<em>UeSho1</em>调节菰黑粉菌致病力的作用研究

doi:10.3969/j.issn.1674-7968.2025.05.015

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Abstract Ustilago esculenta exclusively infected Zizania latifolia and could enlarge the host stems to form edible Jiaobai. Its pathogenicity was closely related to the formation and phenotypic differentiation of Jiaobai. It was found that synthetic high osmolarity- sensitive protein (Sho1), as an environmental signal receptor upstream of the high osmolarity glycerol (HOG) pathway, plays an important role in the regulation of fungal pathogenicity. In order to study the role of Sho1 in the regulation of the pathogenicity of U. esculenta, the UeSho1 gene (GenBank No. MW768948.1) was cloned and identified. Its open reading frame was 1 137 bp in length with one 126 bp intron, encoding 336 amino acids including a SH3 conserved domain. It was obviously induced expressed during in vitro mycelial growth and infection process of U. esculenta. Further in vitro growth and infection experiments were carried out after knocking out UeSho1 in U. esculenta, and the results showed that the deletion of UeSho1 did not affect the haploid morphology, growth rate, or mating process of U. esculenta in vitro, but it inhibited the filamentous growth of mycelia, slowed down the infection process, and suppressed the expression of b signaling pathway genes related to pathogenicity. Additionally, the absence of UeSho1 did not affect the growth state of U. esculenta in vitro under osmotic, temperature or oxidative stress. This study reveals the critical role of UeSho1 in the regulation of U. esculenta pathogenicity and provides a theoretical basis for further exploration of its role in the interaction between U. esculenta and Zizania latifolia, particularly in inducing host stem swelling.

Key words： Ustilago esculenta Synthetic high osmolarity- sensitive protein (Sho1) Pathogenicity Filamentous growth

Received: 31 July 2024

ZTFLH:

S645.2

Corresponding Authors: **zjsxhwz@163.com

About author:: * These authors contributed equally to this work

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	ZHANG Ya-Fen
	FENG Yu-Chen
	HU Ying-Li
	YE Zi-Hong
	TANG Jin-Tian
	WU Jun-Cheng
	XIE Lu
	HU Miao-Dan

Cite this article:

ZHANG Ya-Fen,FENG Yu-Chen,HU Ying-Li, et al. Study on the Role of UeSho1 in Regulating the Pathogenicity of Ustilago esculenta[J]. 农业生物技术学报, 2025, 33(5): 1117-1129.

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https://journal05.magtech.org.cn/Jwk_ny/EN/10.3969/j.issn.1674-7968.2025.05.015 OR https://journal05.magtech.org.cn/Jwk_ny/EN/Y2025/V33/I5/1117

[1] 胡映莉. 2021. 菰黑粉菌UeSho1和UeMsb2的功能研究[D]. 硕士学位论文, 中国计量大学, 导师: 张雅芬, pp. 18.(Hu Y L. 2021. Functional properties of UeSho1 and UeMsb2 in Ustilago esculenta[D].Thesis for M.S., China Jiliang University, Supervisor: Zhang Y F. pp. 18.)
[2] 殷淯梅, 张雅芬, 曹乾超, 等. 2019. 茭白人工孕茭体系的建立及优化[J]. 农业生物技术学报, 27(08): 1498-1512.
(Yin Y M, Zhang Y F, Cao Q C, et al.2019. Establishment and optimization of the artificial system for the formation of Jiaobai[J]. Journal of Agricultural Biotechnology, 27(08): 1498-1512.)
[3] Boisnard S, Ruprich-Robert G, Florent M, et al.2008. Role of Sho1p adaptor in the pseudohyphal development, drugs sensitivity, osmotolerance and oxidant stress adaptation in the opportunistic yeast Candida lusitaniae[J]. Yeast (Chichester, England), 25(11): 849-859.
[4] Brachmann A, Schirawski J, Müller P, et al.2003. An unusual MAP kinase is required for efficient penetration of the plant surface by Ustilago maydis[J]. The EMBO Journal, 22(9): 2199-2210.
[5] Brewster J L, Gustin M C.2014. Hog1: 20 years of discovery and impact[J]. Science Signaling, 7(343): re7.
[6] Day A M, Quinn J.2019. Stress-activated protein kinases in human fungal pathogens[J]. Frontiers in Cellular and Infection Microbiology, 9: 261.
[7] Flora B, Ira H.1994. Morphological transitions in the life cycle of Ustilago maydis and their genetic control by the a and b loci[J]. Experimental Mycology,18(3): 247-266.
[8] Fukada F, Rössel N, Münch K, et al.2021. A small Ustilago maydis effector acts as a novel adhesin for hyphal aggregation in plant tumors[J]. The New Phytologist, 231(1): 416-431.
[9] García P M, Baeza M L, Gold S E, et al.2010. Regulation of Ustilago maydis dimorphism, sporulation, and pathogenic development by a transcription factor with a highly conserved APSES domain[J]. Molecular Plant-microbe Interactions: MPMI, 23(2): 211-222.
[10] Gauthier G M.2015. Dimorphism in fungal pathogens of mammals, plants, and insects[J]. PLOS Pathogens, 11(2): e1004608.
[11] Gu Q, Chen Y, Liu Y.2015. The transmembrane protein FgSho1 regulates fungal development and pathogenicity via the MAPK module Ste50-Ste11-Ste7 in Fusarium graminearum[J]. The New Phytologist, 206(1): 315-328.
[12] Guo H B, Li S M, Peng J, et al.2007. Zizania latifolia Turcz. cultivated in China[J]. Genetic Resources and Crop Evolution, 54(6): 1211-1217.
[13] Heimel K, Scherer M, Vranes M, et al.2010. The transcription factor Rbf1 is the master regulator for b-mating type controlled pathogenic development in Ustilago maydis[J]. PLOS Pathogens, 6(8): e1001035.
[14] Klosterman S J, Perlin M H, Garcia-Pedrajas M, et al.2007. Genetics of morphogenesis and pathogenic development of Ustilago maydis[J]. Advances in Genetics, 57: 1-47.
[15] Konte T, Terpitz U, Plemenitaš A, et al.2016. Reconstruction of the high-osmolarity glycerol (HOG) signaling pathway from the halophilic fungus Wallemia ichthyophaga in Saccharomyces cerevisiae[J]. Frontiers in Microbiology, 7: 901.
[16] Lam M H, Snider J, Rehal M, et al.2015. A comprehensive membrane interactome mapping of Sho1p reveals Fps1p as a Novel key player in the regulation of the HOG pathway in S. cerevisiae[J]. Journal of Molecular Biology, 27(11): 2088-2103.
[17] Lanver D, Mendoza A., Brachmann A, et al.2010. Sho1 and Msb2 related proteins regulate appressorium development in the smut fungus Ustilago maydis[J]. The Plant Cell, 22(6): 2085-2101.
[18] Lanver D, Müller A N, Happel P, et al.2018. The biotrophic development of Ustilago maydis studied by RNA-Seq analysiss[J]. The Plant Cell, 30(2): 300-323.
[19] Liu W, Zhou X, Li G, et al.2011. Multiple plant surface signals are sensed by different mechanisms in the rice blast fungus for appressorium formation[J]. PLOS Pathogens, 7(1): e1001261
[20] Ma Y, Qiao J, Liu W, et al.2008. The sho1 sensor regulates growth, morphology, and oxidant adaptation in Aspergillus fumigatus but is not essential for development of invasive pulmonary aspergillosis[J]. Infection and Immunity, 76(4): 1695-1701.
[21] Maeda T, Takekawa M, Saito H, et al.1995. Activation of yeast PBS2 MAPKK by MAPKKKs or by binding of an SH3-containing osmosensor[J]. Science, 269(5223): 554-558.
[22] Matei A, Doehlemann G.2016. Cell biology of corn smut disease-Ustilago maydis as a model for biotrophic interactions[J]. Current Opinion in Microbiology, 34: 60-66.
[23] Mendoza A, Eskova A, Weise C, et al.2009. Hap2 regulates the pheromone response transcription factor prf1 in Ustilago maydis[J]. Molecular Microbiology, 72(3): 683-698.
[24] Meike P, Matthias S, Franz O, et al.2002. The generic position of Ustilago maydis, Ustilago scitaminea, and Ustilago esculenta (Ustilaginales)[J]. Mycological Progress, 1(1): 71-80.
[25] Nadal M, García-Pe M D, Gold S E.et al.2008. Dimorphism in fungal plant pathogens[J]. FEMS Microbiology Letters, 284(2): 127-134.
[26] O'Rourke S M, Herskowitz I.2002. A third osmosensing branch in Saccharomyces cerevisiae requires the Msb2 protein and functions in parallel with the Sho1 branch[J]. Molecular and Cellular Biology, 22(13): 4739-4749.
[27] Perez N E, Di P A.2015. The transmembrane protein Sho1 cooperates with the mucin Msb2 to regulate invasive growth and plant infection in Fusarium oxysporum[J]. Molecular Plant Pathology, 16(6): 593-603.
[28] Pothiratana C.2007. Functional characterization of the homeodomain transcription factor Hdp1 in Ustilago maydis[D]. Thesis for ph. D., Dissertation of the Faculty of Biology, Philipps-University Marburg, Germany, Supervisor: Bölker M, pp. 18-25.
[29] Ramezani R M.2003. The role of adaptor protein Ste50-dependent regulation of the MAPKKK Ste11 in multiple signalling pathways of yeast[J]. Current Genetics, 43(3): 161-170.
[30] Ren W, Liu N, Yang Y, et al.2019. The sensor proteins BcSho1 and BcSln1 are involved in, though not essential to, vegetative differentiation, pathogenicity and osmotic stress tolerance in Botrytis cinerea[J]. Frontiers in Microbiology, 10: 328.
[31] Román E, Nombela C, Pla J.2005. The Sho1 adaptor protein links oxidative stress to morphogenesis and cell wall biosynthesis in the fungal pathogen Candida albicans[J]. Molecular and Cellular Biology, 25(23): 10611-10627.
[32] Tatebayashi K, Yamamoto K, Tanaka K, et al.2006. Adaptor functions of Cdc42, Ste50, and Sho1 in the yeast osmoregulatory HOG MAPK pathway[J]. The EMBO Journal, 25(13): 3033-3044
[33] Tatebayashi K, Yamamoto K, Nagoya M, et al.2015. Osmosensing and scaffolding functions of the oligomeric four-transmembrane domain osmosensor Sho1[J]. Nature Communications, 6:6975.
[34] Tollot M, Assmann D, Becker C, et al.2016. The WOPR protein Ros1 is a master regulator of sporogenesis and late effector gene expression in the maize pathogen Ustilago maydis[J]. PLOS Pathog, 12(6): e1005697.
[35] Wang Z, An N, Xu W, et al.2018 Functional characterization of the upstream components of the Hog1-like kinase cascade in hyperosmotic and carbon sensing in Trichoderma reesei[J]. Biotechnology for Biofuels, 11: 97.
[36] Wang X, Lu D, Tian C.2021. Mucin Msb2 cooperates with the transmembrane protein Sho1 in various plant surface signal sensing and pathogenic processes in the poplar anthracnose fungus Colletotrichum gloeosporioides[J]. Molecular Plant Pathology, 22(12): 1553-1573.
[37] Wang J, Huang Z, Huang P, et al.2022. The plant homeodomain protein Clp1 regulates fungal development, virulence, and autophagy homeostasis in Magnaporthe oryzae[J]. Microbiology Spectrum, 10(5): e0102122.
[38] Yamamoto K, Tatebayashi K, Saito H.2015. Binding of the extracellular eight-cysteine motif of Opy2 to the putative osmosensor Msb2 is essential for activation of the yeast high-osmolarity glycerol pathway[J]. Molecular and Cellular Biology, 36(3): 475-487.
[39] Yan Z, Sun S, Shahid M, et al.2007. Environment factors can influence mitochondrial inheritance in the fungus Cryptococcus neoformans[J]. Fungal Genetics and Biology, 44(5): 315-322.
[40] Yang F, Ma D, Wan Z, et al.2011. The role of sho1 in polarized growth of Aspergillus fumigatus[J]. Mycopathologia, 172(5): 347-355.
[41] Ye Z H, Pan Y, Zhang Y F, et al.2017. Comparative whole-genome analysis reveals artificial selection effects on Ustilago esculenta genome[J]. DNA Research, 24(6): 635-648.
[42] You W, Liu Q, Zou K Q, et al.2011. Morphological and molecular differences in two strains of Ustilago esculenta[J]. Current Microbiology, 62(1): 44-54.
[43] Yu J, Zhang Y, Cui H, et al.2015. An efficient genetic manipulation protocol for Ustilago esculenta[J]. FEMS Microbiology Letters, 362(12): fnv087.
[44] Zhao Y, Song Z, Zhong L, et al.2019. Inferring the origin of cultivated Zizania latifolia, an aquatic vegetable of a plant-fungus complex in the Yangtze River Basin[J]. Front Plant, 10: 01406.
[45] Zhang Y F, Cao Q C, Hu P, et al.2017. Investigation on the differentiation of two Ustilago esculenta strains implications of a relationship with the host phenotypes appearing in the fields[J]. BMC Microbiology, 17: 228.
[46] Zhang Y F, Hu Y L, Cao Q C, et al.2020. Functional Properties of the MAP Kinase UeKpp2 in Ustilago esculenta[J]. Frontiers in Microbiology, 11: 1053.
[47] Zhang X, Wang Z Y, Jiang C, et al.2021. Regulation of biotic interactions and responses to abiotic stresses by MAP kinase pathways in plant pathogenic fungi[J]. Stress Biology, 1(1): 5.