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Journal of Integrative Agriculture  2025, Vol. 24 Issue (7): 2686-2703    DOI: 10.1016/j.jia.2024.01.002
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Acidic environment favors the development and pathogenicity of the grape white rot fungus Coniella vitis

Lifang Yuan1, Hang Jiang2, Qibao Liu1, Xilong Jiang1, Yanfeng Wei1, Xiangtian Yin1#, Tinggang Li1#

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

 Highlights 
The growth rate and pathogenicity of Coniella vitis were decreased in alkaline environments.
TCA cycle and aspartate synthesis pathway in C. vitis were sigificantly affected by the alkaline environments.
Aspartate supplementation enables C. vitis to grow under alkaline environment.
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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在酸性(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pH(pH=3)相比,在pH 5、pH 7和pH 9中分别鉴定出728、1780、3386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均响应环境pH变化。此外,在碱性环境中,与TCA相关的天冬氨酸合成代谢途径是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 Cvitis 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 Cvitis to acidic (pH 5), neutral (pH 7) and alkaline environments (pH 9).  We identified 728, 1,780 and 3,386 differentially expressed genes (DEGs) at pH 5, pH 7 and pH 9, when compared with the host pH (pH 3), and 2,122 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 Cvitis in alkaline environments, and aspartate supplementation enables Cvitis to grow in alkaline environments.  Plant cell wall-degrading enzymes (PCWDEs) could contribute to the pathogenicity, when Cvitis infected at pH 3.  Importantly, aflatrem biosynthesis in acidic environment might contribute to the virulence of Cvitis 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  
Received: 24 July 2023   Online: 05 January 2024   Accepted: 07 November 2023
Fund: This research was supported by the Shandong Provincial Natural Science Foundation, China (ZR2021QC131), the Shandong Province Key Research and Development Plan, China (2022TZXD001102), the Shandong Province Demonstration Project for Model Construction in Rural Revitalization Service, China (2022DXAL0226), and the Innovation Project of Shandong Academy of Agricultural Sciences, China (CXGC2023F15, CXGC2023A41, and CXGC2023A47).
About author:  Lifang Yuan, E-mail: ylifang1225@126.com; #Correspondence Xiangtian Yin, E-mail: yxt1985@163.com; Tinggang Li, E-mail: weifengluolu@126.com

Cite this article: 

Lifang Yuan, Hang Jiang, Qibao Liu, Xilong Jiang, Yanfeng Wei, Xiangtian Yin, Tinggang Li. 2025. Acidic environment favors the development and pathogenicity of the grape white rot fungus Coniella vitis. Journal of Integrative Agriculture, 24(7): 2686-2703.

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