1. Introduction
Fungi are eukaryotic microorganisms that possess a structure similar to plant roots, known as hyphae, which are responsible for absorbing water and nutrients from the soil and providing support to the fungi. Unicellular fungi that do not produce hyphae are referred to as yeasts [1].
Fungi exhibit a vast range of metabolic and physiological capabilities, allowing them to produce an extensive array of secondary metabolites, as well as a variety of enzymes that play critical roles in the soil’s biochemical cycles. Additionally, these organisms play a crucial role in increasing the availability of essential nutrients in the soil [2].
Some saprotrophic fungi, possessing the ability to decompose organic matter and release nutrients trapped within their components, have evolved to develop the capacity to interact with the roots of plants, which are called mycorrhiza fungi. This interaction necessitates several physiological and morphological adaptations in both fungi and plants. The ability of saprotrophic fungi to thrive in living plants is hindered by their inability to suppress the immune systems of plants. Consequently, these fungi were confined to the decomposition of organic matter. Notably, some fungi have lost their capacity for saprotrophic growth and now rely entirely on plants for their survival [3].
Fungi engage in a mutually beneficial partnership with the host plant, providing the latter with various advantages, while simultaneously obtaining carbohydrates and energy-rich molecules from the host [4]. Fungi are categorized into various types of mycorrhiza, based on their level of interaction with plants. One of these is Arbuscular Mycorrhizal Fungi (AMF), which establishes intricate branching structures called arbuscules within the root cells of plants, facilitating the transfer of nutrients and water from the soil to the plants through hyphae and the recycling of energy and carbohydrates from the host plant. The consequence of this interaction is increased plant growth [5]
In contrast, another type of mycorrhizal fungi is less intimate with the plant host Ectomycorrhiza Fungi (EMF). This type of mycorrhiza forms a structure known as ectosclerotium within the roots. EMF provides nutrients such as phosphorus, nitrogen, and water to plants. The relationship between plants and EMF is not totally integrated, and EMF does not colonize the entire root system [6].
Mycoheterotrophic mycorrhizae are a significant type of mycorrhizal fungi that include non-photosynthetic plant species, such as Indian or ghost pipes, and fungi. In this type of mycorrhizal association, the plant obtains nutrients solely from the fungus, which leads to a complex network of roots and fungi [7]. Another type of mycorrhizal fungus is ericoid mycorrhiza. This type of mycorrhizae is primarily associated with ericaceous plants, such as heathers and blueberries, and shares similarities with arbuscular mycorrhizae but exhibits distinct interactions with its host [1].
Orchid mycorrhizae, another type of mycorrhizae, is essential for seed germination and the early growth of many orchid species. The fungus forms dense coils around the roots of the orchid, which are crucial for its survival [8]. The existence of monotropoid mycorrhizae, a type of mycorrhizal fungus, is noteworthy. This type of mycorrhizae is unique because it is found in plants that lack chlorophyll, such as in ghost pipes. Plants rely entirely on fungi for their nutritional needs, resulting in the development of a complex root-fungus network [3].
Mycorrhizal fungi are unique in that they are influenced by different types of plants, making them a distinct type of fungus that colonizes soils worldwide. Approximately 250 species of mycorrhizal fungi are found in various families and genera. These fungi are obligate symbionts, meaning that they rely on plants to obtain energy and carbohydrate for survival. At the same time, they are essential participants in several nutrient cycles that are important for all living organisms, including nutrients such as phosphorus, nitrogen, and potassium [6].
It is widely believed that the relationship between land plants and mycorrhizal fungi has existed since the dawn of the former, which stretches back hundreds of millions of years. Among the various mutually beneficial interactions that exist between plants and microorganisms, arbuscular mycorrhizal symbiosis (AMF) is the most prevalent. Research indicates that AMF play a pivotal role in the nutrition and growth of plants, particularly under stress conditions, and help to maintain several crucial ecosystem processes. This association benefits both parties, as fungi assist plants in absorbing essential nutrients while receiving carbohydrates from them. In addition to decomposing dead organic matter, ectomycorrhizal fungi also form partnerships with forest trees and contribute to the storage of soil carbon [9].
Mycorrhizal fungi are crucial for the proper functioning of soils, element cycling, and the development of sustainable soil and land-use practices [10]. These fungi contribute significantly to sustainable agriculture by improving the soil structure, enhancing nutrient acquisition, and reducing biotic and abiotic stress, leading to increased plant growth and productivity. They form mutualistic relationships with plant roots, facilitating the efficient absorption of essential mineral nutrients, such as nitrogen, phosphorus, and potassium, and reducing dependence on chemical fertilizers. Additionally, mycorrhizal fungi can help manage plant diseases by antagonizing pathogens and can assist plants in enduring abiotic stresses, such as drought, salinity, and heavy metal toxicity. They also enhance soil quality and stability by increasing soil structure through the secretion of glomalin. The integration of mycorrhizal fungi into agricultural production offers a viable alternative for addressing the challenges faced by conventional agricultural systems. By promoting plant growth, decreasing dependence on chemical inputs, and enhancing soil health, this approach provides a sustainable solution for agriculture [11].
2. Mycorrhizal fungi and nitrogen
Nitrogen (N) is a crucial macronutrient for plants and plays a vital role in several physiological processes. The significance of nitrogen is highlighted by the fact that it is an essential component of amino acids, which are the building blocks of proteins. Proteins are vital to the structure and function of plant cells. Nitrogen is a part of chlorophyll, the pigment responsible for photosynthesis in plants, and its deficiency can result in chlorosis and yellowing of leaves due to reduced chlorophyll synthesis. Nitrogen is also a component of nucleic acids (DNA and RNA) that provides genetic instructions for plant growth and development. Several coenzymes and adenosine triphosphate (ATP), the main cellular energy sources, also contain nitrogen [12]. It is important to note that plants require substantial amounts of nitrogen for growth; however, a significant portion of the nitrogen present in the biosphere is unavailable to them and other microorganisms. Only nitrogenase carriers, a select group of bacteria, can obtain nitrogen from the air and make it accessible to several organisms. An adequate amount of nitrogen is crucial for the vigorous vegetative growth of plants, leading to faster growth, larger leaves, and more intense green coloration. Nitrogen deficiency usually results in stunted growth, small pale leaves, and low productivity [13]. It is not possible to measure the amount of nitrogen through soil fertility analysis because of its instability. Consequently, the appropriate amount of nitrogen for crop production must be determined by considering the crop species and estimated productivity. This amount of nitrogen must be applied through mineral fertilization, and its application must be divided many times throughout crop production to reduce nitrogen loss [14].
Although mycorrhizal fungi cannot obtain atmospheric nitrogen and convert it into a form accessible to plants, they can release nitrogen that is trapped in organic matter, rendering it available to plants, thereby facilitating plant growth. Mycorrhizal fungi offer a promising alternative for sustainably supplying nitrogen to plants, as they are an effective means of addressing the increasing demand for nitrogen in agricultural production [15].
3. Mycorrhizal fungi and phosphorus
Phosphorus (P) is an indispensable element for all living organisms, as it plays a vital role in energy transfer and cell structures. Unlike nitrogen, which has a gaseous phase, phosphorus mainly exists in a solid form, making its cycle distinct. Phosphorus (P) is a crucial macronutrient for plants and is central to several physiological processes. The significance of phosphorus in plants is demonstrated by the following points: Phosphorus is a key component of adenosine triphosphate (ATP) molecules, which serve as the primary “energy currency” of cells. ATP is essential for many biochemical reactions and provides energy for various cellular functions [16].
Phosphorus is a vital component of nucleic acids, DNA and RNA, and carries the genetic information of plants. Many coenzymes and related molecules essential for many biochemical reactions contain phosphorus in their composition [17]. Phosphorus is crucial for photosynthesis and respiration processes, as well as the synthesis and breakdown of carbohydrates. Phosphorus is essential for proper root development, especially for primary roots that grow deeper into the soil. Adequate amounts of phosphorus are vital for the formation of flowers and fruits and directly affect plant production. Phosphorus aids the proper maturation of plants and seeds [18, 19].
Plants with an adequate supply of phosphorus generally exhibit enhanced resistance to diseases and various forms of abiotic stress. Conversely, phosphorus deficiency in plants may result in stunted growth and leaves that are dark in color with a bronze or purple tinge. This is attributable to the accumulation of anthocyanins and a concurrent reduction in seed and fruit production [20]. The mobility of phosphorus in the soil is limited, which means that it does not readily migrate to the roots of plants, particularly in alkaline or extremely acidic soils. Consequently, even when phosphorus is present in the soil, its availability to plants maybe diminished [21].
Arbuscular mycorrhizal fungi (AMF) are important for the uptake of phosphorus (P) by plants, as they form symbiotic relationships with plant roots, providing essential nutrients such as phosphorus and nitrogen, while obtaining carbon from the plant root system. Soils with increased levels of available phosphorus can have detrimental effects on both the diversity of microorganisms and interactions between mycorrhizae and their plant hosts. This is because high levels of available phosphorus decrease the need for plants to rely on beneficial fungi. Consequently, when there is excess available phosphorus, plants may allocate less carbon to mycorrhizae, leading to a reduction in the diversity and abundance of mycorrhizae. This decrease in AMF diversity and abundance suggested a less symbiotic relationship. On the other hand, when the soil is phosphorus deficient, the use of arbuscular mycorrhizal fungi (AMF) to provide phosphorus to the plant is a great alternative. AMF can supply phosphorus even in soils with phosphorus deficiency, thereby promoting good crop yield [22].
4. Conclusion
Mycorrhizal fungi are widespread organisms found in various regions across the globe and are closely related to a broad range of root plant species, including agricultural crops. These fungi exhibit multiple traits that promote plant growth, and numerous studies have demonstrated their ability to increase plant growth by improving the efficiency of nutrient and water uptake from the soil as well as their availability. Specifically, mycorrhizal fungi have been shown to increase the availability of nitrogen and phosphorus in plants. While these fungi cannot fix nitrogen from the atmosphere, they are capable of mineralizing organic matter, releasing nitrogen that is trapped in molecules and cellular organelles. In addition, arbuscular mycorrhizal fungi (AMF) can increase phosphorus availability in plants. However, high levels of phosphorus in the soil can decrease the interactions between the fungus and the host plant. Some studies have shown that mycorrhizal fungi can enhance plant tolerance to environmental stress. In summary, mycorrhizal fungi can be used to promote plant growth, improve nutrient utilization efficiency, reduce environmental impacts and production costs, and enhance plant tolerance to cope with stress conditions. The use of AMF is an excellent strategy to achieve sustainable production.
References
- 1.
Parniske M. Arbuscular mycorrhiza: The mother of plant root endosymbioses. Nature Reviews Microbiology. 2008; 6 (10):763-775. DOI: 10.1038/NRMICRO1987 - 2.
Wang B, Qiu YL. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza. 2006; 16 (5):299-363. DOI: 10.1007/S00572-005-0033-6 - 3.
Marks GC. Causal morphology and evolution of mycorrhizas. Agriculture, Ecosystems & Environment. 1991; 35 (2-3):89-104 - 4.
Rooney DC, Killham K, Bending GD, Baggs E, Weih M, Hodge A. Mycorrhizas and biomass crops: Opportunities for future sustainable development. Trends in Plant Science. 2009; 14 (10):542-549. DOI: 10.1016/j.tplants.2009.08.004 - 5.
Smith SE, Smith FA. Roles of arbuscular mycorrhizas in plant nutrition and growth: New paradigms from cellular to ecosystem scales. Annual Review of Plant Biology. 2011; 62 :227-250. DOI: 10.1146/ANNUREV-ARPLANT-042110-103846 - 6.
Messa VR, Savioli MR. Improving sustainable agriculture with arbuscular mycorrhizae. Rhizosphere. 2021; 19 :1-3, 100412 - 7.
Pozo MJ, Azcón-Aguilar C. Unraveling mycorrhiza-induced resistance. Current Opinion in Plant Biology. 2007; 10 (4):393-398. DOI: 10.1016/j.pbi.2007.05.004 - 8.
Sawers RJH, Gutjahr C, Paszkowski U. Cereal mycorrhiza: An ancient symbiosis in modern agriculture. Trends in Plant Science. 2008; 13 (2):93-97. DOI: 10.1016/j.tplants.2007.11.006 - 9.
Cavagnaro TR, Bender SF, Asghari HR, van der Heijden MGA. The role of arbuscular mycorrhizas in reducing soil nutrient loss. Trends in Plant Science. 2015; 20 (5):283-290. DOI: 10.1016/j.tplants.2015.03.004 - 10.
Keymer A, Gutjahr C. Cross-kingdom lipid transfer in arbuscular mycorrhiza symbiosis and beyond. Current Opinion in Plant Biology. 2018; 44 :137-144. DOI: 10.1016/j.pbi.2018.04.005 - 11.
Cameron DD, Neal AL, van Wees SCM, Ton J. Mycorrhiza-induced resistance: More than the sum of its parts? Trends in Plant Science. 2013; 18 (10):539-545. DOI: 10.1016/j.tplants.2013.06.004 - 12.
Novoa R, Loomis RS. Nitrogen and plant production. Plant and Soil. 1981; 58 (1-3):177-204. DOI: 10.1007/BF02180053/METRICS - 13.
Sheoran S, Kumar S, Kumar P, Meena RS, Rakshit S. Nitrogen fixation in maize: Breeding opportunities. Theoretical and Applied Genetics. 2021; 134 (5):1263-1280. DOI: 10.1007/S00122-021-03791-5 - 14.
Hedin LO, Brookshire ENJ, Menge DNL, Barron AR. The nitrogen paradox in tropical forest ecosystems. Annual Review of Ecology, Evolution, and Systematics. 2009; 40 :613-635. DOI: 10.1146/ANNUREV.ECOLSYS.37.091305.110246 - 15.
Jansa J, Forczek ST, Rozmoš M, Püschel D, Bukovská P, Hršelová H. Arbuscular mycorrhiza and soil organic nitrogen: Network of players and interactions. Chemical and Biological Technologies in Agriculture. 2019; 6 (1):1-10 - 16.
Adnan M, Fahad S, Zamin M, Shah S, Mian IA, Danish S, et al. Coupling phosphate-solubilizing bacteria with phosphorus supplements improve maize phosphorus acquisition and growth under lime induced salinity stress. Plants. 2020; 9 (7):1-18. DOI: 10.3390/plants9070900 - 17.
Bindraban PS, Dimkpa CO, Pandey R. Exploring phosphorus fertilizers and fertilization strategies for improved human and environmental health. Biology and Fertility of Soils. 2020; 56 (3):299-317. DOI: 10.1007/S00374-019-01430-2/FIGURES/4 - 18.
Malhotra H, Vandana, Sharma S, Pandey R. Phosphorus nutrition: Plant growth in response to deficiency and excess. Plant Nutrients and Abiotic Stress Tolerance. 2018; 1 :171-190 - 19.
Malhotra M, Srivastava S. Stress-responsive indole-3-acetic acid biosynthesis by Azospirillum brasilense SM and its ability to modulate plant growth. European Journal of Soil Biology. 2009; 45 (1):73-80. DOI: 10.1016/j.ejsobi.2008.05.006 - 20.
Parvin S, Van Geel M, Yeasmin T, Verbruggen E, Honnay O. Effects of single and multiple species inocula of arbuscular mycorrhizal fungi on the salinity tolerance of a Bangladeshi rice (Oryza sativa L.) cultivar. Mycorrhiza. 2020; 30 (4):431-444. DOI: 10.1007/s00572-020-00957-9 - 21.
Pereira NCM, Galindo FS, Gazola RPD, Dupas E, Rosa PAL, Mortinho ES, et al. Corn yield and phosphorus use efficiency response to phosphorus rates associated with plant growth promoting bacteria. Frontiers in Environmental Science. 2020; 8 (40):1-12 - 22.
Ma J, Xie Y, Sun J, Zou P, Ma S, Yuan Y, et al. Co-application of chitooligosaccharides and arbuscular mycorrhiza fungi reduced greenhouse gas fluxes in saline soil by improving the rhizosphere microecology of soybean. Journal of Environmental Management. 2023; 345 :118836. DOI: 10.1016/j.jenvman.2023.118836