Impact of pea growth and arbuscular mycorrhizal fungi on the decomposition of 15N-labeled maize residues

Biology and Fertility of Soils

Volumn 48, Issue 5, 2012, Pages 547-560

  Jannoura, Ramia ^a   Kleikamp, Bernd ^b   Dyckmans, Jens ^c   Joergensen, Rainer Georg ^a  

^a UNIVERSITY OF KASSEL   (Germany)

^b Life Science Coach and Consult   (Germany)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

13C; 15N; Arbuscular mycorrhizal fungi; Decomposition; Maize residues; Microbial biomass; Particulate organic matter; Peas

Indexed keywords

ARBUSCULAR MYCORRHIZA; CARBON ISOTOPE; CROP RESIDUE; CROP YIELD; DECOMPOSITION; FUNGUS; GROWTH RATE; LEGUME; NITROGEN ISOTOPE; PARTICULATE ORGANIC MATTER; ROOT COLONIZATION; SOIL MICROORGANISM; SOIL NITROGEN; SOIL NUTRIENT; SYMBIOSIS;

ARBUSCULAR; FUNGI; PISUM SATIVUM; ZEA MAYS;

EID: 84862659170     PISSN: 01782762     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00374-011-0647-0     Document Type: Article

References (96)

1. Abbott LK, Robson AD (1978) Growth of subterranean clover in relation to the formation of endomycorrhizas by introduced and indigenous fungi in a field soil. New Phytol 81: 575-585.
2. 15N-ammonium sulphate. New Phytol 97: 269-276.
3. Appuhn A, Joergensen RG (2006) Microbial colonisation of roots as a function of plant species. Soil Biol Biochem 38: 1040-1051.
4. Appuhn A, Joergensen RG, Raubuch M, Scheller E, Wilke B (2004) The automated determination of glucosamine, galactosamine, muramic acid and mannosamine in soil and root hydrolysates by HPLC. J Plant Nutr Soil Sci 167: 17-21.
5. Baird JM, Walley FL, Shirtliffe SJ (2010) Arbuscular mycorrhizal fungi colonization and phosphorus nutrition in organic field pea and lentil. Mycorrhiza 20: 541-549.
6. 13C natural abundance. In: Boutton TW, Yamasaki SI (eds) Mass spectrometry of soils. Marcel Dekker, New York, pp 83-111.
7. 2 and bulk organic matter occurs during the transition between heterotrophy and autotrophy in Phaseolus vulgaris plants. New Phytol 177: 406-418.
8. 15N isotope dilution technique. Soil Biol Biochem 22: 649-655.
9. Brookes PC, Powlson DS, Jenkinson DS (1982) Measurement of microbial biomass phosphorus in soil. Soil Biol Biochem 14: 319-329.
10. Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method for measuring microbial biomass nitrogen in soil. Soil Biol Biochem 17: 837-842.
11. Butenschoen O, Poll C, Langel R, Kandeler E, Marhan S, Scheu S (2007) Endogeic earthworms alter carbon translocation by fungi at the soil-litter interface. Soil Biol Biochem 39: 2854-2864.
12. Cavagnaro TR, Jackson LE, Six J, Ferris H, Goyal S, Asami D, Scow KM (2006) Arbuscular mycorrhizas, microbial communities, nutrient availability, and soil aggregates in organic tomato production. Plant Soil 282: 209-225.
13. 3 plants? Review and synthesis of current hypotheses. Funct Plant Biol 36: 199-213.
14. Chander K, Hartmann G, Joergensen RG, Khan KS, Lamersdorf N (2008) Comparison of three methods for measuring heavy metals in soils contaminated by different sources. Arch Agron Soil Sci 54: 413-422.
15. Christensen BT (1985) Wheat and barley straw decomposition under field conditions: effect of soil type and plant cover on weight loss, nitrogen and potassium content. Soil Biol Biochem 17: 691-697.
16. Christensen H, Jakobsen I (1993) Reduction of bacterial growth by a vesicular-arbuscular mycorrhizal fungus in the rhizosphere of cucumber (Cucumis sativus L.). Biol Fertil Soils 15: 253-258.
17. Costa R, Götz M, Mrotzek N, Lottmann J, Berg G, Smalla K (2006) Effects of site and plant species on rhizosphere community structure as revealed by molecular analysis of microbial guilds. FEMS Microbiol Ecol 56: 236-249.
18. 15N natural abundance of the soil microbial biomass. Soil Biol Biochem 38: 3257-3266.
19. Dijkstra FA, Morgan JA, Blumenthal D, Follett RF (2010) Water limitation and plant inter-specific competition reduce rhizosphere-induced C decomposition and plant N uptake. Soil Biol Biochem 42: 1073-1082.
20. Djajakirana G, Joergensen RG, Meyer B (1996) Ergosterol and microbial biomass relationship in soil. Biol Fertil Soils 22: 299-304.
21. Dormaar JF (1990) Effect of active roots on the decomposition of soil organic materials. Biol Fertil Soils 10: 121-126.
22. -) obtained in pea (Pisum sativum L.) and fababean (Vicia faba L.). Plant Sci 60: 215-222.
23. Endlweber K, Scheu S (2006) Establishing arbuscular mycorrhiza-free soil: a comparison of six methods and their effects on nutrient mobilization. Appl Soil Ecol 34: 276-279.
24. Engelking B, Flessa H, Joergensen RG (2007) Shifts in amino sugar and ergosterol contents after addition of sucrose and cellulose to soil. Soil Biol Biochem 39: 2111-2118.
25. Farquhar GD, Ehleringe RJ, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Ann Rev Plant Physiol Plant Mol Biol 40: 503-537.
26. Fitter AH, Helgason T, Hodge A (2011) Nutritional exchanges in the arbuscular mycorrhizal symbiosis: implications for sustainable agriculture. Fungal Biol Rev 25: 68-72.
27. 2 evolution, water content, temperature, and bulk density. App Soil Ecol 2: 95-109.
28. Frey B, Buser HR, Schüepp H (1992) Identification of ergosterol in vesicular-arbuscular mycorrhizae. Biol Fertil Soils 13: 229-234.
29. Fujiyoshi M, Nakatsubo T, Ogura S, Horikoshi T (2000) Estimation of mycelial biomass of arbuscular mycorrhizal fungi associated with the annual legume Kummerowia striata by ergosterol analysis. Ecol Res 15: 121-131.
30. Fustec J, Lesuffleur F, Mahieu S, Cliquet JB (2010) Nitrogen rhizodeposition of legumes. A review. Agron Sustain Develop 30: 57-66.
31. Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84: 489-500.
32. Haider K, Heinemeyer O, Mosier AR (1989) Effects of growing plants on humus and plant residue decomposition in soil; uptake of decomposition product by plants. Sci Tot Environ 81(82): 661-670.
33. 13C values of Eucalyptus globulus and Ricinus communis. Plant Cell Env 16: 375-382.
34. Hauggaard-Nielsen H, Ambus P, Jensen ES (2003) The comparison of nitrogen use and leaching in sole cropped versus intercropped pea and barley. Nutr Cycl Agroecosyst 65: 289-300.
35. Heckman JR, Kluchinski D (1995) Soybean nodulation and nitrogen fixation on soil amended with plant residues. Biol Fertil Soils 20: 284-288.
36. 15N in nitrogen-limited forests and tundra can estimate nitrogen cycling through mycorrhizal fungi: a review. Ecosystems 11: 815-830.
37. 13C-labelled cultures. Mycol Res 108: 725-736.
38. Hobbie EA, Colpaert JV, White MW, Ouimette AP, Macko SA (2008) Nitrogen form, availability, and mycorrhizal colonization affect biomass and nitrogen isotope patterns in Pinus sylvestris. Plant Soil 310: 121-136.
39. Hodge A, Campbell CD, Fitter AH (2001) An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413: 297-299.
40. 15N. New Phytol 133: 487-494.
41. Indorf C, Dyckmans J, Khan KS, Joergensen RG (2011) Optimisation of amino sugar quantification by HPLC in soil and plant hydrolysates. Biol Fertil Soils 47: 387-396.
42. Jackson LE, Miller D, Smith SE (2002) Arbuscular mycorrhizal colonization and growth of wild and cultivated lettuce in response to nitrogen and phosphorus. Sci Hortic 94: 205-218.
43. Jenkinson DS, Powlson DS (1976) The effects of biocidal treatments on metabolism in soil. V. A method for measuring soil biomass. Soil Biol Biochem 8: 209-213.
44. Jensen ES (1986) The influence of rate and time of nitrate supply on nitrogen fixation and yield in pea (Pisum sativum L.). Fert Res 10: 193-202.
45. Jingguo W, Bakken LR (1997) Competition for nitrogen during decomposition of plant residues in soil: effect of spatial placement of N-rich and N-poor plant residues. Soil Biol Biochem 29: 153-162.
46. Joergensen RG, Wichern F (2008) Quantitative assessment of the fungal contribution to microbial tissue in soil. Soil Biol Biochem 40: 2977-2991.
47. Joergensen RG, Brookes PC, Jenkinson DS (1990) Survival of the soil microbial biomass at elevated temperatures. Soil Biol Biochem 22: 1129-1136.
48. Joergensen RG, Kübler H, Meyer B, Wolters V (1995) Microbial biomass phosphorus in soils of beech (Fagus sylvatica L.) forests. Biol Fertil Soils 19: 215-219.
49. Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phytol 163: 459-480.
50. Kahiluoto H, Ketoja E, Vestberg M (2000) Creation of a non-mycorrhizal control for a bioassay of AM effectiveness: 1. Comparison of methods. Mycorrhiza 9: 241-258.
51. Khan KS, Müller T, Dyckmans J, Joergensen RG (2010) Development of ergosterol, microbial biomass C, N, and P after steaming as a result of sucrose addition, and Sinapis alba cultivation. Biol Fertil Soils 46: 323-331.
52. Kleikamp B, Joergensen RG (2006) Evaluation of arbuscular mycorrhiza with symbiotic and nonsymbiotic pea isolines at three sites in the Alentejo, Portugal. J Plant Nutr Soil Sci 169: 661-669.
53. Leigh J, Hodge A, Fitter AH (2009) Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytol 181: 199-207.
54. 15N from a soil compartment separated by a polytetrafluoroethylene membrane to plant roots via the hyphae of arbuscular mycorrhizal fungi. New Phytol 146: 155-161.
55. Magid J, Kjaergaard C (2001) Recovering decomposing plant residues from the particulate soil organic matter fraction: size versus density separation. Biol Fertil Soils 33: 252-257.
56. Marschner P, Baumann K (2003) Changes in bacterial community structure induced by mycorrhizal colonisation in split-root maize. Plant Soil 251: 279-289.
57. Matcham SE, Jordan BR, Wood DA (1985) Estimation of fungal biomass in a solid substrate by three independent methods. Appl Microbiol Biotechnol 21: 108-112.
58. 15N in situ stem labelling method. Soil Biol Biochem 35: 21-28.
59. Miyauchi MYH, Lima DS, Nogueira MA, Lovato GM, Murate LS, Cruz MF, Ferreira JM, Zangaro W, Andrade G (2008) Interactions between diazotrophic bacteria and mycorrhizal fungus in maize genotypes. Sci Agric 65: 525-531.
60. Muhammad S, Müller T, Joergensen RG (2006) Decomposition of pea and maize straw in Pakistani soils along a gradient in salinity. Biol Fertil Soils 43: 93-101.
61. Muhammad S, Müller T, Mayer J, Joergensen RG (2007) Impact of growing maize (Zea mays) on the decomposition of incorporated fresh alfalfa residues. Biol Fertil Soils 43: 399-407.
62. Müller J (1999) Mycorrhizal fungal structures are stimulated in wildtype peas and in isogenic mycorrhiza-resistant mutants by tri-iodo-benzoic acid (TIBA), an auxin-transport-inhibitor. Symbiosis 26: 379-389.
63. 13C) of Acacia tortilis subsp. spirocarpa (A. Rich.) Brenan growing at three semi-arid sites in Kenya. J Arid Environ 34: 325-330.
64. 15N-labelled catch-crop residues in soil: evaluation of N mineralization and plant-uptake potentials under controlled conditions. Eur J Soil Sci 46: 115-123.
65. Olsson PA, Bååth E, Jakobsen I, Söderström B (1996) Soil bacteria respond to presence of roots but not to mycelium of arbuscular mycorrhizal fungi. Soil Biol Biochem 28: 463-470.
66. Olsson PA, Larsson L, Bago B, Wallander H, van Aarle IM (2003) Ergosterol and fatty acids for biomass estimation of mycorrhizal fungi. New Phytol 159: 7-10.
67. Paré T, Gregorich EG, Nelson SD (2000) Mineralization of nitrogen from crop residues and N recovery by maize inoculated with vesicular-arbuscular mycorrhizal fungi. Plant Soil 218: 11-20.
68. Phillips JM, Hayman DS (1970) Improved procedures for clearing and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transact Brit Mycol Soc 55: 158-161.
69. Plassard C, Bonafos B, Touraine B (2000) Differential effects of mineral and organic N sources, and of ectomycorrhizal infection by Hebeloma cylindrosporum, on growth and N utilization in Pinus pinaster. Plant Cell Environ 23: 1195-1205.
70. 13C in soil microbial biomass using fumigation-extraction. Soil Biol Biochem 35: 947-954.
71. Powlson DS, Hirsch PR, Brookes PC (2001) The role of soil microorganisms in soil organic matter conservation in the tropics. Nutr Cycl Agroecosyst 61: 41-51.
72. 13C and water use efficiency to arbuscular mycorrhizal infection in two aridland woody plant species. Oecol 135: 510-515.
73. Quintern M, Lein M, Joergensen RG (2006) Changes in soil biological quality indices after long-term addition of shredded shrubs and biogenic waste compost. J Plant Nutr Soil Sci 169: 488-493.
74. Read DJ, Perez-Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems-a journey towards relevance? New Phytol 157: 475-492.
75. 2 efflux-a modified model. Plant Soil 268: 21-33.
76. Rost U, Joergensen RG, Chander K (2001) Effects of Zn enriched sewage sludge on microbial activities and biomass in soil. Soil Biol Biochem 33: 633-638.
77. Rottmann N, Dyckmans J, Joergensen RG (2010) Microbial use and decomposition and of maize leaf straw incubated in packed soil columns at different depths. Eur J Soil Biol 46: 27-33.
78. Ruiz-Lozano JM, Roussel H, Gianinazzi S, Gianinazzi-Pearson V (1999) Defence genes are differentially induced by a mycorrhizal fungus and Rhizobium sp. in wild-type and symbiosis-defective pea genotypes. Mol Plant Microbe Interact 12: 976-984.
79. Ruschel AP, Vose PB, Victoria RL, Salati E (1979) Comparison of isotope techniques on nodulating and non-nodulating isolines to study the effect of ammonium fertilization on dinitrogen fixation in soybean, Glycine max (L). Merrill Plant Soil 53: 513-525.
80. Schimel JP, Jackson LE, Firestone MK (1989) Spatial and temporal effects on plant-microbial competition for inorganic nitrogen in a California annual grassland. Soil Biol Biochem 21: 1059-1066.
81. 15N abundance. Aust J Plant Physiol 13: 699-756.
82. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London.
83. Thingstrup I, Rubaek G, Sibbesen E, Jakobsen I (1998) Flax (Linum usitatissimum L.) depends on arbuscular mycorrhizal fungi for growth and P uptake at intermediate but not high soil P levels in the field. Plant Soil 203: 37-46.
84. van Veen JA, Ladd JN, Frissel MJ (1984) Modelling C and N turnover through the microbial biomass in soil. Plant Soil 76: 257-274.
85. Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19: 703-707.
86. Vestberg M, Kahiluoto H, Wallius E (2010) Arbuscular mycorrhizal fungal diversity and species dominance in a temperate soil with long-term conventional and low-input cropping systems. Mycorrhiza. doi: 10. 1007/s00572-010-0346-y.
87. Vestergård M, Henry F, Rangel-Castro JI, Michelsen A, Prosser JI, Christensen S (2008) Rhizosphere bacterial community composition responds to arbuscular mycorrhiza, but not to reductions in microbial activity induced by foliar cutting. FEMS Microbiol Ecol 64: 78-89.
88. 2- or nitrate-fed Pisum sativum L. Ann Bot 91: 539-546.
89. 13C-labelling. Ann Bot 92: 557-563.
90. Wallander H, Massicotte HB, Nylund JE (1997) Seasonal variation in protein, ergosterol and chitin in five morphotypes of Pinus sylvestris L. ectomycorrhizae in a mature Swedish forest. Soil Biol Biochem 29: 45-53.
91. Wamberg C, Christensen S, Jakobsen I, Müller AK, Sørensen SJ (2003) The mycorrhizal fungus (Glomus intraradices) affects microbial activity in the rhizosphere of pea plants (Pisum sativum). Soil Biol Biochem 35: 1349-1357.
92. 15N in four species of Casuarina. J Exp Bot 51: 287-297.
93. 15N double labelling under field conditions. Soil Biol Biochem 39: 2527-2537.
94. Wu J, Joergensen RG, Pommerening B, Chaussod R, Brookes PC (1990) Measurement of soil microbial biomass C by fumigation-extraction-an automated procedure. Soil Biol Biochem 22: 1167-1169.
95. 15N: progress over the last 30 years. Phytochem Rev 2: 121-132.
96. 15N-labelled maize leaves in soil affected by endogeic geophagous Aporrectodea caliginosa. Soil Biol Biochem 42: 276-282.