Arbuscular Mycorrhizal Fungus Mediate Changes in Mycorrhizosphere Soil Aggregates
Affiliation(s)
1 College of Resources and Environment, Southwest University, Chongqing, China. 2 The National Monitoring Base for Purple Soil Fertility and Fertilizer Efficiency, Southwest University, Chongqing, China. 3 Beibei District Agricultural Committee, Chongqing, China.
1 College of Resources and Environment, Southwest University, Chongqing, China. 2 The National Monitoring Base for Purple Soil Fertility and Fertilizer Efficiency, Southwest University, Chongqing, China. 3 Beibei District Agricultural Committee, Chongqing, China.
ABSTRACT
Many studies have shown that arbuscular mycorrhizal (AM) fungus has an important role in soil aggregate formation and stabilization. While most studies about the effects of AM fungus on soil aggregate have experimental set-ups in single pots or containers with two compartments, these studies cannot differentiate the effects of roots, mycorrhizal roots or hyphae. In this study we used containers with four compartments to split the roots and quantitatively compare the change of soil aggregate in the mycorrhizosphere soil, rhizosphere soil, hyphosphere soil and bulk soil. Our results demonstrate a significant positive correlation among hyphal length density, easily extractable glomalin (EEG) and aggregate mean weight diameter (MWD), geometric mean diameter (GMD) and percentage of soil macroaggregate with a diameter larger than 0.25 mm (R0.25). The GMD and MWD of R0.25 in the hyphal compartment were higher than those in the non-inoculated root compartment, but were lower than those in the mycorrhizal compartment. This suggests the mycorrhizal hyphae had a greater effect than the non-inoculated roots, but less of an effect than the mycorrhizal roots on the formation and stabilization of soil aggregate. The results reveal that plant roots, mycorrhizal roots and mycorrhizal hyphae contribute to aggregate stability in individual ways and that their effects are additive, creating a synergistic stabilizing effect.
Many studies have shown that arbuscular mycorrhizal (AM) fungus has an important role in soil aggregate formation and stabilization. While most studies about the effects of AM fungus on soil aggregate have experimental set-ups in single pots or containers with two compartments, these studies cannot differentiate the effects of roots, mycorrhizal roots or hyphae. In this study we used containers with four compartments to split the roots and quantitatively compare the change of soil aggregate in the mycorrhizosphere soil, rhizosphere soil, hyphosphere soil and bulk soil. Our results demonstrate a significant positive correlation among hyphal length density, easily extractable glomalin (EEG) and aggregate mean weight diameter (MWD), geometric mean diameter (GMD) and percentage of soil macroaggregate with a diameter larger than 0.25 mm (R0.25). The GMD and MWD of R0.25 in the hyphal compartment were higher than those in the non-inoculated root compartment, but were lower than those in the mycorrhizal compartment. This suggests the mycorrhizal hyphae had a greater effect than the non-inoculated roots, but less of an effect than the mycorrhizal roots on the formation and stabilization of soil aggregate. The results reveal that plant roots, mycorrhizal roots and mycorrhizal hyphae contribute to aggregate stability in individual ways and that their effects are additive, creating a synergistic stabilizing effect.
Cite this paper
Liang, T. , Shi, X. , Guo, T. and Peng, S. (2015) Arbuscular Mycorrhizal Fungus Mediate Changes in Mycorrhizosphere Soil Aggregates. Agricultural Sciences, 6, 1455-1463. doi: 10.4236/as.2015.612141.
Liang, T. , Shi, X. , Guo, T. and Peng, S. (2015) Arbuscular Mycorrhizal Fungus Mediate Changes in Mycorrhizosphere Soil Aggregates. Agricultural Sciences, 6, 1455-1463. doi: 10.4236/as.2015.612141.
References
[1] Amezketa, E. (1999) Soil Aggregate Stability: A Review. Journal of Sustainable Agriculture, 14, 83-151.
http://dx.doi.org/10.1300/J064v14n02_08 [2] van Bavel, C.H.M. (1949) Mean Weight-Diameter of Soil Aggregates as a Statistical Index of Aggregation. Soil Science Society of America Journal, 14, 20-23.
http://dx.doi.org/10.2136/sssaj1950.036159950014000C0005x [3] Gardner, W.R. (1956) Representation of Soil Aggregate-Size Distribution by a Logarithmic-Normal Distribution. Soil Science Society of America Journal, 20, 151-153.
http://dx.doi.org/10.2136/sssaj1956.03615995002000020003x [4] Koide, R.T. and Mosse, B. (2004) A History of Research on Arbuscular Mycorrhiza. Mycorrhiza, 14, 145-163.
http://dx.doi.org/10.1007/s00572-004-0307-4 [5] Smith, S.E. and Read, D.J. (2008) Mycorrhizal Symbiosis. Academic Press, Elsevier, New York. [6] Rillig, M.C. and Mummey, D.L. (2006) Mycorrhizas and Soil Structure. New Phytologist, 171, 41-53.
http://dx.doi.org/10.1111/j.1469-8137.2006.01750.x [7] Rillig, M.C., Wright, S.F and Eviner, V.T. (2002) The Role of Arbuscular Mycorrhizal Fungi and Glomalin in Soil Aggregation: Comparing Effects of Five Plant Species. Plant and Soil, 238, 325-333.
http://dx.doi.org/10.1023/A:1014483303813 [8] Wright, S. and Upadhyaya, A. (1998) A Survey of Soils for Aggregate Stability and Glomalin, a Glycoprotein Produced by Hyphae of Arbuscular Mycorrhizal Fungi. Plant and Soil, 198, 97-107.
http://dx.doi.org/10.1023/A:1004347701584 [9] Rillig, M.C. (2004) Arbuscular Mycorrhizae, Glomalin, and Soil Aggregation. Canadian Journal of Soil Science, 84, 355-363.
http://dx.doi.org/10.4141/S04-003 [10] Tisdall, J.M. and Oades, J. (1982) Organic Matter and Water-Stable Aggregates in Soils. Journal of Soil Science, 33, 141-163.
http://dx.doi.org/10.1111/j.1365-2389.1982.tb01755.x [11] Miller, R. and Jastrow, J. (1990) Hierarchy of Root and Mycorrhizal Fungal Interactions with Soil Aggregation. Soil Biology and Biochemistry, 22, 579-584.
http://dx.doi.org/10.1016/0038-0717(90)90001-G [12] Piotrowski, J.S., Denich, T., Klironomos, J.N., Graham, J.M. and Rillig, M.C. (2004) The Effects of Arbuscular Mycorrhizas on Soil Aggregation Depend on the Interaction between Plant and Fungal Species. New Phytologist, 164, 365-373.
http://dx.doi.org/10.1111/j.1469-8137.2004.01181.x [13] Bedini, S., Avio, L., Argese, E. and Giovannetti, M. (2007) Effects of Long-Term Land Use on Arbuscular Mycorrhizal Fungi and Glomalin-Related Soil Protein. Agriculture Ecosystems & Environment, 120, 463-466.
http://dx.doi.org/10.1016/j.agee.2006.09.010 [14] Siddiky, M.R.K., Kohler, J., Cosme, M. and Rillig, M.C. (2012) Soil Biota Effects on Soil Structure: Interactions between Arbuscular Mycorrhizal Fungal Mycelium and Collembola. Soil Biology & Biochemistry, 50, 33-39.
http://dx.doi.org/10.1016/j.soilbio.2012.03.001 [15] Hontoria, C., Velasquez, R., Benito, M., Almorox, J. and Moliner, A. (2009) Bradford-Reactive Soil Proteins and Aggregate Stability under Abandoned versus Tilled Olive Groves in a Semi-Arid Calcisol. Soil Biology & Biochemistry, 41, 1583-1585.
http://dx.doi.org/10.1016/j.soilbio.2009.04.025 [16] Wilson, G.W.T., Rice, C.W., Rillig, M.C., Springer, A. and Hartnett, D.C. (2009) Soil Aggregation and Carbon Sequestration Are Tightly Correlated with the Abundance of Arbuscular Mycorrhizal Fungi: Results from Long-Term Field Experiments. Ecology Letters, 12, 452-461.
http://dx.doi.org/10.1111/j.1461-0248.2009.01303.x [17] Caruso, T. and Rillig, M.C. (2011) Direct, Positive Feedbacks Produce Instability in Models of Interrelationships among Soil Structure, Plants and Arbuscular Mycorrhizal Fungi. Soil Biology & Biochemistry, 43, 1198-1206.
http://dx.doi.org/10.1016/j.soilbio.2011.02.009 [18] Miller, R. and Jastrow, J. (2000) Mycorrhizal Fungi Influence Soil Structure. In: Kapulnik, Y. and Douds Jr., D.D., Eds., Arbuscular Mycorrhizas: Physiology and Function, Kluwer Academic, Dordrecht, 3-18.
http://dx.doi.org/10.1007/978-94-017-0776-3_1 [19] Andrade, G., Mihara, K.L., Linderman, R.G. and Bethlenfalvay, G.J. (1998) Soil Aggregation Status and Rhizobacteria in the Mycorrhizosphere. Plant and Soil, 202, 89-96.
http://dx.doi.org/10.1023/A:1004301423150 [20] Giovannetti, M. and Mosse, B. (1980) An Evaluation of Techniques for Measuring Vesicular Arbuscular Mycorrhizal Infection in Roots. New Phytologist, 84, 489-500.
http://dx.doi.org/10.1111/j.1469-8137.1980.tb04556.x [21] Kemper, W. and Rosenau, R. (1986) Aggregate Stability and Size Distribution. In: Klute, A., Ed., Methods of Soil Analysis, Part 1. Physical and Mineralogical Methods, Agronomy Monograph, American Society of Agronomy and Soil Science Society of America, Madison, 425-442. [22] Abbott, L.K., Robson, A.D. and Deboer, G. (1984) The Effect of Phosphorus on the Formation of Hyphae in Soil by the Vesicular Arbuscular Mycorrhizal Fungus, Glomus fasciculatum. New Phytologist, 97, 437-446.
http://dx.doi.org/10.1111/j.1469-8137.1984.tb03609.x [23] Bearden, B.N. and Petersen, L. (2000) Influence of Arbuscular Mycorrhizal Fungi on Soil Structure and Aggregate Stability of a Vertisol. Plant and Soil, 218, 173-183.
http://dx.doi.org/10.1023/A:1014923911324 [24] Rillig, M.C., Mardatin, N.F., Leifheit, E.F. and Antunes, P.M. (2010) Mycelium of Arbuscular Mycorrhizal Fungi Increases Soil Water Repellency and Is Sufficient to Maintain Water-Stable Soil Aggregates. Soil Biology & Biochemistry, 42, 1189-1191.
http://dx.doi.org/10.1016/j.soilbio.2010.03.027 [25] Siddiky, M.R.K., Schaller, J., Caruso, T. and Rillig, M.C. (2012) Arbuscular Mycorrhizal Fungi and Collembola Non-Additively Increase Soil Aggregation. Soil Biology & Biochemistry, 47, 93-99.
http://dx.doi.org/10.1016/j.soilbio.2011.12.022 [26] Stefano, B., Elisa, P., Luciano, A., Sergio, P., Paolo, B., Emanuele, A. and Manuela, G. (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 Biology & Biochemistry, 41, 1491-1496.
http://dx.doi.org/10.1016/j.soilbio.2009.04.005 [27] Fokom, R., Adamou, S., Teugwa, M.C., Boyogueno, A.D.B., Nana, W.L., Ngonkeu, M.E.L., Tchameni, N.S., Nwaga, D., Ndzomo, G.T. and Zollo, P.H.A. (2012) Glomalin Related Soil Protein, Carbon, Nitrogen and Soil Aggregate Stability as Affected by Land Use Variation in the Humid Forest Zone of South Cameroon. Soil & Tillage Research, 120, 69-75.
http://dx.doi.org/10.1016/j.still.2011.11.004 [28] Driver, J.D., Holben, W.E. and Rillig, M.C. (2005) Characterization of Glomalin as a Hyphal Wall Component of Arbuscular Mycorrhizal Fungi. Soil Biology & Biochemistry, 37, 101-106.
http://dx.doi.org/10.1016/j.soilbio.2004.06.011 [29] David, P.J., Sara, G. and Bray, B. (2008) Glomalin Extraction and Measurement. Soil Biology and Biochemistry, 240, 728-739.
[1] Amezketa, E. (1999) Soil Aggregate Stability: A Review. Journal of Sustainable Agriculture, 14, 83-151.
http://dx.doi.org/10.1300/J064v14n02_08 [2] van Bavel, C.H.M. (1949) Mean Weight-Diameter of Soil Aggregates as a Statistical Index of Aggregation. Soil Science Society of America Journal, 14, 20-23.
http://dx.doi.org/10.2136/sssaj1950.036159950014000C0005x [3] Gardner, W.R. (1956) Representation of Soil Aggregate-Size Distribution by a Logarithmic-Normal Distribution. Soil Science Society of America Journal, 20, 151-153.
http://dx.doi.org/10.2136/sssaj1956.03615995002000020003x [4] Koide, R.T. and Mosse, B. (2004) A History of Research on Arbuscular Mycorrhiza. Mycorrhiza, 14, 145-163.
http://dx.doi.org/10.1007/s00572-004-0307-4 [5] Smith, S.E. and Read, D.J. (2008) Mycorrhizal Symbiosis. Academic Press, Elsevier, New York. [6] Rillig, M.C. and Mummey, D.L. (2006) Mycorrhizas and Soil Structure. New Phytologist, 171, 41-53.
http://dx.doi.org/10.1111/j.1469-8137.2006.01750.x [7] Rillig, M.C., Wright, S.F and Eviner, V.T. (2002) The Role of Arbuscular Mycorrhizal Fungi and Glomalin in Soil Aggregation: Comparing Effects of Five Plant Species. Plant and Soil, 238, 325-333.
http://dx.doi.org/10.1023/A:1014483303813 [8] Wright, S. and Upadhyaya, A. (1998) A Survey of Soils for Aggregate Stability and Glomalin, a Glycoprotein Produced by Hyphae of Arbuscular Mycorrhizal Fungi. Plant and Soil, 198, 97-107.
http://dx.doi.org/10.1023/A:1004347701584 [9] Rillig, M.C. (2004) Arbuscular Mycorrhizae, Glomalin, and Soil Aggregation. Canadian Journal of Soil Science, 84, 355-363.
http://dx.doi.org/10.4141/S04-003 [10] Tisdall, J.M. and Oades, J. (1982) Organic Matter and Water-Stable Aggregates in Soils. Journal of Soil Science, 33, 141-163.
http://dx.doi.org/10.1111/j.1365-2389.1982.tb01755.x [11] Miller, R. and Jastrow, J. (1990) Hierarchy of Root and Mycorrhizal Fungal Interactions with Soil Aggregation. Soil Biology and Biochemistry, 22, 579-584.
http://dx.doi.org/10.1016/0038-0717(90)90001-G [12] Piotrowski, J.S., Denich, T., Klironomos, J.N., Graham, J.M. and Rillig, M.C. (2004) The Effects of Arbuscular Mycorrhizas on Soil Aggregation Depend on the Interaction between Plant and Fungal Species. New Phytologist, 164, 365-373.
http://dx.doi.org/10.1111/j.1469-8137.2004.01181.x [13] Bedini, S., Avio, L., Argese, E. and Giovannetti, M. (2007) Effects of Long-Term Land Use on Arbuscular Mycorrhizal Fungi and Glomalin-Related Soil Protein. Agriculture Ecosystems & Environment, 120, 463-466.
http://dx.doi.org/10.1016/j.agee.2006.09.010 [14] Siddiky, M.R.K., Kohler, J., Cosme, M. and Rillig, M.C. (2012) Soil Biota Effects on Soil Structure: Interactions between Arbuscular Mycorrhizal Fungal Mycelium and Collembola. Soil Biology & Biochemistry, 50, 33-39.
http://dx.doi.org/10.1016/j.soilbio.2012.03.001 [15] Hontoria, C., Velasquez, R., Benito, M., Almorox, J. and Moliner, A. (2009) Bradford-Reactive Soil Proteins and Aggregate Stability under Abandoned versus Tilled Olive Groves in a Semi-Arid Calcisol. Soil Biology & Biochemistry, 41, 1583-1585.
http://dx.doi.org/10.1016/j.soilbio.2009.04.025 [16] Wilson, G.W.T., Rice, C.W., Rillig, M.C., Springer, A. and Hartnett, D.C. (2009) Soil Aggregation and Carbon Sequestration Are Tightly Correlated with the Abundance of Arbuscular Mycorrhizal Fungi: Results from Long-Term Field Experiments. Ecology Letters, 12, 452-461.
http://dx.doi.org/10.1111/j.1461-0248.2009.01303.x [17] Caruso, T. and Rillig, M.C. (2011) Direct, Positive Feedbacks Produce Instability in Models of Interrelationships among Soil Structure, Plants and Arbuscular Mycorrhizal Fungi. Soil Biology & Biochemistry, 43, 1198-1206.
http://dx.doi.org/10.1016/j.soilbio.2011.02.009 [18] Miller, R. and Jastrow, J. (2000) Mycorrhizal Fungi Influence Soil Structure. In: Kapulnik, Y. and Douds Jr., D.D., Eds., Arbuscular Mycorrhizas: Physiology and Function, Kluwer Academic, Dordrecht, 3-18.
http://dx.doi.org/10.1007/978-94-017-0776-3_1 [19] Andrade, G., Mihara, K.L., Linderman, R.G. and Bethlenfalvay, G.J. (1998) Soil Aggregation Status and Rhizobacteria in the Mycorrhizosphere. Plant and Soil, 202, 89-96.
http://dx.doi.org/10.1023/A:1004301423150 [20] Giovannetti, M. and Mosse, B. (1980) An Evaluation of Techniques for Measuring Vesicular Arbuscular Mycorrhizal Infection in Roots. New Phytologist, 84, 489-500.
http://dx.doi.org/10.1111/j.1469-8137.1980.tb04556.x [21] Kemper, W. and Rosenau, R. (1986) Aggregate Stability and Size Distribution. In: Klute, A., Ed., Methods of Soil Analysis, Part 1. Physical and Mineralogical Methods, Agronomy Monograph, American Society of Agronomy and Soil Science Society of America, Madison, 425-442. [22] Abbott, L.K., Robson, A.D. and Deboer, G. (1984) The Effect of Phosphorus on the Formation of Hyphae in Soil by the Vesicular Arbuscular Mycorrhizal Fungus, Glomus fasciculatum. New Phytologist, 97, 437-446.
http://dx.doi.org/10.1111/j.1469-8137.1984.tb03609.x [23] Bearden, B.N. and Petersen, L. (2000) Influence of Arbuscular Mycorrhizal Fungi on Soil Structure and Aggregate Stability of a Vertisol. Plant and Soil, 218, 173-183.
http://dx.doi.org/10.1023/A:1014923911324 [24] Rillig, M.C., Mardatin, N.F., Leifheit, E.F. and Antunes, P.M. (2010) Mycelium of Arbuscular Mycorrhizal Fungi Increases Soil Water Repellency and Is Sufficient to Maintain Water-Stable Soil Aggregates. Soil Biology & Biochemistry, 42, 1189-1191.
http://dx.doi.org/10.1016/j.soilbio.2010.03.027 [25] Siddiky, M.R.K., Schaller, J., Caruso, T. and Rillig, M.C. (2012) Arbuscular Mycorrhizal Fungi and Collembola Non-Additively Increase Soil Aggregation. Soil Biology & Biochemistry, 47, 93-99.
http://dx.doi.org/10.1016/j.soilbio.2011.12.022 [26] Stefano, B., Elisa, P., Luciano, A., Sergio, P., Paolo, B., Emanuele, A. and Manuela, G. (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 Biology & Biochemistry, 41, 1491-1496.
http://dx.doi.org/10.1016/j.soilbio.2009.04.005 [27] Fokom, R., Adamou, S., Teugwa, M.C., Boyogueno, A.D.B., Nana, W.L., Ngonkeu, M.E.L., Tchameni, N.S., Nwaga, D., Ndzomo, G.T. and Zollo, P.H.A. (2012) Glomalin Related Soil Protein, Carbon, Nitrogen and Soil Aggregate Stability as Affected by Land Use Variation in the Humid Forest Zone of South Cameroon. Soil & Tillage Research, 120, 69-75.
http://dx.doi.org/10.1016/j.still.2011.11.004 [28] Driver, J.D., Holben, W.E. and Rillig, M.C. (2005) Characterization of Glomalin as a Hyphal Wall Component of Arbuscular Mycorrhizal Fungi. Soil Biology & Biochemistry, 37, 101-106.
http://dx.doi.org/10.1016/j.soilbio.2004.06.011 [29] David, P.J., Sara, G. and Bray, B. (2008) Glomalin Extraction and Measurement. Soil Biology and Biochemistry, 240, 728-739.