Abstract
To screen for Aspergillus activity against Xanthomonas oryzae pv. oryzae and analyse the antimicrobial components involved, 60 Aspergillus spp. were isolated and purified from fruits, soil and other habitats. As-75, an Aspergillus strain that can antagonize Xanthomonas oryzae pv. oryzae, was identified based on the zone of inhibition formed during co-culture. According to morphological, ITS rDNA gene sequencing and phylogenetic tree results, the strain showed close homology to Aspergillus sclerotiorum. The biochemical characterization tests showed that the fermentation broth of strain As-75 exhibited a high capacity for environmental adaptation. The results of the antimicrobial spectrum experiments demonstrated that As-75 exhibited fairly strong antagonistic activity against five plant pathogenic fungi and six plant pathogenic bacteria in vitro. The fermentation broth of strain As-75 displayed maximum stability under fluorescent illumination at temperatures below 60°C at pH 6.5. A substance with antagonistic activity was obtained from strain As-75 via fractional extraction, silica gel column chromatography and thin-layer chromatography. Through mass spectrometry, nuclear magnetic resonance and electrospray ionization mass spectrometry (ESI-MS) analyses, the target compound was identified as (2Z)-2-butenedioic acid-2-(1-methylethenyl)-4-methyl ester; its molecular weight of 170.06 daltons and formula of C8H10O4 identify it as a novel compound. Trials of the preventative and curative effects demonstrated that compound S1 exhibited a better control efficiency than the control against rice bacterial blight. Additionally, the M1 processing method was better, and the efficiency of compound S1 in preventing rice bacterial blight in six rice varieties, TN1, IR24, ZF802, Zhonghua 11, Wuyunjing 21, and Nipponbare, was 78.3%, 77.5%, 74.2%, 75.3%, 70.9%, and 72.1%, respectively.
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Babu, R.M., Sajeena, A., Samundeeswari, A.V., Sreedhar, A., Vidhyasekeran, P., and Reddy, M.S. 2003. Induction of bacterial blight (Xanthomonas oryzae pv. oryzae) resistance in rice by treatment with acibenzolar-S-methyl. Ann. Appl. Biol. 143, 333–340.
Bui, N.Q., Christophe, G., and Gilles, B. 2015. Maleic acid, an efficient additive for the activation of regenerated CoMo/Al2O3 hydrotreating catalysts. J. Catal. 330, 374–386.
Chen, G., Zhang, L., Wang, H.F., Wu, H.H., Lu, X., Pei, Y.H., Wu, X., Pan, B., Hua, H.M., and Bai, J. 2013. A new compound along with seven known compounds from an endophytic fungus Asper-gillus sp. HS-05. Rec. Nat. Prod. 7, 320–324.
Chithrashree, A.C., Udayashankar, A.C., Chandra, N.S., Reddy, M.S., and Srinivas, C. 2011. Plant growth-promoting rhizobac-teria mediate induced systemic resistance in rice against bacterial leaf blight caused by Xanthomonas oryzae pv. oryzae. Biocontrol 59, 114–122.
Cui, Y.Q., Fang, D., Cui, C.H., and Zhou, L.X. 2014. Isolation and identification of Aspergillus niger Y9 and its role in bioleaching of metal contaminants from soils. Chin. J. Appl. Environ. Biol. 20, 420–425.
D’Imperio, M., Cardinali, A., Linsalata, V., Minervini, F.W., Redan, B., and Ferruzzi, M.G. 2014. Stability-activity of verbascoside, a known antioxidant compound, at different pH conditions. Food Res. Int. 66, 373–378.
El-Shakh, A.S.A., Kakar, K.U., Wang, X., Almoneafy, A.A., Ojaghian, M.R., Li, B., Anjum, S.I., and Xie, G.L. 2015. Controlling bacterial leaf blight of rice and enhancing the plant growth with endophytic and rhizobacterial Bacillus strains. Toxicol. Environ. Chem. 97, 766–785.
Fu, B.P., Yuan J., Qian, W.X., Shen, Q.Y., Sun, X.M., and Hannig, M. 2004. Evidence of chemisorption of maleic acid to enamel and hydroxyapatite. Eur. J. Oral Sci. 112, 362–367.
Hop, D.V., Phuong, H.P.T., Quang, N.D., Ton, P.H., Ha, T.H., Hung, N.V., Vna, N.T., Hai, T.V., Kim, Q.N.T., Anh, D.N.T., et al. 2014. Biological control of Xanthomonas oryzae pv. oryzae causing rice bacterial blight disease by Streptomyces toxytricini VN08-A-12, isolated from soil and leaf-litter samples in Vietnam. Biocontrol Sci. 19, 103–111.
Jang, J.H., Park, Y.D., Ahn, H.K., Kim, S.J., Lee, J.Y., Kim, E.C., Chang, Y.S., Song, Y.J., and Kwon, H.J. 2014. Analysis of green tea compounds and their stability in dentifrices of different pH levels. Chem. Pharm. Bull. 62, 328–335.
Jiang, D.H., Liu, Q.Y., Song, Y.M., and Ji, H. 2013. Antimicrobial compound from a novel Streptomyces termitum strain ATC-2 against Xanthomonas oryzae pv. oryzae. Res. J. Biotechnol. 8, 66–70.
Ji, G., Zhang, S., and Qian, J. 2003. Preliminary analysis on races of Xanthomonas oryzae pv. oryzae in Yunnan Province. Plant Prot. 29, 19–21. (in Chinese)
Khan, M.A., Naeem, M., and Iqbal, M. 2014. Breeding approaches for bacterial leaf blight resistance in rice (Oryza sativa L.), current status and future directions. Eur. J. Plant Pathol. 139, 27–37.
Khoa, N.Đ., Giàu, N.Đ.N., and Tuấn, T.Q. 2016. Effects of Serratia nematodiphila CT-78 on rice bacterial leaf blight caused by Xan-thomonas oryzae pv. oryzae. Biol. Control 103, 1–10.
Lee, S.E., Gupta, R., Jayaramaiah, R.H., Lee, S.H., Wang, Y., Park, S.R., and Kim, S.T. 2017. Global transcriptome profiling of Xan-thomonas oryzae pv. oryzae under in planta growth and in vitro culture conditions. Plant Pathol. J. 33, 458–466.
Li, S.B., Xu, S.R., Zhang, R.M., Liu, Y., and Zhou, R.C. 2016. The antibiosis action and rice-induced resistance, mediated by a lip-opeptide from Bacillus amyloliquefaciens B014, in controlling rice disease caused by Xanthomonas oryzae pv. oryzae. J. Microbiol. Biotechnol. 26, 748–756.
Mew, T.W. 1987. Current status and future prospects of research on bacterial blight of rice. Annu. Rev. Phytopathol. 25, 359–382.
Motohashi, K., Inaba, S., Takagi, M., and Shinya, K. 2009. JBIR-15, a new aspochracin derivative, isolated from a sponge-derived fungus, Aspergillus sclerotiorum Huber Sp080903f04. Biosci. Biotechnol. Biochem. 73, 1898–1900.
Mosier, N.S., Wiker, J.J., and Ladisch, M.R. 2004. Rapid chromato-graphy for evaluating adorption characteristics of cellulose binding domain mimetics. Biotechnol. Bioeng. 86, 757–763.
Nehme, H., Saulnier, P., Ramadan, A., Cassisa, V., Guillet, C., Eveillard, M., and Umerska, A. 2018. Antibacterial activity of anti-psychotic agents, their association with lipid nanocapsules and its impact on the properties of the nanocarriers and on antibacterial activity. PLoS One 13, e0189950.
Oliveira, L.C., Silveira, A.M.M., Monteiro, A.S., Dos-Santos, V.L., Nicoli, J.R., Azevedo, V.A.C., Soares S.C., Dias-Souza, M.V., and Nardi, R.M.D. 2017. In silico prediction, in vitro antibacterial spectrum, and physicochemical properties of a putative bacter-iocin produced by Lactobacillus rhamnosus strain L156.4. Front. Microbiol. 8, 876–891.
Phainuphong, P., Rukachaisirikul, V., Saithong, S., Phongpaichit, S., Bowornwiriyapan, K., Muanprasat, C., Srimaroeng, C., Duangjai, A., and Sakayaroj, J. 2016. Lovastatin analogues from the soil-derived fungus Aspergillus sclerotiorum PSU-RSPG178. J. Nat. Prod. 79, 1500–1507.
Phainuphong, P., Rukachaisirikul, V., Saithong, S., Phongpaichit, S., Sakayaroj, J., Srimaroeng, C., Ontawong, A., Duangjai, A., Muangnil, P., and Muanprasat, P. 2018. Asperidines A-C, pyrrolidine and piperidine derivatives from the soil-derived fungus Aspergillus sclerotiorum PSU-RSPG178. Bioorg. Med. Chem. Lett. 26, 4502–4508.
Phainuphong, P., Rukachaisirikul, V., Tadpetch, K., Sukpondma, Y., Saithong, S., Phongpaichit, S., Preedanon, S., and Sakayaroj, J. 2017. ψ-Butenolide and furanone derivatives from the soil-derived fungus Aspergillus sclerotiorum PSU-RSPG178. Phytochemistry 137, 165–173.
Rintala, H., Nevalainen, A., Ronka, E., and Suutari, M. 2001. PCR primers targeting the 16S rRNA gene for the specific detection of Streptomycetes. Mol. Cell. Probe 15, 337–347.
Ryan, R.P., Vorhölter, F.J., Potnis, N., Jones, J.B., Van-Sluys, M.A., Bogdanove, A.J., and Dow, J.M. 2011. Pathogenomics of Xanthomonas: understanding bacterium-plant interactions. Nat. Rev. Microbiol. 9, 344–355.
Son, H.G., Kim, J., Muthaiay, M.J., Lee, S., Kim, H.Y., and Lee, C.H. 2011. Antimicrobial compounds profile during Cheonggukjang fermentation anginst Xanthomonas oryzae pv. oryzae (Xoo). J. Microbiol. Biotechnol. 21, 1147–1150.
Teng, Y., Yang, Q., Yu, Z.Y., Zhou, G.P., Sun, Q., Jin, H., and Hou, T.P. 2010. In vitro antimicrobial activity of the leaf essential oil of Spiraea alpina Pall. World J. Microbiol. Biotechnol. 26, 9–14.
Thimmegowda, P.R., Ambika, D.S., Manjunatha, L., Arun, R.S., Prasad, P.S., and Chandrashekar, M. 2011. Screening germplasm for resistance to bacterial blight of rice caused by Xanthomonas oryzae pv. oryzae. J. Nat. Sci. 2, 659–661.
Victoria, G. and Evgenia, V. 2012. Production of enzymes and antimicrobial compounds by halophilic Antarctic Nocardioides sp. grown on different carbon source. World J. Microbiol. Biotechnol. 28, 2069–2076.
Vivek, K.B., Nguyen, T.D., Jin, H.S., and Sun, C.K. 2010. Antibacterial activity of essential oil and extracts of Cleistocalyx operculatus buds against the bacteria of Xanthomonas spp. J. Am. Oil Chem. Soc. 87, 1341–1349.
Wang, H., Zheng, J.K., Qu, H.J., Liu, P.P., Wang, Y., and Zhu, W.M. 2011. A new cytotoxic indole-3-ethenamide from the halotolerant fungus Aspergillus sclerotiorum PT06-1. J. Antibiot. 64, 679–681.
Weiss, K., Kroschewski, B., and Auerbach, H. 2016. Effects of air exposure, temperature and additives on fermentation characteristics, yeast count, aerobic stability and volatile organic compounds in corn silage. J. Dairy Sci. 99, 8053–8069.
Xu, J., Audenaert, K., Hofte, M., and De, V.D. 2013. Abscisic acid promotes susceptibility to the rice leaf blight pathogen Xanthomonas oryzae pv. oryzae by suppressing salicylic acid-mediated defenses. PLoS One 8, e67413.
Zeng, Y.I., Zhao, S., Wei, H., Tucker, M.P., Himmel, M.E., Mosier, N.S., Meilan, R., and Ding, S.Y. 2015. In situ micro-spectroscopic investigation of lignin in poplar cell walls pretreated by maleic acid. Biotechnol. Biofuels 8, 126.
Zhang, H.T. and Wang, S.P. 2013. Rice versus Xanthomonas oryzae pv. oryzae: a unique pathosystem. Curr. Opin. Plant Biol. 16, 188–195.
Zheng, J.K., Xu, Z.H., Wang, Y., Hong, K., Liu, P.P., and Zhu, W.M. 2010. Cyclic tripeptides from the halotolerant fungus Aspergillus sclerotiorum PT06-1. J. Nat. Prod. 73, 1133–1137.
Zhou, M., Miao, M.M., Du, G., Li, X.N., Shang, S.Z., Zhao, W., Liu, Z.H., Yang, G.Y., Che, C.T., Hu, Q.F., et al. 2014. Aspergillines A-E, highly oxygenated hexacyclic indole-tetrahydrofuran-tetramic acid derivatives from Aspergillus versicolor. Org. Lett. 16, 5016–5019.
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This research was supported by the National Natural Science Foundation of China (Grant 31570013) and was supported by the Zhejiang Provincial Basic Public Welfare Research Project of China (Grant GN18C010004).
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Jiang, B., Wang, Z., Xu, C. et al. Screening and identification of Aspergillus activity against Xanthomonas oryzae pv. oryzae and analysis of antimicrobial components. J Microbiol. 57, 597–605 (2019). https://doi.org/10.1007/s12275-019-8330-5
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DOI: https://doi.org/10.1007/s12275-019-8330-5