Arbuscular Mycorrhizal Fungi Alleviate Ozone Stress on Nitrogen Nutrition of Field Wheat

Authors
X. C. Cui
J. L. Hu
X. G. Lin
F. Y. Wang
R. R. Chen
J. H. Wang
J. G. Zhu
State Key Laboratory of Soil and Sustainable Agriculture, Joint Open Laboratory of Soil and the Environment, Hong Kong Baptist University & Institute of Soil Science, Chinese Academy of Sciences, Nanjing 21008, People’s Republic of China.
Abstract
The nitrogen (N) nutrition, crop yield, and responses of wheat to arbuscular mycorrhizal fungi (AMF) were tested in an experimental field under free-air ozone concentration [O3] enrichment (FACE) conditions. The experiment included three treatments: ambient [O3] (Ambient), elevated [O3] (FACE, targeted at ambient [O3]×1.5), and elevated [O3] inoculated with an AMF consortium consisting of several Glomus species (FACE+AMF). AMF inoculation responsiveness of wheat was estimated by comparing plants grown in unsterilized soil inoculated with the exogenous AMF and in untreated soil containing indigenous AMF. Compared with the Ambient, relatively higher N contents but lower shoot biomasses of wheat plants were observed in the FACE treatment without AMF inoculation from the tillering stage in February and heading stage in April, respectively, which significantly (P< 0.05) decreased grain yield by 28% at harvest in June. Under the FACE condition, compared with the non-inoculated treatment, AMF inoculation significantly (P< 0.05) increased root colonization rates both at the tillering stage and heading stage, and also significantly (P< 0.05) increased shoot biomass at the heading stage and, hence, significantly (P< 0.05) increased grain yield by 40% at harvest. However, AMF inoculation significantly (P< 0.05) decreased total N content in wheat shoots at the tillering stage, suggesting that AMF consortia may enhance plant tolerance to elevated [O3] by elevating root colonization rate rather than plant total N content at early growing stages.

Keywords

1. Andersen, C. P. 2003. Source-sink Balance and Carbon Allocation below Ground in Plants Exposed to Ozone. New Phytol., 157: 213–228.
2. Azcón-Aguilar, C. and Barea, J. M. 1996. Arbuscular Mycorrhizas and Biological Control of Soil-borne Plant Pathogens: An Overview of the Mechanisms Involved. Mycorrhiza, 6: 457–464.
3. Bremner, J. M. and Mulvaney, R. L. 1978. Urease Activity in Soils. In: "Soil Enzymes", (Ed.): Burns, R. G.. Academic Press, London, PP. 149–196.
4. Bueeker, J. 1994. Response of Cellular Antioxidants to Ozone in Wheat Flag Leaves at Different Stages of Plant Development. Environ. Pollut., 84: 15–21.
5. Chameides, W. L., Kasibhatla, P. S., Yienger, J. and Levy, II. H. 1994. Growth of Continental-scale Metro-Agro-Plexes, Regional Ozone Pollution and World Food Production. Sci., 264: 74–77.
6. Duckmanton, L. and Widden, P. 1994. Effect of Ozone on the Development of Vesicular-Arbuscular Mycorrhizae in Sugar Maple Saplings. Mycologia, 86: 181–186.
7. Feng, Z. Z., Kobayashi, K. and Ainsworth, E. A. 2008. Impact of Elevated Ozone Concentration on Growth, Physiology and Yield of Wheat (Triticum aestivum L.): A Metaanalysis, Global Change Biol., 14: 2696–2708.
8. Feng, Z. Z., Pang, J., Kobayashi, K., Zhu, J. G. and Ort, D. R. 2011. Differential Responses in Two Varieties of Winter Wheat to Elevated Ozone Concentration under Fully Open-air Field Conditions. Global Change Biol., 17: 580–591.
9. Giovannetti, M. and Mosse, B. 1980. An Evaluation of Techniques for Measuring Vesicular–Arbuscular Mycorrhizal Infection in Roots. New Phytol., 84: 489–500.
10. Guo, J. P., Wang, C. Y., Bai, Y. M., Wen, M., Huo, Z. G., Liu, J. G. and Li, L. 2001. Effects of Atmospheric Ozone Concentration Alteration on Physiological Process and Grain Quality of Winter Wheat. Quart. J. Appl. Meteorol., 12: 255–256.
11. Hu, J. L., Lin, X. G., Wang, J. H., Cui, X. C., Wu, S., Zhang, J. and Zhu, J. G. 2009. Arbuscular Mycorrhizal Fungal Effects on Wheat Growth in Response to Elevated Tropospheric O3 Concentration. Environ. Sci., 30: 3393–3398.
12. Hu, J. L., Lin, X. G., Wang, J. H., Shen, W. S., Wu, S., Peng, S. P. and Mao, T. T. 2010. Arbuscular Mycorrhizal Fungal Inoculation Enhances Suppressiveness of Cucumber Fusarium Wilt in Greenhouse Soils. Pedosphere, 20: 586–593.
13. Jakobsen, I., Gazey, C. and Abbott, L. K. 2001. Phosphate Transport by Communities of Arbuscular Mycorrhizal Fungi in Intact Soil Cores. New Phytol., 149: 95–103.
14. Kandeler, E. and Gerber, H. 1988. Short-term Assay of Soil Urease Activity Using Colorimetric Determination of Ammonium. Biol. Fert. Soils, 6: 68–72.
15. Kanerva, T., Palojärvi, A., Rämö, K., Ojanperä, K., Esala, M., and Manninen, S. 2006. A 3-year Exposure to CO2 and O3 Induced Minor Changes in Soil N Cycling in a Meadow Ecosystem. Plant Soil, 286: 61–73.
16. Karlsson, G. P., Pleijel, H., Sild, E., Danielsson, H., Selldén, G., Ericson, L. and Skärby, L. 1995. Clover Sweden: A National Three-year Study of the Effects of Tropospheric Ozone on Trifolium subterraneum L. Water Air Soil Poll., 85: 1503–1508.
17. Lakshmipathy, R., Balakrishna, A. N. and Bagyaraj, D. J. 2012. Abundance and Diversity of AM Fungi Across a Gradient of Land Use Intensity and Their Seasonal Variations in Niligiri Biosphere of the Western Ghats, India. J. Agr. Sci. Tech., 14: 903–918.
18. Lu, R. K. 1999. Analytical Methods of Soil and Agricultural Chemistry. China Agricultural Science and Technology Press, Beijing, 638PP.
19. McCool, P. M. and Menge, J. A. 1984. Interaction of Ozone and Mycorrhizal Fungi on Tomato as Influenced by Fungal Species and Host Variety. Soil Biol. Biochem., 16: 425–427.
20. McCrady, J. K. and Andersen, C. P. 2000. The Effect of Ozone on Below-ground Carbon Allocation in Wheat. Environ. Poll., 107: 465–472.
21. Pang, J., Kobayashi, K. and Zhu, J. 2009. Yield and Photosynthetic Characteristics of Flag Leaves in Chinese rice (Oryza sativa L.) Varieties Subjected to Free-Air Release of Ozone. Agri. Ecosyst. Environ., 132: 203–211.
22. Phillips, J. M. and Hayman, D. S. 1970. Improved Procedures for Clearing Roots and Staining Parasitic and Vesicular-arbuscular Mycorrhizal Fungi for Rapid Assessment of Infection. Trans. Br. Mycol. Soc., 55: 158–161.
23. Polle, A. and Pell, E. 1999. Role of Carbon Dioxide in Modifying the Plant Response to Ozone. In: "Carbon Dioxide and Environmental Stress", (Eds.): Luo, Y. and Mooner, H. A.. Academic Press, New York, PP. 193–213.
24. Sharma, D., Kapoor, R., and Bhatnagar, A. K. 2009. Differential Growth Response of Curculigo orchioides to Native Arbuscular Mycorrhizal Fungal (AMF) Communities Varying in Number and Fungal Components. Europ. J. Soil Biol., 45: 328–333.
25. Shi, G., Yang, L., Wang, Y., Kobayashi, K., Zhu, J., Pan, S., Chen, T., Liu, G. and Wang, Y. 2009. Impact of Elevated Ozone Concentration on Yield of Four Chinese Rice Cultivars under Fully Open-air Field Conditions. Agri. Ecosyst. Environ., 131: 178–184.
26. Smith, S. E. and Read, D. J. 2008. Mycorrhizal Symbiosis. 3rd Edition, Academic Press, London, 600 PP.
27. Turner, N. C., Rich, S. and Waggoner, P. E. 1973. Removal of Ozone by Soil. J. Environ. Qual., 2: 259–264.
28. Wang, F. Y., Lin, X. G., Yin, R. and Wu, L. H. 2006a. Effects of Arbuscular Mycorrhizal Inoculation on the Growth of Elsholtzia splendens and Zea mays and the Activities of Phosphatase and Urease in a Multi-metal-contaminated Soil under Unsterilized Conditions. App. Soil Ecol., 31: 110–119.
29. Wang, S. G., Feng, Z. Z., Wang, X. K. and Feng, Z. W. 2006b. Effects of Elevated Atmospheric O3 on Arbuscular Mycorrhizae (AM) and Its Function. Environ. Sci., 27: 1872–1877.
Journal of Agricultural Science and Technology
Volume 15, Issue 5
September and October 2013
Pages 1043-1052