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Journal of Integrative Agriculture
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Acidic environment favors the development and pathogenicity of the grape white rot fungus Coniella vitis
YUAN Li-fang1, JIANG Hang2, LIU Qi-bao1, JIANG Xi-long1, WEI Yan-feng1, YIN Xiang-tian1#, LI Ting-gang1#

1 Shandong Academy of Grape, Shandong Academy of Agricultural Sciences, Jinan 250100, China

2 Institute of Plant Protection, Shandong Academy of Agricultural Sciences, Jinan 250100, China

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摘要  环境pH是调控植物病原真菌生长、繁殖和致病性的重要因素。葡萄白腐病在全球范围内均有发生,严重影响了葡萄产业的发展。本研究检测了不同pH环境对葡萄白腐病菌(Coniella vitis)生长、产孢和致病的影响,结果表明,在碱性pH条件下,C. vitis的生长速率、产孢能力和致病性显著下降。通过对C. vitis酸性(pH=5)、中性(pH=7)和碱性环境(pH=9)条件下转录组和代谢组进行分析,结果表明,与寄主pHpH=3)相比,在pH 5pH 7pH 9中分别鉴定出72817803386个差异表达基因(DEGs),以及2122个差异表达代谢物(DEMs)。其中,大部分DEGs参与碳水化合物代谢过程、跨膜转运、三羧酸循环(TCA)、肽代谢过程、酰胺生物合成过程和有机酸代谢过程。代谢组学分析显示,ABC转运体、生物碱生物合成和类胡萝卜素生物合成途径响应环境pH变化。此外,在碱性环境中,TCA相关的天冬氨酸合成代谢途径C. vitis生长发育的关键限制因素,补充天冬氨酸后,C. vitis的生长速率显著加快;同时研究发现,琥珀酸、苹果酸和柠檬酸通过TCA可以逆转天冬氨酸合成抑制的作用。细胞壁降解酶(PCWDEs和真菌毒素是C. vitis重要的致病因子,在pH9环境条件下,PCWDEs和真菌毒素(aflatrem)相关合成基因显著下调,C. vitis分泌PCWDEs的能力显著降低,致病力丧失。综上所述,酸性环境有利于C. vitis的菌丝生长、孢子形成及萌发,碱性条件不利于C. vitis的侵染和致病。本研究揭示了C. vitis在不同pH环境下的生长和致病机制,可为葡萄白腐病防控策略的制定提供科学依据。

Abstract  Grape white rot caused by Coniella vitis is a global concern in the grape industry. pH regulation is essential for cell growth, reproductive processes and pathogenicity in phytopathogenic fungi. In this study, we observed that the growth rate, spore production and virulence of C. vitis significantly declined in alkaline pH, as well as the suppressive effect on secretion of hydrolytic enzymes. Transcriptomic and metabolomic analyses were used to investigate the responses of C. vitis to acidic (pH=5), neutral (pH=7) and alkaline environments (pH=9). We identified 728, 1780 and 3386 differentially expressed genes (DEGs) at pH 5, pH 7 and pH 9, when compared with the host pH (pH=3), and 2122 differently expressed metabolites (DEMs) in negative and positive ion mode. Most DEGs were involved in carbohydrate metabolic process, transmembrane transport, tricarboxylic acid cycle, peptide metabolic process, amide biosynthetic process, and organic acid metabolic process. In addition, metabolomic analysis revealed ABC transporters, indole alkaloid biosynthesis, diterpenoid biosynthesis, and carotenoid biosynthesis pathways in response to the pH change. Furthermore, we found that the aspartate synthesis metabolic route associated with the TCA cycle is a key limiting factor for the growth and development of C. vitis in alkaline environments, and aspartate supplementation enables C. vitis to grow in alkaline environments. Plant cell wall-degrading enzymes (PCWDEs) could contribute to the pathogenicity, when C. vitis infected at pH 3. Importantly, aflatrem biosynthesis in acidic environment might contribute to the virulence of C. vitis and has a risk of causing human health problems due to its acute neurotoxic effects.
Keywords:  grape white rot       ambient pH       growth       pathogenicity       transcriptomic       metabolome  
Online: 25 January 2024  
About author:  YUAN-Lifang, E-mail: ylifang1225@126.com; #Correspondence YIN Xiang-tian, E-mail: yxt1985@163.com; LI Ting-gang, E-mail: weifengluolu@126.com

Cite this article: 

YUAN Li-fang, JIANG Hang, LIU Qi-bao, JIANG Xi-long, WEI Yan-feng, YIN Xiang-tian, LI Ting-gang. 2024. Acidic environment favors the development and pathogenicity of the grape white rot fungus Coniella vitis. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2024.01.002

Alkan N, Espeso E A, Prusky D. 2013. Virulence regulation of phytopathogenic fungi by pH. Antioxidants & Redox Signaling, 19, 1012–1025.

Alshannaq A, Yu J H. 2017. Occurrence, toxicity, and analysis of major mycotoxins in food. International Journal of Environmental Reaearch and Public Health, 14, 632.

Barda O, Maor U, Sadhasivam S, Bi Y, Zakin V, Prusky D, Sionov E. 2020. The pH-Responsive transcription factor PacC governs pathogenicity and ochratoxin a biosynthesis in Aspergillus carbonarius. Frontiers in Microbiology, 11, 210.

Berenbaum M, Calla B, 2021a. Editorial overview: Cytochrome P450s in plant-insect interactions: new insights on gut reactions. Current Opinion Insect Science, 43, vi–ix.

Berenbaum M R, Bush D S, Liao L H. 2021b. Cytochrome P450-mediated mycotoxin metabolism by plant-feeding insects. Current Opinion Insect Science, 43, 85–91.

Bethke G, Grundman R E, Sreekanta S, Truman W, Katagiri F, Glazebrook J. 2014. Arabidopsis pectin methylesterases contribute to immunity against Pseudomonas syringae. Plant Physiology, 164, 1093–1107.

Billon-Grand G, Rascle C, Droux M, Rollins J A, Poussereau N. 2012. pH modulation differs during sunflower cotyledon colonization by the two closely related necrotrophic fungi Botrytis cinerea and Sclerotinia sclerotiorum. Molecular Plant Pathology, 13, 568–578.

Birsoy K, Wang T, Chen W W, Freinkman E, Abu-Remaileh M, Sabatini D M. 2015. An essential role of the mitochondrial electron transport chain in cell proliferation is to enable aspartate synthesis. Cell, 162, 540–551.

Burbidge C A, Ford C M, Melino V J, Wong D C J, Jia Y, Jenkins C L D, Kathleen L S, Castellarin S D, Darriet P, Rienth M, Bonghi C, Walker R P, Famiani F, Sweetman C. 2021. Biosynthesis and cellular functions of tartaric acid in grapevines. Frontiers in Plant Science, 12, 643024.

Cadenas S, 2018. Mitochondrial uncoupling, ROS generation and cardioprotection. Biochimica er Biophysica Acta. Bioenergetics, 1859, 940–950.

Chang H X, Yendrek C R, Caetano-Anolles G, Hartman G L. 2016. Genomic characterization of plant cell wall degrading enzymes and in silico analysis of xylanases and polygalacturonases of Fusarium virguliforme. BMC Microbiology, 16, 147.

Chatterjee A, Cui Y, Liu Y, Dumenyo C K, Chatterjee A K. 1995. Inactivation of rsmA leads to overproduction of extracellular pectinases, cellulases, and proteases in Erwinia carotovora subsp. carotovora in the absence of the starvation/cell density-sensing signal, N-(3-oxohexanoyl)-L-homoserine lactone. Applied and Environmental Microbiology, 61, 1959–1967.

Chethana K W T, Zhou Y, Zhang W, Liu M, Xing Q K, Li X H, Yan J Y, Chethana K W T, Hyde K D. 2017. Coniella vitis sp. nov. is the common pathogen of white rot in Chinese vineyards. Plant Disease, 101, 2123–2136.

Choi J, Kim K T, Jeon J, Lee Y H. 2013. Fungal plant cell wall-degrading enzyme database: a platform for comparative and evolutionary genomics in fungi and Oomycetes. BMC Genomics, 14, S7.

Espino J J, Gutiérrez-Sánchez G, Brito N, Shah P, Orlando R, González C. 2010. The Botrytis cinerea early secretome. Proteomics, 10, 3020–3034.

Farh M E, Abdellaoui N, Seo J A. 2021. pH changes have a profound effect on gene expression, hydrolytic enzyme production, and dimorphism in Saccharomycopsis fibuligera. Frontiers in Microbiology, 12, 672661.

Fernie A R, Carrari F, Sweetlove L J, 2004. Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport. Current Opinion in Plant Biology, 7, 254–261.

Fonseca-García C, León-Ramírez C G, Ruiz-Herrera J. 2012. The regulation of different metabolic pathways through the Pal/Rim pathway in Ustilago maydis. FEMS Yeast Research, 12, 547–56.

Fueki S, Tokiwano T, Toshima H, Oikawa H. 2004. Biosynthesis of indole diterpenes, emindole, and paxilline: involvement of a common intermediate. Organic Letters, 6, 2697–2700.

Gordon T R, Stueven M, Pastrana A M, Henry P M, Dennehy C M, Kirkpatrick C, Daugovish O. 2019. The effect of pH on spore germination, growth, and infection of strawberry roots by Fusarium oxysporum f. sp. fragariae, cause of fusarium wilt of strawberry. Plant Disease, 103, 697–704.

He Z, Cui C, Jiang J. 2017. First report of white rot of grape caused by Pilidiella castaneicola in China, 101.

Ji T, Languasco L, Li M, Rossi V. 2021. Effects of temperature and wetness duration on infection by Coniella diplodiella, the fungus causing white rot of grape berries. Plants, 10, 1696.

Jimdjio C K, Xue H, Bi Y, Nan M, Li L, Zhang R, Liu Q, Pu L. 2021. Effect of ambient pH on growth, pathogenicity, and patulin production of Penicillium expansum. Toxins, 13, 550.

Juntachai W, Chaichompoo A, Chanarat S. 2020. Ambient pH regulates secretion of lipases in Malassezia furfur. Microbiology, 166, 288–295.

Kukurba K R, Montgomery S B. 2015. RNA sequencing and analysis. Cold Spring Harbor Protocols, 2015, 951–969.

Landraud P, Chuzeville S, Billon-Grande G, Poussereau N, Bruel C. 2013. Adaptation to pH and role of PacC in the rice blast fungus Magnaporthe oryzae. PLoS One, 8, e69236.

Lane A N, Fan T W. 2015. Regulation of mammalian nucleotide metabolism and biosynthesis. Nucleic Acids Research, 43, 2466–2485.

Lazar E E, Wills R B, Ho B T, Harris A M, Spohr L J. 2008. Antifungal effect of gaseous nitric oxide on mycelium growth, sporulation and spore germination of the postharvest horticulture pathogens, Aspergillus niger, Monilinia fructicola and Penicillium italicum. Letters in Applied. Microbiology, 46, 688–692.

Li B, Lai T, Qin G, Tian S. 2010. Ambient pH stress inhibits spore germination of Penicillium expansum by impairing protein synthesis and folding: a proteomic-based study. Journal Proteome Research, 9, 298–307.

Li B, Zhang C, Cao B, Qin G, Wang W, Tian S. 2012. Brassinolide enhances cold stress tolerance of fruit by regulating plasma membrane proteins and lipids. Amino Acids, 43, 2469–2480.

Li D, Wan Y, Wang Y, He P. 2008. Relatedness of resistance to anthracnose and to white rot in Chinese wild grapes. Vitis, 47, 213–215.

Li L, Hao B, Zhang Y, Ji S, Chou G. 2020. Metabolite profiling and distribution of militarine in rats using UPLC-Q-TOF-MS/MS. Molecules, 25, 1082.

Li S, Zhang X, Li Y, Tao L, Li T. 2020. Optimization of pH conditions to improve the spore production of Clostridium butyricum NN-2 during fermentation process. Archives Microbiology, 202, 1251–1256.

Liew W P, Mohd-Redzwan S. 2018. Mycotoxin: its impact on gut health and microbiota. Frontiers in Cellular and Infection Microbiology, 8, 60.

Liu R, Wang Y, Li P, Sun L, Jiang J, Fan X, Liu C, Zhang Y. 2021. Genome assembly and transcriptome analysis of the fungus Coniella diplodiella during infection on grapevine (Vitis vinifera L.). Frontiers in Microbiology, 11, 599150.

Liu Y, Qu J, Shi Z, Zhang P, Ren M. 2021. Comparative genomic analysis of the tricarboxylic acid cycle members in four Solanaceae vegetable crops and expression pattern analysis in Solanum tuberosum. BMC Genomics, 22, 821.

Manteau S. 2003. Differential regulation by ambient pH of putative virulence factor secretion by the phytopathogenic fungus Botrytis cinerea. FEMS. Microbiology Ecology, 43, 359–366.

Markina-Iñarrairaegui A, Spielvogel A, Etxebeste O, Ugalde U, Espeso E A. 2020. Tolerance to alkaline ambient pH in Aspergillus nidulans depends on the activity of ENA proteins. Scientific Reports, 10, 14325.

Mhaindarkar D, Gasper R, Lupilov N, Hofmann E, Leichert L I. 2018. Loss of a conserved salt bridge in bacterial glycosyl hydrolase BgIM-G1 improves substrate binding in temperate environments. Communications Biology, 1, 171.

Nicholson M J, Koulman A, Monahan B J, Pritchard B L, Payne G A, Scott B. 2009. Identification of two aflatrem biosynthesis gene loci in Aspergillus flavus and metabolic engineering of Penicillium paxilli to elucidate their function. Applied and Environmental Microbiology, 75, 7469–7481.

Prusky D, Alkan N, Mengiste T, Fluhr R. 2013. Quiescent and necrotrophic lifestyle choice during postharvest disease development. Annual Review of Phytopathology, 51, 155–176.

Prusky D, McEvoy J L, Leverentz B, Conway W S. 2001. Local modulation of host pH by Colletotrichum species as a mechanism to increase virulence. Molecular Plant-Microbe Interactions, 14, 1105–1113.

Qin J, Li B, Zhou S. 2020. A novel glycoside hydrolase 74 xyloglucanase CvGH74A is a virulence factor in Coniella vitis. Journal of Integrative Agriculture, 19, 2725–2735.

Rascle C, Dieryckx C, Dupuy J W, Muszkieta L, Souibgui E, Droux M, Bruel C, Girard V, Poussereau. 2018. The pH regulator PacC: a host-dependent virulence factor in Botrytis cinerea. Environmental Microbiology Reports, 10, 555–568.

Rippke F, Berardesca E, Weber T M. 2018. pH and microbial infections. Current Problems Dermatology, 54, 87–94.

Sazanov L. 2015. A giant molecular proton pump: structure and mechanism of respiratory complex I. Nature Reviews. Molecular Cell Biology, 16, 375–388.

Sella L, Castiglioni C, Paccanaro M C, Janni M, Schäfer W, D'Ovidio R, Favaron F. 2016. Involvement of fungal pectin methylesterase activity in the interaction between Fusarium graminearum and Wheat. Molecular Plant-Microbe Interactions29, 258–267.

Shi L, Tu B P. 2015. Acetyl-CoA and the regulation of metabolism: mechanisms and consequences. Current Opinion in Cell Biology, 33, 125–131.

Sun L, Liu L, Wang Y, Feng Y, Yang W, Wang D, Gao S, Miao X, Sun W. 2022. Integration of metabolomics and transcriptomics for investigating the tolerance of foxtail millet (Setaria italica) to atrazine stress. Frontiers in Plant Science, 13:890550.

ten Have A, Mulder W, Visser J, van Kan J A. 1998. The endopolygalacturonase gene Bcpg1 is required for full virulence of Botrytis cinerea. Molecular Plant-Microbe. Interactions, 11, 1009–1016.

Tizro P, Choi C, Khanlou N. 2019. Sample preparation for transmission electron microscopy. Methods in Molecular Biology, 1897, 417–424.

Valdes J J, Cameron J E, Cole R J. 1985. Aflatrem: a tremorgenic mycotoxin with acute neurotoxic effects. Environmental Health Perspectives, 62, 459–463.

Valette-Collet O, Cimerman A, Reignault P, Levis C, Boccara M. 2003. Disruption of Botrytis cinerea pectin methylesterase gene Bcpme1 reduces virulence on several host plants. Molecular Plant-Microbe Interactions, 16, 360–367.

Wang Q, Sun J, Wang W, Ren W, Li B, Zhou S. 2023. Baseline sensitivity of Coniella vitis to fluazinam and resistance risk assessment. Plant Pathology, 72, 807–818.

Wetzel D, McBride S M. 2020. The Impact of pH on clostridioides difficile sporulation and physiology. Applied and Environmental Microbiology, 86, e02706-19.

Yang X, Gu C Y, Sun J Z, Bai Y, Zang H Y, Chen Y. 2021. Biological activity of pyraclostrobin against Coniella granati causing pomegranate crown rot. Plant Disease, 105, 3538–3544.

Yin X, Li T, Wei Y, Liu Q, Jiang X, Yuan L. 2023. First report of Coniella vitis causing white rot on Virginia creeper (Parthenocissus quinquefolia [L.] Planch.) in China. Plant Disease, 9, 27.

Yuan L, Yin X, Jiang X, Li T, Wei Y. 2022. Identification of the pathogen Coniella vitis causing grape white rot in Shandong province, Acta Phytopathologica Sinica, 53, 729–733.

Zhang J, Liang L, Xie Y, Zhao Z, Su L, Tang Y, Sun B, Lai Y, Li H. 2022. Transcriptome and metabolome analyses reveal molecular responses of two pepper (Capsicum annuum L.) cultivars to cold stress. Frontiers in Plant Science, 13, 819630.

Zhang Y, Yao J L, Feng H, Jiang J, Fan X, Jia Y F, Wang R, Liu C. 2019. Identification of the defense-related gene VdWRKY53 from the wild grapevine Vitis davidii using RNA sequencing and ectopic expression analysis in Arabidopsis. Hereditas, 156, 14.

Zhou S, Li B. 2020. Genome sequence resource of Coniella vitis, a fungal pathogen causing grape white rot disease. Molecular Plant-Microbe Interactions, 33, 787–789. 

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