Self-digestive solution of Lysobacter enzymogenes LE16 as a biofungicide to control plant powdery mildew

References

• Alemu K, Adugna G, Lemessa F, Muleta D. 2019. Induction of systemic resistance in Arabica coffee (Coffea arabica L.) against coffee berry disease (Colletotrichum kahawae Waller & Bridge) mediated through plant defense activator. International Journal of Pest Management. 65(4):313–323. doi:10.1080/09670874.2018.1506190.
   Web of Science ®Google Scholar
• Ardebili ZO, Ardebili NO, Mohammad S. 2011. Physiological effects of Pseudomonas fluorescens CHA0 on tomato (Lycopersicon esculentum Mill.) plants and its possible impact on Fusarium oxysporum f. sp. Lycopersici. Aust J Crop Sci. 5(12):1631–1638.
   Web of Science ®Google Scholar
• Bargabus RL, Zidack NK, Sherwood JE, Jacobsen BJ. 2004. Screening for the identification of potential biological control agents that induce systemic acquired resistance in sugar beet. Biol Control. 30:342–350.
   Web of Science ®Google Scholar
• Bito LZ. 2017. Eicosanoid transport systems: mechanisms, physiological roles, and inhibitors. In CRC handbook of eicosanoids: prostaglandins and related lipids. Cachan: CRC Press; p. 211–232.
   Google Scholar
• Boesewinkel HJ. 1980. The morphology of the imperfect states of powdery mildews (Erysiphaceae). Bot Rev. 46:167–224.
   Web of Science ®Google Scholar
• Brent KJ, Holloman DW. 2007a. Fungicide resistance in crop pathogens: how can it be managed? Fungicide resistance action committee monograph 1. Crop Life International, Brussels
   Google Scholar
• Brent KJ, Holloman DW. 2007b. Fungicide resistance in crop pathogens: the assessment of risk. Fungicide resistance action committee monograph 2. Crop Life International, Brussels
   Google Scholar
• Carroll JE, Wilcox WF. 2003. Effects of humidity on the development of grapevine powdery mildew. Phytopathology. 93:1137.
   PubMed Web of Science ®Google Scholar
• Chen DM, Yang HJ, Huang JG, Yuan L. 2020. Lysobacter enzymogenes LE16 autolysates have potential as biocontrol agents. J Appl Microbiol. 129:1684–1692.
   PubMed Web of Science ®Google Scholar
• Cho IC, Lee SH, Cha BJ. 1998. Effects of soluble silicon and several surfactants on the development of powdery mildew of cucumber. Korean J Environ Agric. 17:306–311.
   Google Scholar
• Christensen P, Cook FD. 1978. Lysobacter, a new genus of nonfruiting, gliding bacteria with a high base ratio. Int J Syst Bacteriol. 28:367–393.
   Google Scholar
• Dietz J, Winter C. 2019. Recently introduced powdery mildew fungicides. In: Jeschke P, Witschel M, Krämer W, Schirmer U, editors. Modern crop protection compounds. Weinheim: Wiley-VCH Verlag GmbH & Co. KGaA; p. 933–947.
   Google Scholar
• Elad Y, Kirshner B, Yehuda N, Sztejnberg A. 1998. Management of powdery mildew and gray mold of cucumber by Trichoderma harzianum T39 and Ampelomyces quisqualis AQ10. BioControl. 43:241–251.
   Web of Science ®Google Scholar
• Ferrandino FJ, Smith VL. 2007. The effect of milk-based foliar sprays on yield components of field pumpkins with powdery mildew. Crop Prot. 26:657–663.
   Web of Science ®Google Scholar
• Folman LB, Postma J, Veen JAV. 2003. Characterisation of Lysobacter enzymogenes (Christensen and Cook 1978) strain 3.1 T8, a powerful antagonist of fungal diseases of cucumber. Microbiol Res. 158:107–115.
   PubMedGoogle Scholar
• Fondevilla S, Rubiales D. 2012. Powdery mildew control in pea. A Review. Agron Sustain Dev 32:401–409.
   Web of Science ®Google Scholar
• Gálvez-Iriqui AC, Cortez-Rocha MO, Burgos-Hernández Calderón-Santoyo M, Argüelles-Monal WM, Plascencia-Jatomea M. 2019. Synthesis of chitosan biocomposites loaded with pyrrole-2-carboxylic acid and assessment of their antifungal activity against Aspergillus Niger. Appl Microbiol Biotechnol. 103:2985–3000.
   PubMed Web of Science ®Google Scholar
• Gang FL, Zhu F, Li XT, Wei JL, Wu WJ, Zhang JW. 2018. Synthesis and bioactivities evaluation of L-pyroglutamic acid analogues from natural product lead. Bioorgan Med Chem. 26(16):4644–4649.
   PubMed Web of Science ®Google Scholar
• Garavito MF, Narváez-Ortiz HY, Zimmermann BH. 2015. Pyrimidine metabolism: dynamic and versatile pathways in pathogens and cellular development. J Genet Genomics. 42:195–205.
   PubMed Web of Science ®Google Scholar
• Ghosh SK, Pal S, Chakraborty N. 2015. The qualitative and quantitative assay of siderophore production by some microorganisms and effect of different media on its production. Int J Chem. 13:1621–1629.
   Google Scholar
• Gilardi G, Baudino M, Garibaldi A, Gullino ML. 2012. Efficacy of biocontrol agents and natural compounds against powdery mildew of zucchini. Phytoparasitica. 40:147–155.
   Web of Science ®Google Scholar
• Green AJ, Berger G, Griffey CA, Pitman R, Thomason W, Balota M. 2014. Genetic resistance to and effect of leaf rust and powdery mildew on yield and its components in 50 soft red winter wheat cultivars. Crop Prot. 64:177–186.
   Web of Science ®Google Scholar
• Guzman-Plazola RA, Davis RM, Marois JJ. 2003. Effects of relative humidity and high temperature on spore germination and development of tomato powdery mildew (Leveillula taurica). Crop Prot. 22(10):1157–1168.
   Web of Science ®Google Scholar
• Hammerschmidtm R, Nuckles EM, Kuc J. 1982. Association of enhanced peroxidase activity with induced systemic resistance of cucumber to colletotrchum lagenarium. Physiol Plant Pathol. 20:73–82.
   Google Scholar
• Herrera-Tellez VI, Cruz-Olmedo AK, Plansencia J, Gavilanes-Ruíz M, Arce-Cervantes O, Hernández-León S, Saucedo-García M. 2019. The protective effect of Trichoderma asperellum on tomato plants against fusarium oxysporum and Botrytis cinerea diseases involves inhibition of reactive oxygen species production. Int J Mol Sci. 20:2007.
   PubMed Web of Science ®Google Scholar
• Jiao R, Munir S, He PF, Yang HW, Wu YX, Wang JW, Cai YZ, Wang G, He YQ. 2020. Biocontrol potential of the endophytic Bacillus amyloliquefaciens YN201732 against tobacco powdery mildew and its growth promotion. Biol Control. 143:104160.
   Web of Science ®Google Scholar
• Jin XL, Fitt BDL, Hall AM, Huang YJ. 2013. The role of chasmothecia in the initiation of epidemics of powdery mildew (Podospheara aphanis) and the role of silicon in controlling the epidemics on strawberry. Aspects of Applied Biology. 119:151–155.
   Google Scholar
• Ji ZL, Peng S, Zhu W, Dong JP, Zhu F. 2020. Induced resistance in nectarine fruit by Bacillus licheniformis W10 for the control of brown rot caused by Monilinia fructicola. Food Microbiology. 92:103558.
   PubMed Web of Science ®Google Scholar
• Keinath AP, Dubose VB. 2012. Controlling powdery mildew on cucurbit rootstock seedlings in the greenhouse with fungicides and biofungicides. Crop Prot. 42:338–344.
   Web of Science ®Google Scholar
• Kind T, Wohlgemuth G, Lee DY, Lu Y, Palazoglu M, Shahbaz S, Fiehn O. 2009. FiehnLib: mass spectral and retention index libraries for metabolomics based on quadrupole and time-of-flight gas chromatography/mass spectrometry. Anal Chem. 81:10038–10048.
   PubMed Web of Science ®Google Scholar
• Kiss L. 2003. A review of fungal antagonists of powdery mildews and their potential as biocontrol agents. Pest Manage Sci. 59:475–483.
   PubMed Web of Science ®Google Scholar
• Kumar D. 2014. Salicylic acid signaling in disease resistance. Plant Science. 228:127–134.
   PubMed Web of Science ®Google Scholar
• Lee KS, Kim EH, Lee YS, Lee SH, Seo YB, Hwang SA, Cho JY. 2009. Control efficacy of bordeaux mixture against powdery mildew on omija (Schizandra chinensis). J Korean Soc Appl Biol Chem. 52:58–62.
   Google Scholar
• Li YL, Gu YL, Li J, Xu MZ, Wei Q, Wang YH. 2015. Biocontrol agent Bacillus amyloliquefaciens LJ02 induces systemic resistance against cucurbits powdery mildew. Front Microbiol. 6:883.
   PubMed Web of Science ®Google Scholar
• Lilai SA, Kapinga FA, Nene WA, Mbasa WV, Tibuhwa DD. 2022. The efficacy of biofungicides on cashew wilt disease caused by Fusarium oxysporum. Eur J Plant Pathol. 163(2):453–465.
   Web of Science ®Google Scholar
• Liu J, Sui Y, Wisniewski M, Droby S, Liu YS. 2013. Review: utilization of antagonistic yeasts to manage postharvest fungal diseases of fruit. Int J Food Microbiol. 167(2):153–160.
   PubMed Web of Science ®Google Scholar
• Luo Y, Shang J, Zhao P, Xi D, Yuan S, Lin H. 2011. Application of jasmonic acid followed by salicylic acid inhibits cucumber mosaic virusreplication. The Plant Pathology Journal. 27(1):53–58.
   Web of Science ®Google Scholar
• McGrath MT. 2001. Fungicide resistance in cucurbit powdery mildew: experiences and challenges. Plant Dis. 85:236–245.
   PubMed Web of Science ®Google Scholar
• McGrath MT, Shishkoff N. 1999. Evaluation of biocompatible products for managing cucurbit powdery mildew. Crop Prot. 18:471–478.
   Web of Science ®Google Scholar
• Miccoli C, Palmieri D, De Curtis F, Lima G, Heitman J, Castoria R, Ianiri G. 2020. The necessity for molecular classification of basidiomycetous biocontrol yeasts. BioControl. 65:489–500.
   Web of Science ®Google Scholar
• Moyer C, Peres NA. 2008. Evaluation of biofungicides for control of powdery mildew of gerbera daisy. Proc Fla State Hortic Soc. 121:389–394.
   Google Scholar
• Nam MH, Jung SK, Ra SW, Kim HG. 2003. Control efficacy of sodium bicarbonate alone and in mixture with polyoxyethylene sorbitanmonolaurate on powdery mildew of strawberry. Korean J Hortic Sci. 21:98–101.
   Google Scholar
• Odhiambo BO, Xu GG, Qian GL, Liu FQ. 2017. Evidence of an unidentified extracellular heat-stable factor produced by Lysobacter enzymogenes (OH11) that degrade Fusarium graminearum PH1 hyphae. Curr Microbiol. 74:437–448.
   PubMed Web of Science ®Google Scholar
• Palumbo JD, Yuen GY, Jochum CC, Tatum K, Kobayashi DY. 2005. Mutagenesis of beta-1,3-glucanase genes in Lysobacter enzymogenes strain C3 results in reduced biological control activity toward bipolaris leaf spot of tall fescue and pythium damping-off of sugar beet. Phytopathology. 95:701–707.
   PubMed Web of Science ®Google Scholar
• Panthee S, Hamamoto H, Paudel A, Sekimizu K. 2016. Lysobacter species: a potential source of novel antibiotics. Arch Microbiol. 198:839–845.
   PubMed Web of Science ®Google Scholar
• Parnell JJ, Berka R, Young HA, Sturino JM, Kang Y, Barnhart DM, DiLeo MV. 2016. From the lab to the farm: an industrial perspective of plant beneficial microorganisms. Front Plant Sci. 7:1110.
   PubMed Web of Science ®Google Scholar
• Pikovskaya RI. 1948. Mobilization of phosphorus in soil in connection with the vital activity of some microbial species. Mikrobiologiya. 17:362–370.
   Google Scholar
• Pokora W, Reszka J, Tukaj Z. 2003. Activities of superoxide dismutase (SOD) isoforms during growth of Scenedesmus (Chlorophyta) species and strains grown in batch-cultures. Acta Physiol Plant. 25:375–384.
   Web of Science ®Google Scholar
• Postma J, Stevens LH, Wiegers GL, Davelaar E, Nijhuis EH. 2009. Biological control of Pythium aphanidermatum in cucumber with a combined application of Lysobacter enzymogenes strain 3.1 T8 and chitosan. Biol Control. 48:301–309.
   Web of Science ®Google Scholar
• Praveen PM, Dhandapani N. 2001. Eco-friendly management of major pests of okra (Abelmoschus esculentus (L.) Moench). J Veg Crop Prod. 7:3–12.
   Google Scholar
• Qian GL, Hu BS, Jiang YH, Liu FQ. 2009. Identification and characterization of Lysobacter enzymogenes as a biological control agent against some fungal pathogens. Agric Sci China. 8:68–75.
   Google Scholar
• Rais A, Jabeen Z, Shair F, Hafeez FY, Hassan MN. 2017. Bacillus spp., a bio-control agent enhances the activity of antioxidant defense enzymes in rice against Pyricularia oryzae. Plos one. 12(11):e0187412.
   PubMed Web of Science ®Google Scholar
• Russell PE. 2004. Sensitivity baselines in fungicide resistance research and management. Cambridge: AIMPRINT; p. 3–12.
   Google Scholar
• Sadiq FA, Yan B, Zhao J, Zhang H, Chen W. 2020. Untargeted metabolomics reveals metabolic state of Bifidobacterium bifidum in the biofilm and planktonic states. Lwt. 118:108772.
   Web of Science ®Google Scholar
• Schwyn B, Jb N. 1987. Universal chemical assay for the detection and determination of siderophores. Anal Biochem. 160:47–56.
   PubMed Web of Science ®Google Scholar
• Shi Q, Ding F, Wang X, Wei M. 2007. Exogenous nitric oxide protect cucumber roots against oxidative stress induced by salt stress. Plant Physiol Biochem. 45:542–550.
   PubMed Web of Science ®Google Scholar
• Shishkoff N, McGrath MT. 2002. AQ10 biofungicide combined with chemical fungicides or AddQ spray adjuvant for control of cucurbit powdery mildew in detached leaf culture. Plant Dis. 86:915–918.
   PubMed Web of Science ®Google Scholar
• Sillero JC, Rojas-Molina MM, Avila CM, Rubiales D. 2012. Induction of systemic acquired resistance against rust, Ascochytablight and broomrape in faba bean by exogenous application of salicylic acid and benzothiadiazole. Crop Protection. 34:65–69.
   Web of Science ®Google Scholar
• Simaei M, Khavarinejada RA, Saadatmanda S, Bernardb F, Fahimia H. 2011. Interactive effects of salicylic acid and nitric oxide on soybean plants under NaCl salinity. Russ J Plant Physiol. 58:783–790.
   Web of Science ®Google Scholar
• Singh RS. 1999. Plant diseases. New Delhi: Oxford and IBH.
   Google Scholar
• Sugahara I, Hayashi K, Kimura T. 1982. Studies on marine bacteria producing lytic enzymes-VII: autolytic activity of bacteria capable of producing lytic enzymes. Bull Fac Fish Mie Univ. 9:31–37.
   Google Scholar
• Tang B, Laborda P, Sun C, Xu G, Zhao Y, Liu F. 2019. Improving the production of a novel antifungal alteramide B in Lysobacter enzymogenes OH11 by strengthening metabolic flux and precursor supply. Bioresour Technol. 273:196–202.
   PubMed Web of Science ®Google Scholar
• Tariq A, Masroor M, Khan A, Jaime A, da Teixeira S, Mohd I, Naeem M. 2011. Role of salicylic acid in promoting salt stress tolerance and enhanced artemisinin production in Artemisia annua L. J Plant Growth Regul. 30:425–435.
   Web of Science ®Google Scholar
• Tsugawa H, Cajka T, Kind T, Ma Y, Higgins B, Ikeda K, Kanazawa M, VanderGheynst J, Fiehn O, Arita M. 2015. MS-DIAL: data-independent MS/MS deconvolution for comprehensive metabolome analysis. Nat Methods. 12:523–526.
   PubMed Web of Science ®Google Scholar
• Vellosillo T, Vicente J, Kulasekaran S, Hamberg M, Castresana C. 2010. 25,000th article commemorative issue || emerging complexity in reactive oxygen species production and signaling during the response of plants to pathogens. Plant Physiol. 154(2):444–448.
   PubMed Web of Science ®Google Scholar
• Wang HC, Li WH, Xia HQ, Wang MS, Meng L, Shi XJ, Shang SH, Wang JJ. 2012. Toxicity and control efficacy of azoxystrobin and pyraclostrobin against Erysiphe cichoracearum on tobacco during seedling developing period. Chin J Pestic Sci. 14:412–416.
   Google Scholar
• Wheeler BEJ. 1969. An introduction to plant disease. London: John Wiley and Sons Ltd.
   Google Scholar
• Wod S-M, Figueiredo-Júnior EC, Fieire JCP, Costa, BP, Lira, AB, Freiers, IA, Cavalcanti, YE, Lopes, JV, Tavares, JF, Pessoa, HLF, Pereira, JV . 2021. Phytochemistry, antifungal and antioxidant activity, and cytotoxicity of byrsonima gardneriana (A. Juss) Extract. Arch Oral Biol 123:104994.
   PubMed Web of Science ®Google Scholar
• Wu XX, Zhu WM, Zhang H, Ding HD, Zhang HJ. 2011. Exogenous nitric oxide protects against salt-induced oxidative stress in the leaves from two genotypes of tomato (Lycopersicom esculentum Mill). Acta Physiol Plant. 33:1199–1209.
   Web of Science ®Google Scholar
• Xu N, Chu YL, Chen HL, Li XX, Wu Q, Jin L, Wang GX, Huang JL. 2018. Rice transcription factor OsMADS25 modulates root growth and confers salinity tolerance via the ABA-mediated regulatory pathway and ROS scavenging. PLoS Genet. 14(10):e1007662.
   PubMed Web of Science ®Google Scholar
• Yan ZF, Dolstra O, Prins TW, Stam P, Visser PB. 2006. Assessment of partial resistance to powdery mildew (Podosphaera pannosa) in a tetraploid rose population using a spore-suspension inoculation method. Eur J Plant Pathol. 114:301–308.
   Web of Science ®Google Scholar
• Yuen GY, Steadman JR, Lindgren DT, Schaff D, Jochum C. 2001. Bean rust biological control using bacterial agents. Crop Prot. 20:95–402.
   Web of Science ®Google Scholar
• Yuen G, Zhang Z. 2001. Control of brown patch disease using the bacterium Stenotrophomonas maltophilia strain C3 and culture fluid. ITSRJ. 9:742–747.
   Google Scholar
• Yu CL, Li SX, Zhang B, Lin F. 2012. Safety of tetraconazole to cucumber and its efficacy against cucumber powdery mildew. Acta Phytophylacica Sin. 39:265–270.
   Google Scholar
• Zhang SQ, Liu YD. 2001. Activation of salicylic acid-induced protein kinase, a mitogen-activated protein kinase, induces multiple defense responses in tobacco. Plant Cell. 13(8):1877–1889.
   PubMed Web of Science ®Google Scholar
• Zhang S, Vallad GE, White TL, Huang CH. 2011. Evaluation of microbial products for management of powdery mildew on summer squash and cantaloupe in Florida. Plant Dis. 95:461–468.
   PubMed Web of Science ®Google Scholar
• Zhang Z, Yuen GY. 1999. Biological control of Bipolaris sorokiniana on tall fescue by Stenotrophomonas maltophilia strain C3. Phytopathology. 89:817–822.
   PubMed Web of Science ®Google Scholar
• Zhang Z, Yuen GY. 2000. The role of chitinase production by Stenotrophomonas maltophilia strain c3 in biological control of Bipolaris sorokiniana. Phytopathology. 90:384–389.
   PubMed Web of Science ®Google Scholar