Arbuscular mycorrhizal Fungi as Inspiration for Sustainable Technology: History
View Latest Version
Please note this is an old version of this entry, which may differ significantly from the current revision.
Contributor:
Maria J. Torres
,
Geisianny Moreira
,
Jehangir H. Bhadha
,
Eric S. McLamore

This review illuminates established knowledge of root–arbuscular mycorrhizal fungi (AMF)–plant mutualism to study the uptake of phosphorus (P) as a critical element for plant nutrition. We focus on P cycling, underscoring the role of AMF in enhancing P acquisition and plant resilience in the rhizosphere. The role(s) of plant roots, root exudates, and biomolecules in relevant soil processes is emphasized in this manuscript. Enhancing P uptake efficiency through AMF interaction presents a promising avenue for sustainable agriculture, with future research opportunities focusing on understanding underlying mechanisms and developing innovative technologies as a need to transition from the use of AMF as a biofertilizer or as an inoculation alternative for seeds to being an inspiration for the development of technology adapted to different crops. This is important to promote responsible agricultural practices and improve crop yields. We provide definitions of key terms and concepts for one of the best-known natural sustainable phosphorus systems. This manuscript illuminates and aims to inspire technology development to overcome the challenge of plant nutrition under P scarcity conditions.

  • arbuscular mycorrhizal
  • fungi
  • phosphorus
  • technology
  • sensors
Plants, being primarily sessile organisms, utilize their roots for communication and nutrient transport to ensure survival [1]. Under nutrient scarcity or environmental stress, plants must form associations with rhizosphere microorganisms to ensure nutrient and water supply. These mutualistic associations enhance plant root traits and defense mechanisms. One example of such a keystone interaction is mutualism between plants and arbuscular mycorrhizal fungi.

1.1. Arbuscular mycorrhizal Fungi

Arbuscular mycorrhizal fungi (AMF) colonize the root cortex of numerous crop species (Figure 1). This is one of the strategies plants use to uptake phosphorus (P) from soil. Given the central role in P uptake, AMF is critically important to many agricultural systems, especially for soils with limited bio-accessible P [2]. AMF forms associations with 70–90% of terrestrial land plants [3] (excluding cabbage, lupin, and other plants in the Brassicaceae family). The fungi develop extraradical mycelium to uptake crucial nutrients from the soil, including organic phosphorus (Po). AMF–plant interactions are mutually beneficial (referred to as mutualism). Fungi supply nutrients and protection against environmental stress, while plants provide essential carbon to the fungi in return [4]. Some nutrients, particularly P, are not bioavailable to plants [5], limiting crop production [6].
Figure 1. AMF root colonization is a mutualistic relationship for phosphate uptake by plants. The ectomycorrhizae shown on the left side of the diagram depict fungal hyphae [7] extending into the plant root during AMF colonization. The exploded view (middle, right) shows endomycorrhizae, where AMF hyphae extend into the root cortex. The diagrams expand on the work by [5] and highlight seven key structures in purple color. These key structures include: (i) AMF, (ii) root exudates (PubChem ID: 15102684; [8]), (iii) D-glucose-6-phosphate (as an example of organic phosphorus) (PubChem ID: 5958, [9]), (iv) inorganic phosphorus transporters (PiPT; PBD Entry: 8FVZ, [10]), and (v) hyphae. Malic acid was used as an example of an organic acid in soil (PubChem ID: 525). Figure created in Biorender.com.
The exchange of inorganic phosphorus (Pi), photosynthates, and other beneficial carbon plays a crucial role in AMF–root associations. Figure 1 summarizes plant–AMF–soil interactions, highlighting seven key structures related to P uptake. The processes take place in an area surrounding roots known as the ectorhizosphere. This review illuminates each of these seven structures and highlights recent research on P uptake by plants. A systems-level view of these interactions enables a nuanced understanding of factors influencing plant P uptake, including soil conditions and plant adaptive strategies.

1.2. Phosphorus Is a Key Element

Phosphorus (P) is a crucial element for many biological processes and is a core component of several critical bio-macromolecules, including deoxyribonucleic acid (DNA), adenosine triphosphate (ATP), and phospholipid cell membranes, among others [11]. Plant roots acquire P in the form of dissolved inorganic phosphorus (DIP), also referred to as orthophosphate (ortho-P) [12]. In most soils, ortho-P is present at extremely low concentrations. For this reason, plant association with soil microorganisms such as AMF is an evolved strategy for overcoming P-deficiency conditions [13]. Symbiotic AMF facilitates ortho-P uptake to plants through specialized structures, such as arbuscles or mycorrhizal hyphae branches, as shown in Figure 2.
Extraradical hyphae create extensive networks, often extending beyond the plant root–soil volume. Thus, the sequestration of nutrients extends to a spatial region that is not accessible by the plant roots alone. In addition to hyphae, micro- and nano-scale structures such as vesicles store nutrients (including P) [14]. Vesicle-stored nutrients serve as chemical pools in the rhizosphere network. The root–AMF network ensures sustained nutrient/carbon supply to each partner. This mutualism enhances ortho-P absorption, P mobilization in the soil, and overall nutrient use efficiency [15].
Figure 2. The root–AMF network involves AMF–exudate interactions for P uptake and transport to the plant. The diagram expands on the work by [16][17] and highlights seven key structures in purple color: (i) root exudates (PubChem ID: 15102684; [8]), (ii) D-glucose-6-phosphate as representative Po (PubChem ID: 5958, [9]), (iii) inorganic phosphorus (Pi) (PubChem ID: 1003, [18]), (iv) inorganic phosphorus transporters to the plant membrane (PiPT (PBD Entry: 8FVZ, [10]), (v) Enzymes (PubChem ID: 18985873, [19]) transformation of Po to Pi in the plant cells, (vi) arbuscules, (vii) hyphae, and (viii) vesicles. Figure created in Biorender.com.
Here, we review AMF–plant interactions for (indirect) ortho-P uptake by plants. We summarize seven key structures that are involved in P cycling within soils and highlight the major mechanisms of uptake. We also provide a summary table with key references to the seven key biomolecules involved in the process. Definitions of key terms and concepts are provided in the Supplementary Material. We close by discussing challenges and opportunities for research in AMF–plant interactions related to sustainable agriculture technology development.

This entry is adapted from the peer-reviewed paper 10.3390/encyclopedia4030077

References

  1. Bagyaraj, D.J.; Sharma, M.P.; Maiti, D. Phosphorus Nutrition of Crops through Arbuscular Mycorrhizal Fungi. Curr. Sci. 2015, 108, 1288–1293.
  2. Bhattacharya, A. Chapter 5—Changing Environmental Condition and Phosphorus-Use Efficiency in Plants. In Changing Climate and Resource Use Efficiency in Plants; Bhattacharya, A., Ed.; Academic Press: Cambridge, MA, USA, 2019; pp. 241–305. ISBN 978-0-12-816209-5.
  3. Lee, E.-H.; Eo, J.-K.; Ka, K.-H.; Eom, A.-H. Diversity of Arbuscular Mycorrhizal Fungi and Their Roles in Ecosystems. Mycobiology 2013, 41, 121.
  4. Maldonado-Mendoza, I.E.; Dewbre, G.R.; Harrison, M.J. A Phosphate Transporter Gene from the Extra-Radical Mycelium of an Arbuscular Mycorrhizal Fungus Glomus Intraradices Is Regulated in Response to Phosphate in the Environment. Mol. Plant-Microbe Interact. 2001, 14, 1140–1148.
  5. Doydora, S.; Gatiboni, L.; Grieger, K.; Hesterberg, D.; Jones, J.L.; McLamore, E.S.; Peters, R.; Sozzani, R.; Van den Broeck, L.; Duckworth, O.W. Accessing Legacy Phosphorus in Soils. Soil Syst. 2020, 4, 74.
  6. Qin, Z.; Peng, Y.; Yang, G.; Feng, G.; Christie, P.; Zhou, J.; Zhang, J.; Li, X.; Gai, J. Relationship between Phosphorus Uptake via Indigenous Arbuscular Mycorrhizal Fungi and Crop Response: A 32P-Labeling Study. Appl. Soil Ecol. 2022, 180, 104624.
  7. Ahammed, G.J.; Hajiboland, R. Introduction to Arbuscular Mycorrhizal Fungi and Higher Plant Symbiosis: Characteristic Features, Functions, and Applications. In Arbuscular Mycorrhizal Fungi and Higher Plants: Fundamentals and Applications; Ahammed, G.J., Hajiboland, R., Eds.; Springer Nature: Singapore, 2024; pp. 1–17. ISBN 978-981-9982-20-2.
  8. National Center for Biotechnology Information PubChem Compound Summary for CID 15102684, 5-Deoxystrigol. Available online: https://pubchem.ncbi.nlm.nih.gov/compound/15102684 (accessed on 25 May 2024).
  9. National Center for Biotechnology Information PubChem Compound Summary for CID 5958, Glucose 6-Phosphate. Available online: https://pubchem.ncbi.nlm.nih.gov/compound/5958 (accessed on 25 May 2024).
  10. Gupta, M.; Finer-Moore, J.; Stroud, R.M. PDB Entry - 8FV- PiPT Y150A. Available online: https://www.wwpdb.org/pdb?id=pdb_00008fvz (accessed on 1 June 2024).
  11. Aggarwal, A.; Kadian, N.; Tanwar, A.; Yadav, A.; Gupta, K.K. Role of Arbuscular Mycorrhizal Fungi (AMF) in Global Sustainable Development. J. Appl. Nat. Sci. 2011, 3, 340–351.
  12. Shen, J.; Yuan, L.; Zhang, J.; Li, H.; Bai, Z.; Chen, X.; Zhang, W.; Zhang, F. Phosphorus Dynamics: From Soil to Plant. Plant Physiol. 2011, 156, 997–1005.
  13. Etesami, H.; Jeong, B.R.; Glick, B.R. Contribution of Arbuscular Mycorrhizal Fungi, Phosphate–Solubilizing Bacteria, and Silicon to P Uptake by Plant. Front. Plant Sci. 2021, 12, 699618.
  14. Yang, S.-Y.; Huang, T.-K.; Kuo, H.-F.; Chiou, T.-J. Role of Vacuoles in Phosphorus Storage and Remobilization. J. Exp. Bot. 2017, 68, 3045–3055.
  15. Qi, S.; Wang, J.; Wan, L.; Dai, Z.; da Silva Matos, D.M.; Du, D.; Egan, S.; Bonser, S.P.; Thomas, T.; Moles, A.T. Arbuscular Mycorrhizal Fungi Contribute to Phosphorous Uptake and Allocation Strategies of Solidago Canadensis in a Phosphorous-Deficient Environment. Front. Plant Sci. 2022, 13, 831654.
  16. Chen, L.; Liu, Y. The Function of Root Exudates in the Root Colonization by Beneficial Soil Rhizobacteria. Biology 2024, 13, 95.
  17. Chiu, C.H.; Paszkowski, U. Mechanisms and Impact of Symbiotic Phosphate Acquisition. Cold Spring Harb. Perspect. Biol. 2019, 11, a034603.
  18. National Center for Biotechnology Information PubChem Compound Summary for CID 1003, Dihydrogenphosphate. Available online: https://pubchem.ncbi.nlm.nih.gov/compound/1003 (accessed on 25 May 2024).
  19. National Center for Biotechnology Information PubChem Compound Summary for CID 18985873, Alkaline Phosphatase. Available online: https://pubchem.ncbi.nlm.nih.gov/compound/18985873 (accessed on 25 May 2024).
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license; additional terms may apply. By using this site, you agree to the Terms and Conditions and Privacy Policy.
This entry is offline, you can click here to edit this entry!
ScholarVision Creations
Feedback