Abstract
Aims
Arbuscular mycorrhizal fungi play important roles in plant phosphorus (P) accumulation. The aim of this study was to uncover how and to what extent soil plant-available P levels and maize genotypes influence the contribution of mycorrhizal P uptake pathway to plant P nutrition.
Methods
We selected an old genotype HMY and a modern genotype XY335, combined with 32P labeling and qPCR to quantify P uptake efficiency of the direct pathway (DP) and the mycorrhizal pathway (MP) at three Olsen-P levels: 4.5 (low), 8 (medium) and 50 (high) mg kg−1.
Results
The P uptake efficiency ratio PAE-MP/PAE-DP was highest in the treatment with medium Olsen-P, and was correlated positively with MP contribution. The traits of arbuscular mycorrhizal fungi, such as percent colonization, hyphal length density, P uptake per unit hyphae length, and the expression of the mycorrhiza-specific P transporter ZmPT1;6 were higher in XY335 than HMY in high-P soil, which was in accordance with the importance of the MP contribution.
Conclusions
Greater mycorrhizal responsiveness in the modern maize genotype than the old genotype under high P soil condition is related to higher P uptake efficiency of MP than DP; the inherent potential of MP can be maximized by managing soil plant P availability to achieve optimal P supply in intensive farming.
Similar content being viewed by others
Abbreviations
- AMF:
-
arbuscular mycorrhizal fungi
- DP:
-
direct P uptake pathway
- MP:
-
mycorrhizal P uptake pathway
- MGR:
-
mycorrhizal growth response
- MPR:
-
mycorrhizal phosphorus response
- NM:
-
non-mycorrhizal
- PAE:
-
phosphorus acquisition efficiency
References
An G, Kobayashi S, Enoki H, Sonobe K, Muraki M, Karasawa T, Ezawa T (2010) How does arbuscular mycorrhizal colonization vary with host plant genotype? An example based on maize (Zea mays) germplasms. Plant Soil 327:441–453
Baon JB, Smith SE, Alston AM (1993) Mycorrhizal responses of barley cultivars differing in P efficiency. Plant Soil 157:97–105
Benbi DK, Biswas CR (1999) Nutrient budgeting for phosphorus and potassium in a long-term fertilizer trial. Nutr Cycl Agroecosyst 54:125–132
Chu Q, Wang XX, Yang Y, Chen FJ, Zhang FS, Feng G (2013) Mycorrhizal responsiveness of maize (Zea mays L.) genotypes as related to releasing date and available P content in soil. Mycorrhiza 23:497–505
Culman SW, Young-Mathews A, Hollander AD, Ferris H, Sánchez-Moreno S, O’Geen AT, Jackson LE (2010) Biodiversity is associated with indicators of soil ecosystem functions over a landscape gradient of agricultural intensification. Landsc Ecol 25:1333–1348
Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139:5–17
Deng Y, Chen KR, Teng W, Zhan A, Tong YP, Feng G, Cui ZL, Zhang FS, Chen XP (2014) Is the inherent potential of maize roots efficient for soil phosphorus acquisition? PLoS One 9:e90287
Deng Y, Feng G, Chen XP, Zou CQ (2017) Arbuscular mycorrhizal fungal colonization is considerable at optimal Olsen-P levels for maximized yields in an intensive wheat-maize cropping system. Field Crop Res 209:1–9
Estaún V, Calvet C, Camprubí A (2010) Effect of differences among crop species and cultivars on the arbuscular mycorrhizal symbiosis. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function. Springer, Heidelberg, Germany, pp 279–295
Facelli E, Duan T, Smith SE, Christophersen HM, Facelli JM, Smith FA (2014) Opening the black box: outcomes of interactions between arbuscular mycorrhizal (AM) and non-host genotypes of Medicago depend on fungal identity, interplay between P uptake pathways and external P supply. Plant Cell Environ 37:1382–1392
Facelli E, Smith SE, Facelli JM, Christophersen HM, Andrew Smith F (2010) Underground friends or enemies: model plants help to unravel direct and indirect effects of arbuscular mycorrhizal fungi on plant competition. New Phytologist 185(4):1050–1061
Gai JP, Gao WJ, Liu L, Chen Q, Feng G, Zhang JL, Li XL (2015) Infectivity and community composition of arbuscular mycorrhizal fungi from different soil depths in intensively managed agricultural ecosystems. J Soils Sediments 15:1200–1211
Galván GA, Kuiper TW, Burger K, Keizer LCP, Hoekstra RF, Kik C, Scholten OE (2011) Genetic analysis of the interaction between Allium species and arbuscular mycorrhizal fungi. Theor Appl Genet 122:947–960
Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500
Gomez SK, Javot H, Deewatthanawong P, Torres-Jerez I, Tang Y, Blancaflor EB, Udvardi MK, Harrison MJ (2009) Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis. BMC Plant Biol 9:10
Hayman DS, Mosse B (1972) Plant growth responses to vesicular–arbuscular mycorrhiza. III. Increased uptake of labile P from soil. New Phytol 71:41–47
Hetrick BAD, Wilson GWT, Cox TS (1992) Mycorrhizal dependence of modern wheat varieties, landraces, and ancestors. Can J Bot 70:2032–2040
Hildermann I, Messmer M, Dubois D, Boller T, Wiemken A, Mäder P (2010) Nutrient use efficiency and arbuscular mycorrhizal root colonisation of winter wheat cultivars in different farming systems of the DOK long-term trial. J Sci Food Agric 90:2027–2038
Hinsinger P, Betencourt E, Bernard L, Brauman A, Plassard C, Shen JB, Tang XY, Zhang FS (2011) P for two, sharing a scarce resource: soil phosphorus acquisition in the rhizosphere of intercropped species. Plant Physiol 156:1078–1086
Hodge A, Fitter AH (2013) Microbial mediation of plant competition and community structure. Funct Ecol 27:865–875
Jakobsen I, Abbott L, Robson A (1992) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. New Phytol 120:371–380
Janos DP (2007) Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza 17:75–91
Javot H, Pumplin N, Harrison MJ (2007) Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant Cell Environ 30:310–322
Johnson NC (1993) Can fertilization of soil select less mutualistic mycorrhizae? Ecol Appl 3:749–757
Johnson NC, Graham J-H, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism–parasitism continuum. New Phytol 135:575–585
Kalkhajeh YK, Huang B, Hu W, Holm PE, Hansen HC (2017) Phosphorus saturation and mobilization in two typical Chinese greenhouse vegetable soils. Chemosphere 172:316–324
Kitson RE, Mellon MG (1944) Colorimetric determination of phosphorus as molybdovanadophosphoric acid. Ind Eng Chem Anal Ed 16:379–383
Lehmann A, Barto EK, Powell JR, Rillig MC (2012) Mycorrhizal responsiveness trends in annual crop plants and their wild relatives—a meta-analysis on studies from 1981 to 2010. Plant Soil 355:231–250
Leiser WL, Olatoye MO, Rattunde HFW, Neumann G, Weltzien E, Haussmann BIG (2016) No need to breed for enhanced colonization by arbuscular mycorrhizal fungi to improve low-P adaptation of west African sorghums. Plant Soil 401:51–64
Li H, Huang Q, Meng L, Ma L, Yuan F, Wang W, Zhang Z, Cui J, Shen X, Chen R et al (2011) Integrated soil and plant phosphorus management for crop and environment in China. A review. Plant Soil 349:157–167
Liu SL, Guo XL, Bai DS, Fan JL, He XH, Feng G (2016) Indigenous arbuscular mycorrhizal fungi alleviate salt stress and promote cotton and maize growth in saline fields. Plant Soil 398:195–206
Liu W, Jiang SS, Zhang YL, Yue SC, Christie P, Murray PJ, Li XL, Zhang JL (2014) Spatiotemporal changes in arbuscular mycorrhizal fungal communities under different nitrogen inputs over a 5-year period in intensive agricultural ecosystems on the North China plain. FEMS Microbiol Ecol 90:436–453
Lynch JP (2007) Turner review no. 14. Roots of the second green revolution. Aust J Bot 55:493–512
Matson PA, Parton WJ, Power AG, Swift MJ (1997) Agricultural intensification and ecosystem properties. Science 277:504–509
Mosse B (1973) Plant growth responses to vesicular-arbuscular mycorrhiza. New Phytol 72:127–136
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
Nagy R, Drissner D, Amrhein N, Jakobsen I, Bucher M (2009) Mycorrhizal phosphate uptake pathway in tomato is phosphorus-repressible and transcriptionally regulated. New Phytol 181:950–959
Oehl F, Sieverding E, Ineichen K, Mäder P, Boller T, Wiemken A (2003) Impact of land use intensity on the species diversity of arbuscular mycorrhizal fungi in agroecosystems of Central Europe. Appl Environ Microbiol 69:2816–2824
Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. Circ. No. 939. USDA, Washington DC
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:45–45
Plenchette C, Fortin JA, Furlan V (1983) Growth responses of several plant species to mycorrhizae in a soil of moderate P-fertility. Plant Soil 70:199–209
Postma-Blaauw MB, de Goede RGM, Bloem J, Faber JH, Brussaard L (2010) Soil biota community structure and abundance under agricultural intensification and extensification. Ecology 91:460–473
Reynolds HL, Vogelsang KM, Hartley AE, Bever JD, Schultz PA (2006) Variable responses of old-field perennials to arbuscular mycorrhizal fungi and phosphorus source. Oecologia 147:348–358
Sawers RJH, Svane SF, Quan C, Grønlund M, Wozniak B, Gebreselassie MN, González-Muñoz E, Chávez Montes RA, Baxter I, Goudet J, Jakobsen I, Paszkowski U (2017) Phosphorus acquisition efficiency in arbuscular mycorrhizal maize is correlated with the abundance of root-external hyphae and the accumulation of transcripts encoding PHT1 phosphate transporters. New Phytol 214:632–643
Shen JB, Yuan LX, Zhang JL, Li HG, Bai ZH, Chen XP, Zhang WF, Zhang FS (2011) Phosphorus dynamics: from soil to plant. Plant Physiol 156:997–1005
Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16–20
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
Smith SE, Read DJ (2008) Mycorrhizal Symbiosis, edition 3. Academic Press, London, UK
Smith SE, Jakobsen I, Grønlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156:1050–1057
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
Teng W, Deng Y, Chen XP, Xu XF, Chen YR, Lv Y, Zhao YY, Zhao XQ, He X, Li B et al (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 (1992) The effect of long-term applications of phosphorus-fertilizer on populations of vesicular arbuscular mycorrhizal fungi in pastures. Aust J Agri Res 43:1131–1142
Treseder KK (2013) The extent of mycorrhizal colonization of roots and its influence on plant growth and phosphorus content. Plant Soil 371:1–13
Tsiafouli MA, Thébault E, Sgardelis SP, de Ruiter PC, van der Putten WH, Birkhofer K, Hemerik L, de Vries FT, Bardgett RD, Brady MV et al (2014) Intensive agriculture reduces soil biodiversity across Europe. Glob Chang Biol 21:973–985
Van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72
Verbruggen E, Heijden MGA, Rillig MC, Kiers ET (2013) Mycorrhizal fungal establishment in agricultural soils: factors determining inoculation success. New Phytol 197:1104–1109
Vestberg M, Kahiluoto H, Wallius E (2011) Arbuscular mycorrhizal fungal diversity and species dominance in a temperate soil with long-term conventional and low-input cropping systems. Mycorrhiza 21:351–361
Wang XR, Shen JB, Liao H (2010) Acquisition or utilization, which is more critical for enhancing phosphorus efficiency in modern crops? Plant Sci 179:302–306
Wang YT, Li T, Li YW, Björn LO, Rosendahl S, Olssen PA, Li SS, Fu XL (2015) Community dynamics of arbuscular mycorrhizal fungi in high-input and intensively irrigated rice cultivation systems. Appl Environ Microbiol 81:2958–2965
Wetzel K, Silva G, Matczinski U, Oehl F, Fester T (2014) Superior differentiation of arbuscular mycorrhizal fungal communities from till and no-till plots by morphological spore identification when compared to T-RFLP. Soil Biol Biochem 72:88–96
Willmann M, Gerlach N, Buer B, Polatajko A, Nagy R, Koebke E, Jansa J, Flisch R, Bucher M (2013) Mycorrhizal phosphate uptake pathway in maize: vital for growth and cob development on nutrient poor agricultural and greenhouse soils. Front Plant Sci 4:533
Wright DP, Scholes JD, Read DJ, Rolfe SA (2005) European and African maize cultivars differ in their physiological and molecular responses to mycorrhizal infection. New Phytol 167:881–896
York LM, Galindo-Castañeda T, Schussler JR, Lynch JP (2015) Evolution of US maize (Zea mays L.) root architectural and anatomical phenes over the past 100 years corresponds to increased tolerance of nitrogen stress. J Exp Bot 66:2347–2358
Zhu JM, Kaeppler SM, Lynch JP (2005) Topsoil foraging and phosphorus acquisition efficiency in maize (Zea mays). Funct Plant Biol 32:749–762
Zhu YG, Smith SE, Barritt AR, Smith FA (2001) Phosphorus (P) efficiencies and mycorrhizal responsiveness of old and modern wheat cultivars. Plant Soil 237:249–255
Acknowledgments
This study was financially supported by the National Natural Science Foundation of China (U1703232) and National Key R&D Program of China (2017YFD0200200). We thank Professor Andrew Smith from The University of Adelaide for kindly revising the early manuscript version.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Felipe E. Albornoz.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOC 424 kb)
Rights and permissions
About this article
Cite this article
Chu, Q., Zhang, L., Zhou, J. et al. Soil plant-available phosphorus levels and maize genotypes determine the phosphorus acquisition efficiency and contribution of mycorrhizal pathway. Plant Soil 449, 357–371 (2020). https://doi.org/10.1007/s11104-020-04494-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-020-04494-4