A novel fucosylation-specific cell wall-degrading enzyme promotes Magnaporthe oryzae infection

doi:10.1016/j.jia.2025.06.004

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A novel fucosylation-specific cell wall-degrading enzyme promotes Magnaporthe oryzae infection

Chang’an Ji, Zhao Hu, Yifang Zhang, Xia Song, Lei Su, Jintao Wang, Linxun Wu, Muxing Liu, Gang Li, Haifeng Zhang, Leiyun Yang, Xinyu Liu^#, Zhengguang Zhang^#

StateKey Laboratory of Agricultural and Forestry Biosecurity, Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University/Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing 210095, China

Highlights

1. The α-L-fucosidase MoFco1 specifically hydrolyzes XXFG, an α-1,2-fucosylated xyloglucan oligosaccharide derived from plant hemicellulose.

2. MoFco1 enzymatic activity is crucial for the full virulence of M. oryzae.

3. Compound 0989, identified through structure-based virtual screening, binds MoFco1 and significantly suppresses M. oryzae infection.

Abstract
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摘要

病原真菌与寄主互作时，病原物释放细胞壁降解酶降解植物细胞壁以促进侵染。木葡聚糖侧链的岩藻糖基化修饰是植物半纤维素中常见的糖基化形式之一，但稻瘟病菌是否通过分泌岩藻糖苷酶调控水稻木葡聚糖的岩藻糖基化水平，尚不清楚。有研究报道，禾谷镰刀菌α-L-岩藻糖苷酶FgFco1对豌豆木葡聚糖寡糖XXFG具有活性。本研究聚焦于FgFco1在稻瘟病菌中的同源蛋白MoFco1，探讨其在致病过程中的功能。通过序列比对和系统发育分析，我们发现稻瘟病菌中存在三个FgFco1同源基因，其中MoFco1与FgFco1最为相似，并在序列和结构上均高度保守。酶活检测表明，MoFco1可水解α-1,2连接的岩藻糖修饰寡糖，如2’-FL和XXFG。进一步通过定位观察发现MoFco1在侵染过程中分泌到质外体空间。进一步对MoFco1的功能进行解析，发现其调控稻瘟病菌的致病力，并且其功能依赖于其酶活。在此基础上，以AlphaFold3构建的MoFco1结构进行虚拟筛选，获得了化合物0989，采用微量热泳动技术明确0989与MoFco1结合关系，进一步实验证实，0989可显著抑制稻瘟病菌的致病力。综上，本研究揭示了MoFco1在稻瘟病菌致病过程中的关键作用，并提出靶向其酶活的抑制剂作为潜在的植物保护手段，拓展了结构生物学在病害防控中的应用前景。

Abstract

Plant pathogenic fungi release cell wall degrading enzymes (CWDEs), which are significant weapons for breaking down plant cell walls, although only a few reports focus on their pathogenesis. The current study demonstrates that MoFco1, a conserved α-L-fucosidase in several pathogenic fungi, degrades the hemicellulose component XXFG and contributes to the pathogenicity of Magnaporthe oryzae. In addition, MoFco1 enzyme activity is essential for its pathogenic function, as the enzyme activity mutation induced pathogenesis defects identical to the ΔMofco1 mutant. We further performed a structure-based virtual screening targeting MoFco1 and discovered 0989, which binds to MoFco1 and effectively inhibits M. oryzae pathogenesis. In brief, our study revealed the pathogenic mechanism of α-L-fucosidase and explored the application of structure-based virtual screening in plant protection.

Keywords: Magnaporthe oryzae α-L-fucosidase cell wall-degrading enzyme virtual screening

Online: 02 June 2025

Fund:

This research was supported by the National Key Research and Development Program of China (2022YFD1700200), the Young Elite Scientists Sponsorship Program by CAST (2022QNRC001), the Natural Science Foundation of China (NSFC) (32272496, 32293241 and 32293245). Virtual screening supported by the high-performance computing platform of Bioinformatics Center, Nanjing Agricultural University.

About author: Chang’an Ji, E-mail: 2019202011@njau.edu.cn; #Correspondence Zhengguang Zhang, E-mail: zhgzhang@njau.edu.cn; Xinyu Liu, E-mail: xinyuliu@njau.edu.cn

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Chang’an Ji, Zhao Hu, Yifang Zhang, Xia Song, Lei Su, Jintao Wang, Linxun Wu, Muxing Liu, Gang Li, Haifeng Zhang, Leiyun Yang, Xinyu Liu, Zhengguang Zhang. 2025. A novel fucosylation-specific cell wall-degrading enzyme promotes Magnaporthe oryzae infection. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.06.004

Alonso Baez L, Bacete L, Geitmann A. 2023. Cell wall dynamics: novel tools and research questions. Journal of Experimental Botany, 74: 6448-6467.

Becker DJ, Lowe JB. 2003. Fucose: biosynthesis and biological function in mammals. Glycobiology, 13: 41R-53R.

Blay V, Tolani B, Ho SP, Arkin MR. 2020. High-Throughput Screening: today’s biochemical and cell-based approaches. Drug Discovery Today, 25: 1807-1821.

Bruno KS, Tenjo F, Li L, Hamer JE, Xu J-R. 2004. Cellular localization and role of kinase activity of PMK1 in Magnaporthe grisea. Eukaryotic Cell, 3: 1525-1532.

Cao H, Walton JD, Brumm P, Phillips GN, Jr. 2014. Structure and substrate specificity of a eukaryotic fucosidase from Fusarium graminearum. Journal of Biological Chemistry, 289:25624-25638.

Cai X, Seitl I, Mu W, Zhang T, Stressler T, Fischer L, Jiang B. 2018. Biotechnical production of trehalose through the trehalose synthase pathway: current status and future prospects. Applied Microbiology and Biotechnology, 102: 2965-2976.

Chen Y, Tang L, Jiang Z, Wang S, Qi L, Tian X, Deng H, Kong Z, Gao W, Zhang X, Li S, Chen M, Zhang X, Duan H, Yang J, Peng YL, Wang D, Liu J. 2024. Dual-specificity inhibitor targets enzymes of the trehalose biosynthesis pathway. Journal of Agricultural and Food Chemistry, 72: 209-218.

Fernandez J, Marroquin-Guzman M, Wilson RA. 2014. Mechanisms of nutrient acquisition and utilization during fungal infections of leaves. Annual Review of Phytopathology, 52:155-174.

García-García A, Ceballos-Laita L, Serna S, Artschwager R, Reichardt NC, Corzana F, Hurtado-Guerrero R. 2020. Structural basis for substrate specificity and catalysis of α1,6-fucosyltransferase. Nature Communications, 11(1): 973.

Gibson DM, King BC, Hayes ML, Bergstrom GC. 2011. Plant pathogens as a source of diverse enzymes for lignocellulose digestion. Current Opinion in Microbiology, 14: 264-270.

Goldman WE, Tournu H, Fiori A, Van Dijck P. 2013. Relevance of trehalose in pathogenicity: some general rules, yet many exceptions. PLOS Pathogens, 9(8): e1003447.

Grantham NJ, Wurman-Rodrich J, Terrett OM, Lyczakowski JJ, Stott K, Iuga D, Simmons TJ, Durand-Tardif M, Brown SP, Dupree R, Busse-Wicher M, Dupree P. 2017. An even pattern of xylan substitution is critical for interaction with cellulose in plant cell walls. Nature Plants, 3:859-865.

Homma F, Huang J, van der Hoorn RAL. 2023. AlphaFold-Multimer predicts cross-kingdom interactions at the plant-pathogen interface. Nature Communications, 14(1): 6040.

Hu J, Liu M, Zhang A, Dai Y, Chen W, Chen F, Wang W, Shen D, Telebanco-Yanoria MJ, Ren B, Zhang H, Zhou H, Zhou B, Wang P, Zhang Z. 2022. Co-evolved plant and blast fungus ascorbate oxidases orchestrate the redox state of host apoplast to modulate rice immunity. Molecular Plant, 15: 1347-1366.

Jumper J, Evans R, Pritzel A, Green T, Figurnov M, Ronneberger O, Tunyasuvunakool K, Bates R, Žídek A, Potapenko A, Bridgland A, Meyer C, Kohl SAA, Ballard AJ, Cowie A, Romera-Paredes B, Nikolov S, Jain R, Adler J, Back T, Petersen S, Reiman D, Clancy E, Zielinski M, Steinegger M, Pacholska M, Berghammer T, Bodenstein S, Silver D, Vinyals O, Senior AW, Kavukcuoglu K, Kohli P, Hassabis D. 2021. Highly accurate protein structure prediction with AlphaFold. Nature, 596: 583-589.

Khan MA, Al Mamun Khan MA, Mahfuz AMUB, Sanjana JM, Ahsan A, Gupta DR, Hoque MN, Islam T. 2022. Highly potent natural fungicides identified in silico against the cereal killer fungus Magnaporthe oryzae. Scientific Reports, 12(1): 20232.

Levesque-Tremblay G, Pelloux J, Braybrook SA, Müller K. 2015. Tuning of pectin methylesterification: consequences for cell wall biomechanics and development. Planta, 242: 791-811.

Li H, Mo P, Zhang J, Xie Z, Liu X, Chen H, Yang L, Liu M, Zhang H, Wang P, Zhang Z. 2023. Methionine biosynthesis enzyme MoMet2 is required for rice blast fungus pathogenicity by promoting virulence gene expression via reducing 5mC modification. PLOS Genetics, 19(9): e1010927.

Li J, Hsu H-C, Mountz JD, Allen JG. 2018. Unmasking fucosylation: from cell adhesion to immune system regulation and diseases. Cell Chemical Biology, 25:499-512.

Liu M, Wang F, He B, Hu J, Dai Y, Chen W, Yi M, Zhang H, Ye Y, Cui Z, Zheng X, Wang P, Xing W, Zhang Z. 2024. Targeting Magnaporthe oryzae effector MoErs1 and host papain-like protease OsRD21 interaction to combat rice blast. Nature Plants, 10: 618-632.

Liu X, Qian B, Gao C, Huang S, Cai Y, Zhang H, Zheng X, Wang P, Zhang Z. 2016. The putative protein phosphatase MoYvh1 functions upstream of MoPdeH to regulate the development and pathogenicity in Magnaporthe oryzae. Molecular Plant-Microbe Interactions, 29: 496-507.

Li W, Zhan P, De Clercq E, Lou H, Liu X. 2013. Current drug research on PEGylation with small molecular agents. Progress in Polymer Science, 38: 421-444.

Li X, Gao C, Li L, Liu M, Yin Z, Zhang H, Zheng X, Wang P, Zhang Z. 2017. MoEnd3 regulates appressorium formation and virulence through mediating endocytosis in rice blast fungus Magnaporthe oryzae. PLOS Pathogens, 13: e1006449.

Lu X, Zhang D, Shoji H, Duan C, Zhang G, Isaji T, Wang Y, Fukuda T, Gu J. 2019. Deficiency of α1,6-fucosyltransferase promotes neuroinflammation by increasing the sensitivity of glial cells to inflammatory mediators. Biochimica et Biophysica Acta-General Subjects, 1863: 598-608.

Mall R, Kaushik R, Martinez ZA, Thomson MW, Castiglione F. 2025. Benchmarking protein language models for protein crystallization. Scientific Reports, 15: 2381.

Min J, Lin D, Zhang Q, Zhang J, Yu Z. 2012. Structure-based virtual screening of novel inhibitors of the uridyltransferase activity of Xanthomonas oryzae pv. oryzae GlmU. European Journal of Medicinal Chemistry, 53: 150-158.

Ma D, Xu J, Wu M, Zhang R, Hu Z, Ji C-a, Wang Y, Zhang Z, Yu R, Liu X, Yang L, Li G, Shen D, Liu M, Yang Z, Zhang H, Wang P, Zhang Z. 2024. Phenazine biosynthesis protein MoPhzF regulates appressorium formation and host infection through canonical metabolic and noncanonical signaling function in Magnaporthe oryzae. New Phytologist, 242: 211-230.

Miura K, Tsukagoshi T, Hirano T, Nishio T, Hakamata W. 2019. Development of fluorogenic Substrates of α-L-fucosidase useful for inhibitor screening and gene-expression profiling. ACS Medicinal Chemistry Letters, 10: 1309-1313.

Pan Q, Zhang X-L. 2025. Roles of core fucosylation modification in immune system and diseases. Cell Insight, 4(1): 100211.

Paper JM, Scott-Craig JS, Cavalier D, Faik A, Wiemels RE, Borrusch MS, Bongers M, Walton JD. 2013. Alpha-fucosidases with different substrate specificities from two species of Fusarium. Applied Microbiology and Biotechnology, 97:5371-5380.

Qian B, Guo L, Song C, Ji H. 2023. MoMaf1 mediates vegetative growth, conidiogenesis, and pathogenicity in the rice blast fungus Magnaporthe oryzae. Journal of Fungi, 9: 106.

Quoc NB, Bao Chau NN. 2017. The role of cell wall degrading enzymes in pathogenesis of Magnaporthe oryzae. Current Protein & Peptide Science, 18(10): 1019-1034.

Schultink A, Liu L, Zhu L, Pauly M. 2014. Structural diversity and function of xyloglucan sidechain substituents. Plants, 3: 526-542.

Skamnioti P, Gurr SJ. 2009. Against the grain: safeguarding rice from rice blast disease. Trends in Biotechnology, 27:141-150.

Talbot NJ, Ebbole DJ, Hamer JE. 1993. Identification and characterization of MPG1, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea. Plant Cell, 5: 1575-1590.39.

Sweigard JA, Chumley FG, Valent B. 1992. Disruption of a Maanaporthe arisea cutinase gene. Molecular and General Genetics 232: 183-190.

Wang B-h, Ebbole DJ, Wang Z-h. 2017. The arms race between Magnaporthe oryzae and rice: Diversity and interaction of Avr and R genes. Journal of Integrative Agriculture, 16: 2746-2760.

Wan J, He M, Hou Q, Zou L, Yang Y, Wei Y, Chen X. 2021. Cell wall associated immunity in plants. Stress Biology, 1(1): 3.

Wan J-X, Zhu X-F, Wang Y-Q, Liu L-Y, Zhang B-C, Li G-X, Zhou Y-H, Zheng S-J. 2018. Xyloglucan fucosylation modulates Arabidopsis cell wall hemicellulose aluminium binding capacity. Scientific Reports, 8(1): 428.

Wei Wang, Tianshun Hu, Patrick A. Frantom TZ, Brian Gerwe, David Soriano del Amo SG, Ronald D. Seidel I, Wu P. 2009. Chemoenzymatic synthesis of GDP-L-fucose and the Lewis X glycan derivatives. Proceedings of the National Academy of Sciences of the United States of America, 106(38): 16096-101.

Yang X, Yan S, Li G, Li Y, Li J, Cui Z, Sun S, Huo J, Sun Y. 2024. Rice-Magnaporthe oryzae interactions in resistant and susceptible rice cultivars under panicle blast infection based on defense-related enzyme activities and metabolomics. PLOS One, 19(3): e0299999.

Zhang HF, Islam T, Liu WD. 2022. Integrated pest management programme for cereal blast fungus Magnaporthe oryzae. Journal of Integrative Agriculture, 21: 3420-3433.

Zhang L, Paasch BC, Chen J, Day B, He SY. 2019. An important role of l‐fucose biosynthesis and protein fucosylation genes in Arabidopsis immunity. New Phytologist, 222: 981-994.

Zhao Z, Liu H, Wang C, Xu J-R. 2013. Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genomics, 14: 274.

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