Can Arbuscular Mycorrhizal Fungi Enhance Crop Productivity and Quality in Hydroponics? A Meta-Analysis
Abstract
:1. Introduction
2. AMF and Hydroponics Culture
3. Does the Plant Consistently Exhibit a Positive Response to AMF Inoculation in Hydroponic Systems?
4. Potential Use of AMF in Hydroponic Culture
5. The Percentage of AMF Root Colonization over Time within Hydroponic Systems
6. How to Enhance AMF Activity in Hydroponic Systems?
6.1. Phosphorus Level in Nutrient Solution
6.2. Static vs. Dynamic Hydroponic System
6.3. Effects of Aeration, Substrate Type, pH, and Inoculation Frequency on Mycorrhizal Colonization
7. Conclusions
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Raymond, F.; Pierre, E.; Souleymanou, A.; Therese, N.O.; Fabrice, F.B.; Dieudonne, N. Arbuscular mycorrhizal fungi symbiosis and food security. In Unravelling Plant-Microbe Synergy; Chandra, D., Bhatt, P., Eds.; Academic Press: Cambridge, MA, USA, 2023; pp. 227–244. [Google Scholar]
- Tzortzakis, N.; Massa, D.; Vandecasteele, B. The tripartite of soilless systems, growing media, and plants through an Intensive Crop Production Scheme. Agronomy 2022, 12, 1896. [Google Scholar] [CrossRef]
- Fussy, A.; Papenbrock, J. An Overview of Soil and Soilless Cultivation Techniques—Chances, Challenges and the Neglected Question of Sustainability. Plants 2022, 1, 1153. [Google Scholar] [CrossRef]
- Shrestha, A.; Dunn, B. Hydroponics. Oklahoma Cooperative Extension Fact Sheets, HLA-6442. 2017. Available online: https://extension.okstate.edu/fact-sheets/print-publications/hla/hydroponics-hla-6442.pdf (accessed on 9 April 2024).
- MMRP. Hydroponics Market by Type (Aggregate Systems, Liquid Systems), Crop Type (Vegetables, Fruits, Flowers), Equipment (HVAC, LED Grow Lights, Irrigation Systems, Material Handling Equipment, Control Systems), Input Type, and Region—Global Forecast to 2026. Available online: https://www.marketsandmarkets.com/Market-Reports/hydroponic-market-94055021.html (accessed on 9 April 2024).
- Tüzel, Y.; Gül, A.; Tüzel, I.; Öztekin, G. Different soilless culture systems and their management. J. Agric. Environ. Sci. 2019, 73, 7–12. [Google Scholar] [CrossRef]
- Azizoglu, U.; Yilmaz, N.; Simsek, O.; Ibal, J.; Tagele, S.; Shin, J. The fate of plant growth-promoting rhizobacteria in soilless agriculture: Future perspectives. 3 Biotech 2021, 11, 382. [Google Scholar] [CrossRef]
- Dasgan, H.Y.; Aldiyab, A.; Elgudayem, F.; Ikiz, B.; Gruda, N.S. Effect of biofertilizers on leaf yield, nitrate amount, mineral content and antioxidants of basil (Ocimum basilicum L.) in a floating culture. Sci. Rep. 2022, 12, 20917. [Google Scholar] [CrossRef]
- Othman, Y.; Tahat, M.; Alananbeh, K.; Al-Ajlouni, M. Arbuscular mycorrhizal fungi inoculation improves flower yield and postharvest quality component of gerbera grown under different salinity levels. Agriculture 2022, 12, 978. [Google Scholar] [CrossRef]
- Utkhede, R. Increased growth and yield of hydroponically grown greenhouse tomato plants inoculated with arbuscular mycorrhizal fungi and Fusarium oxysporum f. sp. radicis-lycopersici. Biocontrol 2006, 51, 393–400. [Google Scholar] [CrossRef]
- Martinez-Garcia, L.; Garcia, K.; Hammer, E.; Vayssières, A. Mycorrhiza for all: An under-earth revolution. New Phytol. 2013, 198, 652–655. [Google Scholar] [CrossRef]
- Sudheer, S.; Johny, L.; Srivastava, S.; Adholeya, A. The trade-in-trade: Multifunctionalities, current market and challenges for arbuscular mycorrhizal fungal inoculants. Symbiosis 2023, 89, 259–272. [Google Scholar] [CrossRef]
- Cano, C.; Bago, A. Aseptic Mycorrhization Inoculant and In Vitro and Ex Vitro Application Methods. WO/2007/014974, 8 February 2007. Available online: https://patentimages.storage.googleapis.com/5e/63/28/a40078860f75e6/WO2007014974A1.pdf (accessed on 9 April 2024).
- Ijdo, M.; Cranenbrouck, S.; Declerck, S. Methods for large-scale production of AM fungi: Past, present, and future. Mycorrhiza 2011, 21, 1–16. [Google Scholar] [CrossRef]
- Sylvia, D.; Jarstfer, A. Sheared Roots as a VA-Mycorrhizal Inoculum and Methods for Enhancing Growth. U.S. Patent No. 5096481, 17 March 1992. Available online: https://patentimages.storage.googleapis.com/e2/f3/94/a39f2da36be624/US5096481.pdf (accessed on 9 April 2024).
- MIO. Mycorrhiza-Based Biofertilizer Market Growth Trends and Forecast (2020–2025). Mordor Intelligence Organization. 2020. Available online: https://www.mordorintelligence.com/industry-reports/mycorrhiza-based-biofertilizer-market (accessed on 9 April 2024).
- Dasgan, H.Y.; Kacmaz, S.; Arpaci, B.B.; Ikiz, B.; Gruda, N.S. Biofertilizers improve the leaf quality of hydroponically grown baby spinach (Spinacia oleracea L.). Agronomy 2023, 13, 575. [Google Scholar] [CrossRef]
- Dasgan, H.Y.; Yilmaz, M.; Dere, S.; Ikiz, B.; Gruda, N.S. Bio-fertilizers reduced the need for mineral fertilizers in soilless-grown Capia pepper. Horticulturae 2023, 9, 188. [Google Scholar] [CrossRef]
- Amaranthus, M.; Eagan, J. Do mycorrhizae have a role in hydroponics? Urban. Gard. Mag. 2009, 8, 72–79. [Google Scholar]
- Cela, F.; Avio, L.; Giordani, T.; Vangelisti, A.; Cavallini, A.; Turrini, A.; Sbrana, C.; Pardossi, A.; Incrocci, L. Arbuscular mycorrhizal fungi increase nutritional quality of soilless grown lettuce while overcoming low phosphorus supply. Foods 2022, 11, 3612. [Google Scholar] [CrossRef]
- Saouy, M.; Pengchai, P.; Choonluchanon, S. Development of arbuscular mycorrhizal spore production in hydroponic culture on leaf lettuce (Lactuca sativar var crispa L.). Chiang Mai Univ. J. Nat. Sci. 2011, 10, 147–158. [Google Scholar]
- Lee, Y.; George, E. Development of a nutrient film technique culture system for arbuscular mycorrhizal plants. HortScience 2005, 40, 378–380. [Google Scholar] [CrossRef]
- Oseni, T.O.; Shongwe, N.; Masarirambi, M. Effect of arbuscular mycorrhiza (AM) inoculation on the performance of tomato nursery seedlings in vermiculite. Int. J. Agric. Biol. 2010, 12, 789–792. [Google Scholar]
- Akiyama, K. Chemical identification and functional analysis of apocarotenoids involved in the development of arbuscular mycorrhizal symbiosis. Biosci. Biotechnol. Biochem. 2007, 71, 1405–1414. [Google Scholar] [CrossRef]
- Smith, S.; Read, D. Mycorrhizal Symbiosis, 3rd ed.; Elsevier Ltd.: Amsterdam, The Netherlands, 2008; pp. 1–9. [Google Scholar]
- Das, D.; Torabi, S.; Chapman, P.; Gutjahr, C.A. Flexible, low-cost hydroponic co-cultivation system for studying arbuscular mycorrhiza symbiosis. Front. Plant Sci. 2020, 11, 63. [Google Scholar] [CrossRef]
- Smith, S.; Smith, F. Roles of arbuscular mycorrhizas in plant nutrition and growth: New paradigms from cellular to ecosystem scales. Annu. Rev. Plant Biol. 2011, 62, 227–250. [Google Scholar] [CrossRef] [PubMed]
- Spanu, P.; Panstruga, R. Editorial, Biotrophic Plant-Microbe Interactions. Front. Plant Sci. 2017, 8, 192. [Google Scholar] [CrossRef]
- Gutjahr, C.; Parniske, M. Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annu. Rev. Cell Dev. Biol. 2013, 29, 593–617. [Google Scholar] [CrossRef]
- Wu, Q.; Srivastava, A.; Zou, Y.; Malhotra, S. Mycorrhizas in citrus: Beyond soil fertility and plant nutrition. Ind. J. Agric. Sci. 2017, 87, 427–443. [Google Scholar] [CrossRef]
- Rask, K.; Johansen, J.; Kjøller, R.; Ekelund, F. Differences in arbuscular mycorrhizal colonization influence cadmium uptake in plants. Environ. Exp. Bot. 2019, 162, 223–229. [Google Scholar] [CrossRef]
- Al-Karaki, G.; Othman, Y.; Al-Ajmi, A. Effects of mycorrhizal fungi inoculation on landscape turf establishment under Arabian Gulf region conditions. Arab. Gulf J. Sci. Res. 2007, 25, 147–152. [Google Scholar]
- Liu, X.; Xie, M.; Hashem, A.; Abd-Allah, E.; Wu, Q. Arbuscular mycorrhizal fungi and rhizobia synergistically promote root colonization, plant growth, and nitrogen acquisition. Plant Growth Regul. 2023, 100, 691–701. [Google Scholar] [CrossRef]
- Tahat, M.; Alananbeh, K.; Othman, Y.; Leskovar, D. Soil health and sustainable agriculture. Sustainability 2020, 12, 4859. [Google Scholar] [CrossRef]
- Robinson, B.L.; Feng, W.; Gulbis, N.; Hajdu, K.; Harrison, R.; Jeffries, P.; Xu, X. The use of arbuscular mycorrhizal fungi to improve strawberry production in coir substrate. Front. Plant Sci. 2016, 7, 1237. [Google Scholar] [CrossRef]
- Hung, L.; Sylvia, D. Production of vesicular–arbuscular mycorrhizal fungus inoculum in aeroponic culture. Appl. Environ. Microbiol. 1988, 54, 353–357. [Google Scholar] [CrossRef]
- Miller, S.; Sharitz, R. Manipulation of flooding and arbuscular mycorrhiza formation influences growth and nutrition of two semiaquatic grass species. Funct. Ecol. 2000, 14, 738–748. [Google Scholar] [CrossRef]
- Sembok, W.; Kassim, N.; Hamzah, Y.; Rahman, Z. Effects of mycorrhizal inoculation on growth and quality f Roselle (Hibiscus sabdariffa L. ) grown in soilless culture system. Malays. Appl. Bio. 2015, 44, 57–62. [Google Scholar]
- Íkiz, Ö.; Abak, K.; Daşgan, H.Y.; Ortaş, I. Effects of mycorrhizal inoculation in soilless culture on pepper plant growth. Acta Hortic. 2009, 807, 533–540. [Google Scholar] [CrossRef]
- Besmer, Y.; Koide, R. Effect of mycorrhizal colonization and phosphorus on ethylene production by snapdragon (Antirrhinum majus L.) flowers. Mycorrhiza 1999, 9, 161–166. [Google Scholar] [CrossRef]
- Dugassa, D.; Grunewaldt-Stöcker, G.; Schönbeck, F. Growth of Glomus intraradices and its effect on linseed (Linum usitatissimum L.) in hydroponic culture. Mycorrhiza 1995, 5, 279–282. [Google Scholar]
- Jarstfer, A.; Farmer-Koppenol, S.; Sylvia, D. Tissue magnesium and calcium affect arbuscular mycorrhiza development and fungal reproduction. Mycorrhiza 1988, 7, 237–342. [Google Scholar] [CrossRef]
- Bitterlich, M.; Franken, P.; Graefe, J. Atmospheric drought and low light impede mycorrhizal effects on leaf photosynthesis-a glasshouse study on tomato under naturally fluctuating environmental conditions. Mycorrhiza 2019, 29, 13–28. [Google Scholar] [CrossRef]
- Hayek, S.; Grosch, R.; Gianinazzi-Pearson, V.; Franken, P. Bio-protection and alternative fertilization of petunia using mycorrhiza in a soilless production system. Agron. Sustain. Dev. 2012, 32, 765–771. [Google Scholar] [CrossRef]
- Cekic, C.; Yilmaz, E. Effect of arbuscular mycorrhiza and different doses of phosphor on vegetative and generative components of strawberries applied with different phosphor doses in soilless culture. Afr. J. Agric. Res. 2011, 6, 4736–4739. [Google Scholar]
- Palencia, P.; Martínez, F.; Pestana, M.; Oliveira, J.; Correia, P. Effect of Bacillus velezensis and Glomus intraradices on fruit quality and growth parameters in strawberry soilless growing system. Hortic. J. 2015, 84, 122–130. [Google Scholar] [CrossRef]
- Dasgan, H.; Kusvuran, S.; Ortas, I. Responses of soilless grown tomato plants to arbuscular mycorrhizal fungal (Glomus fasciculatum) colonization in re-cycling and open systems. Afr. J. Biotechnol. 2008, 7, 3606–3613. [Google Scholar]
- Bhowmik, S.; Yadav, G.; Datta, M. Rapid mass multiplication of Glomus mosseae inoculum as influenced by some biotic and abiotic factors. Bangladesh, J. Bot. 2015, 44, 209–214. [Google Scholar] [CrossRef]
- Cecatto, A.; Ruiz, F.; Calvete, E.; Martínez, J.; Palencia, P. Mycorrhizal inoculation affects the phytochemical content in strawberry fruits. Acta Sci. 2016, 38, 227–237. [Google Scholar] [CrossRef]
- Elmes, R.P.; Mosse, B. Vesicular-arbuscular endomycorrhizal inoculum production. II. Experiments with maize (Zea mays) and other hosts in nutrient flow culture. Can. J. Bot. 1984, 62, 1531–1536. [Google Scholar] [CrossRef]
- Eltrop, L.; Marschner, H. Growth and mineral nutrition of nonmycorrhizal and mycorrhizal Norway spruce (Picea abies) seedlings grown in semi-hydroponic sand culture, II. Carbon partitioning in plants supplied with ammonium or nitrate. New Phytol. 1996, 133, 479–486. [Google Scholar] [CrossRef]
- Gryndler, M.; Hršelová, H.; Sudová, R.; Gryndlerová, H.; Řezáčová, V.; Merhautová, V. Hyphal growth and mycorrhiza formation by the arbuscular mycorrhizal fungus Glomus claroideum BEG 23 is stimulated by humic substances. Mycorrhiza 2005, 15, 483–488. [Google Scholar] [CrossRef]
- Hawkins, H.; George, E. Hydroponic culture of the mycorrhizal fungus Glomus mosseae with Linum usitatissimum L., Sorghum bicolor L. and Triticum aestivum L. Plant Soil 1997, 196, 143–149. [Google Scholar] [CrossRef]
- Hawkins, H.; Cramer, M.; George, E. Root respiratory quotient and nitrate uptake in hydroponically grown non-mycorrhizal and mycorrhizal wheat. Mycorrhiza 1999, 9, 57–60. [Google Scholar] [CrossRef]
- Kowalska, I.; Konieczny, A.; Gąstoł, M. Effect of mycorrhiza and the phosphorus content in a nutrient solution on the yield and nutritional status of lettuce grown on various substrates. J. Elem. 2015, 20, 631–642. [Google Scholar] [CrossRef]
- Maboko, M.; Bertling, I.; Plooy, C. Arbuscular mycorrhiza has limited effects on yield and quality of tomatoes grown under soilless cultivation. Acta Agric. Scand. B Soil Plant Sci. 2013, 63, 261–270. [Google Scholar] [CrossRef]
- Medeiros, C.; Clark, R.B.; Ellis, J.R. Growth and nutrient uptake of sorghum cultivated with vesicular-arbuscular mycorrhiza isolates at varying pH. Mycorrhiza 1994, 4, 185–191. [Google Scholar] [CrossRef]
- Mosse, B.; Thompson, J. Vesicular-arbuscular endomycorrhizal inoculum production. I. Exploratory experiments with beans (Phaseolus vu1gnris) in nutrient flow culture. Can. J. Bot. 1983, 62, 1523–1530. [Google Scholar] [CrossRef]
- Nurbaity, A.; Istifadah, N.; Haryantini, B.; Ilhami, M.; Habibullah, M.; Arifin, M. Optimization of hydroponic technology for production of mycorrhiza biofertilizer. IOP Conf. Ser. Environ. Earth Sci. 2019, 347, 012017. [Google Scholar] [CrossRef]
- Ojala, J.; Jarrell, M. Hydroponic sand culture systems for mycorrhizal research. Plant Soil 1980, 57, 297–303. [Google Scholar] [CrossRef]
- Oztekin, G.; Tuzel, Y.; Tuzel, H. Does mycorrhiza improve salinity tolerance in grafted plants? Sci. Hortic. 2013, 149, 55–60. [Google Scholar] [CrossRef]
- Selvakumar, G.; Kim, K.; Walitang, D.; Chanratana, M.; Kang, Y.; Chung, B.; Sa, T. Trap culture technique for propagation of arbuscular mycorrhizal fungi using different host plants. Korean J. Soil Sci. Fert. 2016, 49, 608–613. [Google Scholar] [CrossRef]
- Selvakumar, G.; Shagol, C.; Kang, Y.; Chung, B.N.; Han, S.G.; Sa, T. Arbuscular mycorrhizal fungi spore propagation using single spore as starter inoculum and a plant host. J. Appl. Microbiol. 2018, 124, 1556–1565. [Google Scholar] [CrossRef]
- Tajini, F.; Suriyakup, P.; Vailhe, H.; Jansa, J.; Drevon, J. Assess suitability of hydroaeroponic culture to establish tripartite symbiosis between different AMF species, beans, and rhizobia. BMC Plant Biol. 2009, 9, 73. [Google Scholar] [CrossRef] [PubMed]
- White, J.; Charvat, I. The mycorrhizal status of an emergent aquatic, Lythrum salicaria L., at different levels of phosphorus availability. Mycorrhiza 1999, 9, 191–197. [Google Scholar] [CrossRef]
- Zou, Y.; Wu, Q. Sodium chloride stress induced changes in leaf osmotic adjustment of trifoliate orange (Poncirus trifoliata) seedlings inoculated with mycorrhizal fungi. Not. Bot. Horti Agrobot. Cluj-Napoca 2011, 39, 64–69. [Google Scholar] [CrossRef]
- Al-Karaki, G. Benefit-cost and water-use efficiency of arbuscular mycorrhizal durum wheat grown under drought stress. Mycorrhiza 1998, 8, 41–45. [Google Scholar] [CrossRef]
- Al-Karaki, G. Growth of mycorrhizal tomato and mineral acquisition under salt stress. Mycorrhiza 2000, 10, 51–54. [Google Scholar] [CrossRef]
- Al-Karaki, G. Nursery inoculation of tomato with arbuscular mycorrhizal fungi and subsequent performance under irrigation with saline water. Sci. Hortic. 2006, 109, 1–7. [Google Scholar] [CrossRef]
- Arruda, B.; Herrera, W.; Rojas-García, J.; Turner, C.; Pavinato, P. Cover crop species and mycorrhizal colonization on soil phosphorus dynamics. Rhizosphere 2021, 19, 100396. [Google Scholar] [CrossRef]
- Beltrano, J.; Ronco, M. Improved tolerance of wheat plants (Triticum aestivum L.) to drought stress and rewatering by the arbuscular mycorrhizal fungus Glomus claroideum: Effect on growth and cell membrane stability. Braz. J. Plant Physiol. 2008, 20, 29–37. [Google Scholar] [CrossRef]
- Betancur-Agudelo, M.; Meyer, E.; Lovato, P. Arbuscular mycorrhizal fungus richness in the soil and root colonization in vineyards of different ages. Rhizosphere 2021, 17, 100307. [Google Scholar] [CrossRef]
- Chandrasekeran, A.; Mahalingam, P. Diversity of arbuscular mycorrhizae fungi from orchard ecosystem. J. Plant Pathol. Microbiol. 2014, 5, 2. [Google Scholar] [CrossRef]
- Chenchouni, H.; Mekahlia, M.; Beddiar, A. Effect of inoculation with native and commercial arbuscular mycorrhizal fungi on growth and mycorrhizal colonization of olive (Olea europaea L.). Sci. Hortic. 2020, 261, 108969. [Google Scholar] [CrossRef]
- Chiomento, J.; De Nardi, F.; Filippi, D.; Trentin, T.; Dornelles, A.; Fornari, M.; Nienow, A.; Calvete, E. Morpho-horticultural performance of strawberry cultivated on substrate with arbuscular mycorrhizal fungi and biochar. , Sci. Hortic. 2021, 282, 110053. [Google Scholar] [CrossRef]
- Ding, Y.; Fan, Q.; He, J.; Wu, H.; Zou, Y.; Wu, Q.; Kuča, K. Effects of mycorrhizas on physiological performance and root TIPs expression in trifoliate orange under salt stress. Arch. Agron. Soil Sci. 2020, 66, 182–192. [Google Scholar] [CrossRef]
- Hart, M.; Ehret, D.L.; Krumbein, A.; Leung, C.; Murch, S.; Turi, C.; Franken, P. Inoculation with arbuscular mycorrhizal fungi improves the nutritional value of tomatoes. Mycorrhiza 2015, 25, 359–376. [Google Scholar] [CrossRef]
- Hashem, A.; Akhter, A.; Alqarawi, A.; Singh, G.; Almutairi, K.; Abd_Allah, E. Mycorrhizal fungi induced activation of tomato defense system mitigates Fusarium wilt stress. Saudi J. Biol. Sci. 2021, 28, 5442–5450. [Google Scholar] [CrossRef] [PubMed]
- Hu, J.; Li, M.; Liu, H.; Zhao, Q.; Lin, X. Intercropping with sweet corn (Zea mays L. var. Rugosa Bonaf.) expands P acquisition channels of chili pepper (Capsicum annuum L.) via arbuscular mycorrhizal hyphal networks. J. Soils Sediments 2019, 19, 1632–1639. [Google Scholar] [CrossRef]
- Huang, Y.; Srivastava, A.; Zou, Y.; Ni, Q.; Han, Y.; Wu, Q. Mycorrhizal-induced calmodulin mediated changes in antioxidant enzymes and growth response of drought-stressed trifoliate orange. Front. Microbiol. 2014, 5, 682. [Google Scholar] [CrossRef] [PubMed]
- Keller-Pearson, M.; Liu, Y.; Peterson, A.; Pederson, K.; Willems, L.; Ané, J.; Silva, E. Inoculation with arbuscular mycorrhizal fungi has a more significant positive impact on the growth of open-pollinated heirloom varieties of carrots than on hybrid cultivars under organic management conditions. Agric. Ecosyst. Environ. 2020, 289, 106712. [Google Scholar] [CrossRef]
- Khalil, H.; Eissa, A.; El-Shazly, S.; Aboul-Nasr, A. Improved growth of salinity-stressed citrus after inoculation with mycorrhizal fungi. Sci. Hortic. 2011, 130, 624–632. [Google Scholar] [CrossRef]
- Leventis, G.; Tsiknia, M.; Feka, M.; Ladikou, E.V.; Papadakis, I.E.; Chatzipavlidis, I.; Papadopoulou, K.; Ehaliotis, C. Arbuscular mycorrhizal fungi enhance growth of tomato under normal and drought conditions, via different water regulation mechanisms. Rhizosphere 2021, 19, 100394. [Google Scholar] [CrossRef]
- Mason, P.; Ibrahim, K.; Ingleby, K.; Munro, R.; Wilson, J. Mycorrhizal development and growth of inoculated Eucalyptus globulus (Labill.) seedlings in wet and dry conditions in the glasshouse. For. Ecol. Manag. 2000, 128, 269–277. [Google Scholar] [CrossRef]
- Mathur, N.; Singh, J.; Bohra, S.; Bohra, A.; Vyas, A. Arbuscular mycorrhizal fungi alleviate salt stress of Trichosanthes dioica Roxb. Acta Agric. Scand. B Soil Plant Sci. 2010, 60, 510–516. [Google Scholar]
- Naseer, M.; Zhu, Y.; Li, F.; Yang, Y.; Wang, S.; Xiong, Y. Nano-enabled improvements of growth and colonization rate in wheat inoculated with arbuscular mycorrhizal fungi. Environ. Pollut. 2022, 295, 118724. [Google Scholar] [CrossRef] [PubMed]
- Navarro, J.M.; Pérez-Tornero, O.; Morte, A. Alleviation of salt stress in citrus seedlings inoculated with arbuscular mycorrhizal fungi depends on the rootstock salt tolerance. J. Plant Physiol. 2014, 171, 76–85. [Google Scholar] [CrossRef]
- Ngo, H.; Watts-Williams, S.; Cavagnaro, T. Mycorrhizal growth and phosphorus responses of tomato differ with source but not application rate of phosphorus fertilizers. Appl. Soil Ecol. 2021, 166, 104089. [Google Scholar] [CrossRef]
- Ngwene, B.; Gabriel, E.; George, E. Influence of different mineral nitrogen sources (NO3−-N vs. NH4+-N) on arbuscular mycorrhiza development and N transfer in a Glomus intraradices–cowpea symbiosis. Mycorrhiza 2013, 23, 107–117. [Google Scholar] [CrossRef]
- Ruscitti, M.; Arango, M.; Beltrano, J. Improvement of copper stress tolerance in pepper plants (Capsicum annuum L.) by inoculation with arbuscular mycorrhizal fungi. Theor. Exp. Plant Physiol. 2017, 29, 37–49. [Google Scholar] [CrossRef]
- Saif, S. The influence of soil aeration on the efficiency of vesicular-arbuscular mycorrhizae II. Effect of soil oxygen on growth and mineral uptake in Eupatorium odoratum L., Sorghum bicolor (L.) Moench and Guizotia abyssinica (L.f.) Cass. inoculated with vesicular-arbuscular mycorrhizal fungi. New Phytol. 1983, 95, 405–417. [Google Scholar]
- Schubert, R.; Werner, S.; Cirka, H.; Rödel, P.; Tandron, M.Y.; Mock, H.-P.; Hutter, I.; Kunze, G.; Hause, B. Effects of arbuscular mycorrhization on fruit quality in industrialized tomato production. Int. J. Mol. Sci. 2020, 21, 7029. [Google Scholar] [CrossRef]
- Sensoy, S.; Demir, S.; Turkmen, O.; Erdinc, C.; Savur, O. Responses of some different pepper (Capsicum annuum L.) genotypes to inoculation with two different arbuscular mycorrhizal fungi. Sci. Hortic. 2007, 113, 92–95. [Google Scholar] [CrossRef]
- Singh, A.; Thakur, A.; Sharma, S.; Gill, P.; Kalia, A. Bio-inoculants enhance growth, nutrient uptake, and buddability of citrus plants under protected nursery condition. Commun. Soil Sci. Plant Anal. 2018, 49, 2571–2586. [Google Scholar] [CrossRef]
- Vani, M.S.; Hindumathi, A.; Reddy, B.N. Beneficial effect of arbuscular mycorrhizal fungus, Glomus fasciculatum on plant growth and nutrient uptake in tomato. Indian. Phytopathol. 2018, 71, 115–122. [Google Scholar] [CrossRef]
- Vázquez, E.; Benito, M.; Espejo, R.; Teutscherova, N. No-tillage and liming increase the root mycorrhizal colonization, plant biomass and N content of a mixed oat and vetch crop. Soil Tillage Res. 2020, 200, 104623. [Google Scholar] [CrossRef]
- Wang, H.; An, T.; Huang, D.; Liu, R.; Xu, B.; Zhang, S.; Deng, X.; Siddique, K.; Chen, Y. Arbuscular mycorrhizal symbioses alleviating salt stress in maize is associated with a decline in root-to-leaf gradient of Na+/K+ ratio. BMC Plant Biol. 2021, 21, 457. [Google Scholar] [CrossRef]
- Wilson, G.; Hartnett, D. Interspecific variation in plant responses to mycorrhizal colonization in tallgrass prairie. Am. J. Bot. 1998, 85, 1732–1738. [Google Scholar] [CrossRef]
- Wu, Q.S.; Zou, Y.N.; He, X.H. Contributions of arbuscular mycorrhizal fungi to growth, photosynthesis, root morphology and ionic balance of citrus seedlings under salt stress. Acta Physiol. Plant. 2010, 32, 297–304. [Google Scholar] [CrossRef]
- Wu, Q.S.; Zou, Y.N.; Liu, W.; Ye, X.F.; Zai, H.F.; Zhao, L.J. Alleviation of salt stress in citrus seedlings inoculated with mycorrhiza: Changes in leaf antioxidant defense systems. Plant Soil Environ. 2010, 56, 470–475. [Google Scholar] [CrossRef]
- Wu, Q.; Zou, Y.; He, X. Mycorrhizal symbiosis enhances tolerance to NaCl stress through selective absorption but not selective transport of K+ over Na+ in trifoliate orange. Scient. Horticul. 2013, 160, 366–374. [Google Scholar] [CrossRef]
- Ziane, H.; Hamza, N.; Meddad-Hamza, A. Arbuscular mycorrhizal fungi and fertilization rates optimize tomato (Solanum lycopersicum L.) growth and yield in a Mediterranean agroecosystem. J. Saudi Soc. Agricul. Sci. 2021, 20, 454–458. [Google Scholar] [CrossRef]
- Shaik, A.; Singh, S. Influence of arbuscular mycorrhizal fungi on physiology and yield of eggplant in organic soilless production system. HortScience 2022, 57, 759–768. [Google Scholar] [CrossRef]
- Haghighi, M.; Mohmmadnia, S.; Pessarakli, M. Effects of mycorrhiza colonization on growth, root exudates, antioxidant activity and photosynthesis trait of cucumber grown in Johnson modified nutrient solution. J. Plant Nutr. 2016, 39, 2079–2091. [Google Scholar] [CrossRef]
- Caser, M.; Demasi, S.; Victorino, Í.M.M.; Donno, D.; Faccio, A.; Lumini, E.; Bianciotto, V.; Scariot, V. Arbuscular mycorrhizal fungi modulate the crop performance and metabolic profile of saffron in soilless cultivation. Agronomy 2019, 9, 232. [Google Scholar] [CrossRef]
- Dere, S.; Coban, A.; Akhoundnejad, Y.; Ozsoy, S.; Dasgan, H. Use of mycorrhiza to reduce mineral fertilizers in soilless melon (Cucumis melo L.) cultivation. Not. Bot. Horti Agrobot. Cluj-Napoca 2019, 47, 1331–1336. [Google Scholar] [CrossRef]
- Roussis, I.; Beslemes, D.; Kosma, C.; Triantafyllidis, V.; Zotos, A.; Tigka, E.; Mavroeidis, A.; Karydogianni, S.; Kouneli, V.; Travlos, I.; et al. The Influence of arbuscular mycorrhizal fungus Rhizophagus irregularis on the growth and quality of processing tomato (Lycopersicon esculentum Mill.) seedlings. Sustainability 2022, 14, 9001. [Google Scholar] [CrossRef]
- Cardoso, D.S.C.P.; Martinez, H.E.P.; de Abreu, J.A.A.; Kasuya, M.C.M.; Sediyama, M.A.N. Growth-promoting fungi and potassium doses affects productivity and nutrition of cherry-type tomatoes. J. Plant Nutr. 2023, 46, 835–851. [Google Scholar] [CrossRef]
- Michałojć, Z.; Jarosz, Z.; Pitura, K.; Dzida, K. Effect of mycorrhizal colonization and nutrient solutions concentration on the yielding and chemical composition of tomato grown in rockwool and straw medium. Acta Sci. Pol. Hortorum Cultus 2015, 14, 15–27. [Google Scholar]
- Haghighi, M.; Mozafariyan, M.; Abdolahipour, B. Effect of cucumber mycorrhiza inoculation under low and high root temperature grown on hydroponic conditions. J. Crop Sci. Biotech. 2015, 18, 89–96. [Google Scholar] [CrossRef]
- Fakhro, A.; Andrade-Linares, D.; Bargen, S.; Bandte, M.; Büttner, C.; Grosch, R.; Schwarz, D.; Franken, P. Impact of Piriformospora indica on tomato growth and on interaction with fungal and viral pathogens. Mycorrhiza 2010, 20, 191–200. [Google Scholar] [CrossRef] [PubMed]
- Ghaderi, K.; Nazarideljou, M. Morpho-physiological and quality attributes of gerbera (Gerbera jamesonii) cut flower under inoculated substrate with arbuscular mycorrhizal fungi in soilless system. J. Sci. Technol. 2017, 8, 27–39. [Google Scholar] [CrossRef]
- Dasgan, H.Y.; Cetinturk, T.; Altuntas, O. The effects of biofertilizers on soilless organically grown greenhouse tomato. Acta Hortic. 2017, 1164, 555–561. [Google Scholar] [CrossRef]
- Ullah, F.; Ullah, H.; Ishfaq, M.; Khan, R.; Gul, S.L.; Gulfraz, A.; Wang, C.; Zhifang, L. Genotypic variation of tomato to AMF inoculation in improving growth, nutrient uptake, yield, and photosynthetic activity. Symbiosis 2024, 92, 111–124. [Google Scholar] [CrossRef]
- Noor, H.; Ahmad, H.; Sayuti, Z. Effect of mycorrhiza, fertilizers and planting media on rock melon (Cucumis Melo Linn Cv. Glamour) growth using the canopytechture structure. Int. J. Appl. Agric. Sci. 2019, 5, 14–19. [Google Scholar] [CrossRef]
- Mishra, V.; Ellouze, W.; Howard, R. Utility of arbuscular mycorrhizal fungi for improved production and disease mitigation in organic and hydroponic greenhouse crops. J. Hortic. 2018, 5, 237. [Google Scholar] [CrossRef]
- Garcés-Ruiz, M.; Calonne-Salmon, M.; Plouznikoff, K.; Misson, C.; Navarrete-Mier, M.; Cranenbrouck, S.; Declerck, S. Dynamics of short-term phosphorus uptake by intact mycorrhizal and non-mycorrhizal maize plants grown in a circulatory semi-hydroponic cultivation system. Front. Plant Sci. 2017, 8, 285559. [Google Scholar] [CrossRef]
- Estrada-Luna, A.; Davies, F., Jr. Arbuscular mycorrhizal fungi influence water relations, gas exchange, abscisic acid and growth of micropropagated Chile Ancho pepper (Capsicum annuum) plantlets during acclimatization and post-acclimatization. J. Plant Physiol. 2003, 1, 1073–1083. [Google Scholar] [CrossRef]
- Wang, F.; Adams, C.; Yang, W.; Sun, Y.; Shi, Z. Benefits of arbuscular mycorrhizal fungi in reducing organic contaminant residues in crops: Implications for cleaner agricultural production. Crit. Rev. Environ. Sci. Technol. 2020, 50, 1580–1612. [Google Scholar] [CrossRef]
- Feng, J.; Lv, W.; Xu, J.; Huang, Z.; Rui, W.; Lei, X.; Ju, X.; Li, Z. Overlapping Root Architecture and Gene Expression of Nitrogen Transporters for Nitrogen Acquisition of Tomato Plants Colonized with Isolates of Funneliformis mosseae in Hydroponic Production. Plants 2022, 11, 1176. [Google Scholar] [CrossRef]
- Othman, Y.; A’saf, T.; Al-Ajlouni, M.; Bany-Hani, M.; St-Hilaire, R. Holding solution pH and composition consistently improve vase life of rose, lily and gerbera. J. Phytol. 2023, 15, 57–62. [Google Scholar] [CrossRef]
- Ratte, H. Bioaccumulation and toxicity of silver compounds: A review. Environ. Toxicol. Chem. 1999, 18, 89–108. [Google Scholar] [CrossRef]
- Mohammad, A.; Khan, A.; Kuek, C. Improved aeroponic culture of inocula of arbuscular mycorrhizal fungi. Mycorrhiza 2000, 9, 337–339. [Google Scholar] [CrossRef]
- Qian, Y.; Zhao, G.; Zhou, J.; Zhao, H.; Mutter, T.; Huang, X. Combined bioremediation of bensulfuron-methyl contaminated soils with arbuscular mycorrhizal fungus and Hansschlegelia zhihuaiae S113. Front. Microbiol. 2022, 13, 843525. [Google Scholar] [CrossRef]
- Ballhorn, D.J.; Younginger, B.S.; Kautz, S. An aboveground pathogen inhibits belowground rhizobia and arbuscular mycorrhizal fungi in Phaseolus vulgaris. BMC Plant Biol. 2014, 14, 321. [Google Scholar] [CrossRef] [PubMed]
- Sui, X.; Wu, Q.; Chang, W.; Fan, X.; Song, F. Proteomic analysis of the response of Funnelifor mismosseae/Medicago sativa to atrazine stress. BMC Plant Biol. 2018, 18, 289. [Google Scholar] [CrossRef]
- Douds, D.; Schenck, N. Increased sporulation of vesicular–arbuscular mycorrhizal fungi by manipulation of nutrient regimens. Appl. Environ. Microbiol. 1990, 56, 413–418. [Google Scholar] [CrossRef]
- Kobae, Y.; Ohmori, Y.; Saito, C.; Yano, K.; Ohtomo, R.; Fujiwara, T. Phosphate treatment strongly inhibits new arbuscule development but not the maintenance of arbuscule in mycorrhizal rice roots. Plant Physiol. 2016, 171, 566–579. [Google Scholar] [CrossRef] [PubMed]
- Valentine, A.; Kleinert, A. Respiratory responses of arbuscular mycorrhizal roots to short-term alleviation of P deficiency. Mycorrhiza 2007, 17, 137–143. [Google Scholar] [CrossRef] [PubMed]
- Hinsinger, P.; Herrmann, L.; Lesueur, D.; Robin, A.; Trap, J.; Waithaisong, K.; Plassard, C. Impact of roots, microorganisms and microfauna on the fate of soil phosphorus in the rhizosphere. Annu. Plant Rev. 2015, 48, 377–408. [Google Scholar]
- Vejsadová, H.; Čšatská, V.; Hršelová, H.; Gryndler, M. Influence of bacteria on growth and phosphorus nutrition of mycorrhizal corn. J. Plant Nutr. 1993, 16, 1857–1866. [Google Scholar] [CrossRef]
- Choi, J.; Summers, W.; Paszkowski, U. Mechanisms underlying establishment of arbuscular mycorrhizal symbioses. Annu. Rev. Phytopathol. 2018, 56, 135–160. [Google Scholar] [CrossRef] [PubMed]
- Nadal, M.; Paszkowski, U. Polyphony in the rhizosphere: Presymbiotic communication in arbuscular mycorrhizal symbiosis. Curr. Opin. Plant Biol. 2013, 16, 473–479. [Google Scholar] [CrossRef] [PubMed]
- Montagne, V.; Charpentier, S.; Cannavo, P.; Capiaux, H.; Grosbellet, C.; Lebeau, T. Structure and activity of spontaneous fungal communities in organic substrates used for soilless crops. Sci. Hortic. 2015, 192, 148–157. [Google Scholar] [CrossRef]
- Thompson, J. Soilless culture of vesicular-arbuscular mycorrhizae of cereals: Effects of nutrient concentration and nitrogen source. Can. J. Bot. 1986, 64, 2282–2294. [Google Scholar] [CrossRef]
Plant Host | AMF | Substrate/Hydroponic Type | Response | References |
---|---|---|---|---|
Lettuce (Lactuca sativa L.) | F. mosseae | Calcined clay/Ebb and flow. | AMF improved leaf gas exchanges and the nutritional quality (leaf content of chlorophylls, carotenoids, and phenols) of lettuce even at sub-optimal P. | [20] |
Basil (O. basilicum L.) | Mixture of G. intraradices, G. aggregatum, G. mosseae, G. clarum, G. monosporus, G. deserticola, G. brasilianum, G. etunicatum, and Gigaspora margarita. | No substrate/Floating culture. | Compared to the control (none treated) bacteria, mycorrhiza, and micro-algae treatments increased basil yield by about 18.94%, 13.94%, and 5.72%, respectively. In addition, bio-fertilizers enhanced the intake of nutrients N, P, K, Ca, Mg, Fe, Mn, Zn and Cu. | [8] |
Tomato (L. esculentum Mill.) | Rhizophagus irregularis | Mixture of organic peat and vermiculite (1:1 v/v)/Ebb and flow. | AMF transplants had higher shoot total dry weight, survival rate, leaf N and P content. | [107] |
Tomato | Piriformospora indica fungi + mixture of mixture of AMF (Rhizophagus clarus, C. etunicatum and Gigaspora albida) | Coconut fiber/Ebb and flow. | Growth-promoting fungi and K doses improved cherry tomato yield and fruit quality. | [108] |
Baby Spinach (S. oleracea L.) | G. intraradices, G. aggregatum, G. mosseae, G. clarum, G. monosporus, G. deserticola, G. brasilianum, G. etunicatum, G. margarita | No substrate/Float culture. | Biofertilizers improved the internal leaves’ quality (total phenolic, vitamin C, total soluble solids). | [17] |
Onion (Allium cepa) | Glomus sp. (INVAM-FL329) | Sand/Ebb and flow. | Higher levels of magnesium sulfate (2.6 vs. 11.7 mM MgSO4) in nutrient solution significantly reduced tissue-Ca levels, root colonization and sporulation. | [42] |
Tomato | G. monosporum and G. mosseae | Sawdust/Ebb and flow. | AMF significantly increased plant height, fruit yield and fruit number. | [10] |
Saffron (C. sativus) | R. intraradices | Sand/Ebb and flow. | Corms had similar spice yield compared to soil, but these corms had higher polyphenols, anthocyanins, vitamin C, and elevated antioxidant activity. | [105] |
Tomato | G. mosseae, G. intraradices, G. etunicatum and G. clarum | Rockwool/Ebb and flow. | Although AMF had no effect on the total and marketable yield, tomato fruit inoculated with AMF contained higher sugars compared to the plants growing without mycorrhiza. | [109] |
Tomato | F. mosseae | Sand: vermiculite mixture (1:1 v/v)/Ebb and flow | Leaf photosynthetic capacities were higher in mycorrhizal plants when leaves contained more proteins and/or the plant-internal moisture stress was lower than in non-mycorrhizal plants. | [43] |
Petunia (Petunia × hybrid) | G. mosseae, G. intraradices and Gigaspora rosea | Vermiculite/Ebb and flow. | Disease symptoms caused by the root pathogen Thielaviopsis basicola were significantly reduced in G. mosseae colonized plants. A negative effect of the pathogen on root colonization by G. intraradices was observed. | [44] |
Lettuce | G. mosseae | No substrate/NFT, Perlite/Ebb and flow. | In both systems, AMF-inoculated lettuce had higher shoot dry weight than the non-inoculated. | [22] |
Lettuce | G. verruculosum | No substrate/Float culture. | AMF-inoculated lettuce plants had higher mycorrhizal colonization (86%), spore population (no/g sand, 303) and shoot and root dry weight compared to the control | [21] |
Tomato | G. etunicatum and G. intraradices | Vermiculite/Ebb and flow. | AMF-inoculated seedling had higher biomass and relative growth rate compared to the control. | [23] |
Strawberry (Fragaria × Ananassa) | G. clarum and G. caledonium | Sterilized potting mix soil: sand: perlite (1:1:1 v/v/v)/Ebb and flow. | AMF increased yield and reduced fruit total soluble solids and pH compared to the control. | [45] |
Strawberry | G. intraradices, Bacillus velezensis | Coconut fiber/Ebb and flow. | AMF increased chlorophyll content index (SPAD) and decreased fruit total soluble solids, titratable acidity and pH compared to the control | [46] |
Cucumber (Cucumis sativus) | G. mosseae | Sand/Ebb and flow. | AMF increased leaf SPAD, fresh weight, and fruit quality component (antioxidant activity and phenol content). | [110] |
Snapdragons (Antirrhinum majus) | G. intraradices | 90% perlite and 10% peat-moss/Ebb and flow. | AMF significantly increased flower vase-life and reduced ethylene production. | [40] |
Cucumber | G. mossea | No substrate/Float culture. | AMF-plants had higher shoot SPAD, gas exchange (photosynthesis rate, transpiration, and stomatal conductance), root phenol content, and antioxidant activity. | [104] |
Pepper (Capsicum annuum) | G.caledonium and G. clarum | Perlite/Ebb and flow. | AMF-increased shoot dry weight. | [39] |
Tomato | Piriformospora indica | Sand/Ebb and flow. | AMF increased leaves biomass by 20% and reduced disease severity caused by Verticillium dahliae by more than 30%. | [111] |
Tomato | G. monosporum, G. vesiculiferum, G. deserticola, G. intraradices, G. mosseae | Sawdust/Ebb and flow. | Inoculation with G. monosporum and G. mosseae significantly increased fruit yield and fruit number and reduced Fusarium oxysporum root infection compared to the untreated control plants. | [10] |
gerbera (Gerbera jamesonii) | G. mosseae and G. intradices | Sand/Ebb and flow. | AMF inoculation increased yield by 16% and vase life by 19%. | [112] |
Tomato | G. fasciculatum | Perlite/Ebb and flow. | AMF increased yield significantly. | [47] |
Tomato | 9 species of mychorriza; G. intraradices, G. clarum, G. mosseae, G. margarita, G. aggregatum, G. etunicatum, G. monosporus, G. deserticola, G. brasilianum | Peatmoss: perlite (1:1, v/v)/Ebb and flow. | Mychorriza treatment increased tomato juice electrical conductivity and reduced vitamin C. | [113] |
Melon (Cucumis melo) | G. intraradices, G. aggregatum, G. mosseage, G. clarum, G. monosporus, Glomus deserticola, G. brasilianum, G. etunicatum, Gigaspor margari | Coco-peat: perlite (1:1, v/v)/Ebb and flow. | Growing AMF-inoculated watermelon seedlings in hydroponic system (80% full strength nutrient) increased total yield by 49.5% (12.4 vs. 8.3 kg/m2) compared to the control. | [106] |
Pepper | Mixture of 9 AMF species: G. intraradices, G. aggregatum, G. mosseae, G. clarum, G. monosporus, G. deserticola, G. brasilianum, G. etunicatum, and G. margarita | Coco pith slabs/Ebb and flow. | The use of 80% mineral fertilizers in combination with mycorrhiza and bacteria, provided a 32.4% higher yield than the control (100% mineral fertilizer without bio-fertilizers). | [18] |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Othman, Y.A.; Alananbeh, K.M.; Tahat, M.M. Can Arbuscular Mycorrhizal Fungi Enhance Crop Productivity and Quality in Hydroponics? A Meta-Analysis. Sustainability 2024, 16, 3662. https://doi.org/10.3390/su16093662
Othman YA, Alananbeh KM, Tahat MM. Can Arbuscular Mycorrhizal Fungi Enhance Crop Productivity and Quality in Hydroponics? A Meta-Analysis. Sustainability. 2024; 16(9):3662. https://doi.org/10.3390/su16093662
Chicago/Turabian StyleOthman, Yahia A., Kholoud M. Alananbeh, and Monther M. Tahat. 2024. "Can Arbuscular Mycorrhizal Fungi Enhance Crop Productivity and Quality in Hydroponics? A Meta-Analysis" Sustainability 16, no. 9: 3662. https://doi.org/10.3390/su16093662