Arbuscular Mycorrhizal Fungi and Plant
This entry highlghts the role of Arbuscular Mycorrhizal Fungi (AMF) on plant nutrition and growth. AMFimproves plant nutrition and helps them to cope with environment stresses.
Arbuscular mycorrhizal fungi (AMF) are soil microorganisms that form a symbiotic relationship with 80–90% of vascular plant species and 90% of agricultural plants , including most agricultural crops, particularly cereals, vegetables, and horticultural plants. They have a ubiquitous distribution in global ecosystems that are primarily defined by the global distribution of known plant hosts . AMF are classified as a member of subkingdom Mucoromyceta and the phylum Glomeromycota including three classes (Glomeromycetes, Archaeosporomycetes, and Paraglomeromycetes ). AMF belong to 11 families, 25 genera, and nearly 250 species . Glomeromycota are obligate symbionts that rely on the carbon substrates provided by their host plants (up to 20% of plant-fixed carbon) to survive . In return, the fungi improve the supply of water and nutrients, such as phosphate and nitrogen to the host plant through extraradical and intraradical hyphae, arbuscules, and the root apoplast interface . Based on fossil records and molecular data, this symbiosis dates back to the first appearance of land plants, about 400 to 450 million years ago . The Arbuscular mycorrhizal (AM) symbiosis is probably the most widespread beneficial interaction between plants and microorganisms . Several studies have reported that they play a crucial role in plant nutrition and growth in stressed conditions and enhance a number of essential ecosystem processes .
2. Contribution of Arbuscular Mycorrhizal Fungi to Plant Nutrition and Growth
Among beneficial microbes, AMF are one of the most widespread symbiotic fungi colonizing the majority of agricultural plants . The effects of AMF on plant growth and physiological elements contents have been widely studied in many species including relevant crops such as Solanum lycopersicum L. , Sorghum bicolor (L.) Moench , Withania somnifera (L.) Dunal  Cucurbita maxima Duchesne , Piper longum L. , Phaseolus vulgaris L. , Panicum hemitomon Schult , and some free fruits such as Citrullus lanatus (Thunb.) Matsum. & Nakai , Musa acuminata Colla , and Prunus cerasifera L. . In all these species, AMF improved plant growth parameters  and the uptake of several major nutrients such as nitrogen and phosphorus in stressed conditions . This growth stimulation is linked to the fact that AMF extends the absorbing network beyond the nutrient depletion zones of the rhizosphere, which allows access to a larger volume of soil . Furthermore, fungal hyphae are much thinner than roots and are able to penetrate smaller pores and uptake more nutrients .
By extending the root absorbing area, AMF increases the total absorption surface of inoculated plants and thus improves plant access to nutrients, particularly those whose ionic forms have a poor mobility rate or those which are present in low concentration in the soil solution . It is calculated that the rate of water transport from external hyphae to the root ranges from 0.1  to 0.76 μL H2O h−1 per hyphal infection point . Furthermore, AMF contributes approximately 20% to total plant water uptake , highlighting the role of the symbiosis in the water status of host plants. AMF significantly improved Cucurbita maxima growth and metabolism, such as the concentrations of fat, crude protein, crude fiber, and carbohydrates in shoot and root systems of inoculated plants compared to control treatment . Inoculation with this fungus significantly increased plant growth as well as phytochemical constituents such as sugar, protein, phenol, tannin, and flavonoid content . In watermelon (Citrullus lunatus Thunb.), mycorrhizal colonization was found to improve not only the plant yield and water use efficiency but also the quality of the fruits . Similar results were obtained in mycorrhizal tomato plants with an increase in the concentrations of sugars, organic acids, and vitamin C in fruits . It has been demonstrated by  that AMF improved peach seedlings’ performance under the potted conditions, and also significantly elevated K, Mg, Fe, and Zn concentrations in leaves and roots, Ca concentration in leaves, Cu and Mn concentrations in roots, which were obviously dependent on the AMF species. Compared to three AMF ([Funneliformis mosseae (T.H. Nicolson & Gerd.) C. Walker & A. Schüßler 2010, Glomus versiforme (P. Karst.) S.M. Berch 1983, and Paraglomus occultum (C. Walker) J.B. Morton & D. Redecker 2001), F. mosseae exhibited the best mycorrhizal efficiency on growth and nutrient acquisition of peach seedlings . Compared to uninoculated plants, AMF inoculation had positive effects on the growth of carrot and sorghum . In carrot, Scutellospora heterogama (T.H. Nicolson & Gerd.) C. Walker & F.E. Sanders 1986, Acaulospora longula Spain & N.C. Schenck 1984, and F. mosseae had a positive effect on the growth of the host, whereas AMF had only weak effects on the growth of red pepper and leek .
Therefore, it is important to mention that the extent to which a host plant benefits vary with the AMF species used ; and macro and micro-nutrients uptake could depend partly not only on the fungal partner but also on the host plant . A study carried out by  indicates that the contribution of the mycorrhizal pathway to nutrient acquisition also depends on fungal effects on the activity of the plant pathway and on the efficiency with which both partners interact and exchange nutrients across the mycorrhizal interface . For various crops such as sweet potato  or pepper plant , the beneficial effect on plant nutrient content has also been shown to be dependent on fungal diversity.
A similar positive effect was reported in sorghum with an enhancement of plant height, the number of leaves, biomass, total nitrogen, phophorus and potassium uptake . Although, among some species of native AMF tested (Glomus aggregatum N.C. Schenck & G.S. Sm 1982, F. mosseae, Acaulospora longula, and Acaulospora scrobiculata Trappe 1977) some species like Acaulospora scrobiculata are more efficient for improvement of all these parameters in sorghum . The effect of an AMF, F. mosseae was examined regarding the morphological and biochemical properties of different genotypes of the medicinal plant W. somnifera, commonly called Ashwagandha . In addition, several studies reported that the responses of plants to colonization by AMF vary depending on inoculum composition, and a combination of mycorrhizal fungi is more effective than a monospecific inoculum .
AMF colonization by F. mosseae or R. intraradices (N.C. Schenck & G.S. Sm.) C. Walker & A. Schüßler 2010) increased both the survival and growth (by over 100%) of micropropagated transplants of Prunus cerasifera L., compared with either uninoculated controls or transplants inoculated with the ericoid mycorrhizal species Hymenoscyphus ericae (D.J. Read) Korf & Kernan 1983 . Thus, inoculation of woody species’ seedlings under nursery conditions is a valuable strategy to produce seedlings with good vigor, which would translate into high survival and growth at the field .
AMF play an important role in biofortification . AMF inoculation may affect selenium uptake from soil and the level of antioxidant compounds in vegetable crops such as the green asparagus Asparagus officinalis L. Research carried out by  showed increasing selenium (Se) content in wheat grain through inoculation. It has been found by  that AMF modifies the concentration and distribution of nutrients within wheat and barley grain. Inoculation with AMF improves the grain nutritional content in protein, Fe, and Zn . Under distinct environmental conditions,  concluded that AMF symbiosis positively affected the Zn concentration in various crop plant tissues. AMF can contribute substantially to the Zn nutrition of cereal crops such as bread wheat and barley but the role played by AMF on Zn uptake depends on the functional compatibility between AMF isolate and inoculated cereal species .
It is well-known that AMF symbiosis specifically induces the expression of transporters such as the plant aquaporin (AQ) genes, Pi transporters (PT), ammonium transporter (AMT), nitrate transporter (NT), sulfur (S) transporter, Zn transporter, carbon transporter, protein transporter etc. . In wheat plants treated with F. mosseae and R. intraradices Zn concentration is 1.13–2.76 times higher than non-inoculated plants observed . Further, it has been demonstrated that fungal form a network called mycorrhizal networks (MNs) that improve nutrients transfer between plants through the extension of fungal mycelium . Also called common mycorrhizal networks, these MNs can integrate multiple plant species and multiple fungal species that interact, provide feedback, and adapt, which comprise a complex adaptive social network . Results obtained by  confirm the role of AMF in driving biological interactions among neighboring plants.
AMF play an important role in improving the adaptation to biotic and abiotic plant stresses and to alleviate the effects of these stress on plants. Their role in increasing plant growth and yield, disease resistance, biotic and abiotic tolerance provides an environmentally friendly solution to reduce the use of hazardous pesticides and industrial fertilizers. However, more research is needed to test in the field the results obtained in the laboratory and in the greenhouse. The application of this knowledge in real environments and according to biogeographical zones becomes essential in order to promote their industrial production for a large scale used and increase their impact to ensure enough food for every human being on the planet now and in the future. As an ecofriendly method, some work must be done by researchers, private and public sectors, to promote the use of AMF by increasing their production, particularly in developing countries where AMF inocula are not accessible and not affordable.
The entry is from 10.3390/d12100370
- Smith, S.E.; Read, D.J. Mycorrhizal Symbiosis; Academic Press: Cambridge, MA, USA, 2010; ISBN 978-0-08-055934-6.
- Kivlin, S.N.; Hawkes, C.V.; Treseder, K.K. Global diversity and distribution of arbuscular mycorrhizal fungi. Soil Biol. Biochem. 2011, 43, 2294–2303.
- Wang, B.; Qiu, Y.-L. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 2006, 16, 299–363.
- Tedersoo, L.; Sánchez-Ramírez, S.; Kõljalg, U.; Bahram, M.; Döring, M.; Schigel, D.S.; May, T.; Ryberg, M.; Abarenkov, K. High-level classification of the Fungi and a tool for evolutionary ecological analyses. Fungal Divers. 2018, 90, 135–159.
- Schüβler, A.; Schwarzott, D.; Walker, C. A new fungal phylum, the Glomeromycota: Phylogeny and evolution. Mycol. Res. 2001, 105, 1413–1421.
- Spatafora, J.W.; Chang, Y.; Benny, G.L.; Lazarus, K.; Smith, M.E.; Berbee, M.L.; Bonito, G.; Corradi, N.; Grigoriev, I.V.; Gryganskyi, A.; et al. A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 2016, 108, 1028–1046.
- Siddiqui, Z.A.; Pichtel, J. Mycorrhizae: An Overview. In Mycorrhizae: Sustainable Agriculture and Forestry; Springer Science and Business Media LLC: Berlin, Germany, 2008; pp. 1–35.
- Johns, C.D. Agricultural Application of Mycorrhizal Fungi to Increase Crop Yields, Promote Soil Health and Combat Climate Change. Future Directions International. 2014. Available online: https://www.futuredirections.org.au/publication/agricultural-application-of-mycorrhizal-fungi-to-increase-crop-yields-promote-soil-health-and-combat-climate-change/ (accessed on 11 August 2020).
- Parniske, M. Arbuscular mycorrhiza: The mother of plant root endosymbioses. Nat. Rev. Genet. 2008, 6, 763–775.
- Nakmee, P.S.; Techapinyawat, S.; Ngamprasit, S. Comparative potentials of native arbuscular mycorrhizal fungi to improve nutrient uptake and biomass of Sorghum bicolor Linn. Agric. Nat. Resour. 2016, 50, 173–178.
- Posta, K.; Duc, N.H. Benefits of Arbuscular Mycorrhizal Fungi Application to Crop Production under Water Scarcity. Drought Detect. Solut. 2020. Available online: https://www.intechopen.com/books/drought-detection-and-solutions/benefits-of-arbuscular-mycorrhizal-fungi-application-to-crop-production-under-water-scarcity (accessed on 11 August 2020).
- Bona, E.; Cantamessa, S.; Massa, N.; Manassero, P.; Marsano, F.; Copetta, A.; Lingua, G.; D’Agostino, G.; Gamalero, E.; Berta, G. Arbuscular mycorrhizal fungi and plant growth-promoting pseudomonads improve yield, quality and nutritional value of tomato: A field study. Mycorrhiza 2016, 27, 1–11.
- Gamalero, E.; Trotta, A.; Massa, N.; Copetta, A.; Martinotti, M.G.; Berta, G. Impact of two fluorescent pseudomonads and an arbuscular mycorrhizal fungus on tomato plant growth, root architecture and P acquisition. Mycorrhiza 2003, 14, 185–192.
- Kim, S.J.; Eo, J.-K.; Lee, E.-H.; Park, H.; Eom, A.-H. Effects of Arbuscular Mycorrhizal Fungi and Soil Conditions on Crop Plant Growth. Mycobiology 2017, 45, 20–24.
- Parihar, P.; Bora, M. Effect of mycorrhiza (Glomus mosseae) on morphological and biochemical properties of Ashwagandha (Withania somnifera) (L.) Dunal. J. Appl. Nat. Sci. 2018, 10, 1115–1123.
- Al-Hmoud, G.; Al-Momany, A. Effect of Four Mycorrhizal Products on Squash Plant Growth and its Effect on Physiological Plant Elements. Adv. Crop. Sci. Technol. 2017, 5, 1–6.
- Gogoi, P. Differential effect of some arbuscular mycorrhizal fungi on growth of Piper longum L. (Piperaceae). Indian J. Sci. Technol. 2011, 4, 119–125.
- Ibijbijen, J.; Urquiaga, S.; Ismaili, M.; Alves, B.J.R.; Boddey, R.M. Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition and nitrogen fixation of three varieties of common beans (Phaseolus vulgaris). New Phytol. 1996, 134, 353–360.
- Miller, S.P.; Sharitz, R.R. Manipulation of flooding and arbuscular mycorrhiza formation influences growth and nutrition of two semiaquatic grass species. Funct. Ecol. 2000, 14, 738–748.
- Ban, D.; Ban, S.G.; Oplanić, M.; Horvat, J.; Novak, B.; Žanić, K.; Žnidarčič, D. Growth and Yield Response of Watermelon to in-row Plant Spacings and Mycorrhiza. Chil. J. Agric. Res. 2011, 71, 497–502.
- Rodríguez-Romero, A.S.; Guerra, M.S.P.; Jaizme-Vega, M.D.C. Effect of arbuscular mycorrhizal fungi and rhizobacteria on banana growth and nutrition. Agron. Sustain. Dev. 2005, 25, 395–399.
- Berta, G.; Trotta, A.; Fusconi, A.; Hooker, J.E.; Munro, M.; Atkinson, D.; Giovannetti, M.; Morini, S.; Fortuna, P.; Tisserant, B.; et al. Arbuscular mycorrhizal induced changes to plant growth and root system morphology in Prunus cerasifera. Tree Physiol. 1995, 15, 281–293.
- Jansa, J.; Forczek, S.T.; Rozmoš, M.; Püschel, D.; Bukovská, P.; Hršelová, H. Arbuscular mycorrhiza and soil organic nitrogen: Network of players and interactions. Chem. Biol. Technol. Agric. 2019, 6, 10.
- Song, Z.; Bi, Y.; Zhang, J.; Gong, Y.; Yang, H. Arbuscular mycorrhizal fungi promote the growth of plants in the mining associated clay. Sci. Rep. 2020, 10, 1–9.
- Smith, F.A.; Smith, F.A. Roles of Arbuscular Mycorrhizas in Plant Nutrition and Growth: New Paradigms from Cellular to Ecosystem Scales. Annu. Rev. Plant. Biol. 2011, 62, 227–250.
- Allen, M.F. Linking water and nutrients through the vadose zone: A fungal interface between the soil and plant systems. J. Arid. Land 2011, 3, 155–163.
- Allen, M.F. Influence of vesicular-arbuscular mycorrhizae on water movement through Bouteloua gracilis (H.B.K.) lag ex steud. New Phytol. 1982, 91, 191–196.
- Faber, B.A.; Zasoski, R.J.; Munns, D.N.; Shackel, K. A method for measuring hyphal nutrient and water uptake in mycorrhizal plants. Can. J. Bot. 1991, 69, 87–94.
- Ruth, B.; Khalvati, M.; Schmidhalter, U. Quantification of mycorrhizal water uptake via high-resolution on-line water content sensors. Plant. Soil 2011, 342, 459–468.
- Kaya, C.; Higgs, D.; Kirnak, H.; Taş, I. Mycorrhizal colonisation improves fruit yield and water use efficiency in watermelon (Citrullus lanatus Thunb.) grown under well-watered and water-stressed conditions. Plant. Soil 2003, 253, 287–292.
- Wu, Q.-S.; Li, G.-H.; Zou, Y.N. Roles of arbuscular mycorrhizal fungi on growth and nutrient acquisition of peach (Prunus persica L. Batsch) seedlings. J. Anim. Plant. Sci. 2011, 21, 746–750.
- Trouvelot, S.; Bonneau, L.; Redecker, D.; Van Tuinen, D.; Adrian, M.; Wipf, D. Arbuscular mycorrhiza symbiosis in viticulture: A review. Agron. Sustain. Dev. 2015, 35, 1449–1467.
- Ravnskov, S.; Jakobsen, I. Functional compatibility in arbuscular mycorrhizas measured as hyphal P transport to the plant. New Phytol. 1995, 129, 611–618.
- Farmer, M.; Li, X.; Feng, G.; Zhao, B.; Chatagnier, O.; Gianinazzi, S.; Gianinazzi-Pearson, V.; Van Tuinen, D. Molecular monitoring of field-inoculated AMF to evaluate persistence in sweet potato crops in China. Appl. Soil Ecol. 2007, 35, 599–609.
- Jansa, J.; Smith, F.A.; Smith, S.E. Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytol. 2008, 177, 779–789.
- Zangaro, W.; Nisizaki, S.M.A.; Domingos, J.C.B.; Nakano, E.M. Mycorrhizal response and successional status in 80 woody species from south Brazil. J. Trop. Ecol. 2003, 19, 315–324.
- Vandresen, J.; Nishidate, F.R.; Torezan, J.M.D.; Zangara, W. Inoculação de fungos micorrízicos arbusculares e adubação na formação e pós-transplante de mudas de cinco espécies arbóreas nativas do sul do Brasil. Acta Bot. Bras. 2007, 21, 753–765.
- Tahat, M.; Kamaruzaman, S.; Radziah, O.; Kadir, J.; Masdek, H. Plant Host Selectivity for Multiplication of Glomus mosseae Spore. Int. J. Bot. 2008, 4, 466–470.
- Golubkina, N.A.; Krivenkov, L.; Sękara, A.; Vasileva, V.; Tallarita, A.; Caruso, G. Prospects of Arbuscular Mycorrhizal Fungi Utilization in Production of Allium Plants. Plants 2020, 9, 279.
- Coccina, A.; Cavagnaro, T.R.; Pellegrino, E.E.; Ercoli, L.; McLaughlin, M.; Watts-Williams, S.J. The mycorrhizal pathway of zinc uptake contributes to zinc accumulation in barley and wheat grain. BMC Plant. Biol. 2019, 19, 133.
- Conversa, G.; Lazzizera, C.; Chiaravalle, A.E.; Miedico, O.; Bonasia, A.; La Rotonda, P.; Elia, A. Selenium fern application and arbuscular mycorrhizal fungi soil inoculation enhance Se content and antioxidant properties of green asparagus (Asparagus officinalis L.) spears. Sci. Hortic. 2019, 252, 176–191.
- Luo, W.; Li, J.; Ma, X.; Niu, H.; Hou, S.; Wu, F. Effect of arbuscular mycorrhizal fungi on uptake of selenate, selenite, and selenomethionine by roots of winter wheat. Plant. Soil 2019, 438, 71–83.
- Watts-Williams, S.J.; Gilbert, S.E. Arbuscular mycorrhizal fungi affect the concentration and distribution of nutrients in the grain differently in barley compared with wheat. Plants People Planet 2020.
- Pellegrino, E.; Bedini, S. Enhancing ecosystem services in sustainable agriculture: Biofertilization and biofortification of chickpea (Cicer arietinum L.) by arbuscular mycorrhizal fungi. Soil Biol. Biochem. 2014, 68, 429–439.
- Lehmann, A.; Veresoglou, S.D.; Leifheit, E.F.; Rillig, M.C. Arbuscular mycorrhizal influence on zinc nutrition in crop plants—A meta-analysis. Soil Biol. Biochem. 2014, 69, 123–131.
- Burleigh, S.H.; Bechmann, I.E. Plant nutrient transporter regulation in arbuscular mycorrhizas. Plant. Soil 2002, 244, 247–251.
- Allen, J.W.; Shachar-Hill, Y. Sulfur Transfer through an Arbuscular Mycorrhiza. Plant. Physiol. 2008, 149, 549–560.
- Sieh, D.; Watanabe, M.; Devers, E.A.; Brueckner, F.; Hoefgen, R.; Krajinski, F. The arbuscular mycorrhizal symbiosis influences sulfur starvation responses of Medicago truncatula. New Phytol. 2012, 197, 606–616.
- Giovannetti, M.; Tolosano, M.; Volpe, V.; Kopriva, S.; Bonfante, P. Identification and functional characterization of a sulfate transporter induced by both sulfur starvation and mycorrhiza formation in Lotus japonicus. New Phytol. 2014, 204, 609–619.
- Nguyen, T.D.; Cavagnaro, T.R.; Watts-Williams, S.J. The effects of soil phosphorus and zinc availability on plant responses to mycorrhizal fungi: A physiological and molecular assessment. Sci. Rep. 2019, 9, 14880.
- Ma, J.; Janouskova, M.; Ye, L.; Bai, L.; Dong, R.; Yan, Y.; Yu, X.; Zou, Z.; Li, Y.; He, C. Role of arbuscular mycorrhiza in alleviating the effect of cold on the photosynthesis of cucumber seedlings. Photosynthetica 2019, 57, 86–95.
- Ma, X.; Luo, W.; Li, J.; Wu, F. Arbuscular mycorrhizal fungi increase both concentrations and bioavilability of Zn in wheat (Triticum aestivum L) grain on Zn-spiked soils. Appl. Soil Ecol. 2019, 135, 91–97.
- Gorzelak, M.A.; Asay, A.K.; Pickles, B.; Simard, S.W. Inter-Plant communication through mycorrhizal networks mediates complex adaptive behaviour in plant communities. Aob Plants 2015, 7, 7.
- Ingraffia, R.; Amato, G.; Frenda, A.S.; Giambalvo, D. Impacts of arbuscular mycorrhizal fungi on nutrient uptake, N2 fixation, N transfer, and growth in a wheat/faba bean intercropping system. PLoS ONE 2019, 14, e0213672.