The versatile plant probiotic bacterium Bacillus velezensis SF305 reduces red root rot disease severity in the rubber tree by degrading the mycelia of Ganoderma pseudoferreum

doi:10.1016/j.jia.2024.09.027

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The versatile plant probiotic bacterium Bacillus velezensis SF305 reduces red root rot disease severity in the rubber tree by degrading the mycelia of Ganoderma pseudoferreum

Min Tu^{1, 4*}, Zhongfeng Zhu^{2, 5*}, Xinyang Zhao³, Haibin Cai^{1, 4}, Yikun Zhang^{2, 5}, Yichao Yan^{2, 5}, Ke Yin^{2, 5}, Zhimin Sha², Yi Zhou³, Gongyou Chen^{2, 5}, Lifang Zou^{2, 5}^#

¹ National Key Laboratory for Tropical Crop Breeding, Rubber Research Institute, Chinese Academy of Tropical Agricultural Sciences, Sanya 572024, China
²Shanghai Collaborative Innovation Center of Agri-Seeds/School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, China
³School of Agriculture, Yangtze University, Jingzhou 434000, China
⁴Sanya Research Institute, Chinese Academy of Tropical Agricultural Sciences, Sanya 572020, China
⁵State Key Laboratory of Microbial Metabolism, Shanghai Jiao Tong University, Shanghai 200240, China

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摘要

【目的】本研究旨在探索一种有效的防治橡胶树红根病的生物防治策略。橡胶树红根病由橡胶灵芝菌（Ganoderma pseudoferreum）引起，对中国橡胶树产区构成较大的威胁。通过筛选具有抗真菌活性的细菌菌株，以期找到一种能够显著降低红根病严重程度的生防菌剂。【方法】我们从全国23个省份的248个根际土壤样本中分离出223株候选细菌菌株，并采用双重培养试验评估这些菌株对橡胶灵芝菌的拮抗作用。经过筛选，发现贝莱斯芽孢杆菌（Bacillus velezensis）SF305菌株对橡胶灵芝菌具有显著的拮抗活性。进一步，我们对SF305进行了基因组测序和比较基因组学分析，以确定其潜在的生防机制和植物促生长特性。此外，还通过预防和治疗试验，评估了SF305在橡胶树红根病防治上的实际应用效果。【结果】结果表明，在预防试验中，B. velezensis SF305对红根病的保护效果超过90%；而在治疗试验中，其防病效果接近70%。深入分析显示，SF305通过降解G. pseudoferreum的菌丝体来降低病害的严重程度。基因组测序揭示，SF305含有15个与次生代谢产物合成相关的基因簇，其中两个为独特基因簇，分别预测为合成罗克霉素（locillomycin）和新型非核糖体肽合成酶的基因簇。另外，SF305还含有与运动性、趋化性、生物膜形成、抗逆性、产生挥发性有机化合物以及吲哚-3-乙酸合成相关的基因，表明其具有定殖在植物根际和促进植物生长的潜力。【结论】本研究为首次报道贝莱斯芽孢杆菌作为防治橡胶树红根病的潜力生防菌剂。【创新性】本研究为橡胶树红根病的生物防治提供了新的微生物资源和防治策略，也扩展了贝莱斯芽孢杆菌在林业病害生物防治领域的应用范围；B. velezensis SF305的鉴定具有重要的科学意义和应用价值。

Abstract

Natural rubber is an indispensable material of strategic importance that has critical applications in industry and the military. However, the development of the natural rubber industry is impeded by the red root rot disease of rubber trees caused by Ganoderma pseudoferreum, which is one of the most devastating diseases in the rubber tree growing regions in China. To combat this disease, we screened the antifungal activity of 223 candidate bacterial strains against G. pseudoferreum, and found that Bacillus velezensis strain SF305 exhibited significant antifungal activity against G. pseudoferreum. B. velezensis SF305 had a nearly 70% efficacy against the red root rot disease of rubber trees with the therapeutic treatment (Tre), while it exhibited over 90% protection effectiveness with the preventive treatment (Pre). The underlying biocontrol mechanism revealed that B. velezensis SF305 could reduce the disease severity of red root rot by degrading the mycelia of G. pseudoferreum. An antiSMASH analysis revealed that B. velezensis SF305 contains 15 gene clusters related to secondary metabolite synthesis, 13 of which are conserved in species of B. velezensis, but surprisingly, B. velezensis SF305 possesses 2 unique secondary metabolite gene clusters. One is predicted to synthesize locillomycin, and the other is a novel nonribosomal peptides synthetase (NRPS) gene cluster. Genomic analysis showed that B. velezensis SF305 harbors genes involved in motility, chemotaxis, biofilm formation, stress resistance, volatile organic compounds (VOCs) and synthesis of the auxin indole-3-acetic acid (IAA), suggesting its plant growth-promoting rhizobacteria (PGPR) properties. B. velezensis SF305 can promote plant growth and efficiently antagonize some important phytopathogenic fungi and bacteria. This study indicates that B. velezensis SF305 is a versatile plant probiotic bacterium. To the best of our knowledge, this is the ﬁrst time a B. velezensis strain has been reported as a promising biocontrol agent against the red root rot disease of rubber trees.

Keywords: Bacillus velezensis Ganoderma pseudoferreum red root rot disease rubber tree biocontrol comparative genomics

Online: 26 September 2024

Fund:

This work was ﬁnancially supported by the National Key Research and Development Program of China (2023YFD1200204 to Min Tu) and the Special Fund for Hainan Excellent Team “Rubber Genetics and Breeding” (20210203 to Min Tu).

About author: Min Tu, E-mail: tm_tumin@163.com; Zhongfeng Zhu, E-mail: zhuzhongfeng@sjtu.edu.cn; #Correspondence Lifang Zou, E-mail: zoulifang202018@sjtu.edu.cn *These authors contributed equally to this study.

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Min Tu, Zhongfeng Zhu , Xinyang Zhao, Haibin Cai, Yikun Zhang, Yichao Yan, Ke Yin, Zhimin Sha, Yi Zhou, Gongyou Chen, Lifang Zou. 2024. The versatile plant probiotic bacterium Bacillus velezensis SF305 reduces red root rot disease severity in the rubber tree by degrading the mycelia of Ganoderma pseudoferreum. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2024.09.027

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