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植物–丛枝菌根真菌共生的研究进展
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Abstract:
植物与丛枝菌根真菌(Arbuscular Mycorrhizal Fungi, AMF)共生是自然界中最常见的共生现象之一。菌根共生促进植物磷营养吸收，同时植物以脂肪酸和糖的形式给菌根真菌提供其发育所需的碳源。菌根真菌在根的皮层细胞中形成高度分支的树形结构，称为丛枝。丛枝是共生体间双向营养交换的中介，被认为是共生体的核心功能单位。提高菌根共生介导的营养吸收对植物本身的生长具有重大意义。本文概述了植物和丛枝菌根真菌建立共生的过程，并总结了在共生关系中起关键作用的重要蛋白，为丛枝菌根共生的研究提供理论基础。
Symbiosis between plants and arbuscular mycorrhizal fungi (AMF) is one of the most common symbiosis phenomena in nature. Mycorrhizal symbiosis promotes phosphorus nutrient absorption by plants, and at the same time, plants provide mycorrhizal fungi with carbon sources needed for their development in the form of fatty acids and sugars. Mycorrhizal fungi form highly branched tree-like structures called arbuscules in the cortical cells of the roots. Arbuscules are the mediators of two-way nutrient exchange between symbionts and are considered to be the core functional unit of symbionts. Improving mycorrhizal symbiosis-mediated nutrient uptake is of great significance to the growth of the plant itself. This article outlines the process of establishing symbiosis between plants and arbuscular mycorrhizal fungi, and summarizes the important proteins that play a key role in the symbiotic relationship, providing a theoretical basis for the study of arbuscular mycorrhizal symbiosis.
| [1] | Shi, J., Wang, X. and Wang, E. (2023) Mycorrhizal Symbiosis in Plant Growth and Stress Adaptation: From Genes to Ecosystems. Annual Review of Plant Biology, 74, 569-607. https://doi.org/10.1146/annurev-arplant-061722-090342 |
| [2] | Remy, W., Taylor, T.N., Hass, H., et al. (1994) Four Hundred-Million-Year-Old Vesicular Arbuscular Mycorrhizae. Proceedings of the National Academy of Sciences of the United States of America, 91, 11841-11843. https://doi.org/10.1073/pnas.91.25.11841 |
| [3] | Helber, N., Wippel, K., Sauer, N., et al. (2011) A Versatile Monosaccharide Transporter that Operates in the Arbuscular Mycorrhizal Fungus Glomus sp Is Crucial for the Symbiotic Relationship with Plants. The Plant Cell, 23, 3812-3823. https://doi.org/10.1105/tpc.111.089813 |
| [4] | Spanu, P.D., Abbott, J.C., Amselem, J., et al. (2010) Genome Expansion and Gene Loss in Powdery Mildew Fungi Reveal Tradeoffs in Extreme Parasitism. Science, 330, 1543-1546. https://doi.org/10.1126/science.1194573 |
| [5] | Leigh, J., Hodge, A. and Fitter, A.H. (2009) Arbuscular Mycorrhizal Fungi Can Transfer Substantial Amounts of Nitrogen to Their Host Plant from Organic Material. The New Phytologist, 181, 199-207. https://doi.org/10.1111/j.1469-8137.2008.02630.x |
| [6] | Shi, J., Zhao, B., Zheng, S., et al. (2021) A Phosphate Starvation Response-Centered Network Regulates Mycorrhizal Symbiosis. Cell, 184, 5527-5540. https://doi.org/10.1016/j.cell.2021.09.030 |
| [7] | Bucher, M. (2007) Functional Biology of Plant Phosphate Uptake at Root and Mycorrhiza Interfaces. The New Phytologist, 173, 11-26. https://doi.org/10.1111/j.1469-8137.2006.01935.x |
| [8] | Harrison, M.J. and Van Buuren, M.L. (1995) A Phosphate Transporter from the Mycorrhizal Fungus Glomus versiforme. Nature, 378, 626-629. https://doi.org/10.1038/378626a0 |
| [9] | Poulsen, K.H., Nagy, R., Gao, L.-L., et al. (2005) Physiological and Molecular Evidence for Pi Uptake via the Symbiotic Pathway in a Reduced Mycorrhizal Colonization Mutant in Tomato Associated with a Compatible Fungus. The New Phytologist, 168, 445-454. https://doi.org/10.1111/j.1469-8137.2005.01523.x |
| [10] | Javot, H., Penmetsa, R.V., Terzaghi, N., et al. (2007) A Medicago truncatula Phosphate Transporter Indispensable for the Arbuscular Mycorrhizal Symbiosis. Proceedings of the National Academy of Sciences of the United States of America, 104, 1720-1725. https://doi.org/10.1073/pnas.0608136104 |
| [11] | Maeda, D., Ashida, K., Iguchi, K., et al. (2006) Knockdown of an Arbuscular Mycorrhiza-Inducible Phosphate Transporter Gene of Lotus japonicus Suppresses Mutualistic Symbiosis. Plant & Cell Physiology, 47, 807-817. https://doi.org/10.1093/pcp/pcj069 |
| [12] | Van der Heijden, M.G.A., Martin, F.M., Selosse, M.A., et al. (2015) Mycorrhizal Ecology and Evolution: The Past, the Present, and the Future. The New Phytologist, 205, 1406-1423. https://doi.org/10.1111/nph.13288 |
| [13] | Bago, B., Pfeffer, P.E. and Shachar-Hill, Y. (2000) Carbon Metabolism and Transport in Arbuscular Mycorrhizas. Plant Physiology, 124, 949-958. https://doi.org/10.1104/pp.124.3.949 |
| [14] | Fitter, A.H. (2005) Darkness Visible: Reflections on Underground Ecology. Journal of Ecology, 93, 231-243. https://doi.org/10.1111/j.0022-0477.2005.00990.x |
| [15] | Buee, M., Rossignol, M., Jauneau, A., et al. (2000) The Pre-Symbiotic Growth of Arbuscular Mycorrhizal Fungi Is Induced by a Branching Factor Partially Purified from Plant Root Exudates. Molecular Plant-Microbe Interactions: MPMI, 13, 693-698. https://doi.org/10.1094/MPMI.2000.13.6.693 |
| [16] | Chabaud, M., Genre, A., Sieberer, B.J., et al. (2011) Arbuscular Mycorrhizal Hyphopodia and Germinated Spore Exudates Trigger Ca2 Spiking in the Legume and Nonlegume Root Epidermis. The New Phytologist, 189, 347-355. https://doi.org/10.1111/j.1469-8137.2010.03464.x |
| [17] | Al-Babili, S. and Bouwmeester, H.J. (2015) Strigolactones, a Novel Carotenoid-Derived Plant Hormone. Annual Review of Plant Biology, 66, 161-186. https://doi.org/10.1146/annurev-arplant-043014-114759 |
| [18] | Hayward, A., Stirnberg, P., Beveridge, C., et al. (2009) Interactions between Auxin and Strigolactone in Shoot Branching Control. Plant Physiology, 151, 400-412. https://doi.org/10.1104/pp.109.137646 |
| [19] | Proust, H., Hoffmann, B., Xie, X., et al. (2011) Strigolactones Regulate Protonema Branching and Act as a Quorum Sensing-Like Signal in the Moss Physcomitrella Patens. Development, 138, 1531-1539. https://doi.org/10.1242/dev.058495 |
| [20] | Akiyama, K., Matsuzaki, K. and Hayashi, H. (2005) Plant Sesquiterpenes Induce Hyphal Branching in Arbuscular Mycorrhizal Fungi. Nature, 435, 824-827. https://doi.org/10.1038/nature03608 |
| [21] | Gomez-Roldan, V., Fermas, S., Brewer, P.B., et al. (2008) Strigolactone Inhibition of Shoot Branching. Nature, 455, 189-194. https://doi.org/10.1038/nature07271 |
| [22] | Lopez-Obando, M., Ligerot, Y., Bonhomme, S., et al. (2015) Strigolactone Biosynthesis and Signaling in Plant Development. Development, 142, 3615-3619. https://doi.org/10.1242/dev.120006 |
| [23] | Yoneyama, K., Yoneyama, K., Takeuchi, Y., et al. (2007) Phosphorus Deficiency in Red Clover Promotes Exudation of Orobanchol, the Signal for Mycorrhizal Symbionts and Germination Stimulant for Root Parasites. Planta, 225, 1031-1038. https://doi.org/10.1007/s00425-006-0410-1 |
| [24] | Nadal, M., Sawers, R., Naseem, S., et al. (2017) An N-Acetylglucosamine Transporter Required for Arbuscular Mycorrhizal Symbioses in Rice and Maize. Nat Plants, 3, Article 17073. https://doi.org/10.1038/nplants.2017.73 |
| [25] | Besserer, A., Bécard, G., Jauneau, A., et al. (2008) GR24, a Synthetic Analog of Strigolactones, Stimulates the Mitosis and Growth of the Arbuscular Mycorrhizal Fungus Gigaspora rosea by Boosting Its Energy Metabolism. Plant Physiology, 148, 402-413. https://doi.org/10.1104/pp.108.121400 |
| [26] | Genre, A., Chabaud, M., Balzergue, C., et al. (2013) Short-Chain Chitin Oligomers from Arbuscular Mycorrhizal Fungi Trigger Nuclear Ca2 Spiking in Medicago truncatula Roots and Their Production Is Enhanced by Strigolactone. The New Phytologist, 198, 190-202. https://doi.org/10.1111/nph.12146 |
| [27] | Besserer, A., Puech-Pagès, V., Kiefer, P., et al. (2006) Strigolactones Stimulate Arbuscular Mycorrhizal Fungi by Activating Mitochondria. PLOS Biology, 4, e226. https://doi.org/10.1371/journal.pbio.0040226 |
| [28] | Chabaud, M., Venard, C., Defaux-Petras, A., et al. (2002) Targeted Inoculation of Medicago truncatula in vitro Root Cultures Reveals MtENOD11 Expression during Early Stages of Infection by Arbuscular Mycorrhizal Fungi. The New Phytologist, 156, 265-273. https://doi.org/10.1046/j.1469-8137.2002.00508.x |
| [29] | Maillet, F., Poinsot, V., André, O., et al. (2011) Fungal Lipochitooligosaccharide Symbiotic Signals in Arbuscular Mycorrhiza. Nature, 469, 58-63. https://doi.org/10.1038/nature09622 |
| [30] | Kosuta, S., Chabaud, M., Lougnon, G., et al. (2003) A Diffusible Factor from Arbuscular Mycorrhizal Fungi Induces Symbiosis-Specific MtENOD11 Expression in Roots of Medicago truncatula. Plant Physiology, 131, 952-962. https://doi.org/10.1104/pp.011882 |
| [31] | Oláh, B., Brière, C., Bécard, G., et al. (2005) Nod Factors and a Diffusible Factor from Arbuscular Mycorrhizal Fungi Stimulate Lateral Root Formation in Medicago truncatula via the DMI1/DMI2 Signalling Pathway. The Plant Journal: For Cell and Molecular Biology, 44, 195-207. https://doi.org/10.1111/j.1365-313X.2005.02522.x |
| [32] | Gutjahr, C., Novero, M., Guether, M., et al. (2009) Presymbiotic Factors Released by the Arbuscular Mycorrhizal Fungus Gigaspora margarita Induce Starch Accumulation in Lotus japonicus Roots. The New Phytologist, 183, 53-61. https://doi.org/10.1111/j.1469-8137.2009.02871.x |
| [33] | Kuhn, H., Küster, H. and Requena, N. (2010) Membrane Steroid-Binding Protein 1 Induced by a Diffusible Fungal Signal Is Critical for Mycorrhization in Medicago truncatula. The New Phytologist, 185, 716-733. https://doi.org/10.1111/j.1469-8137.2009.03116.x |
| [34] | Oldroyd, G.E. (2013) Speak, Friend, and Enter: Signalling Systems that Promote Beneficial Symbiotic Associations in Plants. Nature Reviews Microbiology, 11, 252-263. https://doi.org/10.1038/nrmicro2990 |
| [35] | Akiyama, K. and Hayashi, H. (2006) Strigolactones: Chemical Signals for Fungal Symbionts and Parasitic Weeds in Plant Roots. Annals of Botany, 97, 925-931. https://doi.org/10.1093/aob/mcl063 |
| [36] | Harrison, M.J. (2005) Signaling in the Arbuscular Mycorrhizal Symbiosis. Annual Review of Microbiology, 59, 19-42. https://doi.org/10.1146/annurev.micro.58.030603.123749 |
| [37] | Bonfante, P. and Genre, A. (2010) Mechanisms Underlying Beneficial Plant-Fungus Interactions in Mycorrhizal Symbiosis. Nature Communications, 1, Article No. 48. https://doi.org/10.1038/ncomms1046 |
| [38] | Genre, A., Chabaud, M., Faccio, A., et al. (2008) Prepenetration Apparatus Assembly Precedes and Predicts the Colonization Patterns of Arbuscular Mycorrhizal Fungi within the Root Cortex of Both Medicago truncatula and Daucus carota. The Plant Cell, 20, 1407-1420. https://doi.org/10.1105/tpc.108.059014 |
| [39] | Parniske, M. (2008) Arbuscular Mycorrhiza: The Mother of Plant Root Endosymbioses. Nature Reviews Microbiology, 6, 763-775. https://doi.org/10.1038/nrmicro1987 |
| [40] | Sieberer, B.J., Chabaud, M., Fournier, J., et al. (2012) A Switch in Ca2 Spiking Signature Is Concomitant with Endosymbiotic Microbe Entry into Cortical Root Cells of Medicago truncatula. The Plant Journal: For Cell and Molecular Biology, 69, 822-830. https://doi.org/10.1111/j.1365-313X.2011.04834.x |
| [41] | Genre, A., Chabaud, M., Timmers, T., et al. (2005) Arbuscular Mycorrhizal Fungi Elicit a Novel Intracellular Apparatus in Medicago truncatula Root Epidermal Cells before Infection. The Plant Cell, 17, 3489-3499. https://doi.org/10.1105/tpc.105.035410 |
| [42] | Harrison, M.J., Dewbre, G.R. and Liu, J. (2002) A Phosphate Transporter from Medicago truncatula Involved in the Acquisition of Phosphate Released by Arbuscular Mycorrhizal Fungi. The Plant Cell, 14, 2413-2429. https://doi.org/10.1105/tpc.004861 |
| [43] | Kobae, Y. and Fujiwara, T. (2014) Earliest Colonization Events of Rhizophagus irregularis in Rice Roots Occur Preferentially in Previously Uncolonized Cells. Plant & Cell Physiology, 55, 1497-1510. https://doi.org/10.1093/pcp/pcu081 |
| [44] | Kobae, Y., Tamura, Y., Takai, S., et al. (2010) Localized Expression of Arbuscular Mycorrhiza-Inducible Ammonium Transporters in Soybean. Plant & Cell Physiology, 51, 1411-1415. https://doi.org/10.1093/pcp/pcq099 |
| [45] | Pumplin, N., Mondo, S.J., Topp, S., et al. (2010) Medicago truncatula Vapyrin Is a Novel Protein Required for Arbuscular Mycorrhizal Symbiosis. The Plant Journal: For Cell and Molecular Biology, 61, 482-494. https://doi.org/10.1111/j.1365-313X.2009.04072.x |
| [46] | Takeda, N., Sato, S., Asamizu, E., et al. (2009) Apoplastic Plant Subtilases Support Arbuscular Mycorrhiza Development in Lotus japonicus. The Plant Journal: For Cell and Molecular Biology, 58, 766-777. https://doi.org/10.1111/j.1365-313X.2009.03824.x |
| [47] | Takeda, N., Maekawa, T. and Hayashi, M. (2012) Nuclear-Localized and Deregulated Calcium-and Calmodulin-Dependent Protein Kinase Activates Rhizobial and Mycorrhizal Responses in Lotus japonicus. The Plant Cell, 24, 810-822. https://doi.org/10.1105/tpc.111.091827 |
| [48] | Pumplin, N., Zhang, X., Noar, R.D., et al. (2012) Polar Localization of a Symbiosis-Specific Phosphate Transporter Is Mediated by a Transient Reorientation of Secretion. Proceedings of the National Academy of Sciences of the United States of America, 109, E665-E672. https://doi.org/10.1073/pnas.1110215109 |
| [49] | Gutjahr, C. and Parniske, M. (2013) Cell and Developmental Biology of Arbuscular Mycorrhiza Symbiosis. Annual Review of Cell and Developmental Biology, 29, 593-617. https://doi.org/10.1146/annurev-cellbio-101512-122413 |
| [50] | Demchenko, K., Winzer, T., Stougaard, J., et al. (2004) Distinct Roles of Lotus japonicus SYMRK and SYM15 in Root Colonization and Arbuscule Formation. The New Phytologist, 163, 381-392. https://doi.org/10.1111/j.1469-8137.2004.01123.x |
| [51] | Kistner, C., Winzer, T., Pitzschke, A., et al. (2005) Seven Lotus japonicus Genes Required for Transcriptional Reprogramming of the Root during Fungal and Bacterial Symbiosis. The Plant Cell, 17, 2217-2229. https://doi.org/10.1105/tpc.105.032714 |
| [52] | Yang, S.Y., Gr？nlund, M., Jakobsen, I., et al. (2012) Nonredundant Regulation of Rice Arbuscular Mycorrhizal Symbiosis by Two Members of the Phosphate Transporter1 Gene Family. The Plant Cell, 24, 4236-4251. https://doi.org/10.1105/tpc.112.104901 |
