丛枝菌根真菌效应蛋白研究进展

doi:10.11983/CBB25079

摘要/Abstract

摘要： 丛枝菌根真菌(AMF)能与约80%的陆生植物形成共生关系, 其通过根内独特的丛枝结构与宿主细胞紧密接触, 建立双向养分交换界面。这种互惠机制不仅增强了植物抗逆性, 还重塑了生态系统养分循环。与病原真菌类似, AMF的细胞壁也主要由几丁质和β-葡聚糖组成, 这些都是诱导宿主植物免疫反应的主要模式分子。菌根真菌如何有效的躲避宿主植物免疫反应目前尚不清晰, 但病原真菌分泌的效应蛋白被发现对抑制植物免疫反应具有重要作用。在丛枝菌根共生过程中, 大量效应蛋白被诱导表达, 这些效应蛋白可能也会抑制植物的免疫反应, 促进菌根真菌对宿主植物的侵染过程。本文对AMF效应蛋白的研究现状进行了阐述和总结, 并展望了未来研究方向与挑战。对效应蛋白的研究有助于阐明AMF对共生过程建立和维持的调控机理, 加深对互作双方的全面了解, 选育具有最适共生效率的菌株和植物品种, 促进农业可持续发展。

关键词: 效应蛋白, 菌根共生, 免疫反应, 丛枝菌根真菌, 植物-真菌互作

Abstract: Arbuscular mycorrhizal fungi (AMF) can form symbiotic relationships with approximately 80% of terrestrial plants. Through their unique arbuscular structures within roots, they establish close contact with host cells to create a bidirectional nutrient exchange interface. This mutualistic mechanism not only enhances plant stress resistance but also reshapes ecosystem nutrient cycling. Like pathogenic fungi, the cell walls of AMF are primarily composed of chitin and β-glucans, which are key molecular patterns capable of triggering host plant immune responses. How AMF effectively evades host plant immunity remains unclear. Effector proteins secreted by pathogenic fungi have been found to play a crucial role in suppressing plant immune responses. During arbuscular mycorrhizal symbiosis, numerous effector proteins are also induced, which may similarly inhibit plant immunity and facilitate fungal colonization. This article reviewed and summarized current research on AMF effector proteins and discussed the future research directions and challenges. Studying effector proteins will help elucidate the regulatory mechanisms underlying the establishment and maintenance of AMF symbiosis, deepen our understanding of host-fungal interactions, and aid in selecting optimal fungal strains and plant varieties for enhanced symbiotic efficiency, thereby promoting sustainable agricultural development.

Key words: Effectors, mycorrhizal symbiosis, defense response, arbuscular mycorrhizal fungi, plant-fungi interaction

张月璇, 王鹏. 丛枝菌根真菌效应蛋白研究进展. 植物学报, DOI: 10.11983/CBB25079.

Yuexuan Zhang, Peng Wang. Research Progress on Effectors of Arbuscular Mycorrhizal Fungi. Chinese Bulletin of Botany, DOI: 10.11983/CBB25079.

导出引用管理器 EndNote|Ris|BibTeX

链接本文: https://www.chinbullbotany.com/CN/10.11983/CBB25079

参考文献

[1]M. Parniske(Oct. 2008).Arbuscular mycorrhiza: the mother of plant root endosymbioses,.Nat Rev Microbiol, 6:763-775.
[2]L. H. Luginbuehl and G. E. D. Oldroyd(Sep. 2017).Understanding the Arbuscule at the Heart of Endomycorrhizal Symbioses in Plants.Current Biology, 27:R952-R963.
[3]Jiang Y, Wang W, Xie Q, Liu N, Liu L, Wang D, Zhang X, Yang C, Chen X, Tang D, et al(Jun. 2017).Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi.Science (1979), 356:1172-1175.
[4]J Shi, X. Wang, and E. Wang,(May 2023).Mycorrhizal Symbiosis in Plant Growth and Stress Adaptation: From Genes to Ecosystems.Annu Rev Plant Biol, 74:569-607.
[5]Tan X, Wang D, Zhang X, Zheng S, Jia X, Liu H, Liu Z, Yang H, Dai H, Chen X, et al.(Mar. 2025).A pair of LysM receptors mediates symbiosis and immunity discrimination in Marchantia.Cell, 188:1330-1348.e27.
[6]S.Shi, X. Luo, X. Dong, Y. Qiu, C. Xu, and X. He(May 2021).Arbuscular Mycorrhization Enhances Nitrogen, Phosphorus and Potassium Accumulation in Vicia faba by Modulating Soil Nutrient Balance under Elevated CO2.Journal of Fungi, 7:361-/.
[7]S. Ivanov and M. J. Harrison(Jan. 2024).Receptor-associated kinases control the lipid provisioning program in plant–fungal symbiosis.Science (1979), 383:443-448.
[8]Wang P, Jiang H, Boeren S, Dings H, Kulikova O, Bisseling T, and Limpens E.(May 2021).A nuclear‐targeted effector of Rhizophagus irregularis interferes with histone 2B mono‐ubiquitination to promote arbuscular mycorrhization,.New Phytologist, 230,:1142-1155.
[9]K. Kuchitsu(Mar. 1993).N-Acetylchitooligosaccharides, biotic elicitor for phytoalexin production, induce transient membrane depolarization in suspension-cultured rice cells.Protoplasma, 176:89-/.
[10]G. Felix, M. Regenass, and T. Boller,(Aug. 1993).Specific perception of subnanomolar concentrations of chitin fragments by tomato cells: induction of extracellular alkalinization, changes in protein phosphorylation, and establishment of a refractory state.The Plant Journal, vol. 4:307-316.
[11]J. Granado, G. Felix, and T. Boller(Feb. 1995).Perception of Fungal Sterols in Plants (Subnanomolar Concentrations of Ergosterol Elicit Extracellular Alkalinization in Tomato Cells).Plant Physiol, 107:485-490.
[12]C. W. Basse and T. Boller(Apr. 1992).Glycopeptide Elicitors of Stress Responses in Tomato Cells.Plant Physiol, 98:1239-1247.
[13]S. Kloppholz, H. Kuhn, and N. Requena(Jul. 2011).A Secreted Fungal Effector of Glomus intraradices Promotes Symbiotic Biotrophy.Current Biology, 21:1204-1209.
[14]T. Boller and G. Felix(Jun. 2009).A Renaissance of Elicitors: Perception of Microbe-Associated Molecular Patterns and Danger Signals by Pattern-Recognition Receptors.Annu Rev Plant Biol,, 60:379-406.
[15]J. M. Plett and F. Martin(Aug. 2015).Reconsidering mutualistic plant–fungal interactions through the lens of effector biology.Curr Opin Plant Biol, 26:45-50.
[16]C. Selin, T. R. de Kievit, M. F. Belmonte, and W. G. D. Fernando(Apr. 2016).Elucidating the Role of Effectors in Plant-Fungal Interactions: Progress and Challenges.Front Microbiol, 7:/-/.
[17]S. A. Hogenhout, R. A. L. Van der Hoorn, R. Terauchi, and S. Kamoun(Feb. 2009).Emerging Concepts in Effector Biology of Plant-Associated Organisms.Molecular Plant-Microbe Interactions, 22:115-122.
[18]J. Sperschneider and P. N. Dodds(Feb. 2022).EffectorP 3.0: Prediction of Apoplastic and Cytoplasmic Effectors in Fungi and Oomycetes.Molecular Plant-Microbe Interactions, 35:146-156.
[19]Jaswal R, Kiran K, Rajarammohan S, Dubey H, Singh PK, Sharma Y, Deshmukh R, Sonah H, Gupta N, and Sharma TR(Dec. 2020).Effector Biology of Biotrophic Plant Fungal Pathogens: Current Advances and Future Prospects.Microbiol Res, 241:126567-/.
[20]Liu T, Song T, Zhang X, Yuan H, Su L, Li W, Xu J, Liu S, Chen L, Chen T, et al(Aug. 2014).Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis.Nat Commun, 5:4686-/.
[21]J. Sperschneider, P. N. Dodds, D. M. Gardiner, J. M. Manners, K. B. Singh, and J. M. Taylor(May 2015).Advances and Challenges in Computational Prediction of Effectors from Plant Pathogenic Fungi.PLoS Pathog, 11:e1004806-/.
[22]Belair M, Restrepo-Leal JD, Praz C, Fontaine F, Rémond C, Fernandez O, and Besaury L.(May 2023).Botryosphaeriaceae gene machinery: Correlation between diversity and virulence.Fungal Biol, 127:1010-1031.
[23]Wang Y, Zhao S, Zhang B, Ma H-Y, Fang W-H, Sheng W-Q, Yang L-G, and Li X-C(Feb. 2020).A novel ML domain-containing protein (SpMD2) functions as a potential LPS receptor involved in anti-Vibrio immune response.Dev Comp Immunol, 103:103529-/.
[24]S. Cord-Landwehr, R. L. J. Melcher, S. Kolkenbrock, and B. M. Moerschbacher,(Nov. 2016).A chitin deacetylase from the endophytic fungus Pestalotiopsis sp. efficiently inactivates the elicitor activity of chitin oligomers in rice cells.Sci Rep, 6:38018-/.
[25]Zeng T, Holmer R, Hontelez J, te Lintel‐Hekkert B, Marufu L, de Zeeuw T, Wu F, Schijlen E, Bisseling T, and Limpens E(May 2018).Host‐ and stage‐dependent secretome of the arbuscular mycorrhizal fungus Rhizophagus irregularis.The Plant Journal, 94:411-425.
[26]M. V. Aparicio Chacón, J. Van Dingenen, and S. Goormachtig(May 2023).Characterization of Arbuscular Mycorrhizal Effector Proteins.Int J Mol Sci, 24:9125-/.
[27]Lin K, Limpens E, Zhang Z, Ivanov S, Saunders DGO, Mu D, Pang E, Cao H, Cha H, Lin T, et al.(Jan. 2014).Single Nucleus Genome Sequencing Reveals High Similarity among Nuclei of an Endomycorrhizal Fungus.PLoS Genet, 10:e1004078-/.
[28]Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A, Balestrini R, Charron P, Duensing N, Frei dit Frey N, Gianinazzi-Pearson V, et al.(Dec. 2013).Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis.Proceedings of the National Academy of Sciences, 110:20117-20122.
[29]Kamel L, Tang N, Malbreil M, San Clemente H, Le Marquer M, Roux C, and Frei dit Frey N.(Dec. 2017).Corrigendum: The Comparison of Expressed Candidate Secreted Proteins from Two Arbuscular Mycorrhizal Fungi Unravels Common and Specific Molecular Tools to Invade Different Host Plants.Front Plant Sci, 8:/-/.
[30]Zeng T, Rodriguez‐Moreno L, Mansurkhodzaev A, Wang P, van den Berg W, Gasciolli V, Cottaz S, Fort S, Thomma BPHJ, Bono J, et al.(Jan. 2020).A lysin motif effector subverts chitin‐triggered immunity to facilitate arbuscular mycorrhizal symbiosis.New Phytologist, 225:448-460.
[31]S. Vo?, R. Betz, S. Heidt, N. Corradi, and N. Requena(Sep. 2018).RiCRN1, a Crinkler Effector From the Arbuscular Mycorrhizal Fungus Rhizophagus irregularis, Functions in Arbuscule Development.Front Microbiol, 9:/-/.
[32]S. Tsuzuki, Y. Handa, N. Takeda, and M. Kawaguchi(Apr. 2016).Strigolactone-Induced Putative Secreted Protein 1 Is Required for the Establishment of Symbiosis by the Arbuscular Mycorrhizal Fungus Rhizophagus irregularis.Molecular Plant-Microbe Interactions?, 29:277-286.
[33]N. Helber, K. Wippel, N. Sauer, S. Schaarschmidt, B. Hause, and N. Requena(Oct. 2011).A Versatile Monosaccharide Transporter That Operates in the Arbuscular Mycorrhizal Fungus Glomus sp Is Crucial for the Symbiotic Relationship with Plants.Plant Cell, 23:3812-3823.
[34]Xie X, Lin H, Peng X, Xu C, Sun Z, Jiang K, Huang A, Wu X, Tang N, Salvioli A, et al.(Dec. 2016).Arbuscular Mycorrhizal Symbiosis Requires a Phosphate Transceptor in the Gigaspora margarita Fungal Symbiont.Mol Plant, 9:1583-1608.
[35]Tournier B, Sanchez-Ballesta MT, Jones B, Pesquet E, Regad F, Latché A, Pech J-C, and Bouzayen(Aug. 2003).New members of the tomato ERF family show specific expression pattern and diverse DNA‐binding capacity to the GCC box element.FEBS Lett, 550:149-154.
[36]Huang P-Y, Zhang J, Jiang B, Chan C, Yu J-H, Lu Y-P, Chung K, and Zimmerli L.(Feb. 2019).NINJA-associated ERF19 negatively regulates Arabidopsis pattern-triggered immunity.J Exp Bot, 70:1033-1047.
[37]R. Betz, S. Heidt, D. Figueira-Galán, M. Hartmann, T. Langner, and N. Requena(Aug. 2024).Alternative splicing regulation in plants by SP7-like effectors from symbiotic arbuscular mycorrhizal fungi.Nat Commun, 15:7107-/.
[38]G. B. Akcapinar, L. Kappel, O. U. Sezerman, and V. Seidl-Seiboth(May 2015).Molecular diversity of LysM carbohydrate-binding motifs in fungi.Curr Genet, 61:103-113.
[39]A. M. Schmitz, T. E. Pawlowska, and M. J. Harrison(Jan. 2019).A short LysM protein with high molecular diversity from an arbuscular mycorrhizal fungus, Rhizophagus irregularis.Mycoscience, 60:63-70.
[40]D. Zhang, A. M. Burroughs, N. D. Vidal, L. M. Iyer, and L. Aravind(May 2016).Transposons to toxins: the provenance, architecture and diversification of a widespread class of eukaryotic effectors.Nucleic Acids Res, 44:3513-3533.
[41]Farrer RA, Martel A, Verbrugghe E, Abouelleil A, Ducatelle R, Longcore JE, James TY, Pasmans F, Fisher MC, and Cuomo CA(Mar. 2017).Genomic innovations linked to infection strategies across emerging pathogenic chytrid fungi,.Nat Commun, 8:14742-/.
[42]Shen D, Liu T, Ye W, Liu L, Liu P, Wu Y, Wang Y, and Dou D.(Jul. 2013).Gene Duplication and Fragment Recombination Drive Functional Diversification of a Superfamily of Cytoplasmic Effectors in Phytophthora sojae.PLoS One, 8:e70036-/.
[43]B. N. Adhikari, J. P. Hamilton, M. M. Zerillo, N. Tisserat, C. A. Lévesque, and C. R. Buell,(Oct. 2013).Comparative Genomics Reveals Insight into Virulence Strategies of Plant Pathogenic Oomycetes.PLoS One, 8:e75072-/.
[44]McCombe CL, Wegner A, Wirtz L, Zamora CS, Casanova F, Aditya S, Greenwood JR, de Paula S, England E, Shang S, et al.(Feb. 2025).Plant pathogenic fungi hijack phosphate signaling with conserved enzymatic effectors.Science (1979), 387:955-962.
[45]L. B. Martínez-García and F. I. Pugnaire(Jul. 2011).Arbuscular mycorrhizal fungi host preference and site effects in two plant species in a semiarid environment.Applied Soil Ecology, 48:313-317.
[46]E. Torrecillas, M. M. Alguacil, and A. Roldán(Sep. 2012).Host Preferences of Arbuscular Mycorrhizal Fungi Colonizing Annual Herbaceous Plant Species in Semiarid Mediterranean Prairies.Appl Environ Microbiol, 78:6180-6186.
[47]B. Ji and J. D. Bever(May 2016).Plant preferential allocation and fungal reward decline with soil phosphorus: implications for mycorrhizal mutualism.Ecosphere, 7:/-/.