Abstract
Mycorrhizal fungi form symbiotic relationships with most terrestrial plants. Soil nutrients affect the mycorrhizal symbiotic formation, further determine plant growth. However, little is known on the role of mycorrhiza in response of host plant growth to nutritional additions in natural ecosystem. A new database was established including the index of plant growth and their mycorrhizal status based on a global database of interactive effects of nitrogen (N) and phosphorus (P) additions on plant growth. We examined effects of mycorrhizal strategy on the responses of plant growth to N or P addition. We found that plant growth was closely related to mycorrhizal strategies. N addition increased 35% aboveground biomass (AGB) of host plants associated with arbuscular mycorrhiza (AM), whereas decreased it by 9% in plants non-associated with AM (nonAM). P addition or NP addition all increased AGB regardless of mycorrhizal type, but the effect of nonAM plants was stronger than that of AM plants. Structural equation modelling (SEM) analysis showed that N addition had an positive effect on leaf N:P ratios through affecting leaf N of AM plants (r = 0.25) and nonAM plants (r = 0.33) whereas P addition had an negative effect on leaf N:P ratios through affecting leaf P of AM plants (r = 0.29) and nonAM plants (r = 0.45). Our results highlighted the biomass production of plants was controlled mainly by P addition and AM increased the accumulation of AGB by promoting plant P uptake. Moreover, AMF have different functions depending on the nutritional conditions, further regulated plant growth.
Similar content being viewed by others
Abbreviations
- N:
-
Nitrogen
- P:
-
Phosphorus
- AM:
-
Arbuscular mycorrhiza
- AMF:
-
Arbuscular mycorrhizal fungi
- AGB:
-
Aboveground biomass
- BGB:
-
Belowground biomass
- AP:
-
Available phosphorus
- NH4-N:
-
Ammonium nitrogen
- NO3-N:
-
Nitrate nitrogen
- SEM:
-
Structural equation modelling
References
Aslani F, Juraimi AS, Ahmad-Hamdani MS, Alam MA, Hasan MM, Hashemi FSG, Bahram M (2019) The role of arbuscular mycorrhizal fungi in plant invasion trajectory. Plant Soil 441:1–14. https://doi.org/10.1007/s11104-019-04127-5
Augé RM, Toler HD, Saxton AM (2015) Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis. Mycorrhiza 25:13–24. https://doi.org/10.1007/s00572-014-0585-4
Bi YL, Zhou HL (2021) Changes in peanut canopy structure and photosynthetic characteristics induced by an arbuscular mycorrhizal fungus in a nutrient-poor environment. Sci Rep 11:14832. https://doi.org/10.1038/s41598-021-94092-w
Chen LF, Xiang YZ, He ZB, Du J, Lin PF, Zhu X (2020) A meta-analysis of the impacts of forest logging on soil CO2 efflux. Sci Cold Arid Reg 12:165–179. https://doi.org/10.3724/SP.J.1226.2020.00165
Davison J, Moora M, Öpik M et al (2015) Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science 349:970–973. https://doi.org/10.1126/science.aab1161
Du E, Terrer C, Pellegrini AFA et al (2020) Global patterns of terrestrial nitrogen and phosphorus limitation. Nat Geosci 13:221–226. https://doi.org/10.1038/s41561-019-0530-4
Elser JJ, Bracken MES, Cleland EE et al (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142. https://doi.org/10.1111/j.1461-0248.2007.01113.x
Gao XP, Guo HH, Zhang Q, Guo HX, Zeng FC (2020) Arbuscular mycorrhizal fungi (AMF) enhanced the growth, yield, fiber quality and phosphorus regulation in upland cotton (Gossypium hirsutum L.). Sci Rep 10:2084. https://doi.org/10.1038/s41598-020-59180-3
Giesler R, Esberg C, Lagerström A, Graae BJ (2012) Phosphorus availability and microbial respiration across different tundra vegetation types. Biogeochemistry 108:429–445. https://doi.org/10.1007/s10533-011-9609-8
Govindarajulu M, Pfeffer P, Jin H et al (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 43:810–823. https://doi.org/10.1038/nature03610
Han YF, Feng JG, Han MG, Zhu B (2020) Responses of arbuscular mycorrhizal fungi to nitrogen addition: A meta–analysis. Glob Chang Biol 26:7229–7241. https://doi.org/10.1111/gcb.15369
Haugwitz MS, Michelsen A (2011) Long-term addition of fertilizer, labile carbon, and fungicide alters the biomass of plant functional groups in a subarctic-alpine community. Plant Ecol 212:715–726. https://doi.org/10.1007/s11258-010-9857-z
Hou E, Luo Y, Kuang Y, Chen C, Wen D (2020) Global meta-analysis shows pervasive phosphorus limitation of aboveground plant production in natural terrestrial ecosystems. Nat Commun 11:637. https://doi.org/10.1038/s41467-020-14492-w
Jeong SJ, Chang-Hoi HO, Gim HJ, Brown ME (2011) Phenology shifts at start vs. end of growing season in temperate vegetation over the northern hemisphere for the period 1982–2008. Glob Chang Biol 17:2385–2399. https://doi.org/10.1111/j.1365-2486.2011.02397.x
Jiang J, Wang YP, Yang YH, Yu MX, Wang C, Yan JH (2019) Interactive effects of nitrogen and phosphorus additions on plant growth vary with ecosystem type. Plant Soil 440:523–537. https://doi.org/10.1007/s11104-019-04119-5
Jing YL, Tian P, Wang QK, Li WB, Sun ZL, Yang H (2021) Effects of root dominate over aboveground litter on soil microbial biomass in global forest ecosystems. For Ecosyst 8:504–512. https://doi.org/10.1186/s40663-021-00318-8
Kaspari M, Garcia MN, Harms KE, Santana M, Yavitt JB (2010) Multiple nutrients limit litterfall and decomposition in a tropical forest. Ecol Lett 11:35–43. https://doi.org/10.1111/j.1461-0248.2007.01124.x
Koele N, Dickie IA, Jacek O, Richardson SJ, Reich PB (2012) No globally consistent effect of ectomycorrhizal status on foliar traits. New Phytol 196:845–852. https://doi.org/10.1111/j.1469-8137.2012.04297.x
Li Y, Niu S, Yu G (2016) Aggravated phosphorus limitation on biomass production under increasing nitrogen loading: a meta–analysis. Glob Chang Biol 22:934–943. https://doi.org/10.1111/gcb.13125
Li L, Liu B, Gao X, Li XY, Li CD (2019) Nitrogen and phosphorus addition differentially affect plant ecological stoichiometry in desert grassland. Sci Rep 9:18673. https://doi.org/10.1038/s41598-019-55275-8
Liang S, Shi P, Li H (2016) Urban spring phenology in the middle temperate zone of china: dynamics and influence factors. Int J Biometeorol 60:531–544. https://doi.org/10.1007/s00484-015-1049-z
Liu SM, Wang H (2018) N, P, and K characteristics of different age groups of temperate coniferous tree species in northwestern China. J for Res 29:471–478. https://doi.org/10.1007/s11676-017-0442-3
Liu L, Gundersen P, Zhang W, Zhang T, Chen H, Mo JM (2015) Effects of nitrogen and phosphorus additions on soil microbial biomass and community structure in two reforested tropical forests. Sci Rep 5:14378. https://doi.org/10.1038/srep14378
Lu J, Tian H, Zhang H, Xiong J, Liu Y (2021) Shoot-soil ecological stoichiometry of alfalfa under nitrogen and phosphorus fertilization in the loess plateau. Sci Rep 11:15049. https://doi.org/10.1038/s41598-021-94472-2
Maiti D, Singh RK, Variar M (2012) Rice–based crop rotation for enhancing native arbuscular mycorrhizal (AM) activity to improve phosphorus nutrition of upland rice (Oryza sativa L.). Biol Fertil Soils 48:67–73. https://doi.org/10.1007/s00374-011-0609-6
Muthukumar T, Udaiyan K (2018) Coinoculation of bioinoculants improve Acacia auriculiformis seedling growth and quality in a tropical Alfisol soil. J for Res 29:663–673. https://doi.org/10.1007/s11676-017-0497-1
Nguyen TD, Cavagnaro TR, Watts-Williams SJ (2019) The effects of soil phosphorus and zinc availability on plant responses to mycorrhizal fungi: a physiological and molecular assessment. Sci Rep 9:14880. https://doi.org/10.1038/s41598-019-51369-5
Read QD, Henning JA, Classen AT, Sanders NJ (2018) Aboveground resilience to species loss but belowground resistance to nitrogen addition in a montane plant community. J Plant Ecol 11:351–363. https://doi.org/10.1093/jpe/rtx015
Ren HY, Gui WY, Bai YF et al (2018) Long–term effects of grazing and topography on extra–radical hyphae of arbuscular mycorrhizal fungi in semi–arid grasslands. Mycorrhiza 28:117–127. https://doi.org/10.1007/s00572-017-0812-x
Sarabia M, Jakobsen I, Grønlund M, Carreon-Abud Y, Larsen J (2017) Rhizospere yeasts improve p uptake of a maize arbuscular mycorrhizal association. Appl Soil Ecol 125:18–25. https://doi.org/10.1016/j.apsoil.2017.12.012
Sheldrake M, Rosenstock NP, Mangan S et al (2018) Responses of arbuscular mycorrhizal fungi to long-term inorganic and organic nutrient addition in a lowland tropical forest. ISME J 12:2433–2445. https://doi.org/10.1038/s41396-018-0189-7
Shi ZY, Li K, Zhu XY, Wang FY (2020) The worldwide leaf economic spectrum traits are closely linked with mycorrhizal traits. Fungal Ecol 43:100877. https://doi.org/10.1016/j.funeco.2019.100877
Song ZH, Bi YL, Zhang J, Gong YL, Yang HH (2020) Arbuscular mycorrhizal fungi promote the growth of plants in the mining associated clay. Sci Rep 10:2663. https://doi.org/10.1038/s41598-020-59447-9
Sundqvist MK, Liu Z, Giesler R, Wardle DA (2014) Plant and microbial responses to nitrogen and phosphorus addition across an elevational gradient in subarctic tundra. Ecology 95:1819–1835. https://doi.org/10.1890/13-0869.1
Tian H, Yuan XL, Duan JF, Li WH, Zhai BN, Gao YJ (2017) Influence of nutrient signals and carbon allocation on the expression of phosphate and nitrogen transporter genes in winter wheat (Triticum aestivum L.) roots colonized by arbuscular mycorrhizal fungi. PLoS ONE 12:e0172154. https://doi.org/10.1371/journal.pone.0172154
Wang CG, Zong SW, Li MH (2019) The contrasting responses of mycorrhizal fungal mycelium associated with woody plants to multiple environmental factors. Forests 10:973. https://doi.org/10.3390/f10110973
Wang L, Chen X, Du YQ, Zhang D, Tang ZH (2022) Nutrients regulate the effects of arbuscular mycorrhizal fungi on the growth and reproduction of cherry tomato. Front Microbiol 13:843010. https://doi.org/10.3389/fmicb.2022.843010
Ye L, Zhao X, Bao EC, Cao K, Zou ZR (2019) Effects of arbuscular mycorrhizal fungi on watermelon growth, elemental uptake, antioxidant, and photosystem II activities and stress-response gene expressions under salinity–alkalinity stresses. Front Plant Sci 10:863. https://doi.org/10.3389/fpls.2019.00863
Yuan YG, Ge LT, Yang HS, Ren WZ (2018) A meta–analysis of experimental warming effects on woody plant growth and photosynthesis in forests. J for Res 29:727–733. https://doi.org/10.1007/s11676-017-0499-z
Zemunik G, Turner BL, Lambers H, Laliberté E (2015) Diversity of plant nutrient-acquisition strategies increases during long-term ecosystem development. Nat Plants 1:15050. https://doi.org/10.1038/nplants.2015.50
Zhang SJ, Wang L, Ma F, Zhang X, Fu DF (2016) Arbuscular mycorrhiza improved phosphorus efficiency in paddy fields. Ecol Eng 95:64–72. https://doi.org/10.1016/j.ecoleng.2016.06.029
Zhang L, Feng G, Declerck S (2018) Signal beyond nutrient, fructose, exuded by an arbuscular mycorrhizal fungus triggers phytate mineralization by a phosphate solubilizing bacterium. ISME J 12:2339–2351. https://doi.org/10.1038/s41396-018-0171-4
Acknowledgements
This research was funded by National Natural Science Foundation of China (32171620), Scientific and technological research projects in Henan province (232102111005), Natural Science Foundation of Henan Province (402421011901).
Author information
Authors and Affiliations
Contributions
LY and SZY contributed to writing, reviewing and editing the Manuscript; LY, YS and ZMG prepared and analyzed the figures and data for the manuscript; LY wrote the manuscript. All authors have read and agreed to the published version of the manuscript.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare no conflicts of interest relevant to this study.
Ethics Approval
We all declare that manuscript reporting studies do not involve any human participants, human data, or human tissue.
Additional information
Handling Editor: Mikihisa Umehara.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Li, Y., Shi, Z., Yang, S. et al. Responses of Plant Growth to N or P Addition Vary With Mycorrhizal Strategy. J Plant Growth Regul 43, 807–815 (2024). https://doi.org/10.1007/s00344-023-11140-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-023-11140-7