Impact of nitrogen fertilization and soil tillage on arbuscular mycorrhizal fungal communities in a Mediterranean agroecosystem

Soil Biology and Biochemistry

Volumn 67, Issue , 2013, Pages 285-294

  Avio, Luciano ^a   Castaldini, Maurizio ^b   Fabiani, Arturo ^b   Bedini, Stefano ^c   Sbrana, Cristiana ^a   Turrini, Alessandra ^c   Giovannetti, Manuela ^c  

^a Institute of Agricultural Biology and Biotechnology   (Italy)

^b ISTITUTO NAZIONALE DELLA NUTRIZIONE   (Italy)

^c UNIVERSITY OF PISA   (Italy)

Author keywords

Arable systems; Arbuscular mycorrhizal fungi; Fungal diversity; N fertilization; PCR DGGE; Tillage; Trap cultures

Indexed keywords

ARBUSCULAR MYCORRHIZAL FUNGI; FUNGAL DIVERSITY; N-FERTILIZATION; PCR-DGGE; TILLAGE; TRAP CULTURE;

AGRICULTURAL MACHINERY; ECOSYSTEMS; FUNGI; NITROGEN; POLYMERASE CHAIN REACTION; SOILS;

AGRICULTURE;

AGRICULTURAL ECOSYSTEM; AGRICULTURAL MANAGEMENT; ARBUSCULAR MYCORRHIZA; CANONICAL ANALYSIS; DOMINANCE; FERTILIZER APPLICATION; NITROGEN; PROTEIN; SOIL AMENDMENT; SPECIES DIVERSITY; SPORULATION; TILLAGE;

EID: 84884930521     PISSN: 00380717     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.soilbio.2013.09.005     Document Type: Article

References (85)

1. Alguacil M.M., Torres M.P., Torrecillas E., Díaz G., Roldán A. Plant type differently promote the arbuscular mycorrhizal fungi biodiversity in the rhizosphere after revegetation of a degraded, semiarid land. Soil Biol. Biochem. 2011, 43:167-173.
2. Antibus R.K., Lauber C., Sinsabaugh R.L., Zak D.R. Responses of Bradford-reactive soil protein to experimental nitrogen addition in three forest communities in northern lower Michigan. Plant Soil 2006, 288:173-187.
3. Augé R.M. Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 2001, 11:3-42.
4. Avio L., Pellegrino E., Bonari E., Giovannetti M. Functional diversity of arbuscular mycorrhizal fungal isolates in relation to extraradical mycelial networks. New Phytol. 2006, 172:347-357.
5. Balestrini R., Magurno F., Walker C., Lumini E., Bianciotto V. Cohorts of arbuscular mycorrhizal fungi (AMF) in Vitis vinifera, a typical Mediterranean fruit crop. Environ. Microbiol. Rep. 2010, 2:594-604.
6. Bedini S., Avio L., Argese E., Giovannetti M. Effects of long-term land use on arbuscular mycorrhizal fungi and glomalin-related soil protein. Agric Ecosyst Environ 2007, 120:463-466.
7. Bedini S., Pellegrino E., Avio L., Pellegrini S., Bazzoffi P., Argese E., Giovannetti M. Changes in soil aggregation and glomalin-related soil protein content as affected by the arbuscular mycorrhizal fungal species Glomus mosseae and Glomus intraradices. Soil Biol. Biochem. 2009, 41:1491-1496.
8. Blanke V., Wagner M., Renker C., Lippert H., Michulitz M., Kuhn A., Buscot F. Arbuscular mycorrhizas in phosphate-polluted soil: interrelations between root colonization and nitrogen. Plant Soil 2011, 343:379-392.
9. Blaszkowski J. Comparative studies of the occurrence of arbuscular fungi and mycorrhizae (Glomales) in cultivated and uncultivated soils of Poland. Acta Mycol. 1993, 28:93-140.
10. Blaszkowski J., Kovacs G.M., Balazs T. Glomus perpusillum, a new arbuscular mycorrhizal fungus. Mycologia 2009, 101:247-255.
11. Blaszkowski J., Ryszka P., Oehl F., Koegel S., Wiemken A., Kovacs G.M., Redecker D. Glomus achrum and G.bistratum, two new species of arbuscular mycorrhizal fungi (Glomeromycota) found in maritime sand dunes. Botany 2009, 87:260-271.
12. Blaszkowski J., Kovacs G.M., Balazs T.K., Orlowska E., Sadravi M., Wubet T., Buscot F. Glomus africanum and G.iranicum, two new species of arbuscular mycorrhizal fungi (Glomeromycota). Mycologia 2010, 102:1450-1462.
13. Brito I., Goss M.J., de Carvalho M., Chatagnier O., van Tuinen D. Impact of tillage system on arbuscular mycorrhiza fungal communities in the soil under Mediterranean conditions. Soil Till. Res. 2012, 121:63-67.
14. Calvente R., Cano C., Ferrol N., Azcon-Aguilar C., Barea J.M. Analysing natural diversity of arbuscular mycorrhizal fungi in olive tree (Olea europaea L.) plantations and assessment of the effectiveness of native fungal isolates as inoculants for commercial cultivars of olive plantlets. Appl. Soil Ecol. 2004, 26:11-19.
15. Castaldini M., Turrini A., Sbrana C., Benedetti A., Marchionni M., Mocali S., Fabiani A., Landi S., Santomassimo F., Pietrangeli B., Nuti M.P., Miclaus N., Giovannetti M. Impact of Bt corn on rhizospheric and soil eubacterial communities and on beneficial mycorrhizal symbiosis in experimental microcosms. Appl. Environ. Microbiol. 2005, 71:6719-6729.
16. Castillo C.G., Rubio R., Rouanet J.L., Borie F. Early effects of tillage and crop rotation on arbuscular mycorrhizal fungal propagules in an ultisol. Biol. Fertil. Soils 2006, 43:83-92.
17. Ceccarelli N., Curadi M., Martelloni L., Sbrana C., Picciarelli P., Giovannetti M. Mycorrhizal colonization impacts on phenolic content and antioxidant properties of artichoke leaves and flower heads two years after field transplant. Plant Soil 2010, 335:311-323.
18. Cesaro P., van Tuinen D., Copetta A., Chatagnier O., Berta G., Gianinazzi S., Lingua G. Preferential colonization of Solanum tuberosum L. roots by the fungus Glomus intraradices in arable soil of a potato farming area. Appl. Environ. Microbiol. 2008, 74:5776-5783.
19. Chenna R., Sugawara H., Koike T., Lopez R., Gibson T.J., Higgins D.G., Thompson J.D. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 2003, 31:3497-3500.
20. Cole J.R., Chai B., Marsh T.L., Farris R.J., Wang Q., Kulam S.A., Chandra S., McGarrell D.M., Schmidt T.M., Garrity G.M., Tiedje J.M. The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res. 2003, 31:442-443.
21. Daniell T.J., Husband R., Fitter A.H., Young J.P.W. Molecular diversity of arbuscular mycorrhizal fungi colonising arable crops. FEMS Microbiol. Ecol. 2001, 36:203-209.
22. De Sanctis G., Roggero P.P., Seddaiu G., Orsini R., Porter C.H., Jones J.W. Long-term no tillage increased soil organic carbon content of rain-fed cereal systems in a Mediterranean area. Eur. J. Agron. 2012, 40:18-27.
23. Douds D.D., Galvez L., Janke R.R., Wagoner P. Effect of tillage and farming system upon populations and distribution of vesicular-arbuscular mycorrhizal fungi. Agric. Ecosyst. Environ. 1995, 52:111-118.
24. Egerton-Warburton L.M., Allen E.B. Shifts in arbuscular mycorrhizal communities along an anthropogenic nitrogen deposition gradient. Ecol. Appl. 2000, 10:484-496.
25. Ellis J.R., Roder W., Mason S.C. Grain sorghum-soybean rotation and fertilization influence on vesicular-arbuscular mycorrhizal fungi. Soil Sci. Soc. Am. J. 1992, 56:783-794.
26. Evelin H., Kapoor R., Giri B. Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann. Bot. 2009, 104:1263-1280.
27. 2 in a Glomus mosseae-Prunus cerasifera model system. Mycol. Prog. 2012, 11:17-26.
28. Franke-Snyder M., Douds D.D., Galvez L., Phillips J.G., Wagoner P., Drinkwater L., Morton J.B. Diversity of communities of arbuscular mycorrhizal (AM) fungi present in conventional versus low-input agricultural sites in eastern Pennsylvania, USA. Appl. Soil Ecol. 2001, 16:35-48.
29. Gerdemann J.W., Nicolson T.H. Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Trans. Br. Mycol. Soc. 1963, 46:235-244.
30. Gianinazzi S., Gollotte A., Binet M.N., van Tuinen D., Redecker D., Wipf D. Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 2010, 20:519-530.
31. Giovannetti M., Schubert A., Cravero M.C., Salutini L. Spore production by the vesicular-arbuscular mycorrhizal fungus Glomus monosporum as related to host species, root colonization and plant growth enhancement. Biol. Fertil. Soils 1988, 6:120-124.
32. Giovannetti M., Azzolini D., Citernesi A.S. Anastomosis formation and nuclear and protoplasmic exchange in arbuscular mycorrhizal fungi. Appl. Environ. Microbiol. 1999, 65:5571-5575.
33. Giovannetti M., Fortuna P., Citernesi A.S., Morini S., Nuti M.P. The occurrence of anastomosis formation and nuclear exchange in intact arbuscular mycorrhizal networks. New Phytol. 2001, 151:717-724.
34. Giovannetti M., Avio L. Biotechnology of arbuscular mycorrhizas. Agriculture and Food Production 2002, 275-310. Elsevier, Amsterdam. G.G. Khachatourians, D.K. Arora (Eds.).
35. Giovannetti M., Avio L., Barale R., Ceccarelli N., Cristofani R., Iezzi A., Mignolli F., Picciarelli P., Pinto B., Reali D., Sbrana C., Scarpato R. Nutraceutical value and safety of tomato fruits produced by mycorrhizal plants. Br. J. Nutr. 2012, 107:242-251.
36. Hammer Ø., Harper D.A.T., Ryan P.D. Past: paleontological statistics software package for education and data analysis. Palaeontol. Electron. 2001, 4:1-9.
37. Helgason T., Daniell T.J., Husband R., Fitter A.H., Young J.P.W. Ploughing up the wood-wide web?. Nature 1998, 394:431.
38. Hempel S., Renker C., Buscot F. Differences in the species composition of arbuscular mycorrhizal fungi in spore, root and soil communities in a grassland ecosystem. Environ. Microbiol. 2007, 9:1930-1938.
39. Jansa J., Mozafar A., Anken T., Ruh R., Sanders I.R., Frossard E. Diversity and structure of AMF communities as affected by tillage in a temperate soil. Mycorrhiza 2002, 12:225-234.
40. Jansa J., Mozafar A., Kuhn G., Anken T., Ruh R., Sanders I.R., Frossard E. Soil tillage affects the community structure of mycorrhizal fungi in maize roots. Ecol. Appl. 2003, 13:1164-1176.
41. Jansa J., Smith F.A., Smith S.E. Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi?. New Phytol. 2008, 177:779-789.
42. Johnson N.C., Pfleger F.L., Crookston R.K., Simmons S.R., Copeland P.J. Vesicular arbuscular mycorrhizas respond to corn and soybean cropping history. New Phytol. 1991, 117:657-663.
43. Johnson N.C., Rowland D.L., Corkidi L., Egerton-Warburton L.M., Allen E.B. Nitrogen enrichment alters mycorrhizal allocation at five mesic to semiarid grasslands. Ecology 2003, 84:1895-1908.
44. Kabir Z. Tillage or no-tillage: impact on mycorrhizae. Can. J. Plant Sci. 2005, 85:23-29.
45. Klironomos J.N. Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 2003, 84:2292-2301.
46. Koske R.E., Walker C. Species of Scutellospora (Endogonaceae) with smooth- walled spores from maritime sand dunes: two new species and redescription of the spores of Scutellospora pellucida and Scutellospora calospora. Mycotaxon 1986, 27:219-235.
47. Kowalchuk G.A., De Souza F.A., Van-Veen J.A. Community analysis of arbuscular mycorrhizal fungi associated with Ammophila arenaria in Dutch coastal sand dunes. Mol. Ecol. 2002, 11:571-581.
48. Krüger M., Krüger C., Walker C., Stockinger H., Schüssler A. Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytol. 2012, 193:970-984.
49. Kurle J.E., Pfleger F.L. Management influences on arbuscular mycorrhizal fungal species composition in a corn-soybean rotation. Agron. J. 1996, 88:155-161.
50. Land S., Schönbeck F. Influence of different soil types on abundance and seasonal dynamics of vesicular-arbuscular mycorrhizal fungi in arable soils of north Germany. Mycorrhiza 1991, 1:39-44.
51. Lovelock C.E., Wright S.F., Nichols K.A. Using glomalin as an indicator for arbuscular mycorrhizal hyphal growth: an example from a tropical rain forest soil. Soil Biol. Biochem. 2004, 36:1009-1012.
52. Mathew R.P., Feng H.Y., Githinji L., Ankumah R., Balkcom K.S. Impact of no-tillage and conventional tillage systems on soil microbial communities. Appl. Environ. Soil Sci. 2012, 10.1155/2012/548620.
53. Mathimaran N., Ruh R., Vullioud P., Frossard E., Jansa J. Glomus intraradices dominates arbuscular mycorrhizal communities in a heavy textured agricultural soil. Mycorrhiza 2005, 16:61-66.
54. Mirás-Avalos J.M., Antunes P.M., Koch A., Khosla K., Klironomos J.N., Dunfield K.E. The influence of tillage on the structure of rhizosphere and root-associated arbuscular mycorrhizal fungal communities. Pedobiologia 2011, 54:235-241.
55. Moebius-Clune D.J., Anderson Z.U., Pawlowska T.E. Arbuscular mycorrhizal fungi associated with a single agronomic plant host across the landscape: the structure of an assemblage. Soil Biol. Biochem. 2013, 64:181-190.
56. Moebius-Clune D.J., Moebius-Clune B.N., van Es H.M., Pawlowska T.E. Arbuscular mycorrhizal fungi associated with a single agronomic plant host across the landscape: community differentiation along a soil textural gradient. Soil Biol. Biochem. 2013, 64:191-199.
57. Munkvold L., Kjoller R., Vestberg M., Rosendahl S., Jakobsen I. High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol. 2004, 164:357-364.
58. Na Bhadalung N., Suwanarit A., Dell B., Nopamornbodi O., Thamchaipenet A., Rungchuang J. Effects of long-term NP-fertilization on abundance and diversity of arbuscular mycorrhizal fungi under a maize cropping system. Plant Soil 2005, 270:371-382.
59. Oehl F., Sieverding E., Ineichen K., Mäder P., Boller T., Wiemken A. Impact of land use intensity on the species diversity of arbuscular mycorrhizal fungi in agroecosystems of Central Europe. Appl. Environ. Microbiol. 2003, 69:2816-2824.
60. Oehl F., Sieverding E., Mäder P., Dubois D., Ineichen K., Boller T., Wiemken A. Impact of long-term conventional and organic farming on the diversity of arbuscular mycorrhizal fungi. Oecologia 2004, 138:574-583.
61. Oehl F., Sieverding E., Ineichen K., Mäder P., Wiemken A., Boller T. Distinct sporulation dynamics of arbuscular mycorrhizal fungal communities from different agroecosystems in long-term microcosms. Agric. Ecosyst. Environ. 2009, 134:257-268.
62. Oehl F., Laczko E., Bogenrieder A., Stahr K., Bosch R., van der Heijden M., Sieverding E. Soil type and land use intensity determine the composition of arbuscular mycorrhizal fungal communities. Soil Biol. Biochem. 2010, 42:724-738.
63. Oehl F., da Silva G.A., Goto B.T., Maia L.C., Sieverding E. Glomeromycota: two new classes and a new order. Mycotaxon 2011, 116:365-379.
64. Oliveira C.A., Så N.M.H., Gomes E.A., Marriel I.E., Scotti M.R., Guimaraes C.T., Schaffert R.E., Alves V.M.C. Assessment of the mycorrhizal community in the rhizosphere of maize (Zea mays L.) genotypes contrasting for phosphorus efficiency in the acid savannas of Brazil using denaturing gradient gel electrophoresis (DGGE). Appl. Soil Ecol. 2009, 41:249-258.
65. Redecker D., Thierfelder H., Walker C., Werner D. Restriction analysis of PCR-amplified internal transcribed spacers of ribosomal DNA as a tool for species identification in different genera of the order glomales. Appl. Environ. Microbiol. 1997, 63:1756-1761.
66. Rillig M.C., Mummey D.L. Mycorrhizas and soil structure. New Phytol. 2006, 171:41-53.
67. Roldán A., Salinas-García J.R., Alguacil M.M., Caravaca F. Soil sustainability indicators following conservation tillage practices under subtropical maize and bean crops. Soil Till. Res. 2007, 93:273-282.
68. Santos J.C., Finlay R.D., Tehler A. Molecular analysis of arbuscular mycorrhizal fungi colonising a semi-natural grassland along a fertilisation gradient. New Phytol. 2006, 172:159-168.
69. Sbrana C., Fortuna P., Giovannetti M. Plugging into the network: belowground connections between germlings and extraradical mycelium of arbuscular mycorrhizal fungi. Mycologia 2011, 103:307-316.
70. Schreiner R.P., Mihara K.L. The diversity of arbuscular mycorrhizal fungi amplified from grapevine roots (Vitis vinifera L.) in Oregon vineyards is seasonally stable and influenced by soil and vine age. Mycologia 2009, 101:599-611.
71. Sikes B.A., Kottenie K., Klironomos J.N. Plant and fungal identity determines pathogen protection of plant roots by arbuscular mycorrhizas. J.Ecol. 2009, 97:1274-1280.
72. Smalla K., Wieland G., Buchner A., Zock A., Parzy J., Kaiser S., Roskot N., Heuer H., Berg G. Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl. Environ. Microbiol. 2001, 67:4742-4751.
73. Smith S.E., Read D.J. Mycorrhizal Simbiosis 2008, Academic Press, London.
74. Spohn M., Giani L. Water-stable aggregates, glomalin-related soil protein, and carbohydrates in a chronosequence of sandy hydromorphic soils. Soil Biol. Biochem. 2010, 42:1505-1511.
75. Stutz J.C., Morton J.B. Successive pot cultures reveal high species richness of arbuscular endomycorrhizal fungi in arid ecosystems. Can. J. Bot. 1996, 74:1883-1889.
76. Toljander J.F., Santos-Gonzalez J.C., Tehler A., Finlay R.D. Community analysis of arbuscular mycorrhizal fungi and bacteria in the maize mycorrhizosphere in a long-term fertilization trial. FEMS Microbiol. Ecol. 2008, 65:323-338.
77. Turrini A., Avio L., Bedini S., Giovannetti M. In situ collection of endangered arbuscular mycorrhizal fungi in a Mediterranean UNESCO Biosphere Reserve. Biodivers. Conserv. 2008, 17:643-657.
78. Turrini A., Giovannetti M. Arbuscular mycorrhizal fungi in national parks, nature reserves and protected areas worldwide: a strategic perspective for their in situ conservation. Mycorrhiza 2012, 22:81-97.
79. Van de Peer Y., De Wachter R. Treecon for Windows - a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comput. Appl. Biosci. 1994, 10:569-570.
80. Wilson G.W.T., Rice C.W., Rillig M.C., Springer A., Hartnett D.C. Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: results from long-term field experiments. Ecol. Lett. 2009, 12:452-461.
81. Wright S.F., Upadhyaya A. Extraction of an abundant and unusual protein from soil and comparison with hyphal protein of arbuscular mycorrhizal fungi. Soil Sci. 1996, 161:575-586.
82. Wu F.S., Dong M.X., Liu Y.J., Ma X.J., An L.Z., Young J.P.W., Feng H.Y. Effects of long-term fertilization on AM fungal community structure and glomalin-related soil protein in the Loess Plateau of China. Plant Soil 2011, 342:233-247.
83. Wuest S.B., Caesar-TonThat T.C., Wright S.F., Williams J.D. Organic matter addition, N, and residue burning effects on infiltration, biological, and physical properties of an intensively tilled silt-loam soil. Soil Till. Res. 2005, 84:154-167.
84. Yao Q., Gao J.L., Zhu H.H., Long L.K., Xing Q.X., Chen J.Z. Evaluation of the potential of trap plants to detect arbuscular mycorrhizal fungi using polymerase chain reaction-denaturing gradient gel electrophoresis analysis. Soil Sci. Plant Nutr. 2010, 56:205-211.
85. Zhu Y.G., Miller R.M. Carbon cycling by arbuscular mycorrhizal fungi in soil-plant systems. Tr. Plant Sci. 2003, 8:407-409.