Positive plant microbial interactions in perennial ryegrass dairy pasture systems

Annals of Applied Biology

Volumn 159, Issue 1, 2011, Pages 79-92

  Andrews, M ^a   Edwards, G R ^a   Ridgway, H J ^a   Cameron, K C ^a   Di, H J ^a   Raven, J A ^b  

^a LINCOLN UNIVERSITY   (New Zealand)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Ammonia oxidising bacteria; denitrifying bacteria; fungal endophytes; methanogens; mycorrhizas; nitrification inhibitors; nitrifying bacteria; phosphorus solubilising bacteria; rhizobia; rumen microbes

Indexed keywords

ALKALOID; AMMONIA; BACTERIUM; DAIRY FARMING; ENDOPHYTE; ENZYME ACTIVITY; FERTILIZER; FUNGUS; GRASS; GREENHOUSE GAS; HERB; HOST PLANT; INHIBITOR; INOCULATION; METHANE; METHANOGENESIS; MILK PRODUCTION; MYCORRHIZA; NITRIFICATION; NITROGEN FIXATION; NUTRIENT AVAILABILITY; NUTRIENT UPTAKE; PASTURE; PERENNIAL PLANT; SOIL NUTRIENT;

AUSTRALASIA;

BACTERIA (MICROORGANISMS); HEXAPODA; LOLIUM PERENNE; NEOTYPHODIUM; NEOTYPHODIUM LOLII; RHIZOBIACEAE; TRIFOLIUM REPENS;

EID: 79959380398     PISSN: 00034746     EISSN: 17447348     Source Type: Journal    
DOI: 10.1111/j.1744-7348.2011.00473.x     Document Type: Article

References (123)

1. ADAS. (1990) Nitrogen for Grassland. London, UK: MAFF.
2. Amberger A., (1989) Research on dicyandiamide as a nitrification inhibitor and future outlook. Communications in Soil Science and Plant Analysis, 20, 1933-1955.
3. Andrews M., James E.K., Cummings S.P., Zavalin A.A., Vinogradova L.V., McKenzie B.A., (2003) Use of nitrogen fixing bacteria inoculants as a substitute for nitrogen fertiliser for dryland graminaceous crops: progress made, mechanisms of action and future potential. Symbiosis, 35, 209-229. (Pubitemid 36409118)
4. Andrews M., Lea P.J., Raven J.A., Lindsey K., (2004) Can genetic manipulation of plant nitrogen assimilation enzymes result in increased crop yield and greater N-use efficiency? An assessment. Annals of Applied Biology, 145, 25-40. (Pubitemid 41694628)
5. Andrews M., Scholefield D., Abberton M.T., McKenzie B.A., Hodge S., Raven J.A., (2007). Use of white clover as an alternative to nitrogen fertiliser for dairy pastures in nitrate vulnerable zones in the UK: productivity, environmental impact and economic considerations. Annals of Applied Biology, 151, 11-23. (Pubitemid 47174188)
6. Andrews M., Lea P.J., Raven J.A., Azevedo R.A., (2009) Nitrogen use efficiency. 3. Nitrogen fixation. Genes and costs. Annals of Applied Biology, 155, 1-13.
7. Andrews M., Hodge S., Raven J.A., (2010) Positive plant microbial interactions. Annals of Applied Biology, 157, 317-320.
8. Barker G.M., Pottinger R.P., Addison P.J., (1984) Effects of Argentine Stem Weevil on productivity of grasses in the Waikato. New Zealand Journal of Agricultural Research, 27, 93-102.
9. Blaxter K.L., Clapperton J.L., (1965) Prediction of the amount of methane produced by ruminants. British Journal of Nutrition, 19, 511-522.
10. Bluett S.J., Thom E.R., Clark D.A., Macdonald K.A., Minee E.M.K., (2003) Milk solid production from cows grazing perennial ryegrass containing AR1 or wild endophyte. Proceedings of the New Zealand Grassland Association, 65, 83-90.
11. Bluett S.J., Thom E.R., Clark D.A., Macdonald K.A., Minee E.M.K., (2005) Effects of perennial ryegrass infected with either AR1 or wild type endophyte on dairy production in the Waikato. New Zealand Journal of Agricultural Research, 48, 197-212. (Pubitemid 41044943)
12. Bremner J.M., (1997) Sources of nitrous oxide in soils. Nutrient Cycling in Agroecosystems, 49, 7-16.
13. Brown L., Syed B., Jarvis S.C., Sneath R.W., Phillips V.R., Goulding K.W.T., Li C., (2002) Development and application of a mechanistic model to estimate emission of nitrous oxide from UK agriculture. Atmospheric Environment, 36, 917-928. (Pubitemid 34097778)
14. Cheng Y., Edwards J.E., Allison G.G., Zhu W-Y., Theodorou M.K., (2009) Diversity and activity of enriched ruminal cultures of anaerobic fungi and methanogens grown together on lignocellulose in consecutive batch culture. Bioresource Technology, 100, 4821-4828.
15. Clay K., Schardl C.L., (2002) Evolutionary origins and ecological consequences of endophytes symbiosis with grasses. American Naturalist, 160 (Suppl), S99-S127.
16. Cordell D., Drangert J-O., White S., (2009) The story of phosphorus: global food security and food for thought. Global Environmental Change, 19, 292-305.
17. Covacevich F., Marino M.A., Echeverría H.E., (2006) The phosphorus source determines the arbuscular mycorrhizal potential and the native mycorrhizal colonisation of tall fescue and wheatgrass. European Journal of Soil Biology, 42, 127-138. (Pubitemid 44292030)
18. Crush J.R., (1974) Plant growth responses to vesicular-arbuscular mycorrhiza. Vll. Growth and nodulation of some herbage legumes. New Phytologist, 73, 743-749.
19. Cummings S.P., Gyaneshwar P., Vinuesa P., Farrugia F.T., Andrews M., Humphry D., Elliot G.N., Nelson A., Orr C., Pettitt D., Shah G.R., Santos S.R., Krishnan H.B., Odee D., Moreira F.M.S., Sprent J.I., Young J.P.W., James E.K., (2009) Nodulation of Sesbania species by Rhizobium (Agrobacterium) strain IRBG74 and other rhizobia. Environmental Microbiology, 11, 2510-2525.
20. De Clercq P., Gertsis A.C., Hofman G., Jarvis S.C., Neeteson J.J., Sinabell F., (2001) Nutrient Management Legislation in European Countries. Wageningen, the Netherlands: Wageningen Press.
21. DEFRA. (2002) Ammonia in the UK. DEFRA. URL [accessed on September 2010].
22. Di H.J., Cameron K.C., (2002a) Nitrate leaching in temperate agroecosystems: sources, factors and mitigating strategies. Nutrient Cycling in Agroecosystems, 64, 237-256. (Pubitemid 36092962)
23. Di H.J., Cameron K.C., (2002b) The use of a nitrification inhibitor, dicyandiamide (DCD), to decrease nitrate leaching and nitrous oxide emissions in a simulated grazed and irrigated grassland. Soil Use and Management, 18, 395-403. (Pubitemid 36093085)
24. Di H.J., Cameron K.C., (2004) Effects of the nitrification inhibitor, dicyandiamide on potassium, magnesium and calcium leaching in grazed grassland. Soil Use and Management, 20, 2-7. (Pubitemid 38571995)
25. Di H.J., Cameron K.C., (2005) Reducing environmental impacts of agriculture by using a fine particle suspension nitrification inhibitor to decrease nitrate leaching from grazed pastures. Agriculture, Ecosystems and Environment, 109, 202-212. (Pubitemid 40968391)
26. Di H.J., Cameron K.C., Sherlock R.R., (2007) Comparison of the effectiveness of a nitrification inhibitor, dicyandiamide (DCD), in reducing nitrous oxide emissions in four different soils under different climatic and management conditions. Soil Use and Management, 23, 1-9. (Pubitemid 46376247)
27. Di H.J., Cameron K.C., Shen J.P., Winefield C.S., O'Callaghan M., Bowatte S., He J.Z., (2009) Nitrification driven by bacteria and not archaea in nitrogen rich grassland soils. Nature Geoscience, 2, 621-624.
28. Di H.J., Cameron K.C., Shen J.P., Winefield C.S., O'Callaghan M., Bowatte S., He J.Z., (2010) Ammonia oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiology Ecology, 72, 386-394.
29. Dodd I.C., Zinovkina N.Y., Safronova W.I., Belimov A.A., (2010) Rhizobacterial mediation of plant hormone status. Annals of Applied Biology, 157, 361-379.
30. Easton H.S., Fletcher L.R., (2007) The importance of endophyte in agricultural systems-changing plant and animal productivity. In Proceedings of the 6th International Symposium on Fungal Endophytes of Grasses. Grassland Research and Practice Series. Volume 13, pp. 11-18.
31. Edwards G.R., Lucas R.J., Johnson M.R., (1993) Grazing preference for pasture species by sheep is affected by endophyte and nitrogen fertility. Proceedings of the New Zealand Grassland Association, 55, 137-141.
32. Edwards G.R., Parsons A.J., Rasmussen S., (2007a) High sugar ryegrasses for dairy systems. In Meeting the Challenges for Pasture-Based Dairying, Proceedings of the 3rd Dairy Science Symposium, pp. 307-334. Eds, D.F. Chapman, D.A. Clark, K.L. Macmillan, and, D.P. Nation,. Melbourne, Australia: National Dairy Alliance.
33. Edwards G.R., Parsons A.J., Rasmussen S., Bryant R., (2007b) High sugar grasses for livestock systems in New Zealand. Proceedings of the New Zealand Grassland Association, 69, 161-171.
34. Edwards J.E., Kim E.J., Scollan N.D., Newbold C.J., Kingston-Smith A.H., (2009) The plant-microbe interactome in ruminants: identification of control for mitigation of negative ecosystem outputs. Positive plant microbial interactions in relation to plant performance and ecosystem function. Aspects of Applied Biology, 98, 91-99.
35. Faeth S.H., (2002) Are endophytic fungi defensive plant mutualists. Oikos, 98, 25-36. (Pubitemid 34877836)
36. Fletcher L.R., Sutherland B.L., Fletcher C.G., (1999) The impact of endophyte on the health and productivity of sheep grazing perennial ryegrass pastures. In Ryegrass Endophyte: an Essential New Zealand Symbiosis, pp. 11-17. Eds, D.R. Woodfield, and, C. Matthew,. Grassland Research and Practice Series No. 7. Dunedin, New Zealand: New Zealand Grassland Association.
37. Foy R.H., Withers P.J.A., (1995) The contribution of agricultural phosphorus to eutrophication. Fertilizer Society Proceedings, 365, 1-32.
38. Frame J., (1992) Improved Grassland Management. Ipswich, UK: Farming Press Books.
39. Gallagher R.T., Hawkes A.D., Steyn P.S., Vleggaar R., (1984) Tremorgenic neurotoxins from perennial ryegrass causing ryegrass staggers disorder of livestock: structure and elucidation of lolitrem B. Journal of Chemical Society, Chemical Communications, 9, 614-616.
40. Gill M., Smith P., Wilkinson J.M., (2010) Mitigating climate change: the role of domestic livestock. Animal, 4, 323-333.
41. Gourley C.J.P., Awty I., O'Doherty M., Aarons S.R., (2001) Phosphorus fertilizer requirements for temperate dairy pastures and milk production in south eastern Australia. In Proceedings of the XIX Grassland Congress, 11-21 February, Sao Pedro, Sao Paulo, Brazil, pp. 175-176.
42. Grimoldi A.A., Kavanová M., Lattanzi F.A., Schnydeer H., (2005) Phosphorus nutrition-mediated effects of arbuscular mycorrhiza on leaf morphology and carbon allocation in perennial ryegrass. New Phytologist, 168, 435-444.
43. Halder A.K., Chakrabartty P.K., (1993) Solubilization of inorganic phosphate by Rhizobium. Folia Microbiology, 38, 325-330.
44. Haygarth P.M., Chapman P.J., Jarvis S.C., Smith R.V., (1998a) Phosphorus budgets for two contrasting grassland farming systems in the UK. Soil Use and Management, 14, 160-167.
45. Haygarth P.M., Hepworth L., Jarvis S.C., (1998b). Forms of phosphorus transfer in hydrological pathways from soil under grazed grassland. European Journal of Soil Science, 49, 65-72. (Pubitemid 28178453)
46. Haynes R.J., Williams P.H., (1993) Nutrient cycling and soil fertility in the grazed pasture ecosystem. Advances in Agronomy, 49, 119-199.
47. Haystead A., Malajczuk N., Grove T.S., (1988) Underground transfer of nitrogen between pasture plants infected with vesicular-arbuscular mycorrhizal fungi. New Phytologist, 108, 417-423.
48. Hodgson J., White J.G.H., Eds. (1999) New Zealand Pasture and Crop Science. Oxford, UK: Oxford University Press.
49. Hume D.E., Barker D.J., (2005) Growth and management of endophytic grasses in pastoral agriculture. In Neotyphodium in Cool Season Grasses, pp. 201-226. Eds, C.A. Roberts, C.P. West, and, D.E. Spiers,. Ames, IA, USA: Blackwell.
50. Humphreys M.O., (1989) Water-soluble carbohydrates in perennial ryegrass breeding. III. Relationships with herbage production, digestibility and crude protein content. Grass and Forage Science, 44, 423-429.
51. Igbal M.F., Cheng Y-F., Zhu W-Y., Zeshan B., (2008) Mitigation of ruminant methane production: current strategies, constraints and future options. World Journal of Microbiology and Biotechnology, 24, 2747-2755.
52. Igual J.M., Valverde A., Cervantes E., Velazquez E., (2001) Phosphate-solubilizing bacteria as inoculants for agriculture: use of updated molecular techniques in their study. Agronomie, 21, 561-568. (Pubitemid 34018147)
53. Jarvis S.C., (1993) Nitrogen cycling and losses from dairy farms. Soil Use and Management, 9, 99-105.
54. Jarvis S.C., (2000) Progress in studies of nitrate leaching from grassland soils. Soil Use and Management, 16, 152-156. (Pubitemid 30597807)
55. Jasper D.A., Robson A.D., Abbott L.K., (1979) Phosphorus and the formation of vesicular-arbuscular mycorrhizas. Soil Biology and Biochemistry, 11, 501-505.
56. Jensen J.G., Popay A.J., (2004) Perennial ryegrass infected with AR37 endophyte reduces survival of porina larvae. New Zealand Plant Protection, 57, 323-328.
57. 3 deposition processes for mixed moorland vegetation. Atmospheric Environment, 41, 2049-2060.
58. 3 deposition processes for stomatal and non-stomatal moorland species. Atmospheric Environment, 41, 8980-8994.
59. Jorquera M.A., Hernandez M.T., Rengel Z., Marschner P., de la Luz Mora M., (2008) Isolation of culturable phosphobacteria with both phytate-mineralization and phosphate-solubilization activity from the rhizosphere of plants grown in volcanic soil. Biology and Fertility of Soils, 44, 1025-1034.
60. Kingston-Smith A.H., Thomas H.M., (2003) Strategies of plant breeding for improved rumen function. Annals of Applied Biology, 142, 13-24. (Pubitemid 36658556)
61. Latch G.C.M., (1989) Plant improvement using endophytic fungi. In Proceedings of the XVI International Grassland Congress, 4-11 October, Nice, France, pp. 1345-1346.
62. Latch G.C.M., (1994) Influence of Acremonium endophytes on perennial ryegrass improvement. New Zealand Journal of Agricultural Research, 25, 443-448.
63. Latch G.C.M., Hunt W.F., Musgrave D.R., (1985) Endophytic fungi affect growth of perennial ryegrass. New Zealand Journal of Agricultural Research, 28, 165-168.
64. Ledgard S.F., (2001) Nitrogen cycling in low input legume-based agriculture, with emphasis on legume/grass pastures. Plant and Soil, 228, 43-59. (Pubitemid 32145140)
65. Ledgard S.F., Penno J.W., Sprosen M.S., (1999) Nitrogen inputs and losses from clover/grass pastures grazed by dairy cows, as affected by nitrogen fertiliser application. Journal of Agricultural Science, 132, 215-225. (Pubitemid 29139229)
66. Lee M.R.F., Harris L.J., Moorby J.M., Humphreys M.O., Theodorou M.K., MacRae J.C., Scollan N.D., (2002) Rumen metabolism and nitrogen flow to the small intestine in steers offered Lolium perenne containing different levels of water-soluble carbohydrate. Animal Science, 74, 587-596. (Pubitemid 34853682)
67. Lewis G.C., Ravel C., Naffaa W., Astier C., Charmet G., (1997) Occurrence of Acremonium endophytes in wild populations of Lolium spp. in European countries and a relationship between level of infection and climate in France. Annals of Applied Biology, 130, 227-238. (Pubitemid 27383511)
68. Lovett D.K., McGilloway D., Bortolozzo A., Hawkins M., Callan J., Flynn B., O'Mara F.P., (2006) In vitro fermentation patterns and methane production as influenced by cultivar and season of harvest of Lolium perenne L. Grass and Forage Science, 61, 9-21.
69. MAFF. (2000) Fertiliser Recommendations for Agricultural and Horticultural Crops (RB209). London, UK: MAFF, London Stationery Office.
70. Martin C., Morgavi D.P., Doreau M., (2010) Methane mitigation in ruminants: from microbe to the farm scale. Animal, 4, 351-365.
71. McLaren R.G., Cameron K.C., (1996) Soil Science: Sustainable Production and Environmental Protection. Auckland, New Zealand: Oxford University Press. 304 pp.
72. McNeil A.M., Penfold C.M., (2009) Agronomic management options for phosphorus in Australian dryland organic and low-input cropping systems. Crop and Pasture Science, 60, 163-182.
73. Merry R.J., Lee M.R.F., Davies D.R., Moorby J.M., Dewhurst R.J., Scollan N.D., (2003) Nitrogen and energy use efficiency in the rumen of cattle fed high sugar grass and/or red clover silage. Crop quality: its role in sustainable livestock production. Aspects of Applied Biology, 70, 87-92. (Pubitemid 38271246)
74. MfE. (2008) New Zealand's Greenhouse Gas Inventory 1990-2006: the National Inventory Report and Common Reporting Format, July 2007. Wellington, New Zealand: Ministry for the Environment.
75. Miller L.A., Moorby J.M., Davies D.R., Humphreys M.O., Scollan N.D., MacRae J.C., Theodorou M.K., (2001) Increased concentration of water-soluble carbohydrate in perennial ryegrass (Lolium perenne L.). Milk production from late-lactation dairy cows. Grass and Forage Science, 56, 383-394. (Pubitemid 34140176)
76. Moir J.L., Cameron K.C., Di H.J., (2007) Effects of the nitrification inhibitor dicyandiamide on soil mineral N, pasture yield, nutrient uptake and pasture quality in a grazed pasture system. Soil Use and Management, 23, 111-120. (Pubitemid 46800465)
77. Monteny G.J., Smits M.C.J., Van Duinkerken G., Mollenhurst H., de Boer I.J.M., (2002) Prediction of ammonia emission from dairy barns using feed characteristics. Part II: relation between urinary urea concentration and ammonia emission. Journal of Dairy Science, 83, 3389-3394. (Pubitemid 38583331)
78. Nash D.M., Halliwell D.J., (1999) Fertilisers and phosphorus loss from productive grazing systems. Australian Journal of Soil Research, 37, 403-429. (Pubitemid 29228629)
79. Newton A.C., Gravouil C., Fountaine J.M., (2010) Managing the ecology of foliar pathogens: ecological tolerance in crops. Annals of Applied Biology, 157, 343-359.
80. Novak K., (2010) On the efficiency of legume supernodulating mutants. Annals of Applied Biology, 157, 321-342.
81. O'Brien M., Mullins E., (2009) Relevance of genetically modified crops in light of future environmental and legislative challenges to the agri-environment. Annals of Applied Biology, 154, 323-340.
82. Oliveira J.A., Castro V., (1997) Incidence and viability of Acremonium endophytes in tall fescue accessions from northern Spain. Genetic Resources and Crop Evolution, 44, 519-522. (Pubitemid 27456746)
83. Parry M.A.J., Lea P.J., (2009) Food security and drought. Annals of Applied Biology, 155, 299-300.
84. Patra A.K., Saxena J., (2009) Dietary phytochemicals as rumen modifiers: a review of the effects on microbial populations. Antonie van Leeuwenhoek, 96, 363-375.
85. Peix A., Rivas-Boyero A.A., Mateos P.F., Rodríguez-Barrueco C., Martínez-Molina E., Velázquez E., (2001) Growth promotion of chickpea and barley by a phosphate solubilising strain of Mesorhizobium mediterraneum under growth chamber conditions. Soil Biology and Biochemistry, 33, 103-110. (Pubitemid 32062506)
86. Pennell C.G.L., Popay A.J., Ball O.-J.-P., Hume D.E., Baird D.B., (2005) Occurrence and impact of pasture mealybug (Balanococcus poae) and root aphid (Aploneura lentisci) on ryegrass (Lolium spp.) with and without infection by Neotyphodium fungal endophytes. New Zealand Journal of Agricultural Research, 48, 329-337. (Pubitemid 41501095)
87. Piccini D., Azcón R., (1987) Effect of phosphate-solubilizing bacteria and vesicular arbuscular mycorrhizal (VAM) on the utilization of bayoran rock phosphate by alfalfa plants using a sand-vermiculite medium. Plant and Soil, 101, 45-50.
88. Popay A.J., Bonos S.A., (2005) Biotic responses in endophytic grasses. In Neotyphodium in Cool Season Grasses, pp. 163-185. Eds, C.A. Roberts, C.P. West, and, D.E. Spiers,. Ames, IA, USA: Blackwell.
89. Popay A.J., Thom E.R., (2009) Endophyte effects on major insect pests in Waikato dairy pasture. Proceedings of the New Zealand Grassland Association, 71, 121-126.
90. Popay A.J., Hume D.E., Baltus J.G., Latch G.C.M., Tapper B.A., Lyons T.B., Cooper B.M., Pennell C.G., Eerens J.P.J, Marshall S.L., (1999) Field performance in perennial ryegrass (Lolium perenne) infected with toxin-free fungal endophytes (Neotyphodium spp). In Ryegrass Endophyte: an Essential New Zealand Symbiosis, pp. 112-122. Eds, D.R. Woodfield, and, C. Matthew,. Grassland Research and Practice Series No. 7. New Zealand Grassland Association.
91. Powlson D.S., Addiscott T.M., Benjamin N., Cassman K.G., de Kok T.M., van Grinsven H., L'Hirondel J.L., Avery A.A., van Kessel C., (2008) When does nitrate become a risk for humans? Journal of Environmental Quality, 37, 291-295. (Pubitemid 351399248)
92. Prestidge R.A., Pottinger R.P., Barker G.M., (1982) An association of Lolium endophyte with ryegrass resistance to Argentine Stem Weevil. In Proceedings of the 35th New Zealand Weed and Pest Conference, 9-12 August, Waikato, New Zealand, pp. 119-122.
93. Prestidge R.A., Popay A.J., Ball O.J.P., (1994) Biological control of pasture pests using Acremonium spp. endophytes. Proceedings of the New Zealand Grassland Association, 56, 33-38.
94. Ravel C., Charmet G., Balfourier F., (1995) Influence of the fungal endophyte Acremonium lolii on agronomic traits of perennial ryegrass in France. Grass and Forage Science, 50, 75-80.
95. Ravel C., Courty C., Coudret A., Charmet G., (1997) Beneficial effects of Neotyphodium lolii on the growth and water status in perennial ryegrass cultivated under nitrogen deficiency or drought stress. Agronomie, 17, 173-181. (Pubitemid 27237695)
96. Raven J.A., (2010) Why are mycorrhizal fungi and symbiotic nitrogen-fixing bacteria not genetically integrated into plants? Annals of Applied Biology, 157, 381-391.
97. Raven J.A., Taylor R., (2003) Macroalgal growth in a nutrient-enriched estuary: a biogeochemical perspective. Water, Air and Soil Pollution: Focus, 3, 7-26. (Pubitemid 39130862)
98. Raven J.A., Handley L.L., Andrews M., (2004) Global aspects of C/N interactions determining plant-environment interactions: implications for crop production. Journal of Experimental Botany, 55, 11-25. (Pubitemid 38069739)
99. Raven J.A., Andrews M., Quigg A., (2005) The evolution of oligotrophy: implications for the breeding of crop plants for low input agricultural systems. Annals of Applied Biology, 147, 261-280. (Pubitemid 40728383)
100. Rogers J.B., Laidlaw A.S., Christie P., (2001) The role of arbuscular mycorrhizal fungi in the transfer of nutrients between white clover and perennial ryegrass. Chemosphere, 42, 153-159. (Pubitemid 33648273)
101. Royal Society. (2009) Reaping the Benefits: science and the Sustainable Intensification of Global Agriculture. London, UK: Marcel Dekker, Inc.
102. Ryan M., Ash J., (1999) Effects of phosphorus and nitrogen on growth of pasture plants and VAM fungi in SE Australian soils with contrasting fertiliser histories (conventional and biodynamic). Agriculture, Ecosystems and Environment, 73, 51-62. (Pubitemid 29163439)
103. Ryan M.H., Small D.R., Ash J.E., (2000) Phosphorus controls the level of colonisation by arbuscular mycorrhizal fungi in conventional and biodynamic irrigated dairy pastures. Australian Journal of Experimental Agriculture, 40, 663-670.
104. Scullion J., Eason W.R.I., Scott E.P., (1998) The effectivity of arbuscular mycorhizal fungi from high input conventional and organic grassland and grass-arable rotations. Plant and Soil, 204, 243-254. (Pubitemid 29079705)
105. Shepherd M., Pearce B., Cormack B., Philipps L., Cuttle S., Bhogal A., Costigan P., Unwin R., (2003) An assessment of the environmental impacts of organic farming. Review for Defra Funded Project OFO4O5. URL [accessed on 27 November 2010].
106. Sherlock R.R., Sommer S.G., Khan R.Z., Wood C.W., Guertal E.A., Freney J.R., Dawson C.O., Cameron K.C., (2002) Ammonia, methane and nitrous oxide emission from pig slurry applied to a pasture in New Zealand. Journal of Environmental Quality, 31, 1491-1501.
107. Shibata R., Yano K., (2003) Phosphorus acquisition from non-labile sources in peanut and pigeonpea with mycorrhizal interaction. Applied Soil Ecology, 24, 133-141. (Pubitemid 37143284)
108. Smith S.E., Facelli E., Pope S., Smith F.A., (2010) Plant performance in stressful environments: interpreting new and established knowledge of the roles of arbuscular mycorrhizas. Plant and Soil, 326, 3-20.
109. Taylor R., Smith L., (1997) The State of New Zealand's Environment. Wellington, New Zealand: Publications for Ministry for Environment.
110. Taylor R., Fletcher R.J., Raven J.A., (2001) The growth of selected 'green tide' algae in laboratory culture. Botanica Marina, 44, 327-336.
111. Theodorou M.K., France J., (1993) Rumen microorganisms and their interactions. In Quantitative Aspects of Ruminant Digestion and Metabolism, pp. 145-162. Eds, J.M. Forbes, and, J. France,. Wallingford, UK: CAB International.
112. Thom E.R., Clark D.A., Waugh C.D., (1999) Endophyte and dairy production in New Zealand: experience at the Dairying Research Corporation. In Ryegrass Endophyte: an Essential New Zealand Symbiosis, pp. 39-44. Eds, D.R. Woodfield, and, C. Matthew,. Grassland Research and Practice Series No. 7. New Zealand Grassland Association.
113. Thomson B.D., Robson A.D., Abbott L.K., (1992) The effect of long term application of phosphorus fertilizer on populations of vesicular-arbuscular mycorrhizal fungi in pastures. Australian Journal of Agricultural Research, 43, 1131-1142.
114. Thomson N.A., Roberts A.H.C., McCallum A., Judd T.G., Johnson R.J., (1993) How much fertilizer is enough? In Proceedings of the Ruakura Farmers Conference, Hamilton, New Zealand, June 1993.
115. Tikhonovich I.A., Provorov N.A., (2009) From plant-microbe interactions to symbiogenetics: a universal paradigm for the interspecies genetic integration. Annals of Applied Biology, 154, 341-350.
116. Tisdall J.M., Oades J.M., (1979) Stabilisation of soil aggregates by the root systems of ryegrass. Australian Journal of Soil Research, 17, 429-441.
117. Ulyatt M.J., Thomson D.J., Beever D.E., Evans R.T., Haines M.J., (1988) The digestion of perennial rye-grass (Lolium perenne cv. Melle) and white clover (Trifolium repens cv. Blanca) by grazing cattle. British Journal of Nutrition, 60, 137-149.
118. Ward M.H., de Kok T.M., Levallois P., Brender J., Gulis G., Nolan B.T., van Derslice J., (2005) Workgroup Report: drinking-water nitrate and health-recent findings and research needs. Environmental Health Perspectives, 113, 1607-1614. (Pubitemid 41614919)
119. Widdup K.H., Ryan D.L., (1992) Forage potential of wild populations of perennial ryegrass collected from southern New Zealand farms. Proceedings of the New Zealand Grassland Association, 54, 161-165.
120. Williams Y.J., Popovski S., Rea S.M., Skillman L.C., Toovey A.F., Northwood K.S., Wright A.D.G., (2009) A vaccine against rumen methanogens can alter the composition of archaeal populations. Applied and Environmental Microbiology, 75, 1860-1866.
121. 3 by Lolium perenne. Botanica Acta, 106, 42-52.
122. 3 for acid-base and cation-anion balance in Lolium perenne. Physiologia Plantarum, 89, 519-523.
123. Zhu Y.G., Laidlaw A.S., Christie P., Hammond M.E.R., (2000) The specificity of arbuscular mycorrhizal fungi in perennial ryegrass-white clover pasture. Agriculture, Ecosystems & Environment, 77, 211-218. (Pubitemid 30044461)