Contribution of arbuscular mycorrhizal fungi to nitrogen and phosphorus uptake efficiency and productivity of faba bean crop on contrasting cropping systems
DOI:
https://doi.org/10.15835/nbha50312806Keywords:
leaf area index (LAI), nitrogen harvest index (NHI), nitrogen uptake, phosphorus utilization efficiency (PUtE), seed yield, Vicia faba L, weighted mycorrhizal dependency (WMD)Abstract
The present study was focused on evaluating the effect of AMF (Arbuscular Mycorrhizal Fungi) inoculation on nitrogen and phosphorus uptake efficiency and productivity of faba bean (Vicia faba L.) crop, under different fertilization levels on organic or conventional cropping systems. The 2-year field experiment was conducted in central Greece and laid out in a split-plot design, with three replications, two main plots (AMF inoculation treatments) and five sub-plots (fertilization treatments). The results demonstrated that plants of AMF inoculated plots exhibited greater plant height, leaf area index (LAI), leading to higher biomass, and consequently higher final seed yields. Regarding the quality parameters, including nutrients (nitrogen and phosphorus) uptake and their utilization indices, similar results to those of the productivity results were found with the AMF inoculated plants presented the higher values. Finally, all the parameters of the root system, including AMF root colonization and weighted mycorrhizal dependency (WMD), were negatively affected by fertilization level, particularly in an inorganic form. As a conclusion, the current study confirmed that replacement of inorganic inputs by organic in combination with AMF inoculation, should be seriously considered as a sustainable practice of faba bean crop cultivation under Mediterranean conditions.
References
Al-Karaki GN, Hammad R, Rusan M (2001). Response of two tomato cultivars differing in salt tolerance to inoculation with mycorrhizal fungi under salt stress. Mycorrhiza 11:43-47. https://doi.org/10.1007/s005720100098
Amoanimaa-Dede H, Su C, Yeboah A, Zhou H, Zheng D, Zhu H (2022). Growth regulators promote soybean productivity: a review. PeerJ 10:e12556. https://doi.org/10.7717/peerj.12556
Barrett G, Campbell CD, Fitter AH, Hodge A (2011) The arbuscular mycorrhizal fungus Glomus hoi can capture and transfer nitrogen from organic patches to its associated host plant at low temperature. Applied Soil Ecology 48:102-105. https://doi.org/10.1016/j.apsoil.2011.02.002
Barrett G, Campbell CD, Hodge A (2014). The direct response of the external mycelium of arbuscular mycorrhizal fungi to temperature and the implications for nutrient transfer. Soil Biology and Biochemistry 78:109-117. https://doi.org/10.1016/j.soilbio.2014.07.025
Begum N, Qin C, Ahanger MA, Raza S, Khan MI, Ashraf M, Ahmed N, Zhang L (2019). Role of arbuscular mycorrhizal fungi in plant growth regulation: Implications in abiotic stress tolerance. Frontiers in Plant Science 10:1068. https://doi.org/10.3389/fpls.2019.01068
Beslemes D, Tigka E, Vlachostergios D, Bilalis D (2016). Contribution of arbuscular mycorrhiza to productivity of barley on contrasting cropping systems, in Central Greece. Bulletin UASVM Agriculture 73(1):15-21. https://doi.org/10.15835/buasvmcn-agr:11818
Bi Y, Zhou H (2021). Changes in peanut canopy structure and photosynthetic characteristics induced by an arbuscular mycorrhizal fungus in a nutrient-poor environment. Scientific Reports 11(1):14832. https://doi.org/10.1038/s41598-021-94092-w
Bilalis D, Karkanis A, Sidiras N, Travlos I, Efthimiadou A, Thomopoulos P, Kakabouki I (2012). Maize and legumes root growth and yield as influenced by organic fertilization, under Mediterranean environmental conditions. Romanian Agricultural Research 29:211-217.
Biro B, Koves-Pechy K, Voros I, Takacs T, Eggenberg P, Strasser RJ (2000). Interrelations between Azospirillum and Rhizobium nitrogen-fixers and arbuscular mycorrhizal fungi in the rhizosphere of alfalfa at sterile, AMF-free or normal soil conditions. Applied Soil Ecology 15:159-168. https://doi.org/10.1016/S0929-1393(00)00092-5
Bulman P, Smith DL (1994). Post-heading nitrogen uptake, retranslocation, and partitioning in spring barley. Crop Science 34:977-984. https://doi.org/10.2135/cropsci1994.0011183X003400040028x
Cho EJ, Lee DJ, Wee CD, Kim HL, Cheong YH, Cho JS, Sohn BK (2009). Effects of AMF inoculation on growth of Panax ginseng C.A. Meyer seedlings and on soil structures in mycorrhizosphere. Scientia Horticulturae 122(4):633-637. https://doi.org/10.1016/j.scienta.2009.06.025
Clark RB, Zeto SK (2000). Mineral acquisition by arbuscular mycorrhizal plants. Journal of Plant Nutrition 23: 867-902. https://doi.org/10.1080/01904160009382068
Daur I, Sepetoğlu H, Sindel B (2011). Dynamics of faba bean growth and nutrient uptake and their correlation with grain yield. Journal of Plant Nutrition 34(9):1360-1371. https://doi.org/10.1080/01904167.2011.580878
Engels C, Marschner H (1995). Plant uptake and utilization of nitrogen. In: Bacon PE (Ed). Nitrogen fertilization in the Environment. Marcel Dekker Inc., New York, USA pp 41-81.
Estaún V, Camprubí A, Joner EJ (2002). Selecting arbuscular mycorrhizal fungi for field application. In: Gianinazzi S, Schüepp H, Barea JM, Haselwandter K (Eds). Mycorrhizal technology in agriculture. Birkhäuser Verlag, Basel, Switzerland. https://doi.org/10.1007/978-3-0348-8117-3_20
Etesami H, Jeong BR, Glick BR (2021). Contribution of arbuscular mycorrhizal fungi, phosphate–solubilizing bacteria, and silicon to P uptake by plant. Frontiers in Plant Science 12:699618. https://doi.org/10.3389/fpls.2021.699618
Evans J (1983). Nitrogen and photosynthesis in the flag leaf of wheat (Triticum aestivum L.). Plant Physiology 72:297-302.
Fageria NK, Baligar VC (2005). Enhancing nitrogen use efficiency in crop plants. Advances in Agronomy 88:97-185. https://doi.org/10.1016/S0065-2113(05)88004-6
Feddermann N, Finlay R, Boller T, Elfstrand M (2010). Functional diversity in arbuscular mycorrhiza – the role of gene expression, phosphorous nutrition and symbiotic efficiency. Fungal Ecology 3:1-8. https://doi.org/10.1016/j.funeco.2009.07.003
Felföldi Z, Vidican R, Stoian V, Roman IA, Sestras AF, Rusu T, Sestras RE (2022). Arbuscular mycorrhizal fungi and fertilization influence yield, growth and root colonization of different tomato genotype. Plants 11:1743. https://doi.org/10.3390/plants11131743
Feng G, Li X, Zhang F, Li S (2000). Effect of AM fungi on water and nutrition status of corn plants under salt stress. Chinese Journal of Applied Ecology 11:595-598.
Gallais A, Hirel B (2004). An approach to the genetics of nitrogen use efficiency in maize. Journal of Experimental Botany 55:295-306. https://doi.org/10.1093/jxb/erh006
Galleguillos C, Aguirre C, Barea JM, Azcon R (2000). Growth promoting effect of two Sinorhizobium meliloti strains (a wild type and its genetically modified derivative) on a non-legume plant species in specific interaction with two arbuscular mycorrhizal fungi. Plant Science 159:57-63. https://doi.org/10.1016/S0168-9452(00)00321-6
Galvez L, Douds DD, Drinkwater LE, Wagoner P (2001). Effect of tillage and farming system upon VAM fungus populations and mycorrhizas and nutrient uptake of maize. Plant and Soil 118:299-308. https://doi.org/10.1023/A:1004810116854
Gao X, Guo H, Zhang Q, Guo H, Zhang L, Zhang C, …, Zeng F (2020). Arbuscular mycorrhizal fungi (AMF) enhanced the growth, yield, fiber quality and phosphorus regulation in upland cotton (Gossypium hirsutum L.). Scientific Reports 10:2084. https://doi.org/10.1038/s41598-020-59180-3
Gavito ME, Varela L (1995). Response of “criollo” maize to single and mixed-species inocula of arbuscular mycorrhizal fungi. Plant and Soil 176:101-105. https://doi.org/10.1007/BF00017680
Giovannetti M, Mosse B (1980). An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytologist 84:489-500. https://doi.org/10.1111/j.1469-8137.1980.tb04556.x
Golubkina NA, Amagova Z, Matsadze V, Zamana S, Tallarita A, Caruso G (2020). Effects of arbuscular mycorrhizal fungi on yield, biochemical characteristics, and elemental composition of garlic and onion under selenium supply. Plants 9:84. https://doi.org/10.3390/plants9010084
Gosling P, Hodge A, Goodlass G, Bending GD (2006). Arbuscular mycorrhizal fungi and organic farming. Agriculture, Ecosystems and Environment 113:17-35. https://doi.org/10.1016/j.agee.2005.09.009
Govindarajulu M, Pfeffer PE, Jin H, Abubaker J, Douds DD, Allen JW, … Shachar‐Hill Y (2005). Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819-823 https://doi.org/10.1038/nature03610
Hodge A, Campbell CD, Fitter AH (2001). An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413:297-299. https://doi.org/10.1038/35095041
Huber DM, Watson RD (1974). Nitrogen form and plant disease. Annual Review of Phytopathology 12:139-165. https://doi.org/10.1146/annurev.py.12.090174.001035
Ibibijen J, Urquiaga S, Ismaili M, Alves BJ, Boddey RM (1996). Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition and nitrogen fixation of three varieties of common beans (Phaseolus vulgaris). New Phytologist 134:353-360. https://doi.org/10.1111/j.1469-8137.1996.tb04640.x
Jadhav DN, Patil MS (1996). Effect of AM inoculation on growth and NPK uptake of groundnut. Acta Agronomica Hungarica 44:153-159.
Jin L, Wang Q, Wang Q, Wang XJ, Gange AC (2017). Mycorrhizal-induced growth depression in plants. Symbiosis 72:81-88. https://doi.org/10.1007/s13199-016-0444-5
Joner EJ, Jakobsen I (1995). Growth and extracellular phosphatase activity of arbuscular mycorrhizal hyphae as influenced by soil organic matter. Soil Biology and Biochemistry 27:1153-1159. https://doi.org/10.1016/0038-0717(95)00047-I
Kahiluoto H, Ketoja E, Vestberg M (2009). Contribution of arbuscular mycorrhiza to soil quality in contrasting cropping systems. Agriculture, Ecosystems and Environment 134:36-45. https://doi.org/10.1016/j.agee.2009.05.016
Kahiluoto H, Ketoja E, Vestberg M, Saarela I (2001). Promotion of AM utilization through reduced P fertilization. 2. Field studies. Plant and Soil 231:65-79. https://doi.org/10.1023/A:1010366400009
Kakabouki IP, Roussis I, Hela D, Papastylianou P, Folina A, Bilalis D (2019). Root growth dynamics and productivity of quinoa (Chenopodium quinoa Willd.) in response to fertilization and soil tillage. Folia Horticulturae 31(2):277-291. https://doi.org/10.2478/fhort-2019-0023
Karandashov V, Bucher M (2005). Symbiotic phosphate transport in arbuscular mycorrhizas. Trends in Plant Science 10:22-29. https://doi.org/10.1016/j.tplants.2004.12.003
Karkanis A, Ntatsi G, Lepse L, Fernández JA, Vågen IM, Rewald B, Alsiņa I, …, Savvas D (2018). Faba bean cultivation – Revealing novel managing practices for more sustainable and competitive European cropping systems. Frontiers in Plant Science 9:111. https://doi.org/10.3389/fpls.2018.01115
Keselman HJ, Rogan JC (1977). The Tukey multiple comparison test: 1953–1976. Psychological Bulletin 84:1050-1056.
Kogelmann WJ, Lin HS, Bryant RB, Beege DB, Wolf AM, Petersen GW (2004). A statewide assessment of the impacts of phosphorus- index implementation in Pennsylvania. Journal of Soil and Water Conservation 59:9-18.
Koide R (1991). Nutrient supply, nutrient demand and plant-response to mycorrhizal infection. New Phytologist 117:365-386. https://doi.org/10.1111/j.1469-8137.1991.tb00001.x
Koide RT, Mosse B (2004). A history of research on arbuscular mycorrhiza. Mycorrhiza 14:145-163. https://doi.org/10.1007/s00572-004-0307-4
Kormanik PP, McGraw AC (1982). Quantification of vesicular-arbuscular mycorrhizae in plant roots. In: Schenck NC (Ed), Methods and principles of mycorrhizal research. American Phytopathological Society, St. Paul, Minnesota, USA pp 37-45.
Leigh J, Hodge A, Fitter AH (2009). Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytologist 181:199-207. https://doi.org/10.1111/j.1469-8137.2008.02630.x
Lekberg Y, Koide RT (2005). Is plant performance limited by abundance of arbuscular mycorrhizal fungi? a meta-analysis of studies published between 1988 and 2003. New Phytologist 168:189-204. https://doi.org/10.1111/j.1469-8137.2005.01490.x
Lemaire G, Gastal F (1997). N uptake and distribution in plant canopies. In: Lemaire G (Ed). Diagnosis of the nitrogen status in crops. Springer-Verlag, Heidelberg, Germany pp 3-43.
Liang J, An J, Gao J, Zhang X, Song M, Yu F (2019). Interactive effects of biochar and AMF on plant growth and greenhouse gas emissions from wetland microcosms. Geoderma 346:11-17. https://doi.org/10.1016/j.geoderma.2019.03.033
Liu L, Li J, Yue F, Yan X, Wang F, Bloszies S, Wang Y (2018). Effects of arbuscular mycorrhizal inoculation and biochar amendment on maize growth, cadmium uptake and soil cadmium speciation in Cd-contaminated soil. Chemosphere 194:495-503. https://doi.org/10.1016/j.chemosphere.2017.12.025
Liu YJ, Shi GX, Mao L, Cheng G, Jiang SJ, Ma XJ, …, Feng HY (2012). Direct and indirect influences of 8 yr of nitrogen and phosphorus fertilization on Glomeromycota in an alpine meadow ecosystem. New Phytologist 194:523-535. https://doi.org/10.1111/j.1469-8137.2012.04050.x
Lopez-Bellido RJ, Lopez-Bellido L, Benitez-Vega J, Lopez-Bellido FJ (2007). Tillage system, preceding crop and nitrogen fertilizer in wheat crop: water utilization. Agronomy Journal 99: 66-72. https://doi.org/10.2134/agronj2006.0026
Manoharan L, Rosenstock NP, Williams A, Hedlund K (2017). Agricultural management practices influence AMF diversity and community composition with cascading effects on plant productivity. Applied Soil Ecology 115:53-59. https://doi.org/10.1016/j.apsoil.2017.03.012
Matson PA, Parton WJ, Power AG, Swift MJ (1997). Agricultural intensification and ecosystem properties. Science 277:504-509. https://doi.org/10.1126/science.277.5325.504
Maxclaux C, Quilleré I, Gallais A, Hirel B (2001). The challenge of remobilisation in plant nitrogen economy. A survey of physioagronomic and molecular approaches. Annals of Applied Biology 138:69-81. https://doi.org/10.1111/j.1744-7348.2001.tb00086.x
McSwiney CP, Robertson GP (2005). Nonlinear response of N2O flux to incremental fertilizer addition in a continuous maize (Zea mays L.) cropping system. Global Change Biology 11:1712-1719. https://doi.org/10.1111/j.1365-2486.2005.01040.x
Menéndez AB, Scervino JM, Godeas AM (2001). Arbucular mycorrhizal populations associated with natural and cultivated vegetation on a site of Buenos Aires province, Argentina. Biology and Fertility of Soils 33:373-381. https://doi.org/10.1007/s003740000336
Miransari M (2011). Interactions between arbuscular mycorrhizal fungi and soil bacteria. Applied Microbiology and Biotechnology 89:917-930. https://doi.org/10.1007/s00253-010-3004-6
Muchow RC, Davis R (1988). Effect of nitrogen supply on the comparative productivity of maize and sorghum in a semi-arid tropical environment II. Radiation interception and biomass accumulation. Field Crops Research 18:17-30. https://doi.org/10.1016/0378-4290(88)90056-1
Nell M, Wawrosch C, Steinkellner S, Vierheilig H, Kopp B, Lössl A (2010). Root colonization by symbiotic arbuscular mycorrhizal fungi increases sesquiterpenic acid concentrations in Valeriana officinalis L. Planta Medica 76:393-398. https://doi/org/10.1055/s-0029-1186180
Papastylianou P, Vlachostergios DN, Dordas C, Tigka E, Papakaloudis P, Kargiotidou A, …, Kostoula S (2021) Genotype x environment interaction analysis of faba bean (Vicia faba L.) for biomass and seed yield across different environments. Sustainability 13:2586. https://doi.org/10.3390/su13052586
Paustian K, Robertson GP, Elliott ET (1995). Management impacts on carbon storage and gas fluxes (CO2, CH4) in mid‐latitude cropland ecosystems. In: Lal R, Kimble J, Levine E, Stewart BA (Eds). Soil management and greenhouse effect. CRC Press, Florida, USA pp 69-84.
Pellegrino E, Öpik M, Bonari E, Ercoli L (2015). Responses of wheat to arbuscular mycorrhizal fungi: a meta-analysis of field studies from 1975 to 2013. Soil Biology and Biochemistry 84:210-217. https://doi.org/10.1016/j.soilbio.2015.02.020
Plenchette C, Fortm JA, Furlan V (1983). Growth response of several plant species to mycorrhizae in a soil of moderate P fertility. I. Mycorrhizal dependency under field conditions. Plant and Soil 70:199-209. https://doi.org/10.1007/BF02374780
Rueden CT, Schindelin J, Hiner MC, Dezonia BE, Walter AE, Arena ET, Eliceiri KW (2017). ImageJ2: ImageJ for the next generation of scientific image data. BMC Bioinformatics 18:529. https://doi.org/10.1186/s12859-017-1934-z
Qiao X, Bei S, Li C, Dong Y, Li H, Christie P, Zhang F, Zhang J (2015). Enhancement of faba bean competitive ability by arbuscular mycorrhizal fungi is highly correlated with dynamic nutrient acquisition by competing wheat. Scientific Reports 5:8122. https://doi.org/10.1038/srep08122
Ryan MH, Graham JH (2002). Is there a role for arbuscular mycorrhizal fungi in production agriculture? Plant and Soil 244:263-271. https://doi.org/10.1023/A:1020207631893
Sainz MJ, Taboada-Castro MT, Vilarino A (1998). Growth, mineral nutrition and mycorrhizal colonization of red clover and cucumber plants grown in a soil amended with composted urban wastes. Plant and Soil 205:85-92. https://doi.org/10.1023/A:1004357330318
Sbrana C, Avio L, Giovannetti M (2014). Beneficial mycorrhizal symbionts affecting the production of health-promoting phytochemicals. Electrophoresis 35:1535-1546. https://doi.org/10.1002/elps.201300568
Scheublin TR, Ridgway KP, Young JPW, van der Heijden MGA (2004). Nonlegumes, legumes, and root nodules harbor different arbuscular mycorrhizal fungal communities. Applied and Environmental Microbiology 70:6240-6246. https://doi.org/10.1128/aem.70.10.6240-6246.2004
Schussler A, Schwarzott D, Walker C (2001). A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycological Research 105:1413-1421. https://doi.org/10.1017/S0953756201005196
Schweiger PF, Jakobsen I (1999). The role of mycorrhizas in plant P nutrition: Fungal uptake kinetics and genotype variation. In: Gissel-Nielsen G, Jensen A (Eds). Plant nutrition – molecular biology and genetics. Kluwer, Dordrecht, The Netherlands pp 277-289.
Sellami MH, Lavini A, Calandrelli D, De Mastro G, Pulvento C (2021). Evaluation of genotype, environment, and management interactions on fava beans under Mediterranean field conditions. Agronomy 11:1088. https://doi.org/10.3390/agronomy11061088
Smith FA, Smith SE (2011). Mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annual Review of Plant Biology 62: 227-250. https://doi.org/10.1146/annurev-arplant-042110-103846
Sorensen N, Larsen J, Jakobsen I (2005). Mycorrhiza formation and nutrient concentration in leeks (Allium porrum) in relation to previous crop and cover crop management on high P soils. Plant and Soil 273:101-114. https://doi.org/10.1007/s11104-004-6960-8
Steel RGD, Torrie JH, Dickey D (1980). Principles and procedures of statistics: A biometrical approach. McGraw Hill (3rd ed), New York, NY, USA.
Trisilawati O, Hartoyo B, Bermawie N, Pribadi ER (2019). Application of AMF (Arbuscular Mycorrhizal Fungi) and organic fertilizer to increase the growth, biomass and bioactive content of Centella. IOP Conference Series: Earth and Environmental Science 292:012067. https://doi.org/10.1088/1755-1315/292/1/012067
United States Department of Agriculture (USDA) (2010). Natural Resources Conservation Service. Soil Survey Staff, Keys to Soil Taxonomy. United States Department of Agriculture, Natural Resources Conservation Service (11th ed), Washington, DC, USA.
Vazquez MM, Barera JM, Azcon R (2002). Influence of arbuscular mycorrhizae and a genetically modified strain of Sinorhizobium on growth, nitrate reductase activity and protein content in shoots and roots of Medicago sativa as affected by nitrogen concentrations. Soil Biology and Biochemistry 34:899-905. https://doi.org/10.1016/S0038-0717(01)00230-9
Veresoglou SD, Chen B, Rillig MC (2012). Arbuscular mycorrhiza and soil nitrogen cycling. Soil Biology and Biochemistry 46:53-62. https://doi.org/10.1016/j.soilbio.2011.11.018
Vosatka M, Dodd JC (2002). Ecological considerations for successful application of arbuscular mycorrhizal fungi inoculum. In: Gianinazzi S, Schüepp H, Barea JM, Haselwandter K (Eds). Mycorrhizal technology in agriculture. Birkhäuser Verlag, Basel, Switzerland. https://doi.org/10.1007/978-3-0348-8117-3_19
Yang HS, Zhang Q, Dai YJ, Liu Q, Tang JJ, Bian XM, Chen X (2015). Effects of arbuscular mycorrhizal fungi on plant growth depend on root system: A meta-analysis. Plant and Soil 389:361-374. https://doi.org/10.1007/s11104-014-2370-8
Ye Q, Zhang H, Wei H, Zhang Y, Wang B, Xia K, Huo Z, Dai Q, Xu K (2007). Effects of nitrogen fertilizer on nitrogen use efficiency and yield of rice under different soil conditions. Frontiers of Agriculture in China 1:30-36. https://doi.org/10.1007/s11703-007-0005-z
Zhu C, Ling N, Guo J, Wang M, Guo S, Shen Q (2016) Impacts of fertilization regimes on arbuscular mycorrhizal fungal (AMF) community composition were correlated with organic matter composition in maize rhizosphere soil. Frontiers in Microbiology 7:1840. https://doi.org/10.3389/fmicb.2016.01840
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