Propionate serves as a degradable control agent of citrus canker by acidifying cytoplasm and depleting intracellular ATP in Xanthomonas citri
Chaoying Liu,
Jingtian Zhang,
Meirui Song,
Xiaoli Wang,
Weiwei Lv,
Xiaojun Ding,
Junan Zhu,
Yunfei Deng,
Yifei Ge,
Jian Wu,
Utpal Handique,
Shuo Duan,
Yue Shen,
Feng Luo,
Shi Xiao,
Xiaofeng Zhou
Affiliations
Chaoying Liu
State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, School of Agriculture and Biotechnology, Sun Yat-sen University, Shenzhen, Guangdong, China
Jingtian Zhang
State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, School of Agriculture and Biotechnology, Sun Yat-sen University, Shenzhen, Guangdong, China
Meirui Song
State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, School of Agriculture and Biotechnology, Sun Yat-sen University, Shenzhen, Guangdong, China
Xiaoli Wang
State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, School of Agriculture and Biotechnology, Sun Yat-sen University, Shenzhen, Guangdong, China
Weiwei Lv
State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, School of Agriculture and Biotechnology, Sun Yat-sen University, Shenzhen, Guangdong, China
Xiaojun Ding
State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, School of Agriculture and Biotechnology, Sun Yat-sen University, Shenzhen, Guangdong, China
Junan Zhu
State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, School of Agriculture and Biotechnology, Sun Yat-sen University, Shenzhen, Guangdong, China
Yunfei Deng
State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, School of Agriculture and Biotechnology, Sun Yat-sen University, Shenzhen, Guangdong, China
Yifei Ge
State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, School of Agriculture and Biotechnology, Sun Yat-sen University, Shenzhen, Guangdong, China
Jian Wu
Potato Engineering & Technology Research Center, Inner Mongolia University, Hohhot, Inner Mongolia, China
Utpal Handique
Potato Engineering & Technology Research Center, Inner Mongolia University, Hohhot, Inner Mongolia, China
Shuo Duan
National Navel Orange Engineering Research Center, Gannan Normal University, Ganzhou, Jiangxi, China
Yue Shen
BGI-Shenzhen, Beishan Industrial Zone, Shenzhen, China
Feng Luo
School of Computing, Clemson University, Clemson, South Carolina, USA
Shi Xiao
State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, School of Agriculture and Biotechnology, Sun Yat-sen University, Shenzhen, Guangdong, China
Xiaofeng Zhou
State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, School of Agriculture and Biotechnology, Sun Yat-sen University, Shenzhen, Guangdong, China
ABSTRACT Citrus canker, caused by Xanthomonas citri subsp. citri (Xcc), poses a substantial threat to global citrus production. Current disease control relies on the widespread application of copper-based bactericides. However, the excessive and recurrent use of copper has resulted in adverse outcomes, such as the emergence of copper-resistant strains and detrimental impacts on both the environment and human health. In this study, we demonstrate that propionate effectively inhibits the growth of Xanthomonas citri and is degradable by soil microbes, making it a promising and economic alternative for citrus canker management. Propionate exerts pleiotropic effects on Xcc by disrupting membrane potential, motility, and the type III secretion system. It acts as a bacteriostatic agent by acidifying the bacterial cytoplasm and disrupting proton homeostasis, which depletes intracellular ATP and induces cell dormancy. Through a Tn5 mutant library screen, we identified a propionate-sensitive mutant with a disrupted prpC gene, part of the prp operon, which is involved in propionate metabolism and regulated by PrpR. PrpR represses the prp operon by binding to a palindromic motif in the prpB promoter region. Our findings highlight propionate as a favorable control agent for citrus bacterial canker, offering effective disease management while mitigating the environmental and health concerns associated with copper-based treatments.IMPORTANCECitrus canker severely impacts citrus production, threatening a major fruit industry. Traditionally, managing this disease has depended on copper-based bactericides, which bring significant downsides, including copper resistance in pathogens and environmental toxicity. This study identifies propionate as a promising alternative to copper treatments for combating citrus canker caused by Xanthomonas citri subsp. citri. Propionate offers a dual benefit: it disrupts essential bacterial functions, effectively controlling the pathogen, and it is biodegradable in soil, which reduces environmental impact. Our findings show that propionate acidifies cytoplasm and disrupts critical bacterial processes such as membrane potential and motility, while depleting intracellular ATP and inducing cell dormancy. Propionate, therefore, emerges as an eco-friendly, cost-effective option for sustainable management of citrus bacterial canker, addressing both agricultural and environmental challenges in citrus production.
