donoso RO Bustamante M Carú HM Niemeyer 2008 Water deficit as a driver of the mutualistic relationship between the fungus Trichoderma harzianum and two wheat genotypes App Environ Microbiol 74 1412 1417 10.1128/AEM.02013-07 1:CAS:528:DC%2BD1cXjt1aktLw%3D (Pubitemid 351358436)
20. EA Edwards S Rawsthorne PM Mullineaux 1990 Subcellular distribution of multiple forms of glutathione reductase in leaves of pea (Pisum sativum L.) Planta 180 278 284 10.1007/BF00194008 1:CAS:528:DyaK3cXpsFGrtA%3D%3D
21. A Elmi C West 1995 Endophyte infection effects on stomatal conductance, osmotic adjustment and drought recovery of tall fescue New Phytol 131 61 67 10.1111/j.1469-8137.1995.tb03055.x
22. PW Ewald 1994 Host-parasite relations, vectors, and the evolution of disease severity Annu Rev Ecol System 14 465 485 10.1146/annurev.es.14.110183. 002341
23. SH Faeth CE Hamilton 2006 Does an asexual endophyte symbiont alter life stage and long-term survival in a perennial host grass? Microb Ecol 52 748 755 16944342 10.1007/s00248-006-9123-z (Pubitemid 44924012)
24. SH Faeth TJ Sullivan 2003 Mutualistic asexual endophytes in a native grass are usually parasitic Am Nat 161 310 325 12675375 10.1086/345937 (Pubitemid 36242556)
25. SH Faeth CJ Hayes DR Gardner 2010 Asexual endophytes in a native grass: tradeoffs in mortality, growth, reproduction, and alkaloid production Microb Ecol 50 496 504 10.1007/s00248-010-9643-4
26. CH Foyer G Noctor 2000 Oxygen processing in photosynthesis: regulation and signaling New Phytol 146 359 388 10.1046/j.1469-8137.2000.00667.x 1:CAS:528:DC%2BD3cXmsFWqurs%3D (Pubitemid 30441909)
27. CH Foyer G Noctor 2005 Oxidant and antioxidant signaling in plants: a re-evaluation of the concept of oxidative stress in a physiological context Plant Cell Environ 28 1056 1071 10.1111/j.1365-3040.2005.01327.x 1:CAS:528:DC%2BD2MXpslSgs70%3D (Pubitemid 41577022)
28. CH Foyer G Noctor 2011 Ascorbate and glutathione: the heart of the redox hub Plant Physiol 155 2 18 21205630 10.1104/pp.110.167569 1:CAS:528: DC%2BC3MXksFags7g%3D
29. CH Foyer S Shigeoka 2011 Understanding oxidative stress and antioxidant functions to enhance photosynthesis Plant Physiol 155 93 100 21045124 10.1104/pp.110.166181 1:CAS:528:DC%2BC3MXksFagsLY%3D
30. Foyer CH, Gomez LD, van Heerden PDR (2005) Glutathione. In: Smirnoff N (ed) Antioxidants and reactive oxygen species in plants. Blackwell Publishing, Oxford, UK, pp 1-18
31. TS Gechev F Van Breusegem JM Stone I Denev C Laloi 2006 Reactive oxygen species as signals that modulate plant stress responses and programmed cell death BioEssays 28 1091 1101 17041898 10.1002/bies.20493 1:CAS:528: DC%2BD28Xht1ertLnI (Pubitemid 44714119)
32. SS Gill N Tuteja 2010 Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants Plant Physiol 48 909 930 1:CAS:528:DC%2BC3cXhtlKnu7fF
33. Grace SC (2005) Phenolics as antioxidants. In: Smirnoff N (ed) Antioxidants and reactive oxygen species in plants. Blackwell Publishing, Oxford, UK, pp 141-168
34. H Hahn MT McManus K Warnstorff BJ Monahan CA Young E Davies BA Tapper B Scott 2008 Neotyphodium fungal endophytes confer physiological protection to perennial ryegrass (Lolium perenne L.) subjected to a water deficit Environ Experiment Bot 63 183 199 10.1016/j.envexpbot.2007.10.021 (Pubitemid 351313907)
35. CE Hamilton SH Faeth 2005 Asexual, systemic endophytes in grasses: a test of the seed germination and pathogen resistance hypothesis Symbiosis 38 29 32
36. CE Hamilton SH Faeth TE Dowling 2009 Distribution of hybrid fungal symbionts and environmental stress Microbial Ecol 58 408 413 10.1007/s00248-009-9504-1
37. CE Hamilton TE Dowling SH Faeth 2010 Hybridization in endophyte symbionts alters host response to moisture and nutrient treatments Microbial Ecol 59 768 775 10.1007/s00248-009-9606-9
38. GE Harman 2011 Multifunctional fungal plant symbionts: new tools to enhance plant growth and productivity New Phytol 189 647 649 21223281 10.1111/j.1469-8137.2010.03614.x
39. W-Y Huang Y-Z Cai J Xing H Corke M Sun 2007 A potential antioxidant resource: endophytic fungi from medicinal plants Economic Bot 61 14 30 10.1663/0013-0001(2007)61[14:APAREF]2.0.CO;2 1:CAS:528:DC%2BD2sXlt1Ggtro%3D (Pubitemid 46625525)
40. Isaac S (1992) Fungal-plant interactions. Chapman and Hall Publishing, London, UK
41. DA Jakson Y Chen 2004 Robust principal component analysis and outlier detection with ecological data Environmetrics 15 129 139 10.1002/env.628 (Pubitemid 38362339)
42. TA Jones MH Ralphs DR Gardner NH Chatterton 2000 Cattle prefer endophyte-free robust needlegrass J Range Manag 53 427 431 10.2307/4003755
43. K-H Kogel P Franken R Hückelhoven 2006 Endophyte or parasite - what decides? Cur Op Plant Biol 9 358 363 10.1016/j.pbi.2006.05.001 (Pubitemid 43949351)
44. M Kumar V Yadav N Tuteja AK Johri 2009 Antioxidant enzyme activities in maize plants colonized with Piriformospora indica Planta 155 780 790 1:CAS:528:DC%2BD1MXjs1WksLc%3D
45. P Lehtonen M Helander M Wink F Sporer K Saikkonen 2005 Transfer of endophyte-origin defensive alkaloids from a grass to a hemiparasitic plant Ecol Let 8 1256 1263 10.1111/j.1461-0248.2005.00834.x (Pubitemid 41752282)
46. X Liu D Mingsheng X Chen M Jiang X Lv G Yan 2007 Antioxidant activity and phenolics of an endophytic Xylaria sp. from Ginkgo biloba Food Chem 105 548 554 10.1016/j.foodchem.2007.04.008 1:CAS:528:DC%2BD2sXns1KrsLg%3D (Pubitemid 47048546)
47. Logan BA (2005) Reactive oxygen species and photosynthesis. In: Smirnoff N (ed) Antioxidants and reactive oxygen species in plants. Blackwell Publishing, Oxford, UK, pp 250-262
48. BA Logan SC Grace WW Adams B Demmig-Adams 1998 Seasonal differences in xanthophyll cycle characteristics and antioxidants in Mahonia repens growing in different light environments Oecolgia 116 9 17 (Pubitemid 28398086)
49. CP Malinowski DP Beleskey 2000 Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance Crop Sci 40 923 940 10.2135/cropsci2000.404923x 1:CAS:528:DC%2BD3cXns1Gqsb8%3D
50. CP Malinowski DP Beleskey 2006 Ecological importance of Neotyphodium spp. grass endophytes in agroecosystems Grass Sci 52 1 14 10.1111/j.1744-697X.2006. 00041.x
51. CP Malinowski GA Alloush DP Beleskey 2000 Leaf endophyte Neotyphodium coenophialum modifies mineral uptake in tall fescue Plant Soil 277 115 126 10.1023/A:1026518828237 (Pubitemid 32100654)
52. F Matsouri T Björkman GE Harman 2010 Seed treatment with Trichoderma harzianum alleviates biotic, abiotic, and physiological stresses in germinating seeds and seedlings Biological Cont 100 1213 1221
53. R Mittler 2002 Oxidative stress, antioxidants and stress tolerance Trends Plant Sci 7 405 410 12234732 10.1016/S1360-1385(02)02312-9 1:CAS:528: DC%2BD38XntVWnu7Y%3D (Pubitemid 36726490)
54. LJ Morse TA Day SH Faeth 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 10.1016/S0098-8472(02)00042-4 (Pubitemid 35404652)
55. LJ Morse SH Faeth TA Day 2007 Neotyphodium interactions with wild grasses are driven mainly by endophyte haplotype Funct Ecol 21 813 822 10.1111/j.1365-2435.2007.01285.x (Pubitemid 47052340)
56. Y Nakano K Asada 1981 Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts Plant Cell Physiol 22 867 880 1:CAS:528:DyaL3MXltFWqur0%3D
57. C Neuhauser JE Fargione 2004 A mutualism-parasitism continuum model and its application to plant-mycorrhizae interactions Ecol Model 177 337 352 10.1016/j.ecolmodel.2004.02.010 (Pubitemid 38871526)
58. Pang C-H, Wang B-S (2010) Role of ascorbate peroxidase and glutathione reductase in ascorbate-glutathione cycle and stress tolerance in plants. In: Anjum NA, Shahid U, Ming-Tsair C (eds) Ascorbate-glutathione pathway and stress tolerance in plants. Springer Publishing, New York, NY, pp 91-113
59. JL Parrent K Peay AE Arnold L Comas P Avis A Tuininga 2010 Moving from pattern to process in fungal symbioses: linking functional traits, community ecology, and Phylogenetics New Phytol 185 882 886 20356343 10.1111/j.1469-8137. 2010.03190.x
60. L-J Quan B Zhang W-W Shi J Li 2008 Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network J Integrated Plant Biol 50 2 18 10.1111/j.1744-7909.2007.00599.x 1:CAS:528:DC%2BD1cXhvVCnsrY%3D
61. S Rasmussen AJ Parsons S Bassett MJ Christensen DE Hume LJ Johnson RD Johnson WR Simpson C Stacke CR Voisey H Xue JA Newman 2007 High nitrogen supply and carbohydrate content reduce fungal endophyte and alkaloid concentration in Lolium perenne New Phytol 173 787 797 17286827 10.1111/j.1469-8137.2006.01960.x 1:CAS:528:DC%2BD2sXjvFGgsbg%3D (Pubitemid 46238738)
62. S Rasmussen A Parsons K Fraser H Xue JA Newman 2008 Metabolic profiles of endophyte-infected ryegrass Plant Physiol 146 1440 1453 18218971 10.1104/pp.107.111898 1:CAS:528:DC%2BD1cXjsVKgur8%3D (Pubitemid 352844150)
63. S Rasmussen A Parsons JA Newman 2009 Metabolomics analysis of the Lolium perenne-Neotyphodium lolii symbiosis: more than just alkaloids? Phytochem Rev 8 535 550 10.1007/s11101-009-9136-6 1:CAS:528:DC%2BD1MXht1Cqur3K
64. AR Reddy KV Chaitanya M Vivekanandan 1996 Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants J Plant Physiol 161 1189 1202 10.1016/j.jplph.2004.01.013
65. RS Redman YO Kim CJDA Woodward C Greer L Espino SL Doty RJ Rodriguez 2011 Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: a strategy for mitigating impacts of climate change PLoS One 6 e14823 21750695 10.1371/journal.pone.0014823 1:CAS:528:DC%2BC3MXpt1Grtrw%3D
66. AZ Ren X Li R Han LJ Yin MY Wei YB Gao 2010 Benefits of a symbiotic association with endophytic fungi are subject to water and nutrient availability in Achnatherum sibiricum Plant Soil 346 363 373 10.1007/s11104-011-0824-9
67. MD Richardson GW Freeman WA Meyer PV Reddy JF White Jr 1997 Endophytes from fine fescues of Europe and North America Int Turfgrass Soc 8 913 918
68. R Rodriguez R Redman 2008 More than 400 million years of evolution and some plants still can't make it on their own: Plant stress tolerance via fungal symbiosis J Exper Bot 59 1109 1114 10.1093/jxb/erm342 1:CAS:528: DC%2BD1cXjs1KhurY%3D (Pubitemid 351644646)
69. R Rodriguez J Henson E van Volkenburgh M Hoy L Wright F Beckwith K Yong-Ok RS Redman 2008 Stress tolerance in plants via habitat-adapted symbiosis ISME J 2 404 416 18256707 10.1038/ismej.2007.106 (Pubitemid 351518399)
70. N Rouhier J-P Jacquot 2008 Getting sick may help plants overcome abiotic stress New Phytol 180 738 741 19138229 10.1111/j.1469-8137.2008.02673.x 1:CAS:528:DC%2BD1MXivFyltw%3D%3D
71. GJG Ruijter J Bax PJI van de Vondervoort RP de Vries PA vanKuyk J Visser 2003 Mannitol is required for stress tolerance in Aspergillus niger conidiospores Eukaryotic Cell 2 690 698 12912888 10.1128/EC.2.4.690-698.2003 1:CAS:528:DC%2BD3sXmsFymsLs%3D (Pubitemid 36996715)
72. K Saikkonen 2007 Forest structure and fungal endophytes Fung Biol Rev 21 67 74 10.1016/j.fbr.2007.05.001 (Pubitemid 47405317)
73. K Saikkonen SH Faeth M Helander TJ Sullivan 1998 Fungal endophytes: a continuum of interactions with host plants Annu Rev Ecolog Syst 29 319 343 10.1146/annurev.ecolsys.29.1.319 (Pubitemid 29033035)
74. SAS Institute, Inc (2004) version 9.1.3 Car. SAS Institute, North Carolina, USA
75. C Schardl 2002 Epichloë festucae and related mutualistic symbionts of grasses Func Gen Biol 35 69 79
76. CL Schardl TD Phillips 1997 Protective grass endophytes. Where are they from and where are they going? Plant Dis 81 430 438 10.1094/PDIS.1997.81.5.430
77. FM Schulthess SH Faeth 1998 Distribution abundances, and associations of the endophytic fungal community of Arizona fescue (Festuca arizonica) Mycologia 90 569 578 10.2307/3761215 (Pubitemid 28385827)
78. H-B Shao L-Y Chu Z-H Lu C-M Kang 2008 Primary antioxidant free radical scavenging and redox signaling pathways in higher plant cells Int J Biol Sci 4 8 14 10.7150/ijbs.4.8 1:CAS:528:DC%2BD1cXjvVWqs70%3D
79. P Sharma RS Dubey 2005 Modulation of nitrate reductase activity in rice seedlings under aluminum toxicity and water stress: role of osmolytes as enzyme protectant J Plant Physiol 162 854 864 16146311 10.1016/j.jplph.2004.09.011 1:CAS:528:DC%2BD2MXhtVKqtbzL (Pubitemid 41059475)
80. Smirnoff N (2005) Antioxidants and reactive oxygen species in plants. Blackwell Publishing, Oxford, UK
81. IK Smith TL Vierhell CA Thorne 1989 Properties and functions of glutathione reductase in plants Physiologia Plant 77 449 456 10.1111/j.1399-3054.1989.tb05666.x 1:CAS:528:DyaK3cXpsFChsg%3D%3D
82. StatSoft Software version 5.1 for Windows (1998) StatSoft Tulsa, OK, USA
83. G Strobel B Daisy U Castillo J Harper 2004 Natural products from endophytic microorganisms J Nat Prod 67 257 268 14987067 10.1021/np030397v 1:CAS:528:DC%2BD2cXhtVaku7c%3D (Pubitemid 38282917)
84. TJ Sullivan SH Faeth 2004 Gene flow in the endophyte Neotyphodium and implications for coevolution with Festuca arizonica Molec Ecol 13 649 656 10.1046/j.1365-294X.2004.02091.x 1:STN:280:DC%2BD2c%2FntVCguw%3D%3D (Pubitemid 38260946)
85. TJ Sullivan SH Faeth 2008 Local adaptation in Festuca arizonica infected by hybrid and nonhybrid Neotyphodium endophytes Microb Ecol 55 697 704 17943341 10.1007/s00248-007-9312-4 1:STN:280:DC%2BD1cnltlOmsA%3D%3D (Pubitemid 351601283)
86. M Tadych M Bergen FM Dugan JF White Jr 2007 Evaluation of the potential role of water in spread of conidia of the Neotyphodium endophyte of Poa ampla Mycolog Research 111 466 472 10.1016/j.mycres.2007.02.002 (Pubitemid 46819001)
87. A Tanaka MJ Christensen D Takemoto P Pyoyun B Scott 2006 Reactive oxygen species play a role in regulating a fungus-perennial ryegrass mutualistic interaction Plant Cell 18 1052 1066 16517760 10.1105/tpc.105.039263 1:CAS:528:DC%2BD28Xjslaktr4%3D (Pubitemid 43956153)
88. CM Van der Weele WG Spollen RE Sharp TI Baskin 2000 Growth of Arabidopsis thaliana seedlings under water deficit studies by control of water potential in nutrient-agar media J Exp Bot 51 1555 1562 11006306 10.1093/jexbot/51.350.1555
89. PE Verslues EA Bray 2004 LWR1 and LWR2 are required for osmoregulation and osmotic adjustment in Arabidopsis Plant Physiol 136 2831 2842 15347788 10.1104/pp.104.045856 1:CAS:528:DC%2BD2cXnvFOqsrY%3D
90. F Waller B Achatz H Baltruscaht J Fodor K Becker M Fischer T Heier R Hückelhoven C Neumann D von Wettstein P Franken KH Kogel 2005 The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield Proc Nat Acad Sci 102 13386 13391 16174735 10.1073/pnas.0504423102 1:CAS:528:DC%2BD2MXhtVygsbnJ (Pubitemid 41420857)
91. JF White MS Torres 2010 Is plant endophyte-mediated defensive mutualism the result of oxidative stress protection? Physiologia Plant 138 440 446 10.1111/j.1399-3054.2009.01332.x 1:CAS:528:DC%2BC3cXktlOkt7Y%3D
92. White JF, Bacon CW, Hywel-Jones, NL, Spatafora, JW (2003) Historical perspectives: human interactions with Clavicipitalean fungi. In: White JF, Bacon CW, Hywel-Jones, NL, Spatafora, JW eds. Clavicipitalean Fungi: evolutionary biology, chemistry, biocontrol, and cultural impacts. New York, NY, pp 1-14
93. Y Yang C Han Q Liu B Lin W Wang 2008 Effect of drought and low light on growth and enzymatic antioxidant system of Picea asperata seedlings Acta Physiol Plant 30 433 440 10.1007/s11738-008-0140-z 1:CAS:528:DC%2BD1MXitV2jsbo%3D
94. YP Zhang ZB Nan 2007 Growth and anti-oxidative systems changes in Elymus dahuricusis affected by Neotyphodium endophyte under contrasting water availability J Ag Crop Sci 193 377 386 10.1111/j.1439-037X.2007.00279.x 1:CAS:528:DC%2BD2sXhsVGitbzM (Pubitemid 350045686)
95. YP Zhang ZB Nan 2010 Germination and seedling anti-oxidative enzymes of endophyte-infected populations of Elymus dahuricus under osmotic stress Seed Sci Technol 38 522 527