Abstract
From plantations to farms, food safety is a major concern in food industry, particularly for perishable foods like onions. New environment friendly methods like the use of beneficial microbes and organic amendments became requirements to provide long-lasting alternatives. In this study, the impact of the direct use of olive mill wastewater (OMW) and native arbuscular mycorrhizal fungi (AMF) consortium on soil characteristics and onion plant (Allium cepa) growth and physiological responses as a mean to enhance soil quality and onion yield, was investigated. Two doses of OMW (4 and 8 L m−2) were directly applied once in a field experiment, one month after onion plantation. Soil characteristics and growth and physiological variables of onion were evaluated to assess the OMW impact and AMF on them. Among the measured variables, soil levels of phosphorus (Sp), leaf phosphorus (Lp), bulb phosphorus (Bp) and soil total organic carbon (TOC) were the manifestly improved traits with an increase of 108 to 409% for Sp, 60–102% for Lp, 39–74% for Bp and 50–139% for TOC. On the other hand, AMF colonization showed a decrease ranging from 23 to 50% under OMW treatments. In addition, the application of OMW and AMF improved the growth performances including the bulb weight, physiological (stomatal conductance and photosynthetic machinery) and biochemical (sugar, proteins and antioxidant enzymes activity) traits compared to the control. These findings highlight the importance of AMF and OMW, in improving onion agro-physiological, biochemical traits as well as soil characteristics under filed conditions.
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Ait Rahou Y, Ait-El-Mokhtar M, Anli M et al (2021) Use of mycorrhizal fungi and compost for improving the growth and yield of tomato and its resistance to Verticillium dahliae. Arch Phytopathol Plant Prot 54:665–690. https://doi.org/10.1080/03235408.2020.1854938
Ait-El-Mokhtar M, Baslam M, Ben-Laouane R et al (2020) Alleviation of detrimental effects of salt stress on date palm (Phoenix dactylifera L.) by the application of arbuscular mycorrhizal fungi and/or compost. Front Sustain Food Syst 4:131. https://doi.org/10.3389/fsufs.2020.00131
Aktas ES, Imre S, Ersoy L (2001) Characterization and lime treatment of olive mill wastewater. Water Res 35:2336–2340. https://doi.org/10.1016/S0043-1354(00)00490-5
Anli M, Baslam M, Tahiri A et al (2020) Biofertilizers as strategies to improve photosynthetic apparatus, growth, and drought stress tolerance in the date palm. Front Plant Sci 11:516818. https://doi.org/10.3389/fpls.2020.516818
Anli M, Symanczik S, El Abbassi A et al (2021) Use of arbuscular mycorrhizal fungus Rhizoglomus irregulare and compost to improve growth and physiological responses of Phoenix dactylifera ‘Boufgouss. Plant Biosyst 155:763–771. https://doi.org/10.1080/11263504.2020.1779848
Anli M, Boutasknit A, Ait-El-Mokhtar M et al (2022) Improving lettuce yield and quality of an agricultural soil using a combination of arbuscular mycorrhizal fungus and phosphate-green wastes compost. Gesunde Pflanz 74:205–217. https://doi.org/10.1007/s10343-021-00603-0
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15. https://doi.org/10.1104/pp.24.1.1
Audette Y, Smith DS, Parsons CT et al (2020) Phosphorus binding to soil organic matter via ternary complexes with calcium. Chemosphere 260:127624. https://doi.org/10.1016/j.chemosphere.2020.127624
Badawi MA (2020) Saving 45 % of irrigation water saving of date palm tree plantations using soil amendments in UAE. J Mater Sci Res Rev 6:31–44
Barbera AC, Maucieri C, Cavallaro V et al (2013) Effects of spreading olive mill wastewater on soil properties and crops, a review. Agric Water Manag 119:43–53. https://doi.org/10.1016/j.agwat.2012.12.009
Bargougui L, Guergueb Z, Chaieb M et al (2019) Agro-physiological and biochemical responses of Sorghum bicolor in soil amended by olive mill wastewater. Agric Water Manag 212:60–67. https://doi.org/10.1016/j.agwat.2018.08.011
Begum N, Ahanger MA, Zhang L (2020) AMF inoculation and phosphorus supplementation alleviates drought induced growth and photosynthetic decline in Nicotiana tabacum by up-regulating antioxidant metabolism and osmolyte accumulation. Environ Exp Bot 176:104088. https://doi.org/10.1016/j.envexpbot.2020.104088
Ben-Laouane R, Baslam M, Ait-El-mokhtar M et al (2020) Potential of native arbuscular mycorrhizal fungi, rhizobia, and/or green compost as alfalfa (Medicago sativa) enhancers under salinity. Microorganisms 8:1695. https://doi.org/10.3390/microorganisms8111695
Ben-Laouane R, Ait-El-Mokhtar M, Anli M et al (2021) Green compost combined with mycorrhizae and rhizobia: a strategy for improving alfalfa growth and yield under field conditions. Gesunde Pflanz 73:193–207. https://doi.org/10.1007/s10343-020-00537-z
Bendaly Labaied M, Khiari L, Gallichand J et al (2020) Nutrient diagnosis norms for date palm (Phoenix dactylifera L.) in Tunisian Oases. Agronomy 10:886. https://doi.org/10.3390/agronomy10060886
Boutaj H, Boutasknit A, Elhaissoufi W et al (2020) Olive mill wastewater spreading improves growth, physiological and biochemical traits of Phaseolus vulgaris. Desalination Water Treat 185:87–98. https://doi.org/10.5004/dwt.2020.25423
Boutasknit A, Ait-Rahou Y, Anli M et al (2021) Improvement of garlic growth, physiology, biochemical traits, and soil fertility by Rhizophagus irregularis and compost. Gesunde Pflanz 73:149–160. https://doi.org/10.1007/s10343-020-00533-3
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Caruso C, Maucieri C, Cavallaro V et al (2018) Olive mill wastewater spreading and AMF inoculation effects in a low-input semi-arid Mediterranean crop succession. Arch Agron Soil Sci 64:2060–2074. https://doi.org/10.1080/03650340.2018.1476970
Chang W, Sui X, Fan XX et al (2018) Arbuscular mycorrhizal symbiosis modulates antioxidant response and ion distribution in salt-stressed Elaeagnus angustifolia seedlings. Front Microbiol 9:652. https://doi.org/10.3389/fmicb.2018.00652
D’Annibale A, Casa R, Pieruccetti F et al (2004) Lentinula edodes removes phenols from olive-mill wastewater: Impact on durum wheat (Triticum durum Desf.) germinability. Chemosphere 54:887–894. https://doi.org/10.1016/j.chemosphere.2003.10.010
Di Bene C, Pellegrino E, Debolini M et al (2013) Short- and long-term effects of olive mill wastewater land spreading on soil chemical and biological properties. Soil Biol Biochem 56:21–30. https://doi.org/10.1016/j.soilbio.2012.02.019
Djouhou FMC, Nwaga D, Fokou E (2019) Comparative effect of arbuscular mycorrhizal fungi and biostimulants on the antioxidant and nutritional potential of Moringa oleifera. Nutr Food Sci Int J 9:1–6. https://doi.org/10.19080/NFSIJ.2019.09.555758
Doula MK, Kavvadias V, Elaiopoulos K (2013) Proposed soil indicators for olive mill waste (OMW) disposal areas. Water Air Soil Pollut 224:1–11. https://doi.org/10.1007/s11270-013-1621-2
Drais MI, Pannucci E, Caracciolo R et al (2021) Antifungal activity of hydroxytyrosol enriched extracts from olive mill waste against Verticillium dahliae, the cause of Verticillium wilt of olive. Phytopathol Mediterr 60:139–147. https://doi.org/10.36253/phyto-12019
Dubois M, Gilles KA, Hamilton JK et al (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356. https://doi.org/10.1021/ac60111a017
Feria LA (2000) The generated situation by the OMW in Andalusia. In: Actas/proceedings-workshop improlive-2000-anexo A, vol 1, pp 55–63
Gałązka A, Niedźwiecki J, Grządziel J, Gawryjołek K (2020) Evaluation of changes in Glomalin-Related Soil Proteins (GRSP) content, microbial diversity and physical properties depending on the type of soil as the important biotic determinants of soil quality. Agronomy 10:1279. https://doi.org/10.3390/agronomy10091279
Gerdemann JW, Nicolson TH (1963) Spores of mycorrhizal endogone species extracted from soil by wet sieving and decanting. Trans Br Mycol Soc 46:235–244. https://doi.org/10.1016/s0007-1536(63)80079-0
Hanifi S, El Hadrami I (2008) Phytotoxicity and fertilising potential of olive mill wastewaters for maize cultivation. Agron Sustain Dev 28:313–319. https://doi.org/10.1051/agro:2007047
Hori K, Wada A, Shibuta T (1997) Changes in phenoloxidase activities of the galls on leaves of Ulmus davidana formed by Tetraneura fusiformis (Homoptera: Eriosomatidae). Appl Entomol Zool 32:365–371. https://doi.org/10.1303/aez.32.365
Ji L, Tan W, Chen X (2019) Arbuscular mycorrhizal mycelial networks and glomalin-related soil protein increase soil aggregation in Calcaric Regosol under well-watered and drought stress conditions. Soil Tillage Res 185:1–8. https://doi.org/10.1016/j.still.2018.08.010
Karbout N, Mlih R, Latifa D et al (2021) Farm manure and bentonite clay amendments enhance the date palm morphology and yield. Arab J Geosci 14:818. https://doi.org/10.1007/s12517-021-07160-w
Karpouzas DG, Ntougias S, Iskidou E et al (2010) Olive mill wastewater affects the structure of soil bacterial communities. Appl Soil Ecol 45:101–111. https://doi.org/10.1016/j.apsoil.2010.03.002
Khalil J, Habib H, Alabboud M, Mohammed S (2021) Olive mill wastewater effects on durum wheat crop attributes and soil microbial activities: a pilot study in Syria. Energy Ecol Environ 6:469–477. https://doi.org/10.1007/s40974-021-00209-2
Lahbouki S, Anli M, El Gabardi S et al (2021) Evaluation of arbuscular mycorrhizal fungi and vermicompost supplementation on growth, phenolic content and antioxidant activity of prickly pear cactus (Opuntia ficus-indica). Plant Biosyst. https://doi.org/10.1080/11263504.2021.1947408
Mechri B, Cheheb H, Boussadia O et al (2011) Effects of agronomic application of olive mill wastewater in a field of olive trees on carbohydrate profiles, chlorophyll a fluorescence and mineral nutrient content. Environ Exp Bot 71:184–191. https://doi.org/10.1016/j.envexpbot.2010.12.004
Meddich A, Jaiti F, Bourzik W et al (2015) Use of mycorrhizal fungi as a strategy for improving the drought tolerance in date palm (Phoenix dactylifera). Sci Hortic 192:468–474. https://doi.org/10.1016/j.scienta.2015.06.024
Mekki A, Dhouib A, Aloui F, Sayadi S (2006) Olive wastewater as an ecological fertiliser. Agron Sustain Dev 26:61–67. https://doi.org/10.1051/agro:2005061
Mekki A, Dhouib A, Feki F, Sayadi S (2008) Assessment of toxicity of the untreated and treated olive mill wastewaters and soil irrigated by using microbiotests. Ecotoxicol Environ Saf 69:488–495. https://doi.org/10.1016/j.ecoenv.2007.04.008
Mekki A, Dhouib A, Sayadi S (2009) Evolution of several soil properties following amendment with olive mill wastewater. Prog Nat Sci 19:1515–1521. https://doi.org/10.1016/j.pnsc.2009.04.014
Mekki A, Dhouib A, Sayadi S (2013) Review: effects of olive mill wastewater application on soil properties and plants growth. Int J Recycl Org Waste Agric 2:1–7. https://doi.org/10.1186/2251-7715-2-15
Mitra D, Rad KV, Chaudhary P et al (2021) Involvement of strigolactone hormone in root development, influence and interaction with mycorrhizal fungi in plant: mini-review. Curr Res Microb Sci 2:100026. https://doi.org/10.1016/j.crmicr.2021.100026
Mohawesh O, Al-Hamaiedeh H, Albalasmeh A et al (2019) Effect of Olive Mill Wastewater (OMW) Application on soil properties and wheat growth performance under rain-fed conditions. Water Air Soil Pollut. https://doi.org/10.1007/s11270-019-4208-8
Morton JB, Benny GL (1990) Revised classification of arbuscular mycorrhizal fungi (Zygomycetes): a new order, Glomales, two new suborders, Glomineae and Gigasporineae, and two new families, Acaulosporaceae and Gigasporaceae, with an emendation of Glomaceae. Mycotaxon 37:471–491. https://doi.org/10.1016/0163-6383(95)90009-8
Mukerji KG (1996) Taxonomy of endomycorrhizal fungi: in advances in botany. APH Pub Crop, New Delhi https://doi.org/10.24875/GMM.18004115
Nelson DW, Sommers LE (1996) Total carbon, organic carbon, and organic matter. In: Methods of soil analysis, part 3: chemical methods, soil scien, pp 961–1010
Olsen S, Sommers L (1982) Methods of soil analysis. Part 2. Chemical and microbiological properties of phosphorus. ASA Monograp 9:403–430
Olsen SR, Cole CV, Watandbe F, Dean L (1954) Estimation of available phosphorus in soil by extraction with sodium bicarbonate. Phys Sci Basis. https://doi.org/10.1017/CBO9781107415324.004
Peña D, Fernández D, Albarrán A et al (2022) Using olive mill waste compost with sprinkler irrigation as a strategy to achieve sustainable rice crop** under Mediterranean conditions. Agron Sustain Dev 42:36. https://doi.org/10.1007/s13593-022-00769-5
Perez Y, Schenck NC (1990) A unique code for each species of VA mycorrhizal fungi. Mycologia 82:256. https://doi.org/10.2307/3759855
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. https://doi.org/10.1016/S0007-1536(70)80110-3
Plenchette C, Furlan V, Fortin JA (1982) Effects of different endomycorrhizal fungi on Fine host plants grown on calcined Montmorillonite clay. J Am Soc Hortic Sci 107:535–538. https://doi.org/10.1037/xan0000227
Rajhi H, Sanz JL, Abichou M et al (2021) The impact of different techniques of soil management on soil fertility and the associated bacterial communities in semi-arid olive tree fields. J Soil Sci Plant Nutr 21:547–558. https://doi.org/10.1007/s42729-020-00382-z
Redecker D, Schüßler A, Stockinger H et al (2013) An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza 23:515–531. https://doi.org/10.1007/s00572-013-0486-y
Ren AT, Zhu Y, Chen YL et al (2019) Arbuscular mycorrhizal fungus alters root-sourced signal (abscisic acid) for better drought acclimation in Zea mays L. seedlings. Environ Exp Bot 167:103824. https://doi.org/10.1016/j.envexpbot.2019.103824
Rillig MC, Aguilar-Trigueros CA, Bergmann J et al (2015) Plant root and mycorrhizal fungal traits for understanding soil aggregation. New Phytol 205:1385–1388. https://doi.org/10.1111/nph.13045
Rouphael Y, Lucini L, Miras-moreno B et al (2020) Metabolomic responses of maize shoots and roots elicited by combinatorial seed treatments with microbial and non-microbial biostimulants. Front Microbiol 11:644. https://doi.org/10.3389/fmicb.2020.00664
de los Santos B, Brenes M, García P et al (2019) Effect of table olive wastewaters on growth and yield of cucumber, pepper, tomato and strawberry. Sci Hortic 256:108644. https://doi.org/10.1016/j.scienta.2019.108644
Šarapatka B, Alvarado-Solano DP, Čižmár D (2019) Can glomalin content be used as an indicator for erosion damage to soil and related changes in organic matter characteristics and nutrients? CATENA 181:104078. https://doi.org/10.1016/j.catena.2019.104078
Sciubba F, Chronopoulou L, Pizzichini D et al (2020) Olive mill wastes: a source of bioactive molecules for plant growth and protection against pathogens. Biology 9:1–20. https://doi.org/10.3390/biology9120450
Sempiterno CM, Dias JCS (2004) Effects of the application of olive oil wastewater on soil pH during eight weeks [Portugal]. Rev Cienc Agrar 25:374–338
Souilem S, El-Abbassi A, Kiai H et al (2017) Olive oil production sector: olive oil production sector: environmental effects and sustainability challenges. In: Galankis CM (ed) Olive mill waste. Academic P, In, pp 1–28
Strullu DG, Grellier B, Marciniak D, Letouze R (1986) Micropropagation of chestnut and conditions of mycorrhizal syntheses in vitro. New Phytol 102:95–101
Symanczik S, Krützmann J, Nehls U et al (2020) Expression of major intrinsic protein genes in Sorghum bicolor roots under water deficit depends on arbuscular mycorrhizal fungal species. Soil Biol Biochem 140:107643. https://doi.org/10.1016/j.soilbio.2019.107643
Talaat NB, Shawky BT (2014) Protective effects of arbuscular mycorrhizal fungi on wheat (Triticum aestivum L.) plants exposed to salinity. Environ Exp Bot 98:20–31. https://doi.org/10.1016/j.envexpbot.2013.10.005
Toubali S, Tahiri A, Anli M et al (2020) Physiological and biochemical behaviors of date palm vitroplants treated with microbial consortia and compost in response to salt stress. Appl Sci 10:8665. https://doi.org/10.3390/app10238665
Tubeileh A, Abdeen M (2017) Effect of one-Time olive-mill waste water application on yield and water relations of olive trees. Acta Hortic 1150:303–306. https://doi.org/10.17660/ActaHortic.2017.1150.42
Walker C, Mize CW, McNabb HS (1982) Populations of endogonaceous fungi at two locations in central Iowa. Can J Bot 60:2518–2529. https://doi.org/10.1139/b82-305
Wright SF, Upadhyaya A (1998) A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi. Plant Soil 198:97–107. https://doi.org/10.1023/A:1004347701584
Yang Y, He C, Huang L et al (2017) The effects of arbuscular mycorrhizal fungi on glomalin-related soil protein distribution, aggregate stability and their relationships with soil properties at different soil depths in lead-zinc contaminated area. PLoS ONE 12:1–19. https://doi.org/10.1371/journal.pone.0182264
Yangui T, Rhouma A, Gargouri K et al (2008) Efficacy of olive mill waste water and its derivatives in the suppression of crown gall disease of bitter almond. Eur J Plant Pathol 122:495–504. https://doi.org/10.1007/s10658-008-9317-y
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This work was supported by the Socially Responsible Projects, Cadi Ayyad University UCAM/RSU 2018 Marrakech, Morocco and Mixed laboratory Morocco-Tunisia, laboratory of Plant Physiology and Biotechnology and Climate Change (LR11ES09).
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M. Anli, A. Fakhech, A. Boutasknit, M. Ait-El-Mokhtar, R. Ben-Laoaune, Y. Ait-Rahou and A. Meddich declare that they have no competing interests.
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Anli, M., Fakhech, A., Boutasknit, A. et al. Comparing the Response of Growth and Physiologic Variables of Onion to Olive Mill Wastewater Application and Arbuscular Mycorrhizal Fungi Inoculation. Gesunde Pflanzen 75, 655–666 (2023). https://doi.org/10.1007/s10343-022-00731-1
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DOI: https://doi.org/10.1007/s10343-022-00731-1