Please wait a minute...
Journal of Integrative Agriculture
Advanced Online Publication | Current Issue | Archive | Adv Search
Identification of novel Bacillus velezensis zm026 in corn diseases control and fumonisin inhibition

Shan Geng1*, Zhimeng Zhang2*, Yuwei Zhao1, Ruixue Zhao1, Jiaqi Li1, Yingchao Liu1, Zhiyan Cao1#, Bin Zhao1#, Jingao Dong1# 

1 State Key Laboratory of North China Crop Improvement and Regulation, College of Plant Protection, Hebei Agricultural University, Baoding 071001, China

2 Tangshan Plant Protection and Quarantine Station, Tangshan 063000, China

Highlights

1. Bacillus velezensis zm026 functions as an effective in-situ management strain for regulating the microbial community structure within maize kernels.

2. B. velezensis zm026 colonizes the surfaces of maize roots and activates the plant's immune system.

3. Bacillomycin D disrupts the integrity of the fungal cell membrane and inhibits spore germination.

Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  

真菌病害不仅会降低玉米产量,还会产生霉菌毒素威胁人畜健康,其在秸秆还田后愈加严重。本研究通过微生物组技术获得了秸秆还田前后的根系微生物群落变化,并从根际土壤中分离出对拟轮枝镰孢和玉米大斑病菌高度拮抗贝莱斯芽孢杆菌zm026;该菌株可定殖在玉米根表面并激活植物免疫系统,显著增加ZmGSTZmZHDZmPR-1ZmPR-2ZmPR-3等防御基因的表达;通过高分辨质谱技术鉴定了高效抗菌物质bacillomycin D;台盼蓝、DAPI(4',6-二脒基-2-苯基吲哚)和PI(碘化丙啶)等染色结果表明,bacillomycin D通过诱导细胞凋亡导致孢子局部膨胀或破裂,进而破坏真菌细胞膜的完整性、抑制孢子萌发;室内盆栽试验表明,zm026显著促进了玉米的生长,降低了真菌病害的发生率和伏马毒素污染水平,并有效降低了玉米籽粒中镰孢菌丰度。本研究为秸秆还田后玉米病害的生态调控提供了原位修复菌株。



Abstract  

Fungal diseases affecting maize not only reduced maize yields but also generate fungal toxins that pose risks to both human and animal health, particularly when the straw is returned to the field. Microbial in-situ control is considered an environmentally friendly method that effectively addresses the limitations of unstable effects. In this study, we isolated Bacillus velezensis zm026 from rhizosphere soil for in-situ restoration, based on the soil community structure, which exhibits high antagonistic activity against Fusarium verticillioides and Exserohilum turcicum. Zm026 effectively colonized the surface of maize roots within five days and activated the plant immune system, significantly increasing the expression of defense genes such as ZmGST, ZmZHD, ZmPR-1, ZmPR-2, and ZmPR-3. The efficient anti-fungal substance of zm026 was identified by HPLC-MS and determined to be bacillomycin D. Further observations using trypan blue staining, along with DAPI (4',6-diamidino-2-phenylindole) and PI (Propidium iodide) fluorescent staining, revealed that bacillomycin D could inhibit fungal spore germination, disrupt the integrity of fungal cell membranes, induce apoptosis, and cause spore tips to protrude, swell, or rupture. Ultimately, indoor pot experiments demonstrated that the application of zm026 fermentation broth significantly promoted growth, inhibited the onset of fungal diseases in corn, and effectively reduced the abundance of Fusarium spp. in corn grains. This research provides a beneficial in-situ restoration strain for the high-quality development of corn.

Keywords:  Rhizosphere microbiome       Bacillomycin D              Fumonisin B1              Biological control  
Online: 18 February 2025  
Fund: 

This work was supported by the National Key Research & Development Program of China (2023YFD1401500); Natural Science Foundation of Hebei Province (C2021204093, C2020204017 and C2021204137); China Agriculture Research System (No. CARS-02); Key projects of science and technology research in colleges and universities of Hebei Province (ZD2020319); Key Research and Development Projects of Hebei (20326510D and 19226503D).

About author:  #Correspondence Jingao Dong, Tel: +86-312-7528166, E-mail: dongjingao@126.com; Bin Zhao, Tel: +86-312-7528567, E-mail: bdzhaobin@126.com; Zhiyan Cao, Tel: +86-312-7528567, E-mail: caoyan208@126.com * indicates the authors who contributed equally to this study

Cite this article: 

Shan Geng, Zhimeng Zhang, Yuwei Zhao, Ruixue Zhao, Jiaqi Li, Yingchao Liu, Zhiyan Cao, Bin Zhao, Jingao Dong. 2025. Identification of novel Bacillus velezensis zm026 in corn diseases control and fumonisin inhibition. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.02.029

Ali J G, Casteel C L, Mauck K E, Trase O. 2020. Chemical Ecology of Multitrophic Microbial Interactions: Plants, Insects, Microbes and the Metabolites that Connect Them. Journal of Chemical Ecology, 46, 645-648.

Alshannaq A, Yu J H. 2017. Occurrence, Toxicity, and Analysis of Major Mycotoxins in Food. International Journal of Environmental Research and Public Health, 14, 632.

Anwar A, Gould E, Tinson R, Groom M, Hamilton C. 2016. Think Yellow and Keep Green—Role of Sulfanes from Garlic in Agriculture. Antioxidants, 6, 3.

Bai B, Liu W, Qiu X, Zhang J, Zhang J, Bai Y. 2022. The root microbiome: Community assembly and its contributions to plant fitness. Journal of Integrative Plant Biology, 64, 230-243.

Balsanelli E, Serrato R V, De Baura V A, Sassaki G, Yates M G, Rigo L U, Pedrosa F O, De Souza E M, Monteiro R A. 2010. Herbaspirillum seropedicae rfbB and rfbC genes are required for maize colonization. Environmental Microbiology, 12, 2233-2244.

Bastian F, Bouziri L, Nicolardot B, Ranjard L. 2009. Impact of wheat straw decomposition on successional patterns of soil microbial community structure. Soil Biology and Biochemistry, 41, 262-275.

Bennett A E, Grussu D, Kam J, Caul S, Halpin C. 2015. Plant lignin content altered by soil microbial community. New Phytologist, 206, 166-174.

Berg G, Smalla K. 2009. Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiology Ecology, 68, 1-13.

Bhatta U K. 2022. Alternative Management Approaches of Citrus Diseases Caused by Penicillium digitatum (Green Mold) and Penicillium italicum (Blue Mold). Frontiers in Plant Science, 12, 833328.

Bi B, Wang Y, Wang K, Zhang H, Fei H, Pan R, Han F. 2022. Changes in microbial metabolic C- and N- limitations in the rhizosphere and bulk soils along afforestation chronosequence in desertified ecosystems. Journal of Environmental Management, 303, 114215.

Cameron J C, Lehman R M, Sexton P, Osborne S L, Taheri W I. 2017. Fungicidal Seed Coatings Exert Minor Effects on Arbuscular Mycorrhizal Fungi and Plant Nutrient Content. Agronomy Journal, 109, 1005-1012.

Cavazzoni V, Adami A, Castrovilli C. 1998. Performance of broiler chickens supplemented with Bacillus coagulans as probiotic. British Poultry Science, 39, 526-529.

Chen Y-H, Lee P-C, Huang T-P. 2021. Biological Control of Collar Rot on Passion Fruits Via Induction of Apoptosis in the Collar Rot Pathogen by Bacillus subtilis. Phytopathology, 111, 627-638.

Cheng S, Feng X, Liu G, Zhao N, Liu J, Zhang Z, Yang N, Zhou L, Pang M, Tang B, Dong J, Zhao B, Liu Y. 2022. Natural Occurrence of Mycotoxins in Maize in North China. Toxins, 14, 521.

Chetan K K, Varma P K, Chandrasekhar V, Kumar P A, Vasanthi V. 2024. Plant, bacteria and fungi crosstalk: Direct and indirect biocontrol mechanisms of sugarcane rhizoplane Pseudomonas species against Fusarium wilt. Rhizosphere, 31, 100952.

Cordovez V, Dini-Andreote F, Carrión V J, Raaijmakers J M. 2019. Ecology and Evolution of Plant Microbiomes. Annual Review of Microbiology, 73, 69-88.

De Rossi R L, Guerra F A, Plazas M C, Vuletic E E, Brücher E, Guerra G D, Reis E M. 2022. Crop damage, economic losses, and the economic damage threshold for northern corn leaf blight. Crop Protection, 154, 105901.

Du Y, Sun J, Tian Z, Cheng Y, Long C-a. 2023. Effect of blue light treatments on Geotrichum citri-aurantii and the corresponding physiological mechanisms of citrus. Food Control, 145, 109468.

Duan Z, Song H, Shi H, Gao Z, Mao J, Cao Y, Huo H, Li J, Wang X, Lin M. 2024. Postharvest treatment with Bacillus velezensis LX mitigates disease incidence and alters the microbiome on kiwifruit surface. Postharvest Biology and Technology, 211, 112843.

Farzaneh M, Shi Z-Q, Ghassempour A, Sedaghat N, Ahmadzadeh M, Mirabolfathy M, Javan-Nikkhah M. 2012. Aflatoxin B1 degradation by Bacillus subtilis UTBSP1 isolated from pistachio nuts of Iran. Food Control, 23, 100-106.

Fernández-Luqueño F, Valenzuela-Encinas C, Marsch R, Martínez-Suárez C, Vázquez-Núñez E, Dendooven L. 2010. Microbial communities to mitigate contamination of PAHs in soil—possibilities and challenges: a review. Environmental Science and Pollution Research, 18, 12-30.

Figueroa-Lopez A M, Cordero-Ramirez J D, Martinez-Alvarez J C, Lopez-Meyer M, Lizarraga-Sanchez G J, Felix-Gastelum R, Castro-Martinez C, Maldonado-Mendoza I E. 2016. Rhizospheric bacteria of maize with potential for biocontrol of Fusarium verticillioides. Springerplus, 5, 330.

Flemming H-C, Wingender J, Szewzyk U, Steinberg P, Rice S A, Kjelleberg S. 2016. Biofilms: an emergent form of bacterial life. Nature Reviews Microbiology, 14, 563-575.

Gargari G, Taverniti V, Koirala R, Gardana C, Guglielmetti S. 2020. Impact of a Multistrain Probiotic Formulation with High Bifidobacterial Content on the Fecal Bacterial Community and Short-Chain Fatty Acid Levels of Healthy Adults. Microorganisms, 8, 492.

Hamdi H, Benzarti S, Manusadžianas L, Aoyama I, Jedidi N. 2007. Bioaugmentation and biostimulation effects on PAH dissipation and soil ecotoxicity under controlled conditions. Soil Biology and Biochemistry, 39, 1926-1935.

Hosokawa R, Nagai M, Morikawa M, Okuyama H. 2009. Autochthonous bioaugmentation and its possible application to oil spills. World Journal of Microbiology and Biotechnology, 25, 1519-1528.

Huang P, Xu J, Kloepper J W. 2019. Plant–microbe–soil fertility interaction impacts performance of a Bacillus‐containing bioproduct on bell pepper. Journal of Basic Microbiology, 60, 27-36.

Idicula D V, R K, Parappilly S J, Joy N, Balan J, George S M. 2023. Salutary attributes of probiotic human gut lactobacilli for gut health. Letters in Applied Microbiology, 76, 1-8.

Ikunaga Y, Sato I, Grond S, Numaziri N, Yoshida S, Yamaya H, Hiradate S, Hasegawa M, Toshima H, Koitabashi M, Ito M, Karlovsky P, Tsushima S. 2011. Nocardioides sp. strain WSN05-2, isolated from a wheat field, degrades deoxynivalenol, producing the novel intermediate 3-epi-deoxynivalenol. Applied Microbiology and Biotechnology, 89, 419-427.

K R D, D M N, C W P, A F J. 2013. Yield Trends Are Insufficient to Double Global Crop Production by 2050. PloS one, 8.

Kandel S, Joubert P, Doty S. 2017. Bacterial Endophyte Colonization and Distribution within Plants. Microorganisms, 5, 77.

Kuzyakov Y, Hill P W, Jones D L. 2006. Root exudate components change litter decomposition in a simulated rhizosphere depending on temperature. Plant and Soil, 290, 293-305.

Lal S, Tabacchioni S. 2009. Ecology and biotechnological potential of Paenibacillus polymyxa: a minireview. Indian Journal of Microbiology, 49, 2-10.

Li C H, Shi L, Han Q, Hu H L, Zhao M W, Tang C M, Li S P. 2012. Biocontrol of verticillium wilt and colonization of cotton plants by an endophytic bacterial isolate. Journal of Applied Microbiology, 113, 641-651.

Li X, Liu Y, Wang Z, Yang C, Zhang R, Luo Y, Ma Y, Deng Y. 2022. Microbiome analysis and biocontrol bacteria isolation from rhizosphere soils associated with different sugarcane root rot severity. Frontiers in Bioengineering and Biotechnology, 10, 1062351.

Lv J, Yang S, Zhou W, Liu Z, Tan J, Wei M. 2024. Microbial regulation of plant secondary metabolites: Impact, mechanisms and prospects. Microbiological Research, 283, 127688.

Madueño L, Coppotelli B M, Alvarez H M, Morelli I S. 2011. Isolation and characterization of indigenous soil bacteria for bioaugmentation of PAH contaminated soil of semiarid Patagonia, Argentina. International Biodeterioration & Biodegradation, 65, 345-351.

Markakis E A, Tjamos S E, Antoniou P P, Paplomatas E J, Tjamos E C. 2015. Biological control of Verticillium wilt of olive by Paenibacillus alvei, strain K165. BioControl, 61, 293-303.

Meng Q, Jiang H, Hao J J. 2016. Effects of Bacillus velezensis strain BAC03 in promoting plant growth. Biological Control, 98, 18-26.

Ndzelu B S, Dou S, Zhang X. 2021. Corn straw return can increase labile soil organic carbon fractions and improve water-stable aggregates in Haplic Cambisol. Journal of Arid Land, 12, 1018-1030.

Olubajo B, Bacon C W. 2008. Electrotransformation of Bacillus mojavensis with fluorescent protein markers. Journal of Microbiological Methods, 74, 102-105.

Paterson E, Osler G, Dawson L A, Gebbing T, Sim A, Ord B. 2008. Labile and recalcitrant plant fractions are utilised by distinct microbial communities in soil: Independent of the presence of roots and mycorrhizal fungi. Soil Biology and Biochemistry, 40, 1103-1113.

Petchkongkaew A, Taillandier P, Gasaluck P, Lebrihi A. 2008. Isolation of Bacillus spp. from Thai fermented soybean (Thua-nao): screening for aflatoxin B1 and ochratoxin A detoxification. Journal of Applied Microbiology, 104, 1495-1502.

Poll C, Marhan S, Ingwersen J, Kandeler E. 2008. Dynamics of litter carbon turnover and microbial abundance in a rye detritusphere. Soil Biology and Biochemistry, 40, 1306-1321.

Rudrappa T, Czymmek K J, Pare P W, Bais H P. 2008. Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol, 148, 1547-1556.

Rybakova D, Schmuck M, Wetzlinger U, Varo-Suarez A, Murgu O, Müller H, Berg G. 2015. Kill or cure? The interaction between endophytic Paenibacillus and Serratia strains and the host plant is shaped by plant growth conditions. Plant and Soil, 405, 65-79.

Sangare L, Zhao Y, Folly Y M, Chang J, Li J, Selvaraj J N, Xing F, Zhou L, Wang Y, Liu Y. 2014. Aflatoxin B(1) degradation by a Pseudomonas strain. Toxins 6, 3028-3040.

Schmidt J E, Kent A D, Brisson V L, Gaudin A C M. 2019. Agricultural management and plant selection interactively affect rhizosphere microbial community structure and nitrogen cycling. Microbiome, 7, 146.

Shao M, Chen Y, Gong Q, Miao S, Li C, Sun Y, Qin D, Guo X, Yan X, Cheng P, Yu G. 2023. Biocontrol endophytes Bacillus subtilis R31 influence the quality, transcriptome and metabolome of sweet corn. PeerJ-Life and Environment, 11, e14967.

She M, Zhou H, Dong W, Xu Y, Gao L, Gao J, Yang Y, Yang Z, Cai D, Chen S. 2024. Modular metabolic engineering of Bacillus amyloliquefaciens for high-level production of green biosurfactant iturin A. Applied Microbiology and Biotechnology, 108, 311.

Shen H, Li X, Li Z. 2024. Detecting and identifying pathogens and antagonistic bacteria associated with Ginkgo biloba leaf spot disease. Frontiers in Microbiology, 15, 1346318.

Souza R d, Ambrosini A, Passaglia L M P. 2015. Plant growth-promoting bacteria as inoculants in agricultural soils. Genetics and Molecular Biology, 38, 401-419.

Stoev S D. 2013. Food Safety and Increasing Hazard of Mycotoxin Occurrence in Foods and Feeds. Critical Reviews in Food Science and Nutrition, 53, 887-901.

Sun L, Wang W, Zhang X, Gao Z, Cai S, Wang S, Li Y. 2023. Bacillus velezensis BVE7 as a promising agent for biocontrol of soybean root rot caused by Fusarium oxysporum. Frontiers in Microbiology, 14, 1275986.

Sun R, Zhang X-X, Guo X, Wang D, Chu H. 2015. Bacterial diversity in soils subjected to long-term chemical fertilization can be more stably maintained with the addition of livestock manure than wheat straw. Soil Biology and Biochemistry, 88, 9-18.

Taylor W J, Draughon F A. 2001. Nannocystis exedens: a potential biocompetitive agent against Aspergillus flavus and Aspergillus parasiticus. Journal of Food Protection, 64, 1030-1034.

Tejada-Castaneda Z I, Avila-Gonzalez E, Casaubon-Huguenin M T, Cervantes-Olivares R A, Vasquez-Pelaez C, Hernandez-Baumgarten E M, Moreno-Martinez E. 2008. Biodetoxification of aflatoxin-contaminated chick feed. Poultry Science, 87, 1569-1576.

Tjamos E C, Tsitsigiannis D I, Tjamos S E, Antoniou P P, Katinakis P. 2004. Selection and Screening of Endorhizosphere Bacteria from Solarized Soils as Biocontrol Agents Against Verticillium dahliae of Solanaceous Hosts. European Journal of Plant Pathology, 110, 35-44.

Torrijos R, de Melo Nazareth T, Vila-Donat P, Manes J, Meca G. 2022. Use of Mustard Extracts Fermented by Lactic Acid Bacteria to Mitigate the Production of Fumonisin B(1) and B(2) by Fusarium verticillioides in Corn Ears. Toxins, 14, 80.

Wang B, Wan C-x, Zeng H. 2020. Colonization on Cotton Plants with a GFP Labeled Strain of Bacillus axarquiensis. Current Microbiology, 77, 3085-3094.

Wang Y, Wu Y, Cao C, Han S, Zhao W, Li Q, Liu X, Kong L. 2023. Effects of fertilizer reduction coupled with straw returning on soil fertility, wheat root endophytic bacteria, and the occurrence of wheat crown rot. Frontiers in Microbiology, 14, 1143480.

Williams T R, Marco M L, Lindow S. 2014. Phyllosphere Microbiota Composition and Microbial Community Transplantation on Lettuce Plants Grown Indoors. mBio, 5, e01564-01514.

Xing J, Chen M, Deng X, Chen J, Jiang P, Qin H. 2022. Resilience of soil microbial metabolic functions to temporary E. coli invasion. Chemosphere, 307, 135906.

Xu L, Zhou Y, Miao C, Chen H, Zhang J, Qian H, Hou P, Ding Y, Liu Z, Li W, Wang S, Jiang Y, Li G. 2024. Long-term straw return increases fungal residual contribution to soil microaggregate nitrogen pool: An eco-enzymatic stoichiometric study. Soil and Tillage Research, 244, 106278.

Yu L, Zhang Y, Wang Y, Yao Q, Yang K. 2024. Effects of slow-release nitrogen and urea combined application on soil physicochemical properties and fungal community under total straw returning condition. Environmental Research, 252, 118758.

Zhang B, Dong C, Shang Q, Han Y, Li P. 2013. New insights into membrane-active action in plasma membrane of fungal hyphae by the lipopeptide antibiotic bacillomycin L. Biochimica et Biophysica Acta, 1828, 2230-2237.

Zhang F, Moniz H A, Walcott B, Moremen K W, Wang L, Linhardt R J. 2014. Probing the impact of GFP tagging on Robo1-heparin interaction. Glycoconjugate Journal, 31, 299-307.

Zhang J, Liu Y X, Zhang N, Hu B, Jin T, Xu H, Qin Y, Yan P, Zhang X, Guo X, Hui J, Cao S, Wang X, Wang C, Wang H, Qu B, Fan G, Yuan L, Garrido-Oter R, Chu C, Bai Y. 2019. NRT1.1B is associated with root microbiota composition and nitrogen use in field-grown rice. Nature Biotechnology, 37, 676-684.

Zhang S, Li M, Cui X, Pan Y. 2023. Effect of different straw retention techniques on soil microbial community structure in wheat–maize rotation system. Frontiers in Microbiology, 10.3389/fmicb.2022.1069458, 1069458.

Zhang X, Yu J, Huang Z, Li H, Liu X, Huang J, Zhuo R, Wu Z, Qin X, Gao Y, Wang M, Zhu Y. 2021. Enhanced Cd phytostabilization and rhizosphere bacterial diversity of Robinia pseudoacacia L. by endophyte Enterobacter sp. YG-14 combined with sludge biochar. Science of The Total Environment, 787, 147660.

Zhang Y, Fan Y, Dai Y, Jia Q, Guo Y, Wang P, Shen T, Wang Y, Liu F, Guo W, Wu A, Jiao Z, Wang C. 2024. Crude Lipopeptides Produced by Bacillus amyloliquefaciens Could Control the Growth of Alternaria alternata and Production of Alternaria Toxins in Processing Tomato. Toxins, 16, 65.

Zhao C, Liu B, Piao S, Wang X, Lobell D B, Huang Y, Huang M, Yao Y, Bassu S, Ciais P, Durand J-L, Elliott J, Ewert F, Janssens I A, Li T, Lin E, Liu Q, Martre P, Müller C, Peng S, Peñuelas J, Ruane A C, Wallach D, Wang T, Wu D, Liu Z, Zhu Y, Zhu Z, Asseng S. 2017. Temperature increase reduces global yields of major crops in four independent estimates. Proceedings of the National Academy of Sciences, 114, 9326-9331.

Zhao S, Qiu S, Xu X, Ciampitti I A, Zhang S, He P. 2019. Change in straw decomposition rate and soil microbial community composition after straw addition in different long-term fertilization soils. Applied Soil Ecology, 138, 123-133. 

No related articles found!
No Suggested Reading articles found!