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Diversity and vertical distribution of indigenous arbuscular mycorrhizal fungi under two soybean rotational systems

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Abstract

To evaluate the importance of arbuscular mycorrhizal fungi (AMF) to crop production, it is imperative to move beyond the plow layer to include the full soil profile impacted by plant roots. To illustrate this, we investigated the vertical distribution of AMF biomass and community structure within the top 100 cm of soil in soybean (Glycine max (L.) Merr., cv: Enrei) rotational systems cropped to wheat (Triticuma estivum L. cv: Bandowase) or left fallow using fatty acid methyl ester (FAME) biomarkers and molecular analysis, respectively. AMF biomass, as measured by concentration of C16:1cis11, declined during fallow and with increasing soil depth. Greater than 50 % of the stored AMF biomass was found at depths below 35 cm. Phylogenetic analysis revealed 16 AMF phylotypes, including nine Glomus, two Gigaspora, two Scutellospora, and one each of Diversispora, Paraglomus, and an unknown glomeromycete, at different sampling depths in this study. Cluster analysis based on the number and abundance of each AMF phylotype formed two distinct clusters separating wheat from fallow rotations. There was no distinct relationship with soil depth beyond clustering AMF communities above and below 20 cm under wheat. Redundancy analysis (RDA) and hierarchical cluster analysis demonstrated that AMF communities by soil depth within each rotation were not significantly different. However, AMF communities were clearly influenced by crop rotation, where the distribution of specific AMF phylotypes responded to the presence of the wheat crop.

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References

  • Ajwa HA (1998) Carbon and nitrogen mineralization in tallgrass prairie and agricultural soil profiles. Soil Sci Soc Am J 62:942–951

    Article  CAS  Google Scholar 

  • Alguacil MM, Torrecillas E, Hernández G, Roldán A (2012) Changes in the diversity of soil arbuscular mycorrhizal fungi after cultivation for biofuel production in a Guantanamo (Cuba) tropical system. PLoS One 7:e34887. doi:10.1371/journal.pone.0034887

    Article  CAS  Google Scholar 

  • An ZQ, Hendrix JW, Hershman DE, Ferriss RS, Henson GT (1993) The influence of crop rotation and soil fumigation on a mycorrhizal fungal community associated with soybean. Mycorrhiza 3:171–182

    Article  Google Scholar 

  • Anderson RC, Liberta AE, Dickman LA, Katz AJ (1983) Spatial variation in vesicular-arbuscular mycorrhiza spore density. Bull Torrey Bot Club 110:519–525

    Article  Google Scholar 

  • Araki H, Iijima M (2001) Deep rooting in winter wheat: rooting nodes of deep roots in two cultivars with deep and shallow root systems. Plant Prod Sci 4:215–219

    Google Scholar 

  • Arihara J, Karasawa T (2000) Effect of previous crops on arbuscular mycorrhizal formation and growth of succeeding maize. Soil Sci Plant Nutr 46:43–51

    Article  Google Scholar 

  • Borriello R, Lumini E, Girlanda M, Bonfante P, Bianciotto V (2012) Effects of different management practices on arbuscular mycorrhizal fungal diversity in maize fields by a molecular approach. Biol Fertil Soils 48:911–922

    Article  Google Scholar 

  • Brady NC, Weil RR (2002) The nature and properties of soils. Pearson Education, Upper Saddle River

    Google Scholar 

  • Bray RH, Kurtz LT (1945) Determination of total, organic, and available forms of phosphorus in soils. Soil Sci 59:39–45

    Article  CAS  Google Scholar 

  • Buyer JS, Teasdale JR, Roberts DP, Zasada IA, Maul JE (2010) Factor affecting soil microbial community structure in tomato cropping systems. Soil Biol Biochem 42:831–841

    Article  CAS  Google Scholar 

  • Campbell CA, Lafond GP, Zentner RP, Biederbeck VO (1991) Influence of fertilizer and straw baling on soil organic matter in a thick black chernozem in western Canada. Soil Biol Biochem 23:443–446

    Article  CAS  Google Scholar 

  • Chaparro JM, Sheflin AM, Manter DK, Vivanco JM (2012) Manipulating the soil microbiome to increase soil health and plant fertility. Biol Fertil Soils 48:489–499

    Article  Google Scholar 

  • Cuenca G, Lovera M (2010) Seasonal variation and distribution at different soil depths of arbuscular mycorrhizal fungi spores in a tropical sclerophyllous shrubland. Botany 88:54–64

    Article  Google Scholar 

  • Daniell TJ, Husband R, Fitter AH, Young JPW (2001) Molecular diversity of arbuscular mycorrhizal fungi colonizing arable crops. FEMS Microbiol Ecol 36:203–209

    Article  CAS  PubMed  Google Scholar 

  • Drijber RA, Doran JW, Parkhurst AM, Lyon DJ (2000) Changes in soil microbial community structure with tillage under long-term wheat–fallow management. Soil Biol Biochem 32:141–1430

    Article  Google Scholar 

  • Fredeen AL, Terry N (1988) Influence of vesicular-arbuscular mycorrhizal infection and soil phosphorus level on growth and carbon metabolism of soybean. Can J Bot 66:2311–2316

    Google Scholar 

  • Gavito ME, Miller MH (1998) Early phosphorus nutrition, mycorrhizae development, dry matter partitioning and yield of maize. Plant Soil 199:177–186

    Article  CAS  Google Scholar 

  • Gollotte A, van Tuinen D, Atkinson D (2004) Diversity of arbuscular mycorrhizal fungi colonising roots of the grass species Agrostis capillaris and Lolium perenne in a field experiment. Mycorrhiza 14:111–117

    Article  PubMed  Google Scholar 

  • Grigera MS, Drijber RA, Wienhold BJ (2007a) Increased abundance of arbuscular mycorrhizal fungi in soil coincides with the reproductive stages of maize. Soil Biol Biochem 39:1401–1409

    Article  CAS  Google Scholar 

  • Grigera MS, Drijber RA, Shores-Morrow RH, Wienhold BJ (2007b) Distribution of the arbuscular mycorrhizal biomarker C16:1cis11 among neutral, glyco and phospholipids extracted from soil during the reproductive growth of corn. Soil Biol Biochem 39:1589–1596

    Article  CAS  Google Scholar 

  • Guo H, He X, Li Y (2012) Spatial distribution of arbuscular mycorrhiza and glomalin in the rhizosphere of Caragana korshinskii Kom. in the Otindag sandy land, China. Afr J Microbiol Res 6:5745–5753

    CAS  Google Scholar 

  • Harner MJ, Opitz N, Geluso K, Tockner K, Rillig MC (2011) Arbuscular mycorrhizal fungi on developing islands within a dynamic river floodplain: an investigation across successional gradients and soil depth. Aquat Sci 73:35–42

    Article  CAS  Google Scholar 

  • He X, Li Y, Zhao L (2010) Dynamics of arbuscular mycorrhizal fungi and glomalin in the rhizosphere of Artemisia ordosica Krasch. in MuUs Sandland, China. Soil Biol Biochem 42:1313–1319

    Article  CAS  Google Scholar 

  • Higo M, Isobe K, Kang DJ, Ujiie K, Drijber RA, Ishii R (2010) Inoculation with arbuscular mycorrhizal fungi or crop rotation with mycorrhizal plants improves the growth of maize in limed acid sulfate soil. Plant Prod Sci 13:74–79

    Article  Google Scholar 

  • Higo M, Isobe K, Maekawa T, Ishii R (2011a) Community structure of arbuscular mycorrhizal fungi colonized in various winter crop roots. Soil Microorg 65:3–10

    Google Scholar 

  • Higo M, Isobe K, Kang DJ, Maekawa T, Ishii R (2011b) Molecular diversity and spore density of indigenous arbuscular mycorrhizal fungi in acid sulfate soil in Thailand. Ann Microbiol 61:383–389

    Article  Google Scholar 

  • Hijri I, Sýkorová Z, Oehl F, Ineichen K, Mäder 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

    Article  CAS  PubMed  Google Scholar 

  • Isobe K, Tsuboki Y (1998) The relationship between growth promotion by arbuscular mycorrhizal fungi and root morphology and phosphorus absorption in gramineous and leguminous crops. Jpn J Crop Sci 67:347–352

    Article  CAS  Google Scholar 

  • Isobe K, Aizawa E, Iguchi Y, Ishii R (2007) Distribution of arbuscular mycorrhizal fungi in upland field soil of Japan. 1. Relationship between spore density and the soil environment factor. Plant Prod Sci 10:122–128

    Article  CAS  Google Scholar 

  • Isobe K, Sugimura H, Maeshima T, Ishii R (2008) Distribution of arbuscular mycorrhizal fungi in upland field soil of Japan. 2. Spore density of arbusclar mycorrhizal fungi and infection ratio soybean and maize fields. Plant Prod Sci 11:171–177

    Article  Google Scholar 

  • Isobe K, Maruyama K, Nagai S, Higo M, Maekawa T, Mizonobe G, Drijber RA, Ishii R (2011) Arbuscular mycorrhizal fungal community structure in soybean roots: comparison between Kanagawa and Hokkaido, Japan. Adv Microbiol 1:13–22

    Article  Google Scholar 

  • Jakobsen I, Nielsen NE (1983) Vesicular-arbuscular mycorrhiza in field-grown crops. I. Mycorrhizal infection in cereals and peas at various times and soil depths. New Phytol 93:401–413

    Article  Google Scholar 

  • Jansa J, Mozafar A, Anken T, Ruh R, Sanders IR, Frossard E (2002) Diversity and structure of AMF communities as affected by tillage in a temperate soil. Mycorrhiza 12:225–234

    Article  CAS  PubMed  Google Scholar 

  • Jansa J, Mozafar A, Kuhn G, Anken T, Ruh R, Sanders IR, Frossard E (2003) Soil tillage affects the community structure of mycorrhizal fungi in maize roots. Ecol Appl 13:1164–1176

    Article  Google Scholar 

  • Jansa J, Smith FA, Smith SE (2008) Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytol 177:779–789

    Article  CAS  PubMed  Google Scholar 

  • Johnson NC, Pfleger FL, Crookston RK, Simmons SR, Copeland PJ (1991) Vesicular-arbuscular mycorrhizas respond to corn and soybean cropping history. New Phytol 117:657–663

    Article  Google Scholar 

  • Kabir Z (2005) Tillage or no-tillage: impact on mycorrhizae. Can J Plant Sci 85:23–29

    Article  Google Scholar 

  • Kabir Z, O'Halloran IP, Widden P, Hamel C (1998) Vertical distribution of arbuscular mycorrhizal fungi under corn (Zea mays L.) in no-till and conventional tillage systems. Mycorrhiza 8:53–55

    Article  Google Scholar 

  • Karasawa T (2004) Arbuscular mycorrhizal associations and interactions in temperate cropping systems. ResBull Natl Agric Res Cent 179:1–71 (In Japanese with English summary)

    Google Scholar 

  • Karasawa T, Takebe M (2012) Temporal or spatial arrangements of cover crops to promote arbuscular mycorrhizal colonization and P uptake of upland crops grown after nonmycorrhizal crops. Plant Soil 353:355–366

    Article  CAS  Google Scholar 

  • Karlen DL, Varvel GE, Bullock DG, Cruse RM (1994) Crop rotations for the 21st century. Adv Agron 53:1–45

    Article  Google Scholar 

  • Kieft T, Amy P, Brockman F, Fredrickson J, Bjornstad B, Rosacker L (1993) Microbial abundance and activities in relation to water potential in the vadose zones of arid and semiarid sites. Microbial Ecol 26:59–78

    Article  Google Scholar 

  • Legendre P, Legendre L (1998) Numerical ecology, 2nd Englishedn. Elsevier, Amsterdam

    Google Scholar 

  • Lehman RM, Taheri WI, Osborne SL, Buyer JS, Douds DD (2012) Fall cover cropping can increase arbuscular mycorrhizae in soils supporting intensive agricultural production. Appl Soil Ecol 61:300–304

    Article  Google Scholar 

  • Li LF, Li T, Zhao ZW (2007) Differences of arbuscular mycorrhizal fungal diversity and community between a cultivated land and an old field and a never cultivated field in a hot and arid ecosystem of South West China. Mycorrhiza 17:655–665

    Article  CAS  PubMed  Google Scholar 

  • Li T, Li L, Sha T, Zhang H, Zhao Z (2010) Molecular diversity of arbuscular mycorrhizal fungi associated with two dominant xerophytes in a valley-type savanna, southwest China. Appl Soil Ecol 44:61–66

    Article  Google Scholar 

  • Lundquist EJ, Scow KM, Jackson LE, Uesugi SL, Johnson CR (1999) Rapid response of soil microbial communities from conventional, low input, and organic farming systems to a wet/dry cycle. Soil Biol Biochem 31:1661–1675

    Article  CAS  Google Scholar 

  • Maldonado-Mendoza IE, Dewbre GR, Harrison MJ (2001) Expression of a Glomus intraradices phosphate transporter gene (GiPT) in the extra-radical mycelium of an arbuscular mycorrhiza: regulation in response to phosphate. Mol Plant-Microbe Interact 14:1140–1148

    Article  CAS  PubMed  Google Scholar 

  • Michalson EL (1999) A history of conservation research in the Pacific Northwest. In: Michalson EL, Papendick RI, Carlson JE (eds) Conservation farming in the United States. The methods and accomplishments of the STEEP Program. CRC, Boca Raton, pp 1–10

  • Ministry of Agriculture, Forestry and Fisheries (2012) Statistical report on agriculture, forestry and fisheries. Available online athttp://www.maff.go.jp/j/tokei/kouhyou/sakumotu/menseki/index.html

  • Mishima S, Itahashi S, Kimura R, Inoue T (2002) Trends of phosphate fertilizer demand and phosphate balance in farmland soils in Japan. Soil Sci Plant Nutr 49:39–45

    Article  Google Scholar 

  • Muleta D, Assefa F, Nemomissa S, Granhall U (2008) Distribution of arbuscular mycorrhizal fungi spores in soils of smallholder agroforestry and monocultural coffee systems in southwestern Ethiopia. Biol Fertil Soils 44:653–659

    Article  Google Scholar 

  • Neville J, Tessier JL, Morrison I, Scarratt J, Canning B, Klironomos JN (2002) Soil depth distribution of ecto- and arbuscular mycorrhizal fungi associated with Populus tremuloides within a 3-year-old boreal forest clear-cut. Appl Soil Ecol 19:209–216

    Article  Google Scholar 

  • Ngosong C, Gabriel E,Ruess L (2012) Use of the signature fatty acid 16:1 ω5 as a tool to determine the distribution of arbuscular mycorrhizal fungi in soil. J Lipids. doi:10.1155/2012/236807

  • Oehl F, Sieverding E, Ineichen K, Mäder P, Boller T, Wiemken A (2003) Impact of land use intensity on the species diversity of arbuscular mycorrhizal fungi in agroecosystems of central Europe. Appl Environ Microbiol 69:2816–2824

    Article  CAS  PubMed  Google Scholar 

  • Oehl F, Sieverding E, Ineichen K, Ris EA, Boller T, Wiemken A (2005) Community structure of arbuscular mycorrhizal fungi at different soil depths in extensively and intensively managed agroecosystems. New Phytol 165:273–283

    Article  PubMed  Google Scholar 

  • Oehl F, Sieverding E, Ineichen K, Mäder P, Wiemken A, Boller T (2009) Distinct sporulation dynamics of arbuscular mycorrhizal fungal communities from different agroecosystems in long-term microcosms. Agric Ecosyst Environ 134:257–268

    Article  Google Scholar 

  • Oka N, Karasawa T, Okazaki K, Takebe M (2010) Maintenance of soybean yield with reduced phosphorus application by previous cropping with mycorrhizal plants. Soil Sci Plant Nutr 56:824–830

    Article  CAS  Google Scholar 

  • Olsson PA, Johansen A (2000) Lipid and fatty acid composition of hyphae and spores of arbuscular mycorrhizal fungi at different growth stages. Mycol Res 104:429–434

    Article  CAS  Google Scholar 

  • Osorio NW, Alzate JM, Ramírez GA (2002) Coffee seedling growth as affected by mycorrhizal inoculation and organic amendment. Commun Soil Sci Plant Anal 33:1425–1434

    Article  CAS  Google Scholar 

  • Power JF, Peterson GA (1998) Nitrogen transformations, utilization, and conservation as affected by fallow tillage method. Soil Till Res 49:37–47

    Article  Google Scholar 

  • Renker C, Weißhuhn K, Kellner H, Buscot F (2006) Rationalizing molecular analysis of field-collected roots for assessing diversity of arbuscular mycorrhizal fungi: to pool, or not to pool, this is the question. Mycorrhiza 16:525–531

    Article  CAS  PubMed  Google Scholar 

  • Richter DD, Markewitz D (1995) How deep is soil? BioScience 45:600–609

    Article  Google Scholar 

  • Rillig MC, Field CB (2003) Arbuscular mycorrhizae respond to plants exposed to elevated atmospheric CO2 as a function of soil depth. Plant Soil 254:383–391

    Article  CAS  Google Scholar 

  • Sasvári Z, László H, Katalin P (2011) The community structure of arbuscular mycorrhizal fungi in roots of maize grown in a 50-year monoculture. Biol Fertil Soils 47:167–176

    Article  Google Scholar 

  • Schimel JP, Gulledge JM, Clein-Curley JS, Lindstrom JE, Braddock JF (1999) Moisture effects on microbial activity and community structure in decomposing birch litter in the Alaskan taiga. Soil Biol Biochem 31:831–838

    Article  CAS  Google Scholar 

  • Schweiger PF, Jakobsen I (1999) Direct measurement of arbuscular mycorrhizal phosphorus uptake into field-grown winter wheat. Agron J 91:998–1002

    Article  Google Scholar 

  • Smith SE, Read DJ (2008) Arbuscular mycorrhizaes. In: Smith SE, Read DJ (eds) Mycorrhizal symbiosis, 3rd edn. Academic, London, pp 13–187

    Chapter  Google Scholar 

  • Suzuki R, Shimodaira H (2006) Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22:1540–1542

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  Google Scholar 

  • Taniguchi T, Usuki H, Kikuchi J, Hirobe M, Miki N, Fukuda K, Zhang G, Wang L, Yoshikawa K, Yamanaka N (2012) Colonization and community structure of root-associated microorganisms of Sabina vulgaris with soil depth in a semiarid desert ecosystem with shallow groundwater. Mycorrhiza 22:419–428

    Article  PubMed  Google Scholar 

  • Tawaraya K, Hirose R, Wagatsuma T (2012) Inoculation of arbuscular mycorrhizal fungi can substantially reduce phosphate fertilizer application to Allium fistulosum L. and achieve marketable yield under field condition. Biol Fertil Soils 48:839–843

    Article  Google Scholar 

  • terBraak C, Smilauer P (2002) CANOCO reference manual and Canodraw for Windows user's guide: software for canonical community ordination, 4.5 (ed).Microcomputer Power, Ithaca

  • Tian H, Drijber RA, Niu XS, Zhang JL, Li XL (2011) Spatio-temporal dynamics of an indigenous arbuscular mycorrhizal fungal community in an intensively managed maize agroecosystem in North China. Appl Soil Ecol 47:141–152

    Article  Google Scholar 

  • Torrecillas E, Alguacil MM, Roldán A (2012) Host preferences of arbuscular mycorrhizal fungi colonizing annual herbaceous plant species in semiarid Mediterranean prairies. Appl Environ Microbiol 78:6180–6186

    Article  CAS  PubMed  Google Scholar 

  • 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 situhybridization. Mycorrhiza 8:203–206

    Article  CAS  Google Scholar 

  • Trumbore S (2000) Age of soil organic matter and soil respiration: radiocarbon constraints on belowground C dynamics. Ecol Appl 10:399–411

    Article  Google Scholar 

  • van Tuinen D, Jacquot E, Zhao B, Gollotte A, Gianinazzi-Pearson V (1998) Characterization of root colonization profiles by a microcosm community of arbuscular mycorrhizal fungi using25S rDNA-targeted nested PCR. Mol Ecol 7:879–887

    Article  PubMed  Google Scholar 

  • Vilariño A, Arines J, Schüepp H (1993) Extraction of vesicular-arbuscular mycorrhizal mycelium from sand samples. Soil Biol Biochem 25:99–103

    Article  Google Scholar 

  • Wirsel SGR (2004) Homogenous stands of a wetland grass harbour diverse consortia of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 48:129–138

    Article  CAS  PubMed  Google Scholar 

  • Wortmann CS, Quincke JA, Drijber RA, Mamo M, Franti T (2008) Soil microbial community change and recovery after one-time tillage of continuous no-till. Agron J 100:1681–1686

    Article  Google Scholar 

  • Yang FY, Li GZ, Zhang DE, Christie P, Li XL, Gai JP (2010) Geographical and plant genotype effects on the formation of arbuscular mycorrhiza in Avena sativa and Avena nuda at different soil depths. Biol Fertil Soils 46:435–443

    Article  Google Scholar 

  • Zogg GP, Zak DR, Ringelberg DB, MacDonald NW, Pregitzer KS, White DC (1997) Compositional and functional shifts in microbial communities due to soil warming. Soil Sci Soc Am J 61:475–481

    Article  CAS  Google Scholar 

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Higo, M., Isobe, K., Yamaguchi, M. et al. Diversity and vertical distribution of indigenous arbuscular mycorrhizal fungi under two soybean rotational systems. Biol Fertil Soils 49, 1085–1096 (2013). https://doi.org/10.1007/s00374-013-0807-5

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