Abstract
Background and aims
We investigated the genetic diversity of arbuscular mycorrhizal fungi (AMF) in soils and the roots of Phalaris aquatica L., Trifolium subterraneum L., and Hordeum leporinum Link growing in limed and unlimed soil, the influence of lime application on AMF colonization and the relationship between AMF diversity and soil chemical properties.
Methods
The sampling was conducted on a long-term liming experimental site, established in 1992, in which lime was applied every 6 years to maintain soil pH (in CaCl2) at 5.5 in the 0–10 cm soil depth. Polymerase chain reaction, cloning and sequencing techniques were used to investigate the diversity of AMF.
Results
Altogether, 438 AMF sequences from a total of 480 clones were obtained. Sequences of phylotypes Aca/Scu were detected exclusively in soil, while Glomus sp. (GlGr Ab) and an uncultured Glomus (UnGlGr A) were detected only in plant roots. Glomus mosseae (GlGr Aa) was the dominant AMF in the pastures examined; however, the proportion of G. mosseae was negatively correlated with soil pH, exchangeable Ca and available P. Generally, diversity of the AMF phylotypes was greater in the bulk unlimed soil and plants from this treatment when compared to the limed treatments.
Conclusions
Long-term lime application changed soil nutrient availability and increased AMF colonization, but decreased AMF phylotype diversity, implying that soil chemistry may determine the distribution of AMF in acid soils. Future studies are required to explore the functions of these AMF groups and select the most efficient AMF for sustainable farming in acid soils.
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References
Abbott LK, Robson AD (1977) Infectivity and effectiveness of vesicular-carbuncular mycorrhizal fungi: effect of inoculums type. Aust J Agr Res 32:631–639
Akinrinde EA (2008) Lime and phosphorus effects in maize (Zea mays L.) production. Res Crops 9:547–553
Alguacil MM, Lozano Z, Campoy MJ, Rold A (2010) Phosphorus fertilisation management modifies the biodiversity of AM fungi in a tropical savanna forage system. Soil Biol Biochem 42:1114–1122
Alguacil MM, Torres MP, Torrecillas E, Diaz G, Roldan A (2011) Plant type differently promote the arbuscular mycorrhizal fungi biodiversity in the rhizosphere after revegetation of a degraded, semiarid land. Soil Biol Biochem 43:167–173
Alkan N, Gadkar V, Yarden O, Kapulnik Y (2006) Analysis of quantitative interactions between two species of arbuscular mycorrhizal fungi, Glomus mosseae and G. intraradices, by real-time PCR. Appl Environ Microb 72:4192–4199
Altschul SF, Madden TL, Schäffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Bardgett RD, Leemans DK, Cook R, Hobbs PJ (1997) Seasonality of the soil biota of grazed and ungrazed hill grasslands. Soil Biol Biochem 29:1285–1294
Bartolomeesteban H, Schenck N (1994) Spore germination and hyphal growth of arbuscular mycorrhizal fungi in relation to soil aluminum saturation. Mycologia 86:217–226
Bhadalung NN, Suwanarit A, Dell B, Nopamornbodi O, Thamchaipenet A, Rungchuang J (2005) Effects of long-term NP-fertilization on abundance and diversity of arbuscular mycorrhizal fungi under a maize cropping system. Plant Soil 270:371–382
Callaway RM, Mahall BE, Wicks C, Pankey J, Zabinski C (2003) Soil fungi and the effects of an invasive forb on grasses: neighbor identity matters. Ecology 84:129–135
Chang CS, Sung JM (2004) Nutrient uptake and yield responses of peanuts and rice to lime and fused magnesium phosphate in an acid soil. Field Crops Res 89:319–325
Clapp JP, Young JPW, Merryweather JW, Fitter AH (1995) Diversity of fungal symbionts in arbuscular mycorrhizas from a natural community. New Phytol 130:259–265
Clapp JP, Rodriguez A, Dodd JC (2001) Inter- and intra-isolate rRNA large subunit variation in Glomus coronatum spores. New Phytol 149:539–554
Clark RB (1997) Arbuscular mycorrhizal adaptation, spore germination, root colonization, and host plant growth and mineral acquisition at low pH. Plant Soil 192:15–22
Colwell J (1963) The estimation of the phosphorus fertilizer requirements of wheat in southern New South Wales by soil analysis. Aust J Exp Agric Anim Husb 3:190–198
Cuenca G, Lovera M (2010) Seasonal variation and distribution at different soil depths of arbuscular mycorrhizal fungi spores in a tropical sclerophyllous shrubland. Botany-Botanique 88:54–64
Cui MY, Caldwell MM (1996) Facilitation of plant phosphate acquisition by arbuscular mycorrhizas from enriched soil patches.2. Hyphae exploiting root-free soil. New Phytol 133:461–467
Da Silva GA, Lumini E, Costa Maia L, Bonfante P, Bianciotto V (2006) Phylogenetic analysis of Glomeromycota by partial LSU rDNA sequences. Mycorrhiza 16:183–189
Dhillion SS, Gardsjord TL (2004) Arbuscular mycorrhizas influence plant diversity, productivity, and nutrients in boreal grasslands. Can J Bo 82:104–114
Foy CD (1988) Plant adaptation to acid, aluminum-toxic soils. Comm Soil Sci Plant Anal 19:959–987
Gillman G, Sumpter E (1986) Modification to the compulsive exchange method for measuring exchange characteristics of soils. Aust J Soil Res 24:61–66
Gotelli N, Colwell RK (2001) Quantifying biodiversity: Procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391
Grayston SJ, Wang SQ, Campbell CD, Edwards AC (1998) Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol Biochem 30:369–378
Guo Y, Ni Y, Huang J (2010) Effects of rhizobium, arbuscular mycorrhiza and lime on nodulation, growth and nutrient uptake of lucerne in acid purplish soil in China. Trop Grassl 44:109–114
Haling R, Simpson R, Delhaize E, Hocking P, Richardson A (2010) Effect of lime on root growth, morphology and the rhizosheath of cereal seedlings growing in an acid soil. Plant Soil 327:199–212
Hamel C, Dalpe Y, Lapierre C, Simard RR, Smith DL (1996) Endomycorrhizae in a newly cultivated acidic meadow: Effects of three years of barley cropping, tillage, lime, and phosphorus on root colonization and soil infectivity. Biol Fertil Soils 21:160–165
Hijri I, Sykorova Z, Oehl F, Ineichen K, Mader P, Wiemken A, Redecker D (2006) Communities of arbuscular mycorrhizal fungi in arable soils are not necessarily low in diversity. Mol Ecol 15:2277–2289
Husband R, Herre EA, Turner SL, Gallery R, Young JPW (2002) Molecular diversity of arbuscular mycorrhizal fungi and patterns of host association over time and space in a tropical forest. Mol Ecol 11:2669–2678
Jansa J, Smith F, Smith S (2008) Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytol 177:779–789
Johnson NC (1993) Can fertilization of soil select less mutualistic mycorrhizae. Ecol Appl 3:749–757
Johnson D, Ijdo M, Anderson IC, Alexander IJ (2005a) Do plant communities influence microbial diversity and function? Comp Biochem Physiol Mol Integr Physiol 141:S220–S220
Johnson D, Leake JR, Read DJ (2005b) Liming and nitrogen fertilization affects phosphatase activities, microbial biomass and mycorrhizal colonisation in upland grassland. Plant Soil 271:157–164
Johnson D, Anderson IC, Williams A, Whitlock R, Grime JP (2010) Plant genotypic diversity does not beget root-fungal species diversity. Plant Soil 336:107–111
Krebs C (1989) Ecological methodology. HarperCollins, New York
Li GD, Singh RP, Brennan JP, Helyar KR (2010a) A financial analysis of lime application in a long-term agronomic experiment on the south-western slopes of New South Wales. Crop Past Sci 61:12–23
Li L-F, Li T, Zhang Y, Zhao Z-W (2010b) Molecular diversity of arbuscular mycorrhizal fungi and their distribution patterns related to host-plants and habitats in a hot and arid ecosystem, southwest China. FEMS Microbiol Ecol 71:418–427
Lux H, Cumming J (2001) Mycorrhizae confer aluminium resistance to tulip-poplar seedlings. Can J Forest Res 31:694–702
Martinez-Garcia LB, Pugnaire FI (2011) Arbuscular mycorrhizal fungi host preference and site effects in two plant species in a semiarid environment. Appl Soil Ecol 48:313–317
Martini JA, Mutters RG (1985) Effect of lime rates on nutrient availability, mobility, and uptake during the soybean-growing season.1. aluminum, manganese, and phosphorus. Soil Sci 139:219–226
Morton JB (1995) Taxonomic and phylogenetic divergence among 5 scutellospora species based on comparative developmental sequences. Mycologia 87:127–137
Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York
Oehl F, Laczko E, Bogenrieder A, Stahr K, Bosch R, van der Heijden M, Sieverding E (2010) Soil type and land use intensity determine the composition of arbuscular mycorrhizal fungal communities. Soil Biol Biochem 42:724–738
Olsson P, Hansson M, Burleigh S (2006) Effect of P availability on temporal dynamics of carbon allocation and glomus intraradices high-affinity P transporter gene induction in arbuscular mycorrhiza. Appl Environ Microb 72:4115–4120
Payne R, Harding S, Murray D, Soutar D, Baird D, Glaser A, Channing I, Welham S, Gilmour A, Thompson R, Webster R (2010) The Guide to GenStat Release 13, Part 2: statistics. VSN International, Hemel Hempstead
Porter W, Robson A, Abbott L (1987) Factors controlling the distribution of vesicular arbuscular mycorrhizal fungi in relation to soil-pH. J Appl Ecol 24:663–672
Raznikiewicz H, Carlgren K, Martensson A (1994) Impact of phosphorus fertilization and liming on the presence of arbuscular mycorrhizal spores in a swedish long-term field experiment. Swed J Agr Res 24:157–164
Rodriguez A, Dougall T, Dodd JC, Clapp JP (2001) The large subunit ribosomal RNA genes of Entrophospora infrequens comprise sequences related to two different glomalean families. New Phytol 152:159–167
Rosendahl S, McGee P, Morton JB (2009) Lack of global population genetic differentiation in the arbuscular mycorrhizal fungus Glomus mosseae suggests a recent range expansion which may have coincided with the spread of agriculture. Mol Ecol 18:4316–4329
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York
Schwarzott D, Walker C, Schüssler A (2001) Glomus, the largest genus of the arbuscular mycorrhizal fungi (Glomales), is nonmonophyletic. Mol Phylogenet Evolut 21:190–197
Sen R, Hepper CM, Azcon-Aguilar C, Rosendahl S (1990) Competition between introduced and indigenous mycorrhizal fungi (Glomus spp.) for root colonization of leek. Agr Eco Envir 29:355–359
Smith S, Read D (1997) Mycorrhizal symbiosis. Academic, London
Soil Survey Staff (2006) Keys to soil taxonomy. In USDA-Natural resources conservation service, Washington, DC
Sonjak S, Udovic M, Wraber T, Likar M, Regvar M (2009) Diversity of halophytes and identification of arbuscular mycorrhizal fungi colonising their roots in an abandoned and sustained part of Secovlje salterns. Soil Biol Biochem 41:1847–1856
Stackebrandt E, Goebel BM (1994) Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44:846–849
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Troeh ZI, Loynachan TE (2009) Diversity of arbuscular mycorrhizal fungal species in soils of cultivated soybean fields. Agro J 101:1453–1462
Trouvelot A, Kough J, Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization VA d’un système radiculaire. Recherche de méthodes d’estimation ayant une signification fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and genetical aspects of mycorrhizae. INRA Press, Paris, pp 217–221
Trouvelot S, van Tuinen D, Hijri M, Gianinazzi-Pearson V (1999) Visualization of ribosomal DNA loci in spore interphasic nuclei of glomalean fungi by fluorescence in situ hyhridization. Mycorrhiza 8:203–206
Unkovich MJ, Sanford P, Pate JS (1996) Nodulation and nitrogen fixation by subterranean clover in acid soils as influenced by lime application, toxic aluminium, soil mineral N, and competition from annual ryegrass. Soil Biol Biochem 28:639–648
Vandenkoornhuyse P, Leyval C, Bonnin I (2001) High genetic diversity in arbuscular mycorrhizal fungi: evidence for recombination events. Heredity 87:243–253
Vandenkoornhuyse P, Ridgway KP, Watson IJ, Fitter AH, Young JPW (2003) Co-existing grass species have distinctive arbuscular mycorrhizal communities. Mol Ecol 12:3085–3095
van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72
Wakelin SA, Gregg AL, Simpson RJ, Li GD, Riley IT, McKay AC (2009) Pasture management clearly affects soil microbial community structure and N-cycling bacteria. Pedobiologia 52:237–251
Wenke L (2008) N, P contribution and soil adaptability of four arbuscular mycorrhizal fungi. Acta Agr Scand B-S P 58:285–288
Whelan A, Alexander M (1986) Effects of low pH and high Al, Mn and Fe levels on the survival of Rhizobium trifolii and the nodulation of subterranean clover. Plant Soil 92:363–371
Yano K, Takaki M (2005) Mycorrhizal alleviation of acid soil stress in the sweet potato (Ipomoea batatas). Soil Biol Biochem 37:1569–1572
Acknowledgements
The work was supported by the 2010 New Initiative Grant from EH Graham Centre for Agricultural Innovation. The technical help of Mr Xiaocheng Zhu, Dr Rosy Raman, and Ms Rujuan Huang is gratefully acknowledged. Our thanks extended to Dr Benjamin Stodart who kindly reviewed the manuscript and made constructive comments. The senior author received financial support from Chinese Scholarship Council to work in Australia for 12 months.
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Guo, Y.J., Ni, Y., Raman, H. et al. Arbuscular mycorrhizal fungal diversity in perennial pastures; responses to long-term lime application. Plant Soil 351, 389–403 (2012). https://doi.org/10.1007/s11104-011-0976-7
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DOI: https://doi.org/10.1007/s11104-011-0976-7