N-P fertilization did not reduce AMF abundance or diversity but alter AMF composition in an alpine grassland infested by a root hemiparasitic plant

doi:10.1016/j.pld.2018.05.001

Abstract

Abstract:

Fertilization has been shown to have suppressive effects on arbuscular mycorrhizal fungi (AMF) and root hemiparasites separately in numerous investigations, but its effects on AMF in the presence of root hemiparasites remain untested. In view of the contrasting nutritional effects of AMF and root hemiparasites on host plants, we tested the hypothesis that fertilization may not show strong suppressive effects on AMF when a plant community was infested by abundant hemiparasitic plants. Plants and soil samples were collected from experimental field plots in Bayanbulak Grassland, where N and P fertilizers had been applied for three continuous years for control against a spreading root hemiparasite, Pedicularis kansuensis. Shoot and root biomass of each plant functional group were determined. Root AMF colonization levels, soil spore abundance, and extraradical hyphae length density were measured for three soil depths (0-10 cm, 10-20 cm, 20-30 cm). Partial 18S rRNA gene sequencing was used to detect AMF diversity and community composition. In addition, we analyzed the relationship between relative abundance of different AMF genera and environmental factors using Spearman's correlation method. In contrast to suppressive effects reported by many previous studies, fertilization showed no significant effects on AMF root colonization or AMF species diversity in the soil. Instead, a marked increase in soil spore abundance and extraradical hyphae length density were observed. However, fertilization altered relative abundance and AMF composition in the soil. Our results support the hypothesis that fertilization does not significantly influence the abundance and diversity of AMF in a plant community infested by P. kansuensis.

Key words: Arbuscular mycorrhizal fungi, Fertilization, Community structure, Alpine grassland ecosystem, Pedicularis

Xue-Zhao Wang, Xiao-Lin Sui, Yan-Yan Liu, Lei Xiang, Ting Zhang, Juan-Juan Fu, Ai-Rong Li, Pei-Zhi Yang. N-P fertilization did not reduce AMF abundance or diversity but alter AMF composition in an alpine grassland infested by a root hemiparasitic plant[J]. Plant Diversity, 2018, 40(03): 117-126.

References

Al-Babili, S., Bouwmeester, H.J., 2015. Strigolactones, a novel carotenoid-derived plant hormone. Annu. Rev. Plant Biol. 161-186.
Albizua, A., Williams, A., Hedlund, K., et al., 2015. Crop rotations including ley and manure can promote ecosystem services in conventional farming systems. Appl. Soil Ecol. 95, 54-61.
Andreo-Jimenez, B., Ruyter-Spira, C., Bouwmeester, H.J., Lopez-Raez, J.A., 2015. Ecological relevance of strigolactones in nutrient uptake and other abiotic stresses, and in plant-microbe interactions below-ground. Plant Soil 394, 1-19.
Bakhshandeh, S., Corneo, P.E., Mariotte, P., et al., 2017. Effect of crop rotation on mycorrhizal colonization and wheat yield under different fertilizer treatments. Agric. Ecosyst. Environ. 247, 130-136.
Bao, G., Suetsugu, K., Wang, H., et al., 2015. Effects of the hemiparasitic plant Pedicularis kansuensis on plant community structure in a degraded grassland. Ecol. Res. 30, 507-515.
Biermann, B., Linderman, R.G., 1983. Use of vesicular mycorrhizal roots, intraradical vesicles and extraradical vesicles as inoculum. New Phytol. 95, 97-105.
Bonfim, J.A., Vasconcellos, R.L.F., Gumiere, T., et al., 2016. Diversity of arbuscular mycorrhizal fungi in a Brazilian Atlantic forest toposequence. Microb. Ecol. 71, 164-177.
Borowicz, V.A., Armstrong, J.E., 2012. Resource limitation and the role of a hemiparasite on a restored prairie. Oecologia 169, 783-792.
Brady, N.C., Weil, R.R., 2002. The Nature and Properties of Soils. Pearson Education, Upper Saddle River.
Bret-Harte, M.S., Shaver, G.R., Zoerner, J.P., et al., 2001. Developmental plasticity allows Betula nana to dominate tundra subjected to an altered environment. Ecology 82, 18-32.
Brundrett, M., Melville, L., Peterson, L., 1994. Practical Methods in Mycorrhiza Research:Based on a Workshop Organized in Conjunction with the Ninth North American Conference on Mycorrhizae. University of Guelph, Ontario, Canada.
Camenzind, T., Hempel, S., Homeier, J., et al., 2014. Nitrogen and phosphorus additions impact arbuscular mycorrhizal abundance and molecular diversity in a tropical montane forest. Global Change Biol. 20, 3646-3659.
Caporaso, J.G., Kuczynski, J., Stombaugh, J., et al., 2010. QⅡME allows analysis of high-throughput community sequencing data. Nat Methods 7, 335-336.
Chaparro, J.M., Sheflin, A.M., Manter, D.K., et al., 2012. Manipulating the soil microbiome to increase soil health and plant fertility. Biol. Fertil. Soils 48, 489-499.
Chen, Y.-L., Zhang, X., Ye, J.-S., et al., 2014. Six-year fertilization modifies the biodiversity of arbuscular mycorrhizal fungi in a temperate steppe in Inner Mongolia. Soil Biol. Biochem. 69, 371-381.
Cheng, Y., Ishimoto, K., Kuriyama, Y., et al., 2013. Ninety-year, but not single, application of phosphorus fertilizer has a major impact on arbuscular mycorrhizal fungal communities. Plant Soil 365, 397-407.
Clark, C.M., Tilman, D., 2008. Loss of plant species after chronic low-level nitrogen deposition to prairie grasslands. Nature 451, 712-715.
Davies, D.M., Graves, J.D., 2000. The impact of phosphorus on interactions of the hemiparasitic angiosperm Rhinanthus minor and its host Lolium perenne. Oecologia 124, 100-106.
Edgar, R.C., Haas, B.J., Clemente, J.C., et al., 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194-2200.
Gibson, C.C., Watkinson, A.R., 1991. Host selectivity and the mediation of competition by the root hemiparasite Rhinanthus-Minor. Oecologia 86, 81-87.
Giovannetti, M., Azzolini, D., Citernesi, A.S., 1999. Anastomosis formation and nuclear and protoplasmic exchange in arbuscular mycorrhizal fungi. Appl. Environ. Microbiol. 65, 5571-5575.
Giovannetti, M., Mosse, B., 1980. Evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol. 84, 489-500.
Gong, Y., Hu, Y., Adeli, M., et al., 2010. Alpine grassland community characteristics at the different stages of degenerating succession in Bayanbulak. J. Arid Land Resour. Environ. 24, 149-152.
Gosling, P., Mead, A., Proctor, M., et al., 2013. Contrasting arbuscular mycorrhizal communities colonizing different host plants show a similar response to a soil phosphorus concentration gradient. New Phytol. 198, 546-556.
Hedberg, A.M., Borowicz, V.A., Armstrong, J.E., 2005. Interactions between a hemiparasitic plant, Pedicularis canadensis L. (Orobanchaceae), and members of a tallgrass prairie community. J. Torrey Bot. Soc. 132, 401-410.
Irving, L.J., Cameron, D.D., 2009. You are what you eat:interactions between root parasitic plants and their hosts. In:Kader, J.C., Delseny, M. (Eds.), Advances in Botanical Research, vol. 50.
Jakobsen, I., Abbott, L.K., Robson, A.D., 1992. External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium -subterr aneum L. 1.Spread of hyphae and phosphorus inflow into roots. New Phytol. 120, 371-380.
Johnson, N.C., 2010. Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol. 185, 631-647.
Johnson, N.C., Rowland, D.L., Corkidi, L., et al., 2003. Nitrogen enrichment alters mycorrhizal allocation at five mesic to semiarid grasslands. Ecology 84, 1895-1908.
Kabir, Z., O'Halloran, I.P., Widden, P., et al., 1998. Vertical distribution of arbuscular mycorrhizal fungi under corn (Zea mays L.) in no-till and conventional tillage systems. Mycorrhiza 8, 53-55.
Kobae, Y., Sisaphaithong, T., Hanai, S., Tomioka, R., Tanaka, A., Yano, K., et al., 2017. Varietal differences in the growth responses of rice to an arbuscular mycorrhizal fungus under natural upland conditions. Plant Signal. Behav. 12.
Li, K., Gong, Y., Song, W., et al., 2012. No significant nitrous oxide emissions during spring thaw under grazing and nitrogen addition in an alpine grassland. Global Change Biol. 18, 2546-2554.
Lin, X., Feng, Y., Zhang, H., et al., 2012. Long-term balanced fertilization decreases arbuscular mycorrhizal fungal diversity in an arable soil in North China revealed by 454 pyrosequencing. Environ. Sci. Technol. 46, 5764-5771.
Liu, W., Zhang, Y., Jiang, S., et al., 2016. Arbuscular mycorrhizal fungi in soil and roots respond differently to phosphorus inputs in an intensively managed calcareous agricultural soil. Sci. Rep. 6.
Liu, Y., Hu, Y., Yu, J., et al., 2008. Study on harmfulness of Pedicularis myriophylla and its control measures. Arid Zone Res. 25, 778-782.
Liu, Y., Shi, G., Mao, L., et al., 2012. Direct and indirect influences of 8 yr of nitrogen and phosphorus fertilization on Glomeromycota in an alpine meadow ecosystem. New Phytol. 194, 523-535.
Liu, Y., Taxipulati, T., Gong, Y., et al., 2017. N-P Fertilization Inhibits growth of root hemiparasite Pedicularis kansuensis in natural grassland. Front. Plant Sci. 8.
Madan, N.J., Deacon, L.J., Robinson, C.H., 2007. Greater nitrogen and/or phosphorus availability increase plant species cover and diversity at a High Arctic polar semidesert. Polar Biol. 30, 559-570.
Mathimaran, N., Ruh, R., Vullioud, P., et al., 2005. Glomus intraradices dominates arbuscular mycorrhizal communities in a heavy textured agricultural soil. Mycorrhiza 16, 61-66.
Mehlich, A., 1984. Mehlich-3 soil test extractant-a modification of Mehlich-2 extractant. Commun. Soil Sci. Plant Anal. 15, 1409-1416.
Melo, C.D., Luna, S., Kruger, C., et al., 2018. Communities of arbuscular mycorrhizal fungi under Picconia azorica in native forests of Azores. Symbiosis 74, 43-54.
Miller, R.M., Reinhardt, D.R., Jastrow, J.D., 1995. External hyphal production of vesicular-arbuscular mycorrhizal fungi in pasture and tallgrass prairie communities. Oecologia 103, 17-23.
Mori, N., Nishiuma, K., Sugiyama, T., Hayashi, H., Akiyama, K., 2016. Carlactone-type strigolactones and their synthetic analogues as inducers of hyphal branching in arbuscular mycorrhizal fungi. Phytochemistry 130, 90-98.
Oehl, F., Sieverding, E., Mader, P., et al., 2004. Impact of long-term conventional and organic farming on the diversity of arbuscular mycorrhizal fungi. Oecologia 138, 574-583.
Olsson, P.A., Baath, E., Jakobsen, I., 1997. Phosphorus effects on the mycelium and storage structures of an arbuscular mycorrhizal fungus as studied in the soil and roots by analysis of fatty acid signatures. Appl. Environ. Microbiol. 63, 3531-3538.
Phillips, J.M., 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.
de Pontes, J.S., Oehl, F., Pereira, C.D., et al., 2017. Diversity of arbuscular mycorrhizal fungi in the Brazilian's Cerrado and in soybean under conservation and conventional tillage. Appl. Soil Ecol. 117, 178-189.
Press, M.C., Phoenix, G.K., 2005. Impacts of parasitic plants on natural communities. New Phytol. 166, 737-751.
Rodrigues, M., Pavinato, P.S., Withers, P.J.A., et al., 2016. Legacy phosphorus and no tillage agriculture in tropical oxisols of the Brazilian savanna. Sci. Total Environ. 542, 1050-1061.
Rousk, J., Baath, E., Brookes, P.C., et al., 2010. Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J. 4, 1340-1351.
Santos, J.C., Finlay, R.D., Tehler, A., 2006. Molecular analysis of arbuscular mycorrhizal fungi colonising a semi-natural grassland along a fertilisation gradient. New Phytol. 172, 159-168.
Schimel, J.P., Gulledge, J.M., Clein-Curley, J.S., et al., 1999. Moisture effects on microbial activity and community structure in decomposing birch litter in the Alaskan taiga. Soil Biol. Biochem. 31, 831-838.
Sheng, M., Lalande, R., Hamel, C., et al., 2013. Effect of long-term tillage and mineral phosphorus fertilization on arbuscular mycorrhizal fungi in a humid continental zone of Eastern Canada. Plant Soil 369, 599-613.
da Silva, D.K.A., de Souza, R.G., Velez, B.A.D., et al., 2015. Communities of arbuscular mycorrhizal fungi on a vegetation gradient in tropical coastal dunes. Appl. Soil Ecol. 96, 7-17.
Smith, S.E., Read, D.J., 2008. Mycorrhizal Symbiosis, third ed. Academic Press, New York.
Sui, X.-L., Huang, W., Li, Y.-J., et al., 2015. Host shoot clipping depresses the growth of weedy hemiparasitic Pedicularis kansuensis. J. Plant Res. 128, 563-572.
Taniguchi, T., Usuki, H., Kikuchi, J., et al., 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.
Tian, H., Drijber, R.A., Zhang, J.L., et al., 2013. Impact of long-term nitrogen fertilization and rotation with soybean on the diversity and phosphorus metabolism of indigenous arbuscular mycorrhizal fungi within the roots of maize (Zea mays L.). Agric. Ecosyst. Environ. 164, 53-61.
Treseder, K.K., Allen, M.F., 2002. Direct nitrogen and phosphorus limitation of arbuscular mycorrhizal fungi:a model and field test. New Phytol. 155, 507-515.
Vandenkoornhuyse, P., Husband, R., Daniell, T.J., et al., 2002. Arbuscular mycorrhizal community composition associated with two plant species in a grassland ecosystem. Mol. Ecol. 11, 1555-1564.
Verbruggen, E., van der Heijden, M.G.A., Rillig, M.C., et al., 2013. Mycorrhizal fungal establishment in agricultural soils:factors determining inoculation success. New Phytol. 197, 1104-1109.
Verbruggen, E., Van Der Heijden, M.G.A., Weedon, J.T., et al., 2012. Community assembly, species richness and nestedness of arbuscular mycorrhizal fungi in agricultural soils. Mol. Ecol. 21, 2341-2353.
Vogelsang, K.M., Reynolds, H.L., Bever, J.D., 2006. Mycorrhizal fungal identity and richness determine the diversity and productivity of a tallgrass prairie system. New Phytol. 172, 554-562.
Wagg, C., Jansa, J., Schmid, B., et al., 2011. Belowground biodiversity effects of plant symbionts support aboveground productivity. Ecol. Lett. 14, 1001-1009.
Wang, C., White, P.J., Li, C., 2017. Colonization and community structure of arbuscular mycorrhizal fungi in maize roots at different depths in the soil profile respond differently to phosphorus inputs on a long-term experimental site. Mycorrhiza 27, 369-381.
Wang, F.Y., Hu, J.L., Lin, X.G., et al., 2011. Arbuscular mycorrhizal fungal community structure and diversity in response to long-term fertilization:a field case from China. World J. Microbiol. Biotechnol. 27, 67-74.
Wang, G.M., Stribley, D.P., Tinker, P.B., et al., 1993. Effects of pH on arbuscular mycorrhiza. 1. Field observations on the long-term liming experiments at Rothamsted and Woburn. New Phytol. 124, 465-472.
Wang, X.J., Wang, J.P., Zhang, J., 2012. Comparisons of three methods for organic and inorganic carbon in calcareous soils of Northwestern China. PLoS One 7.
Williams, A., Borjesson, G., Hedlund, K., 2013. The effects of 55 years of different inorganic fertiliser regimes on soil properties and microbial community composition. Soil Biol. Biochem. 67, 41-46.
Williams, A., Manoharan, L., Rosenstock, N.P., et al., 2017. Long-term agricultural fertilization alters arbuscular mycorrhizal fungal community composition and barley (Hordeum vulgare) mycorrhizal carbon and phosphorus exchange. New Phytol. 213, 874-885.
Zogg, G.P., Zak, D.R., Ringelberg, D.B., et al., 1997. Compositional and functional shifts in microbial communities due to soil warming. Soil Sci. Soc. Am. J. 61, 475-481.

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