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A GATA transcription factor contributes to the multidrug resistance and pathogenicity though mediating the transcription of hydrolases and xenobiotic detoxification genes in Sclerotinia sclerotiorum
Kunqin Xiao1*, Anmo Li1*, Xun Xu1, Yalan Li1, Ling Liu1,2, Songyang Gu1, Jeffrey A. Rollins3, Rui Wang1, Hongyu Pan1#, Jinliang Liu1#
1 College of Plant Sciences, Jilin University, Changchun 130062, China
2 College of Plant Protection, Jilin Agricultural University, Changchun 130118, China
3 Department of Plant Pathology, University of Florida, Gainesville, FL 32611, USA

 Highlights 

A GATA transcription factor SsGATA1 contributes to multidrug resistance by regulating the transcription of drug efflux pump genes.

SsGATA1 positively regulates pathogenicity, which is attributed to the up-regulation of hydrolases during infection.

SsGATA1 represents a new target for preventing and controlling Sclerotinia stem rot.

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摘要  

作物真菌病害主要通过选育抗病品种和使用化学杀菌剂进行防治,然而杀菌剂的抗药性是保障农作物安全生产所面临的严峻挑战。病原真菌可以通过上调药物外排泵产生多药耐药性,然而仅在少数病原真菌中报道转录因子调控药物外排泵基因表达,且局限在几类转录因子家族。挖掘调控药物外排泵基因转录的新转录因子有助于揭示植物病原真菌多药耐药性的分子机制,并为设计新药物靶点进而开发新杀菌剂提供科学指导。核盘菌(Sclerotinia sclerotiorumLibde Bary)是一种典型的死体营养型植物病原真菌寄主范围广,引致的菌核病流行性强、分布广、危害重。核盘菌可通过解毒酶降解植物的抗真菌化和各种水解酶降解植物组织但调控这些解毒酶和水解酶表达的转录因子鲜有报道。在本研究中,通过基因功能研究和转录调控分析发现,核盘菌GATA类型的转录因子SsGATA1通过与靶标基因启动子结合调控药物外排泵基因的转录,从而增强核盘菌对各种类型化学杀菌剂的耐受性;SsGATA1还通过介导异硫氰酸酯水解酶SsSaxA的转录,增强对植物源广谱抗真菌化学物质的耐受性;重要的是,通过对SsGATA1基因敲除突变体ΔSsGATA1致病性测定发现,SsGATA1正调控核盘菌的致病性,其机制是SsGATA1在侵染过程中通过对细胞壁水解酶和SsSaxA的上调来促进植物组织的水解和植物源化合物的解毒;此外,尽管SsGATA1不参与菌丝体生长、菌核形成和侵染垫的发育,但在对高温、氧化等逆境胁迫耐受中发挥作用。综上所述,本研究通过对核盘菌中GATA转录因子SsGATA1的功能分析,证明SsGATA1通过激活水解酶和外源物质解毒基因的转录,在多药耐药性和致病性中发挥作用;挖掘到一种新型药物外排泵、细胞壁水解酶和硫氰酸酯水解酶的基因转录激活因子,因此,SsGATA1可作为防控菌核病的潜在药物新靶点,基于SsGATA1在多药耐药性中的作用,抑制其功能有望增强杀菌剂药效并延缓抗药性。



Abstract  

Phytopathogenic fungi can weaken the effectiveness of anti-fungal chemicals from plants and artificial synthesis through xenobiotic detoxification system. Nevertheless, the transcription factors responsible for transcriptional activation of xenobiotic detoxification genes in phytopathogenic fungi are rarely reported. Here, we show that a GATA transcription factor SsGATA1 is regulating the transcription of drug efflux pump genes, thus contributing to the tolerance of various types of chemical fungicides, including propiconazole, caspofungin and azoxystrobin in Sclerotinia sclerotiorum. Similarly, SsGATA1 also plays the role of tolerance to isothiocyanate and flavonols, two reported as broad-spectrum anti-fungal chemicals, by mediating the transcription of isothiocyanates hydrolase SsSaxA. Importantly, SsGATA1 positively regulates pathogenicity, which is attributed to the up-regulation of hydrolases and SsSaxA during infection. Furthermore, SsGATA1 is responsible for tolerance to several stresses. Our findings demonstrated that SsGATA1 plays roles in multidrug resistance and pathogenicity by activating the transcription of hydrolases and xenobiotic detoxification genes.

Keywords:  Sclerotinia sclerotiorum        multidrug resistance        GATA transcription factor SsGATA1        transcription        pathogenicity  
Online: 10 December 2024  
Fund: 

This work was financially supported by the National Natural Science Foundation of China (32172505, 323B2055, 32272484), the Natural Science Foundation of Jilin Province (20230101156JC), the Key Research and Development Program of Jilin Province (20210202131NC), and the National Foreign Experts Program (G2023129011L).

About author:  #Correspondence Hongyu Pan, E-mail: panhongyu@jlu.edu.cn; Jinliang Liu, E-mail: jlliu@jlu.edu.cn *These authors contributed equally.

Cite this article: 

Kunqin Xiao, Anmo Li, Xun Xu, Yalan Li, Ling Liu, Songyang Gu, Jeffrey A. Rollins, Rui Wang, Hongyu Pan, Jinliang Liu. 2024. A GATA transcription factor contributes to the multidrug resistance and pathogenicity though mediating the transcription of hydrolases and xenobiotic detoxification genes in Sclerotinia sclerotiorum. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2024.12.010

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