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Journal of Integrative Agriculture  2023, Vol. 22 Issue (9): 2729-2745    DOI: 10.1016/j.jia.2023.01.007
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Colonization by Klebsiella variicola FH-1 stimulates soybean growth and alleviates the stress of Sclerotinia sclerotiorum

ZHAI Qian-hang1*, PAN Ze-qun1*, ZHANG Cheng1, YU Hui-lin2, ZHANG Meng1, GU Xue-hu1, ZHANG Xiang-hui2, PAN Hong-yu2, ZHANG Hao1#

1 College of Plant Protection, Jilin Agricultural University, Changchun 130118, P.R.China 
2 College of Plant Sciences, Jilin University, Changchun 130062, P.R.China 
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摘要  由核盘菌(Sclerotinia sclerotiorum)引起的菌核病是一种毁灭性的土传大豆病害,会造成巨大的产量损失。我们以前报道过变栖克雷伯氏菌FH-1可以降解莠去津除草剂,并且可以增加莠去津敏感作物(如大豆)的营养生长。我们发现FH-1可以促进大豆生长并诱导对菌核病菌的抗性,为了证明FH-1对大豆菌核病菌的生防机制并评价其生防能力,我们在体外培养基试验中证明菌株FH-1可以固定培养基中的氮,溶解无机磷和钾,并产生吲哚乙酸和铁载体,具有促进植物生长的潜力。盆栽试验结果表明,变栖克雷伯氏菌FH-1能促进大豆植株发育,显著提高株高、鲜重和根长,并诱导大豆叶片对菌核病的抗性。用菌株FH-1治疗的疾病进展曲线下面积(AUDPC)显著低于对照,并且在48小时内减少了高达42.2%。(P < 0.001)。此外,紫外分光光度计法测量结果表明菌株FH-1可以增强参与大豆植物防御的过氧化氢酶、超氧化物歧化酶、过氧化物酶、苯丙氨酸解氨酶和多酚氧化酶的酶活性,并减少了叶片中丙二醛的积累。定量实时PCR检测了可能参与大豆抵抗核盘菌胁迫的相关基因的转录水平,结果表明诱导抗性的机制似乎主要是由于变栖克雷伯氏菌FH-1诱导PR10、PR12、AOS、CHS和PDF1.2基因转录水平的提高。利用结晶紫染色法测定了菌株FH-1具有生物膜形成能力,用共聚焦荧光显微镜和扫描电镜观测菌株FH-1在大豆根上的定殖情况,菌株FH-1可以定殖在大豆根表面、根毛和外皮层上形成生物膜。综上所述,变栖克雷伯氏菌FH-1在大豆根部的定殖有助于诱导参与植物保护的防御酶和相关防御基因的表达,诱导大豆对菌核病菌的抗性表现出生物防治潜力。这对大豆的种植和生长具有重要意义。此外,本研究有助于理解变种芽胞杆菌FH-1、大豆植株和核盘菌之间相互作用的有价值的第一步,这为绿色防控提供了新的思路。




Abstract  

Sclerotinia stem rot, caused by Sclerotinia sclerotiorum, is a destructive soil-borne disease leading to huge yield loss.  We previously reported that Klebsiella variicola FH-1 could degrade atrazine herbicides, and the vegetative growth of atrazine-sensitive crops (i.e., soybean) was significantly increased in the FH-1-treated soil.  Interestingly, we found that FH-1 could promote soybean growth and induce resistance to Ssclerotiorum.  In our study, strain FH-1 could grow in a nitrogen-free environment, dissolve inorganic phosphorus and potassium, and produce indoleacetic acid and a siderophore.  The results of pot experiments showed that Kvariicola FH-1 promoted soybean plant development, substantially improving plant height, fresh weight, and root length, and induced resistance against Ssclerotiorum infection in soybean leaves.  The area under the disease progression curve (AUDPC) for treatment with strain FH-1 was significantly lower than the control and was reduced by up to 42.2% within 48 h (P<0.001).  Moreover, strain FH-1 rcovered the activities of catalase, superoxide dismutase, peroxidase, phenylalanine ammonia lyase, and polyphenol oxidase, which are involved in plant protection, and reduced malondialdehyde accumulation in the leaves.  The mechanism of induction of resistance appeared to be primarily resulted from the enhancement of transcript levels of PR10, PR12, AOS, CHS, and PDF1.2 genes.  The colonization of FH-1 on soybean root, determined using CLSM and SEM, revealed that FH-1 colonized soybean root surfaces, root hairs, and exodermis to form biofilms.  In summary, Kvariicola FH-1 exhibited the biological control potential by inducing resistance in soybean against Ssclerotiorum infection, providing new suggestions for green prevention and control.

Keywords:  sclerotinia stem rot of soybean       Klebsiella variicola FH-1        inducing resistance        root colonization        biofilm  
Received: 21 July 2022   Accepted: 19 December 2022
Fund: This work was financially supported by the grants from the Inter-governmental International Cooperation Special Project of National Key R&D Program of China (2019YFE0114200), and the Natural Science Foundation Project of Science and Technology Department of Jilin Province, China (20200201215JC).
About author:  ZHAI Qian-hang, E-mail: zqhjuzi@163.com; PAN Ze-qun, E-mail: 3478551417@qq.com; #Correspondence ZHANG Hao, E-mail: zhanghao100@jlau.edu.cn * These authors contributed equally to this study.

Cite this article: 

ZHAI Qian-hang, PAN Ze-qun, ZHANG Cheng, YU Hui-lin, ZHANG Meng, GU Xue-hu, ZHANG Xiang-hui, PAN Hong-yu, ZHANG Hao. 2023. Colonization by Klebsiella variicola FH-1 stimulates soybean growth and alleviates the stress of Sclerotinia sclerotiorum. Journal of Integrative Agriculture, 22(9): 2729-2745.

Ahemad M, Kibret M. 2014. Mechanisms and applications of plant growth promoting rhizobacteria: Current perspective. Journal of King Saud University (Science), 26, 1–20.

Al-Ali A, Deravel J, Krier F, Bechet M, Ongena M, Jacques P. 2018. Biofilm formation is determinant in tomato rhizosphere colonization by Bacillus velezensis FZB42. Environmental Science and Pollution Research25, 1–11.

Altaf M M, Ahmad I. 2017. In vitro and in vivo biofilm formation by Azotobacter isolates and its relevance to rhizosphere colonization. Rhizosphere3, 138–142.

Attia M S, El-Sayyad G S, Abd Elkodous M, El-Batal A I. 2020. The effective antagonistic potential of plant growth-promoting rhizobacteria against Alternaria solani-causing early blight disease in tomato plant. Scientia Horticulturae266, 109289.

Azabou M C, Gharbi Y, Medhioub I, Ennouri K, Barham H, Tounsi S, Triki M A. 2020. The endophytic strain Bacillus velezensis OEE1: An efficient biocontrol agent against Verticillium wilt of olive and a potential plant growth promoting bacteria. Biological Control142, 104168.

Bazzalo M, Heber E, Del Pero Martinez M, Caso O. 1985. Phenolic compounds in stems of sunflower plants inoculated with Sclerotinia sclerotiorum and their inhibitory effects on the fungus. Journal of Phytopathology112, 322–332.

Beauregard P B, Chai Y, Vlamakis H, Losick R, Kolter R. 2013. Bacillus subtilis biofilm induction by plant polysaccharides. Proceedings of the National Academy of Sciences of the United States of America110, E1621–E1630.

Ben Abdallah D, Frikha-Gargouri O, Tounsi S. 2018. Rizhospheric competence, plant growth promotion and biocontrol efficacy of Bacillus amyloliquefaciens subsp plantarum strain 32a. Biological Control124, 61–67.

Budiharjo A, Chowdhury S P, Dietel K, Beator B, Dolgova O, Fan B, Bleiss W, Ziegler J, Schmid M, Hartmann A, Borriss R. 2014. Transposon mutagenesis of the plant-associated Bacillus amyloliquefaciens ssp. plantarum FZB42 revealed that the nfrA and RBAM17410 genes are involved in plant–microbe-interactions. PLoS ONE9, e98267.

Calla B, Tri V, Radwan O, Hartman G L, Clough S J. 2009. Gene expression profiling soybean stem tissue early response to Sclerotinia sclerotiorum and in silico mapping in relation to resistance markers. Plant Genome2, 149–166.

Cao Y, Zhang Z, Ling N, Yuan Y, Zheng X, Shen B, Shen Q. 2011. Bacillus subtilis SQR 9 can control Fusarium wilt in cucumber by colonizing plant roots. Biology and Fertility of Soils47, 495–506.

Chen H, Seguin P, Jabaji S H. 2009. Differential expression of genes encoding the phenylpropanoid pathway upon infection of soybean seedlings by Rhizoctonia solaniCanadian Journal of Plant Pathology31, 356–367.

Chen Y, Yan F, Chai Y, Liu H, Kolter R, Losick R, Guo J H. 2013. Biocontrol of tomato wilt disease by Bacillus subtilis isolates from natural environments depends on conserved genes mediating biofilm formation. Environmental Microbiology15, 848–864.

Chowdhury S P, Dietel K, Raendler M, Schmid M, Junge H, Borriss R, Hartmann A, Grosch R. 2013. Effects of Bacillus amyloliquefaciens FZB42 on lettuce growth and health under pathogen pressure and its impact on the rhizosphere bacterial community, PLoS ONE8, e68818.

Chung C L, Poland J, Kump K, Benson J, Longfellow J, Walsh E, Balint-Kurti P Nelson R. 2011. Targeted discovery of quantitative trait loci for resistance to northern leaf blight and other diseases of maize. Theoretical and Applied Genetics123, 307–326.

Comas L H, Eissenstat D M, Lakso A N. 2000. Assessing root death and root system dynamics in a study of grape canopy pruning. The New Phytologist147, 171–178.

Compant S, Clement C, Sessitsch A. 2010. Plant growth-promoting bacteria in the rhizo- and endosphere of plants: Their role, colonization, mechanisms involved and prospects for utilization. Soil Biology & Biochemistry42, 669–678.

Cui W, He P, Munir S, He P, Li X, Li Y, Wu J, Wu Y, Yang L, He P, He Y. 2019. Efficacy of plant growth promoting bacteria Bacillus amyloliquefaciens B9601-Y2 for biocontrol of southern corn leaf blight. Biological Control139, 104080.

Du Z, Bramlage W J. 1992. Modified thiobarbituric acid assay for measuring lipid oxidation in sugar-rich plant tissue extracts. Journal of Agricultural and Food Chemistry40, 1566–1570.

Einhardt A M, Oliveira L M, Ferreira S, Araújo W L, Medeiros D B, Fernie A R, Rodrigues F Á. 2022. Defense responses and oxidative metabolism of glyphosate-resistant soybean plants infected by Phakopsora pachyrhizi modulated by glyphosate and nickel. Physiological and Molecular Plant Pathology118, 101817.

Etchells J P, Smit M E, Gaudinier A, Williams C J, Brady S M. 2016. A brief history of the TDIF-PXY signalling module: balancing meristem identity and differentiation during vascular development. New Phytologist209, 474–484.

Gossen B D, Rimmer S R, Holley J D. 2001. First report of resistance to benomyl fungicide in Sclerotinia sclerotiorumPlant Disease85, 1206–1206.

Guo X, Stotz H U. 2007. Defense against Sclerotinia sclerotiorum in Arabidopsis is dependent on jasmonic acid, salicylic acid, and ethylene signaling. Molecular Plant–Microbe Interactions20, 1384–1395.

Hayashi S, Gresshoff P M, Kinkema M. 2008. Molecular analysis of lipoxygenases associated with nodule development in soybean. Molecular Plant–Microbe Interactions21, 843–853.

Hirschi K D. 2004. The calcium conundrum: Both versatile nutrient and specific signal. Plant Physiology136, 2438–2442.

Iniguez A L, Dong Y, Triplett E W. 2004. Nitrogen fixation in wheat provided by Klebsiella pneumoniae 342. Molecular Plant-Microbe Interactions17, 1078–1085.

Jain K, Parida S, Mangwani N, Dash H R, Das S. 2013. Isolation and characterization of biofilm-forming bacteria and associated extracellular polymeric substances from oral cavity. Annals of Microbiology63, 1553–1562.

Jiang C H, Liao M J, Wang H K, Zheng M Z, Xu J J, Guo J H. 2018. Bacillus velezensis, a potential and efficient biocontrol agent in control of pepper gray mold caused by Botrytis cinereaBiological Control126, 147–157.

Jiang C H, Wu F, Yu Z Y, Xie P, Ke H J, Li H W, Yu Y Y, Guo J H. 2015. Study on screening and antagonistic mechanisms of Bacillus amyloliquefaciens 54 against bacterial fruit blotch (BFB) caused by Acidovorax avenae subsp. citrulliMicrobiological Research170, 95–104.

Jiang W, Wang K, Wu Q, Dong S, Liu P, Zhang J. 2013. Effects of narrow plant spacing on root distribution and physiological nitrogen use efficiency in summer maize. The Crop Journal1, 77–83.

Jogaiah S, Satapute P, De Britto S, Konappa N, Udayashankar A C. 2020. Exogenous priming of chitosan induces upregulation of phytohormones and resistance against cucumber powdery mildew disease is correlated with localized biosynthesis of defense enzymes. International Journal of Biological Macromolecules162, 1825–1838.

Jung W J, Mabood F, Souleimanov A, Smith D L. 2011. Induction of defense-related enzymes in soybean leaves by class IId bacteriocins (thuricin 17 and bacthuricin F4) purified from Bacillus strains. Microbiological Research167, 14–19.

Karthika S, Midhun S J, Jisha M S. 2020. A potential antifungal and growth-promoting bacterium Bacillus sp. KTMA4 from tomato rhizosphere. Microbial Pathogenesis142, 104049.

Kumar S, Chauhan P S, Agrawal L, Raj R, Srivastava A, Gupta S, Mishra S K, Yadav, S, Singh P C, Raj S K, Nautiyal C S. 2016. Paenibacillus lentimorbus inoculation enhances tobacco growth and extenuates the virulence of cucumber mosaic virus. PLoS ONE11, e0149980.

Lau E T, Tani A, Khew C Y, Chua Y Q, San Hwang S. 2020. Plant growth-promoting bacteria as potential bio-inoculants and biocontrol agents to promote black pepper plant cultivation. Microbiological Research240, 126549.

Li H, Ding X, Wang C, Ke H, Wu Z, Wang Y, Liu H, Guo J. 2016. Control of Tomato yellow leaf curl virus disease by Enterobacter asburiae BQ9 as a result of priming plant resistance in tomatoes. Turkish Journal of Biology40, 150–159.

Li M, Peng S, Xu S, Yu D, Zhao M, Wen G. 2014. Application of Klebsiella spp. in agriculture and environmental management. Current Biotechnology6, 415–420. (in Chinese)

Liu D, Chen L, Zhu X, Wang Y, Xuan Y, Liu X, Chen L, Duan Y. 2018. Klebsiella pneumoniae SnebYK mediates resistance against Heterodera glycines and promotes soybean growth. Frontiers in Microbiology9, 1134.

Liu Y, Li Y, Bi Y, Jiang Q, Mao R, Liu Z, Prusky D B. 2021. Induction of defense response against Alternaria rot in Zaosu pear fruit by exogenous L-lysine through regulating ROS metabolism and activating defense-related proteins. Postharvest Biology and Technology179, 111567.

Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2–∆∆CT method. Methods25, 402–408.

Van Loon L, Bakker P. 2005. Induced systemic resistance as a mechanism of disease suppression by rhizobacteria. In: PGPRBiocontrol and Biofertilization. Faculty of Biology Section Phytopathology, Utrecht University. The Netherlands. pp. 39–66.

Van Loon L, Bakker P. 2007. Root-associated bacteria inducing systemic resistance. In: Plant-Associated Bacteria. Springer, the Netherlands. pp. 269–316.

Van Loon L, Bakker P, Pieterse C. 1998. Systemic resistance induced by rhizosphere bacteria. Annual Review of Phytopathology36, 453–483.

Lugtenberg B, Kamilova F. 2009. Plant-growth-promoting rhizobacteria. Annual Review of Microbiology63, 541–556.

Ma L, Zhang H Y, Zhou X K, Yang C G, Zheng S C, Duo J L, Mo M H. 2018. Biological control tobacco bacterial wilt and black shank and root colonization by bio-organic fertilizer containing bacterium Pseudomonas aeruginosa NXHG29. Applied Soil Ecology129, 136–144.

Martinez-Viveros O, Jorquera M A, Crowley D E, Gajardo G, Mora M L. 2010. Mechanisms and practical considerations involved in plant growth promotion by rhizobacteria. Journal of Soil Science and Plant Nutrition10, 293–319.

Mayer A, Harel E, Ben-Shaul R. 1966. Assay of catechol oxidase - A critical comparison of methods. Phytochemistry5, 783–789.

Mitter N, Kazan K, Way H M, Broekaert W F, Manners J M. 1998. Systemic induction of an Arabidopsis plant defensin gene promoter by tobacco mosaic virus and jasmonic acid in transgenic tobacco. Plant Science136, 169–180.

Nautiyal C S. 1999. An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiology Letters170, 265–270.

Van Oosten V R, Bodenhausen N, Reymond P, Van Pelt J A, Van Loon L C, Dicke M, Pieterse C M J. 2008. Differential effectiveness of microbially induced resistance against herbivorous insects in ArabidopsisMolecular Plant–Microbe Interactions21, 919–930.

Patel S, Rajput K, Saraf M. 2017. Elicitation of plant defense enzymes against Fusarium oxysporum f. sp. lycopersici in tomato plant using a novel rhizobacteria Providencia rettgeri MSS2. Biocatalysis and Agricultural Biotechnology12, 308–313.

Pathan A, Bond J, Gaskin R. 2010. Sample preparation for SEM of plant surfaces. Materials Today12, 32–43.

Patil V R, Patel R M, Parekh V B, Pathak J, Saripalli G. 2021. Differential gene expression analyses of ten defence response genes during Fusarium wilt infection in resistant and susceptible pigeonpea cultivars. Plant Stress2, 100043.

Peeters E, Nelis H J, Coenye T. 2008. Comparison of multiple methods for quantification of microbial biofilms grown in microtiter plates. Journal of Microbiological Methods72, 157–165.

Penrose D M, Glick B R. 2003. Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiologia Plantarum118, 10–15.

Posada L F, Alvarez J C, Romero-Tabarez M, de-Bashan L, Villegas-Escobar V. 2018. Enhanced molecular visualization of root colonization and growth promotion by Bacillus subtilis EA-CB0575 in different growth systems. Microbiological Research217, 69–80.

Puri A, Padda K P, Chanway C P. 2020. In vitro and in vivo analyses of plant-growth-promoting potential of bacteria naturally associated with spruce trees growing on nutrient-poor soils. Applied Soil Ecology149, 103538.

Ramamoorthy V, Viswanathan R, Raguchander T, Prakasam V, Samiyappan R. 2001. Induction of systemic resistance by plant growth promoting rhizobacteria in crop plants against pests and diseases. Crop Protection20, 1–11

Sachdev D P, Chaudhari H G, Kasture V M, Dhavale D D, Chopade B A. 2009. Isolation and characterization of indole acetic acid (IAA) producing Klebsiella pneumoniae strains from rhizosphere of wheat (Triticum aestivum) and their effect on plant growth. Indian Journal of Experimental Biology47, 993–1000.

Samain E, Aussenac T, Salim S. 2019. The effect of plant genotype, growth stage, and mycosphaerella graminicola strains on the efficiency and durability of wheat-induced resistance by Paenibacillus sp. strain B2. Frontiers in Plant Science10, 587.

Selim S, Sanssene J, Rossard S, Courtois J. 2017. Systemic Induction of the defensin and phytoalexin pisatin pathways in pea (Pisum sativum) against Aphanomyces euteiches by acetylated and nonacetylated oligogalacturonides. Molecules22, 1017.

Senthilraja G, Anand T, Kennedy J S, Raguchander T, Samiyappan R. 2013. Plant growth promoting rhizobacteria (PGPR) and entomopathogenic fungus bioformulation enhance the expression of defense enzymes and pathogenesis-related proteins in groundnut plants against leafminer insect and collar rot pathogen. Physiological and Molecular Plant Pathology82, 10–19.

Shen L, Wang F, Yang J, Qian Y, Dong X, Zhan H. 2014. Control of tobacco mosaic virus by Pseudomonas fluorescens CZ powder in greenhouses and the field. Crop Protection56, 87–90.

Sierotzki H, Scalliet G. 2013. A review of current knowledge of resistance aspects for the next-generation succinate dehydrogenase inhibitor fungicides. Phytopathology103, 880–887.

Singh R P, Jha P, Jha P N. 2015. The plant-growth-promoting bacterium Klebsiella sp. SBP-8 confers induced systemic tolerance in wheat (Triticum aestivum) under salt stress. Journal of Plant Physiology184, 57–67.

Tan S Y, Yang C L, Mei X L, Shen S Y, Raza W, Shen Q R, Xu Y C. 2013. The effect of organic acids from tomato root exudates on rhizosphere colonization of Bacillus amyloliquefaciens t-5. Applied Soil Ecology64, 15–22.

Tank N, Rajendran N, Patel B, Saraf M. 2012. Evaluation and biochemical characterization of a distinctive pyoverdin from a Pseudomonas isolated from chickpea rhizosphere. Brazilian Journal of Microbiology43, 639–648.

Upchurch R G, Ramirez M E. 2010. Defense-related gene expression in soybean leaves and seeds inoculated with Cercospora kikuchii and Diaporthe phaseolorum var. meridionalisPhysiological and Molecular Plant Pathology75, 64–70.

Vlamakis H, Chai Y, Beauregard P, Losick R, Kolter R. 2013. Sticking together: Building a biofilm the Bacillus subtilis way. Nature Reviews Microbiology11, 157–168.

Wang S, Wu H, Qiao J, Ma L, Liu J, Xia Y, Gao X. 2009. Molecular mechanism of plant growth promotion and induced systemic resistance to tobacco mosaic virus by Bacillus spp. Journal of Microbiology and Biotechnology19, 1250–1258.

Van Wees S C M, Van der Ent S, Pieterse C M J. 2008. Plant immune responses triggered by beneficial microbes. Current Opinion in Plant Biology11, 443–448.

Xu P F, Wu J J, Xue A, Li W B, Chen W Y, Wei L, Lv H Y, Lin S F, Fan S J, Li N H, Wang X, Jiang L Y, Zhang S Z. 2012. Differentially expressed genes of soybean during infection by Phytophthora sojaeJournal of Integrative Agriculture11, 368–377.

Yang D, Wang B, Wang J, Chen Y, Zhou M. 2009. Activity and efficacy of Bacillus subtilis strain NJ-18 against rice sheath blight and Sclerotinia stem rot of rape. Biological Control51, 61–65.

Yang W, Yan H, Zhang J, Gao Y, Xu W, Shang J, Luo Y. 2018. Inhibition of biofilm formation by Cd2+ on Bacillus subtilis 1JN2 depressed its biocontrol efficiency against Ralstonia wilt on tomato. Microbiological Research215, 1–6.

Yao M A, Zhang Q L, Yang Z M, Yun L I, Yan Y L, Ping S Z, Wei L U. 2016. Identification of the nitrogen-fixing Pseudomonas stutzeri major flagellar gene regulator FleQ and its role in biofilm formation and root colonization. Journal of Integrative Agriculture15, 339–348.

Yi Y, Kuipers O P. 2017. Development of an efficient electroporation method for rhizobacterial Bacillus mycoides strains. Journal of Microbiological Methods133, 82–86.

Yu X, Ai C, Xin L, Zhou G. 2011. The siderophore-producing bacterium, Bacillus subtilis CAS15, has a biocontrol effect on Fusarium wilt and promotes the growth of pepper. European Journal of Soil Biology47, 138–145.

Yuan H, Zhu Z, Liu S, Ge T, Jing H, Li B, Liu Q, Lynn T M, Wu J, Kuzyakov Y. 2016. Microbial utilization of rice root exudates: C-13 labeling and PLFA composition. Biology and Fertility of Soils52, 615–627.

Zhang F, Ge H, Zhang F, Guo N, Wang Y, Chen L, Ji X, Li C. 2016. Biocontrol potential of Trichoderma harzianum isolate T-aloe against Sclerotinia sclerotiorum in soybean. Plant Physiology and Biochemistry100, 64–74.

Zhang J, Wu X, Zhang X, Pan H, Shearer J E S, Zhang H, Sun F. 2021. Zn2+-dependent enhancement of Atrazine biodegradation by Klebsiella variicola FH-1. Journal of Hazardous Materials411, 125112.

Zhang J, Xiao K, Li M, Hu H, Zhang X, Liu J, Zhang Y. 2022. SsAGM1-mediated uridine diphosphate-n-acetylglucosamine synthesis is essential for development, stress response, and pathogenicity of Sclerotinia sclerotiorumFrontiers in Microbiology13, 938784.

Zhang J, Xu Y, Liang S, Ma X, Lu Z, Sun P, Zhang H, Sun F. 2020. Synergistic effect of Klebsiella sp. FH-1 and Arthrobacter sp. NJ-1 on the growth of the microbiota in the black soil of Northeast China. Ecotoxicology and Environmental Safety190, 110079.

Zhang M, Zhang C, Zhang S, Yu H, Pan H, Zhang H. 2021. Klebsiella jilinsis 2N3 promotes maize growth and induces resistance to northern corn leaf blight. Biological Control156, 104554.

Zhang N, Wang D, Liu Y, Li S, Shen Q, Zhang R. 2014. Effects of different plant root exudates and their organic acid components on chemotaxis, biofilm formation and colonization by beneficial rhizosphere-associated bacterial strains. Plant and Soil374, 689–700.

Zhang N, Wu K, He X, Li S Q, Zhang Z H, Shen B, Yang X M, Zhang R F, Huang, Q W, Shen Q R. 2011. A new bioorganic fertilizer can effectively control banana wilt by strong colonization with Bacillus subtilis N11. Plant and Soil344, 87–97.

Zhao J, Buchwaldt L, Rimmer S R, Sharpe A, McGregor L, Bekkaoui D, Hegedus D. 2009. Patterns of differential gene expression in Brassica napus cultivars infected with Sclerotinia sclerotiorumMolecular Plant Pathology10, 635–649.

Zhao J, Wang J, An L, Doerge R, Chen Z J, Grau C R, Meng J, Osborn T C. 2007. Analysis of gene expression profiles in response to Sclerotinia sclerotiorum in Brassica napusPlanta227, 13–24.

Zhao Q, Shen Q, Ran W, Xiao T, Xu D, Xu Y. 2011. Inoculation of soil by Bacillus subtilis Y-IVI improves plant growth and colonization of the rhizosphere and interior tissues of muskmelon (Cucumis melo L.). Biology and Fertility of Soils, 47, 507–514.

Zhou X, Yang Y, Yin Q, Zhang X, Li M. 2021. Application potential of Comamonas testosteroni ZG2 for vegetable cultivation in nickel and cadmium polluted soil. Environmental Technology & Innovation23, 101626.

Zhu D, Niu Y, Fan K, Zhang F, Wang Y, Wang G, Zheng S. 2021. Selenium-oxidizing Agrobacterium sp. T3F4 steadily colonizes in soil promoting selenium uptake by pak choi (Brassica campestris). Science of the Total Environment791, 148294.

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