Skip to main content

Advertisement

Log in

No tillage enhances arbuscular mycorrhizal fungal population, glomalin-related soil protein content, and organic carbon accumulation in soil macroaggregates

  • Soils, Sec 1 • Soil Organic Matter Dynamics and Nutrient Cycling • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

Mechanisms of soil organic carbon (C) accumulation in response to no tillage (NT) are unclear. The extraradical hyphae of arbuscular mycorrhizal (AM) fungi are known to contribute to the formation and maintenance of soil aggregates through the exudation of glomalin. The objectives of this study were to evaluate the effects of different tillage management treatments on soil aggregates, AM fungal community, and glomalin contents and find out the main factors that influence aggregate C accumulation.

Materials and methods

A field experiment established in a sandy loam soil at Northern China has received 4-year continuous tillage treatments, including conventional tillage (CT), NT, and alternating tillage (AT, tillage in the wheat season and no tillage in the maize season). Undisturbed top soil samples (0–15 cm) from four individual plots per treatment were collected for the analysis of aggregates, which were separated according to the wet-sieving method. The organic C contents in different particle size aggregates were determined by the dichromate oxidization, and the glomalin-related soil protein (GRSP) was then extracted with citrate solution using bovine serum albumin (BSA) as a standard. The population size of AM fungi was determined by real-time PCR, and the community composition was analyzed using polymerase chain reaction plus denature gradient gel electrophoresis (PCR-DGGE), cloning, and sequencing techniques.

Results and discussion

Compared to CT, both NT and AT resulted in higher percentages of macroaggregates (>50 μm), and NT, rather than AT, significantly increased organic C contents in >250- and 50–2-μm aggregates, and also organic C contribution by macroaggregates. Both NT and AT significantly increased AM fungal population in 250–50-μm aggregates, but only NT increased it in >250-μm aggregates. NT, rather than AT, significantly increased easily extractable GRSP contents in 250–50- and <2-μm aggregates, and total GRSP content in 250–50-μm aggregates. In addition, the greatest changes of AM fungal community in response to NT or AT were observed in 250–50-μm aggregates, and the genus of Glomus registered the highest species number from the DGGE profiles.

Conclusions

Four-year NT practice greatly enhanced soil aggregation and increased both AM fungal population and organic C contribution of soil macroaggregates. The contents of GRSP and organic C in aggregates were linearly related across particle sizes for all treatments, suggesting that NT played a vital role in maintaining AM fungal growth and GRSP production (notably in 250–50-μm aggregates), which might contribute to binding within microaggregates (<50 μm) and macroaggregates, and increasing soil organic C sequestration.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alguacil MM, Lumini E, Roldan A, Salinas-Garcia JR, Bonfante P, Bianciotto V (2008) The impact of tillage practices on arbuscular mycorrhizal fungal diversity in subtropical crops. Ecol Appl 18:527–536

    Article  CAS  Google Scholar 

  • Alkan N, Gadkar V, Coburn J, Yarden O, Kapulnik Y (2004) Quantification of the arbuscular mycorrhizal fungus Glomus intraradices in host tissue using real-time polymerase chain reaction. New Phytol 161:877–885

    Article  CAS  Google Scholar 

  • Alvear M, Rosas A, Rouanet JL, Borie F (2005) Effects of three soil tillage systems on some biological activities in an Ultisol from southern Chile. Soil Tillage Res 82:195–202

    Article  Google Scholar 

  • Avio L, Castaldini M, Fabiani A, Bedini S, Sbrana C, Turrini A, Giovannetti M (2013) Impact of nitrogen fertilization and soil tillage on arbuscular mycorrhizal fungal communities in a Mediterranean agroecosystem. Soil Biol Biochem 67:285–294

    Article  CAS  Google Scholar 

  • Bedini S, Avio L, Argese E, Giovannetti M (2007) Effects of long-term land use on arbuscular mycorrhizal fungi and glomalin-related soil protein. Agric Ecosyst Environ 120:463–466

    Article  CAS  Google Scholar 

  • Bedini S, Pellegrino E, Avio L, Pellegrini S, Bazzoffi P, Argese E, Giovanetti M (2009) 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 41:1491–1496

    Article  CAS  Google Scholar 

  • Blanco-Canqui H, Lal R (2008) No-tillage and soil-profile carbon sequestration: an on-farm assessment. Soil Sci Soc Am J 72:693–701

    Article  CAS  Google Scholar 

  • Boddington CL, Dodd JC (2000) The effect of agricultural practices on the development of indigenous arbuscular mycorrhizal fungi. I. Field studies in an Indonesian ultisol. Plant Soil 218:137–144

    Article  CAS  Google Scholar 

  • Borie F, Rubio R, Morales A (2008) Arbuscular mycorrhizal fungi and soil aggregation. J Soil Sci Plant Nutr 8:9–18

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 7:248–254

    Article  Google Scholar 

  • Castillo CG, Rubio R, Rouanet JL, Borie F (2006) Early effects of tillage and crop rotation on arbuscular mycorrhizal fungal propagules in an Ultisol. Biol Fertil Soils 42:83–92

    Article  Google Scholar 

  • Dai J, Hu J, Lin X, Yang A, Wang R, Zhang J, Wong MH (2013) Arbuscular mycorrhizal fungal diversity, external mycelium length, and glomalin-related soil protein content in response to long-term fertilizer management. J Soils Sediments 13:1–11

    Article  CAS  Google Scholar 

  • He J, Li H, Rasaily RG, Wang Q, Cai G, Su Y, Qiao X, Liu L (2011) Soil properties and crop yields after 11 years of no tillage farming in wheat–maize cropping system in North China Plain. Soil Tillage Res 113:48–54

    Article  Google Scholar 

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

    Article  CAS  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 

  • Jiao H, Chen YL, Lin XG, Liu RJ (2011) Diversity of arbuscular mycorrhizal fungi in greenhouse soils continuously planted to watermelon in North China. Mycorrhiza 21:681–688

    Article  Google Scholar 

  • Kittiworawat S, Youpensuk S, Rerkasem B (2010) Diversity of arbuscular mycorrhizal fungi in Mimosa invisa and effect of the soil pH on the symbiosis. Chiang Mai J Sci 37:517–527

    Google Scholar 

  • Lovelock CE, Wright SF, Nichols KA (2004) Using glomalin as an indicator for arbuscular mycorrhizal hyphal growth: an example from a tropical rain forest soil. Soil Biol Biochem 36:1009–1012

    Article  CAS  Google Scholar 

  • Mebius LJ (1960) A rapid method for determination of organic carbon in soil. Anal Chem Acta 22:120–124

    Article  CAS  Google Scholar 

  • Mirás-Avalos JM, Antunes PM, Koch A, Khosla K, Kironomos JN, Dunfield KE (2011) The influence of tillage on the structure of rhizosphere and root-associated arbuscular mycorrhizal fungal communities. Pedobiologia 54:235–241

    Article  Google Scholar 

  • Rillig MC (2004) Arbuscular mycorrhizae, glomalin, and soil aggregation. Can J Soil Sci 84:355–363

    Article  Google Scholar 

  • Rillig MC, Wright SF, Nichols KA, Schmidt WF, Torn MS (2001a) Large contribution of arbuscular mycorrhizal fungi to soil carbon pools in tropical forest soils. Plant Soil 233:167–177

    Article  CAS  Google Scholar 

  • Rillig MC, Wright SF, Tom MS (2001b) Unusually large contribution of arbuscular mycorrhizal fungi to soil organic matter pools in tropical forest soils. Plant Soil 233:167–177

    Article  CAS  Google Scholar 

  • Rillig MC, Wright SF, Eviner VT (2002a) The role of arbuscular mycorrhizal fungi and glomalin in soil aggregation: comparing effects of five plant species. Plant Soil 238:325–333

    Article  CAS  Google Scholar 

  • Rillig MC, Wright SF, Shaw MR, Field CB (2002b) Artificial climate warming positively affects arbuscular mycorrhizae but decreases soil aggregate water stability in an annual grassland. Oikos 97:52–58

    Article  Google Scholar 

  • Rillig MC, Ramsey PW, Morris S, Paul EA (2003) Glomalin, an arbuscular mycorrhizal fungal soil protein, responds to land-use change. Plant Soil 253:293–299

    Article  CAS  Google Scholar 

  • Rillig MC, Mardatin NF, Leifheit EF, Antunes PM (2010) Mycelium of arbuscular mycorrhizal fungi increases soil water repellency and is sufficient to maintain water-stable soil aggregates. Soil Biol Biochem 42:1189–1191

    Article  CAS  Google Scholar 

  • Roldán A, Salinas-García JR, Alguacil MM, Caravaca F (2007) Soil sustainability indicators following conservation tillage practices under subtropical maize and bean crops. Soil Tillage Res 93:273–282

    Article  Google Scholar 

  • Rosier CL, Hoye AT, Rillig MC (2006) Glomalin-related soil protein: assessment of current detection and quantification tools. Soil Biol Biochem 38:2205–2211

    Article  CAS  Google Scholar 

  • Sato K, Suyama Y, Saito M, Sugawara K (2005) A new primer for discrimination of arbuscular mycorrhizal fungi with polymerase chain reaction-denature gradient gel electrophoresis. Grassland Sci 51:179–181

    Article  CAS  Google Scholar 

  • Schindler FV, Mercer EJ, Rice JA (2007) Chemical characteristics of glomalin-related soil protein (GRSP) extracted from soils of varying organic matter content. Soil Biol Biochem 39:320–329

    Article  CAS  Google Scholar 

  • Singh S, Pandey A, Chaurasia B, Palni LMS (2008) Diversity of arbuscular mycorrhizal fungi associated with the rhizosphere of tea growing in ‘natural’ and ‘cultivated’ecosites. Biol Fertil Soils 44:491–500

    Article  Google Scholar 

  • Six J, Elliott ET, Paustian K (2000) Soil macroaggregate turnover and microaggregate formation: a mechanism for C sequestration under no-tillage agriculture. Soil Biol Biochem 32:2099–2103

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, Cambridge

    Google Scholar 

  • Spohn M, Giani L (2010) Water-stable aggregates, glomalin-related soil protein, and carbohydrates in a chronosequence of sandy hydromorphic soils. Soil Biol Biochem 42:1505–1511

    Article  CAS  Google Scholar 

  • Stemmer M, Gerzabek MH, Kandeler E (1998) Organic matter and enzyme activity in particle-size fractions of soils obtained after low energy sonication. Soil Biol Biochem 30:9–18

    Article  CAS  Google Scholar 

  • Wright SF, Anderson RL (2000) Aggregate stability and glomalin in alternative crop rotations for the central great plains. Biol Fertil Soils 31:249–253

    Article  CAS  Google Scholar 

  • Wright SF, Upadhyaya A (1996) Extraction of an abundant and unusual protein from soil and comparison with hyphal protein of arbuscular mycorrhizal fungi. Soil Sci 161:575–586

    Article  CAS  Google Scholar 

  • Wu QS, Cao MQ, Zou YN, He XH (2014) Direct and indirect effects of glomalin, mycorrhizal hyphae, and roots on aggregate stability in rhizosphere of trifoliate orange. Sci Rep 4:5823

    CAS  Google Scholar 

  • Yang A, Hu J, Lin X, Zhu A, Wang J, Dai J, Wong MH (2012a) Arbuscular mycorrhizal fungal community structure and diversity in response to 3-year conservation tillage management in a sandy loam soil in North China. J Soils Sediments 12:835–843

    Article  Google Scholar 

  • Yang SK, Kim MK, Seo YW, Choi KJ, Lee ST, Kwak YS, Lee YH (2012b) Soil microbial community analysis of between no-till and tillage in a controlled horticultural field. World J Microbiol Biotechnol 28:1797–1801

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to Linyun Zhou and Qi’ao Jiang of the Fengqiu Agro-Ecological Experimental Station, Institute of Soil Science, Chinese Academy of Sciences, for their field management and support on soil sampling. We are also grateful to Dr. Xinhua He from The University of Western Australia and the anonymous reviewers, for their vauable comments on the manuscript. This work was supported by the National Basic Research Program (2011CB100505) and the National Natural Science Foundation (No.40801090) of China, and the Knowledge Innovation Program of Chinese Academy of Sciences (ISSASIP1118-3).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xiangui Lin.

Additional information

Responsible Editor: Leo Condron

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dai, J., Hu, J., Zhu, A. et al. No tillage enhances arbuscular mycorrhizal fungal population, glomalin-related soil protein content, and organic carbon accumulation in soil macroaggregates. J Soils Sediments 15, 1055–1062 (2015). https://doi.org/10.1007/s11368-015-1091-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-015-1091-9

Keywords

Navigation