Effects of Arbuscular Mycorrhizal Fungi on Leaf N: P: K Stoichiometry in Agroecosystem

Leaf nitrogen (N), phosphorus (P), and potassium (K) stoichiometry can reflect plant strategies of nutrient allocation, which play key roles in ensuring food security and maintaining nutrient balance in the agroecosystem. Arbuscular mycorrhizal fungi (AMF) inoculation is an effective and green management measure affecting nutrient uptake and utilization strategies, especially in the agroecosystem. However, the interplay between AMF and leaf nutrient stoichiometry that is important for sustainable agriculture remain underexplored. Therefore, the efficacy of AMF in improving leaf nutrients of host plants in agricultural ecosystems were tested with meta-analysis by 1932 pairs of observations in research publications from 1995 to 2022. Overall analysis showed that AMF inoculation increases leaf N, P, and K by 8.75%, 24.61%, and 13.54%, respectively. Moreover, leaf P: K increased by 11.74% by AMF inocula, but leaf N: P and N: K of host plants decreased by 15.38% and 5.52%, respectively. Furthermore, the AMF effect on leaf nutrient stoichiometry was significantly regulated by species, life cycle, and growth habits of host plants. The prominent efficacy of AMF was higher for leaf P in fruit (30.06%), perennial (30.19%), and woody plants (31.6%) than other groups. Moreover, AMF effects on leaf N: P: K stoichiometry of inoculated crops varied depending on the identity of AMF. The Glomeraceae (especially Rhizophagus genera) increased more leaf P content than other AMF families. Thus, the leaf nutrient of host plants significantly increased by AMF inocula, especially leaf P content in the agroecosystem. The effect of AMF on leaf N: P: K stoichiometry was related to plant species, plant life cycle, plant growth habits, and the identity of AMF. These findings highlight the response of AMF to the strategies of nutrient in host plants and provide a theoretical and applicable way for better crop yield and sustainable agriculture.

[1]  Yan Li,et al.  The Effects of Stand Age on Leaf N:P Cannot Be Neglected: A Global Synthesis , 2022, SSRN Electronic Journal.

[2]  M. Chandrasekaran Arbuscular Mycorrhizal Fungi Mediated Enhanced Biomass, Root Morphological Traits and Nutrient Uptake under Drought Stress: A Meta-Analysis , 2022, Journal of fungi.

[3]  Muhammad Zeeshan,et al.  Mycorrhizal symbiosis promotes the nutrient content accumulation and affects the root exudates in maize , 2022, BMC plant biology.

[4]  Xugang Wang,et al.  Arbuscular mycorrhizal fungi increase crop yields by improving biomass under rainfed condition: a meta-analysis , 2022, PeerJ.

[5]  M. Jaizme-Vega,et al.  Mycorrhization of Moringa oleifera improves growth and nutrient accumulation in leaves , 2022, Journal of Plant Nutrition.

[6]  Lei Li,et al.  Effects of short-term nitrogen and phosphorus addition on leaf stoichiometry of a dominant alpine grass , 2021, PeerJ.

[7]  Rakesh Kumar,et al.  Nutrient use efficiency indices of N, P, and K under rice-wheat cropping system in LTFE after 34th crop cycle , 2021, Journal of Plant Nutrition.

[8]  J. Alarcón,et al.  Effect of mixed substrate with different mycorrhizal fungi concentrations on the physiological and productive response of three varieties of tomato , 2021 .

[9]  L. Cui,et al.  Global patterns in leaf stoichiometry across coastal wetlands , 2021 .

[10]  Chen Guo,et al.  Response of ecological stoichiometry and stoichiometric homeostasis in the plant-litter-soil system to re-vegetation type in arid mining subsidence areas , 2021 .

[11]  Huimin Wang,et al.  Foliar, root and rhizospheric soil C:N:P stoichiometries of overstory and understory species in subtropical plantations , 2020 .

[12]  Chunyan Wang,et al.  Effects of Arbuscular Mycorrhizal Fungi on Growth and Physiological Performance of Catalpa bungei C.A.Mey. under Drought Stress , 2020, Forests.

[13]  Zhao-yong Shi,et al.  Leaf Nitrogen and Phosphorus Stoichiometry are Closely Linked with Mycorrhizal Type Traits of Legume Species , 2020, LEGUME RESEARCH - AN INTERNATIONAL JOURNAL.

[14]  X. Lü,et al.  Scaling responses of leaf nutrient stoichiometry to the lakeshore flooding duration gradient across different organizational levels. , 2020, The Science of the total environment.

[15]  Jinchi Zhang,et al.  Comparative physiological mechanisms of arbuscular mycorrhizal fungi in mitigating salt-induced adverse effects on leaves and roots of Zelkova serrata , 2020, Mycorrhiza.

[16]  P. Šmilauer,et al.  Foraging speed and precision of arbuscular mycorrhizal fungi under field conditions: An experimental approach , 2020, Molecular ecology.

[17]  Q. Yan,et al.  Temporal Effects of Thinning on the Leaf C:N:P Stoichiometry of Regenerated Broadleaved Trees in Larch Plantations , 2020, Forests.

[18]  Xuelian Jiang,et al.  Arbuscular Mycorrhizal Fungus Improves Rhizobium–Glycyrrhiza Seedling Symbiosis under Drought Stress , 2019, Agronomy.

[19]  Aleš Látr,et al.  Seed Coating with Arbuscular Mycorrhizal Fungi for Improved Field Production of Chickpea , 2019, Agronomy.

[20]  D. L. Zuluaga,et al.  The Use of Nitrogen and Its Regulation in Cereals: Structural Genes, Transcription Factors, and the Role of miRNAs , 2019, Plants.

[21]  Y. Zou,et al.  Development of propagation technique of indigenous AMF and their inoculation response in citrus , 2019, The Indian Journal of Agricultural Sciences.

[22]  Dongxing Yang,et al.  The soil C:N:P stoichiometry is more sensitive than the leaf C:N:P stoichiometry to nitrogen addition: a four-year nitrogen addition experiment in a Pinus koraiensis plantation , 2019, Plant and Soil.

[23]  G. Durrieu,et al.  Is a mixture of arbuscular mycorrhizal fungi better for plant growth than single-species inoculants? , 2019, Mycorrhiza.

[24]  Jian Sun,et al.  Solar radiation regulates the leaf nitrogen and phosphorus stoichiometry across alpine meadows of the Tibetan Plateau , 2019, Agricultural and Forest Meteorology.

[25]  M. V. D. van der Heijden,et al.  Why farmers should manage the arbuscular mycorrhizal symbiosis. , 2019, The New phytologist.

[26]  M. Quemada,et al.  The cover crop determines the AMF community composition in soil and in roots of maize after a ten-year continuous crop rotation. , 2019, The Science of the total environment.

[27]  M. Iqbal,et al.  Co-Amended Synergistic Interactions between Arbuscular Mycorrhizal Fungi and the Organic Substrate-Induced Cucumber Yield and Fruit Quality Associated with the Regulation of the AM-Fungal Community Structure under Anthropogenic Cultivated Soil , 2019, International journal of molecular sciences.

[28]  N. Ferrol,et al.  Review: Arbuscular mycorrhizas as key players in sustainable plant phosphorus acquisition: An overview on the mechanisms involved. , 2019, Plant science : an international journal of experimental plant biology.

[29]  Jingyun Fang,et al.  Stoichiometric mechanisms of regime shifts in freshwater ecosystem. , 2019, Water research.

[30]  M. Rillig,et al.  Arbuscular mycorrhizal fungi increase grain yields: a meta-analysis. , 2018, The New phytologist.

[31]  P. Bonfante The future has roots in the past: the ideas and scientists that shaped mycorrhizal research. , 2018, The New phytologist.

[32]  J. Graham,et al.  Little evidence that farmers should consider abundance or diversity of arbuscular mycorrhizal fungi when managing crops. , 2018, The New phytologist.

[33]  C. Martino,et al.  Regulation of mycorrhiza development in durum wheat by P fertilization: Effect on plant nitrogen metabolism , 2018 .

[34]  Qiangsheng Wu,et al.  Auxin modulates root-hair growth through its signaling pathway in citrus , 2018, Scientia Horticulturae.

[35]  F. Dijkstra,et al.  Effect of crop rotation on mycorrhizal colonization and wheat yield under different fertilizer treatments , 2017 .

[36]  M. Sindic,et al.  Effects of nitrogen and phosphorus fertilization on fruit yield and quality of cactus pear Opuntia ficus-indica (L.) Mill. , 2017 .

[37]  Mingxiu Long,et al.  Arbuscular mycorrhizal fungi and water availability affect biomass and C:N:P ecological stoichiometry in alfalfa (Medicago sativa L.) during regrowth , 2017, Acta Physiologiae Plantarum.

[38]  N. Garg,et al.  High effectiveness of Rhizophagus irregularis is linked to superior modulation of antioxidant defence mechanisms in Cajanus cajan (L.) Millsp. genotypes grown under salinity stress , 2017, Mycorrhiza.

[39]  D. Sharma,et al.  Effects of arbuscular mycorrhizal fungi (amf) on Camellia sinensis (L.) o. kuntze under greenhouse conditions , 2017 .

[40]  Y. Zou,et al.  Mycorrhizas alter sucrose and proline metabolism in trifoliate orange exposed to drought stress , 2017, Scientific Reports.

[41]  F. Oehl,et al.  Changes in arbuscular mycorrhizal fungal communities along a river delta island in northeastern Brazil. , 2017 .

[42]  Mayumi Kikuta,et al.  Growth and yield responses of upland NERICAs to variable water management under field conditions , 2017 .

[43]  Jason D. Hoeksema,et al.  Taxonomic resolution is a determinant of biodiversity effects in arbuscular mycorrhizal fungal communities , 2017 .

[44]  H. Bücking,et al.  Arbuscular mycorrhizal growth responses are fungal specific but do not differ between soybean genotypes with different phosphate efficiency. , 2016, Annals of botany.

[45]  P. Sale,et al.  The impact of elevated carbon dioxide on the phosphorus nutrition of plants: a review. , 2015, Annals of botany.

[46]  Han Y. H. Chen,et al.  Decoupling of nitrogen and phosphorus in terrestrial plants associated with global changes , 2015 .

[47]  E. F. Abd_Allah,et al.  Enhancing growth performance and systemic acquired resistance of medicinal plant Sesbania sesban (L.) Merr using arbuscular mycorrhizal fungi under salt stress , 2015, Saudi journal of biological sciences.

[48]  Han Y. H. Chen,et al.  Negative effects of fertilization on plant nutrient resorption. , 2015, Ecology.

[49]  N. Johnson,et al.  Uncoupling the effects of phosphorus and precipitation on arbuscular mycorrhizas in the Serengeti , 2015, Plant and Soil.

[50]  S. Kopriva,et al.  Identification and functional characterization of a sulfate transporter induced by both sulfur starvation and mycorrhiza formation in Lotus japonicus. , 2014, The New phytologist.

[51]  Y. Gan,et al.  Spatial and temporal structuring of arbuscular mycorrhizal communities is differentially influenced by abiotic factors and host crop in a semi-arid prairie agroecosystem. , 2014, FEMS microbiology ecology.

[52]  M. Thamrin,et al.  Correlation between nitrogen, phosphorus and potassium leaf nutrient with fruit production of pummelo citrus (Citrus maxima). , 2014 .

[53]  M. Vestberg,et al.  Diversity and abundance of arbuscular mycorrhizal fungi associated with acacia trees from different land use systems in Ethiopia , 2013 .

[54]  J. Elser,et al.  Ecological stoichiometry: An elementary approach using basic principles , 2013 .

[55]  J. Klironomos,et al.  A trait-based framework to understand life history of mycorrhizal fungi. , 2013, Trends in plant science.

[56]  P. Antunes,et al.  Diversity Effects on Productivity Are Stronger within than between Trophic Groups in the Arbuscular Mycorrhizal Symbiosis , 2012, PloS one.

[57]  C. Crisosto,et al.  Fruit Phosphorous and Nitrogen Deficiencies Affect ‘Grand Pearl’ Nectarine Flesh Browning , 2012 .

[58]  J. Graham,et al.  The continuum concept remains a useful framework for studying mycorrhizal functioning , 2012, Plant and Soil.

[59]  A. M. Eissa,et al.  Improved growth of salinity-stressed citrus after inoculation with mycorrhizal fungi , 2011 .

[60]  Stephen Porder,et al.  Relationships among net primary productivity, nutrients and climate in tropical rain forest: a pan-tropical analysis. , 2011, Ecology letters.

[61]  Pramod Kumar,et al.  Screening of AM fungi and Azotobacter chroococcum under natural, solarization, chemical sterilization and moisture conservation practices for commercial mango nursery production in north-west Himalayas , 2011 .

[62]  M. Mardi,et al.  Interactive effects of Arbuscular mycorrhizal fungi and rhizobial strains on chickpea growth and nutrient content in plant , 2011 .

[63]  Daniel Rodriguez,et al.  Modelling the nitrogen-driven trade-off between nitrogen utilisation efficiency and water use efficiency of wheat in eastern Australia , 2010 .

[64]  Wolfgang Viechtbauer,et al.  Conducting Meta-Analyses in R with the metafor Package , 2010 .

[65]  V. Cozzolino,et al.  Effects of arbuscular mycorrhizal inoculation and phosphorus supply on the growth of Lactuca sativa L. and arsenic and phosphorus availability in an arsenic polluted soil under non-sterile conditions , 2010 .

[66]  Jason D. Hoeksema,et al.  A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. , 2010, Ecology letters.

[67]  Heikham Evelin,et al.  Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. , 2009, Annals of botany.

[68]  C. Kaya,et al.  The influence of arbuscular mycorrhizal colonisation on key growth parameters and fruit yield of pepper plants grown at high salinity , 2009 .

[69]  A. Dvořáčková,et al.  Development and activity of Glomus intraradices as affected by co-existence with Glomus claroideum in one root system , 2009, Mycorrhiza.

[70]  J. Jansa,et al.  Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? , 2008, The New phytologist.

[71]  Helmut Hillebrand,et al.  Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. , 2007, Ecology letters.

[72]  J. Klironomos,et al.  Influence of Phylogeny on Fungal Community Assembly and Ecosystem Functioning , 2007, Science.

[73]  R. Koide,et al.  Is plant performance limited by abundance of arbuscular mycorrhizal fungi? A meta-analysis of studies published between 1988 and 2003. , 2005, The New phytologist.

[74]  S. Güsewell N : P ratios in terrestrial plants: variation and functional significance. , 2004, The New phytologist.

[75]  Sean C. Thomas,et al.  The worldwide leaf economics spectrum , 2004, Nature.

[76]  J. C. Dodd,et al.  Mycelium of Arbuscular Mycorrhizal fungi (AMF) from different genera: form, function and detection , 2000, Plant and Soil.

[77]  S. Wright,et al.  Time-course study and partial characterization of a protein on hyphae of arbuscular mycorrhizal fungi during active colonization of roots , 1996, Plant and Soil.

[78]  A. Allaith,et al.  Mechanism of osmotically regulated N-acetylglutaminylglutamine amide production inRhizobium meliloti , 2004, Plant and Soil.

[79]  J. Elser,et al.  Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere , 2002 .

[80]  N. Stavropoulos,et al.  Effect of Verticillium wilt (Verticillium dahliae Kleb.) and mycorrhiza (Glomus mosseae) on root colonization, growth and nutrient uptake in tomato and eggplant seedlings , 2002 .

[81]  M. Hart,et al.  Colonization of roots by arbuscular mycorrhizal fungi using different sources of inoculum , 2002, Mycorrhiza.

[82]  A. Fitter,et al.  Selectivity and functional diversity in arbuscular mycorrhizas of co‐occurring fungi and plants from a temperate deciduous woodland , 2002 .

[83]  M. Hart,et al.  Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi , 2002 .

[84]  R. Azcón,et al.  Symbiotic efficiency and infectivity of an autochthonous arbuscular mycorrhizal Glomus sp. from saline soils and Glomus deserticola under salinity , 2000, Mycorrhiza.

[85]  L. Abbott,et al.  Glomalean mycorrhizal fungi from tropical Australia , 1999, Mycorrhiza.

[86]  G. Berta,et al.  Arbuscular mycorrhizal induced changes to plant growth and root system morphology in Prunus cerasifera. , 1995, Tree physiology.