Abstract
Effects of soil depth and plant growth stages on arbuscular mycorrhizal fungal (AMF) colonization and community structure in maize roots and their potential contribution to host plant phosphorus (P) nutrition under different P-fertilizer inputs were studied. Research was conducted on a long-term field experiment over 3 years. AMF colonization was assessed by AM colonization rate and arbuscule abundances and their potential contribution to host P nutrition by intensity of fungal alkaline phosphatase (ALP)/acid phosphatase (ACP) activities and expressions of ZmPht1;6 and ZmCCD8a in roots from the topsoil and subsoil layer at different growth stages. AMF community structure was determined by specific amplification of 18S rDNA. Increasing P inputs up to 75–100 kg ha−1 yr−1 increased shoot biomass and P content but decreased AMF colonization and interactions between AMF and roots. AM colonization rate, intensity of fungal ACP/ALP activities, and expression of ZmPht1;6 in roots from the subsoil were greater than those from topsoil at elongation and silking but not at the dough stage when plants received adequate or excessive P inputs. Neither P input nor soil depth influenced the number of AMF operational taxonomic units (OTUs) present in roots, but P-fertilizer input, in particular, influenced community composition and relative AMF abundance. In conclusion, although increasing P inputs reduce AMF colonization and influence AMF community structure, AMF can potentially contribute to plant P nutrition even in well-fertilized soils, depending on the soil layer in which roots are located and the growth stage of host plants.
Similar content being viewed by others
References
Abbott LK, Robson AD (1991) Factors influencing the occurrence of vesicular-arbuscular mycorrhizas. Agric Ecosyst Environ 35:121–150
Alder A, Jamil M, Marzorati M, Bruno M, Vermathen M, Bigler P, Ghisla S, Bouwmeester H, Beyer P, Al-Babili S (2012) The path from β-carotene to carlactone, a strigolactone-like plant hormone. Science 335:1348–1351
Anderson EL, Millner PD, Kunishi HM (1987) Maize root length density and mycorrhizal infection as influenced by tillage and soil phosphorus. J Plant Nutr 10:1349–1356
Aulakh MS, Garg AK, Kabba BS (2007) Phosphorus accumulation, leaching and residual effects on crop yields from long-term applications in the subtropics. Soil Use Manage 23:417–427
Bai Z, Li H, Yang X, Zhou B, Shi X, Wang B, Li D, Shen J, Chen Q, Qin W, Oenema O, Zhang F (2013) The critical soil P levels for crop yield, soil fertility and environmental safety in different soil types. Plant Soil 372:27–37
Bainard LD, Bainard JD, Hamel C, Gan Y (2014) Spatial and temporal structuring of arbuscular mycorrhizal communities is differentially influenced by abiotic factors and host crop in a semi-arid prairie agroecosystem. FEMS Microbiol Ecol 88:333–344
Balzergue C, Puech-Pagès V, Bécard G, Rochange SF (2011) The regulation of arbuscular mycorrhizal symbiosis by phosphate in pea involves early and systemic signalling events. J Exp Bot 32:1049–1060
Beauregard MS, Gauthier MP, Hamel C, Zhang T, Welacky T, Tan CS, St-Arnaud M (2013) Various forms of organic and inorganic P fertilizers did not negatively affect soil-and root-inhabiting AM fungi in a maize–soybean rotation system. Mycorrhiza 23:143–154
Bennett AE, Daniell TJ, White PJ (2013) Benefits of breeding crops for yield response to soil organisms. In: de Bruijn FJ (ed) Molecular microbial ecology of the rhizosphere. Wiley-Blackwell, Hoboken, pp 17–27
Besserer A, Puech-Pagès V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S, Portais JC, Roux C, Bécard G, Séjalon-Delmas N (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol 4:1239–1247
Breuillin F, Schramm J, Hajirezaei M, Ahkami A, Favre P, Druege U, Hause B, Bucher M, Kretzschmar T, Bossolini E, Kuhlemeier C, Martinoia E, Franken P, Scholz U, Reinhardt D (2010) Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant J 64:1002–1017
Buee M, Rossignol M, Jauneau A, Ranjeva R, Bécard G (2000) The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Mol Plant-Microbe Interact 13:693–698
Camenzind T, Hempel S, Homeier J, Horn S, Velescu A, Wilcke W, Rillig MC (2014) Nitrogen and phosphorus additions impact arbuscular mycorrhizal abundance and molecular diversity in a tropical montane forest. Glob Chang Biol 20:3646–3659
Caporaso G, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Rob K (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336
Chen Y, Zhang X, Ye J, Han H, Wan S, Chen B (2014) Six-year fertilization modifies the biodiversity of arbuscular mycorrhizal fungi in a temperate steppe in Inner Mongolia. Soil Biol Biochem 69:371–381
Colomb B, Debaeke P, Jouany C, Nolot JM (2007) Phosphorus management in low input stockless cropping systems: crop and soil responses to contrasting P regimes in a 36-year experiment in southern France. Eur J Agron 26:154–165
Deng Y, Chen K, Teng W, Zhan A, Tong Y, Feng G, Cui Z, Zhang F, Chen X (2014) Is the inherent potential of maize roots efficient for soil phosphorus acquisition? PLoS One 9:e90287
Fester T, Schmidt D, Lohse S, Walter MH, Giuliano G, Bramley PM, Fraser PD, Hause B, Strack D (2002) Stimulation of carotenoid metabolism in arbuscular mycorrhizal roots. Planta 216:148–154
Glassop D, Smith SE, Smith FW (2005) Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake into roots. Planta 222:688–698
Gosling P, Hodge A, Goodlass G, Bendinga GD (2006) Arbuscular mycorrhizal fungi and organic farming. Agr Ecosyst Enviro 113:17–35
Gosling P, Mead A, Proctor M, Hammond JP, Bending GD (2013) Contrasting arbuscular mycorrhizal communities colonizing different host plants show a similar response to a soil phosphorus concentration gradient. New Phytol 198:546–556
Guan JC, Koch KE, Suzuki M, Wu S, Latshaw S, Petruff T, Goulet C, Klee HJ, McCarty DR (2012) Diverse roles of strigolactone signaling in maize architecture and the uncoupling of a branching-specific subnetwork. Plant Physiol 160:1303–1317
Islas AJT, Guijarro KH, Eyherabide M, Rozasa SHR, Echeverríaa HE, Covacevicha F (2016) Can soil properties and agricultural land use affect arbuscular mycorrhizal fungal communities indigenous from the Argentinean Pampas soils? Appl Soil Ecol 101:47–56
Jansa J, Erb A, Oberholzer H, Šmilauer P, Egli S (2014) Soil and geography are more important determinants of indigenous arbuscular mycorrhizal communities than management practices in Swiss agricultural soils. Mol Ecol 23:2118–2135
Javot H, Penmetsa RV, Terzaghi N, Cook DR, Harrison MJ (2007a) A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. P Natl Acad Sci USA 104:1720–1725
Javot H, Pumplin N, Harrison MJ (2007b) Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant Cell Environ 30:310–322
Jungk A, Claassen N (1989) Availability in soil and acquisition by plants as the basis for phosphorus and potassium supply to plants. Z Pflanz Bodenk 152:151–157
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
Kahiluoto H, Ketoja E, Vestberg M, Saarela I (2001) Promotion of AM utilization through reduced P fertilization 2. Field studies. Plant Soil 231:65–79
Kobae Y, Hata S (2010) Dynamics of periarbuscular membranes visualized with a fluorescent phosphate transporter in arbuscular mycorrhizal roots of rice. Plant Cell Physiol 51:341–353
Koch AM, Croll D, Sanders IR (2006) Genetic variability in a population of arbuscular mycorrhizal fungi causes variation in plant growth. Ecol Lett 9:103–110
Lee J, Lee S, Young JPW (2008) Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 65:339–349
Li H, Huang G, Meng Q, Ma L, Yuan L, Wang F, Zhang W, Cui Z, Shen J, Chen X, Jiang R, Zhang F (2011) Integrated soil and plant phosphorus management for crop and environment in China. A review. Plant Soil 349:157–167
Lin X, Feng Y, Zhang H, Chen R, Wang J, Zhang J, Chu H (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 Y, Shi G, Mao L, Cheng G, Jiang S, Ma X, An L, Du G, Johnson NC, Feng H (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 W, Zhang Y, Jiang S, Deng Y, Christie P, Murray PJ, Li X, Zhang J (2016) Arbuscular mycorrhizal fungi in soil and roots respond differently to phosphorus inputs in an intensively managed calcareous agricultural soil. Sci Rep 6:24902
Lynch JP (2007) Roots of the second green revolution. Aust J Bot 55:493–512
Mallarino AP, Atia AM (2005) Correlation of a resin membrane soil phosphorus test with corn yield and routine soil tests. Soil Sci Soc Am J 69:266–272
Marschner P (2012) Rhizosphere biology. In: Marschner P (ed) Marschner’s mineral nutrition of higher plants. Academic Press, London, pp 369–388
Menge JA, Steirle D, Bagyaraj DJ, Johnson ELV, Leonard RT (1978) Phosphorus concentrations in plants responsible for inhibition of mycorrhizal infection. New Phytol 80:575–578
Munkvold L, Kjøller R, Vestberg M, Rosendahl S, Jakobsen I (2004) High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 164:357–364
Nagy R, Vasconcelos MJV, Zhao S, Mcelver J, Bruce W, Amrhein N, Raghothama KG, Bucher M (2006) Differential regulation of five Pht1 phosphate transporters from maize (Zea mays L.). Plant Biol 8:186–197
Ning P, Li S, Yu P, Zhang Y, Li C (2013) Post-silking accumulation and partitioning of dry matter, nitrogen, phosphorus and potassium in maize varieties differing in leaf longevity. Field Crop Res 144:19–27
Ning P, Li S, White PJ, Li C (2015) Maize varieties released in different eras have similar root length density distributions in the soil, which are negatively correlated with local concentrations of soil mineral nitrogen. PLoS One 10:e0121892
Oehl F, Sieverding E, Ineichen K, Ris E, 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
Öpik M, Vanatoa A, Vanatoa E, Moora M, Davison J, Kalwij JM, Reier U, Zobel M (2010) The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol 188:223–241
Pautler MC, Sims JT (2000) Relationships between soil test phosphorus, soluble phosphorus, and phosphorus saturation in Delaware soils. Soil Sci Soc Am J 64:765–773
Peng Y, Li X, Li C (2012a) Temporal and spatial profiling of root growth revealed novel response of maize roots under various nitrogen supplies in the field. PLoS One 7:e37726
Peng Y, Yu P, Zhang Y, Sun G, Ning P, Li X, Li C (2012b) Temporal and spatial dynamics in root length density of field-grown maize and NPK in the soil profile. Field Crop Res 131:9–16
Phillips JM, Hayman DS (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
Pote DH, Daniel TC, Sharpley AN, Moore PA, Edwards DR, Nichols DJ (1996) Relating extractable soil phosphorus to phosphorus losses in runoff. Soil Sci Soc Am J 60:855–859
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. Grassl Sci 51:179
Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116:447–453
Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6:e27310
Schmitz AM, Harrison MJ (2014) Signaling events during initiation of arbuscular mycorrhizal symbiosis. J Integr Plant Biol 56:250–261
Schwarzott D, Schüßler A (2001) A simple and reliable method for SSU rRNA gene DNA extraction, amplification, and cloning from single AM fungal spores. Mycorrhiza 10:203–207
Simon L, Lalonde M, Bruns TD (1992) Specific amplification of 18S fungal ribosomal genes from vesicular-arbuscular endomycorrhizal fungi colonizing roots. Appl Environ Microb 58:291–295
Smith SE, Read DJ (2008) Arbuscular mycorrhizas. In: Smith SE, Read DJ (eds) Mycorrhizal Symbiosis. Academic Press, London, pp 11–145
Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250
Smith SE, Smith FA, Jakobsen I (2004) Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytol 162:511–524
Soon YK, Kalra YP (1995) Short communication: a comparison of plant tissue digestion methods for nitrogen and phosphorus analyses. Can J Soil Sci 75:243–245
Sparling GP, Tinker PB (1978) Mycorrhizal infection in Pennine grassland. I. Levels of infection in the field. J Appl Ecol 15:943–950
Taguchi Y, Oono Y (2005) Relational patterns of gene expression via non-metric multidimensional scaling analysis. Bioinformatics 21:730–740
Tatsuhiro E, Sally E (2001) Differentiation of polyphosphate metabolism between the extra- and intraradical hyphae of arbuscular mycorrhizal fungi. New Phytol 149:555–563
Teng W, Deng Y, Chen X, Xu X, Chen R, Lv Y, Zhao Y, Zhao X, He X, Li B, Tong Y, Zhang F, Li Z (2013) Characterization of root response to phosphorus supply from morphology to gene analysis in field-grown wheat. J Exp Bot 64:1403–1411
Thomson BD, Robson AD, Abbott LK (1991) Soil mediated effects of phosphorus supply on the formation of mycorrhizas by Scutellispora calospora (Nicol. & Gerd.) Walker & Sanders on subterranean clover. New Phytol 118:463–469
Tisserant B, Gianinazzi-Pearson V, Gianinazzi S, Gollotte A (1993) In planta histochemical staining of fungal alkaline phosphatase activity for analysis of efficient arbuscular mycorrhizal infections. Mycol Res 97:245–250
Tisserant B, Gianinazzi S, Gianinazzi-Pearson V (1996) Relationships between lateral root order, arbuscular mycorrhiza development, and the physiological state of the symbiotic fungus in Platanus acerifolia. Can J Bot 74:1947–1955
Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization VA d’un système radiculaire. Recherche de méthodes d’estimation ayant une signification fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and genetical aspects of mycorrhizae. INRA Press, Paris, pp 217–221
Van Aarle IM, Rouhier H, Saito M (2002) Phosphatase activities of arbuscular mycorrhizal intraradical and extraradical mycelium, and their relation to phosphorus availability. Mycol Res 106:1224–1229
Veneklaas EJ, Lambers H, Bragg J, Finnegan PM, Lovelock CE, Plaxton WC, Price CA, Scheible W-R, Shane MW, White PJ, Raven JA (2012) Opportunities for improving phosphorus-use efficiency in crop plants. New Phytol 195:306–320
Verbruggen E, Heijden MGA, Rillig MC, Kier ET (2013) Mycorrhizal fungal establishment in agricultural soils: factors determining inoculation success. New Phytol 197:1104–1109
Wakelin S, Mander C, Gerard E, Jansa J, Erb A, Young S, Condron L, O’Callaghan M (2012) Response of soil microbial communities to contrasted histories of phosphorus fertilization in pastures. Appl Soil Ecol 61:40–48
White PJ, George TS, Gregory PJ, Bengough AG, Hallett PD, McKenzie BM (2013) Matching roots to their environment. Ann Bot-London 112:207–222
Zhang X, Shen D, Feng H, Wang Y, Na L, Han J, Long Y (2015) Cooperative role of electrical stimulation on microbial metabolism and selection of thermophilic communities for p-fluoronitrobenzene treatment. Bioresource Techn 189:23–29
Acknowledgements
C.W. and C.L.’s research is supported by grants from the State Key Basic Research and Development Plan of China (No. 2013CB127402) and the Innovative Group Grant of the National Natural Science Foundation of China (NSFC) (No. 31421092). P.J.W.’s research is supported by the Rural and Environmental Science and Analytical Services Division (RESAS) of the Scottish Government Strategic Programme (2016–2021).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
ESM 1
(DOC 682 kb)
Rights and permissions
About this article
Cite this article
Wang, C., White, P.J. & Li, C. 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 (2017). https://doi.org/10.1007/s00572-016-0757-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00572-016-0757-5