Abstract
Phytophthora species cause enormous economic loss every year worldwide. Xenocoumacin 1 (Xcn1), isolated from the bacterium Xenorhabdus nematophilus, is a broad-spectrum antibiotic against agricultural pathogens, especially Phytophthora. To understand the inhibitory mode of Xcn1 toward Phytophthora pathogens, we determined the inhibitory effects of Xcn1 on Phytophthora capsici both in vitro and in vivo. In vitro, Xcn1 inhibited different stages in the life cycle of P. capsici, including sporangium formation, zoospore germination, and mycelial growth, with 50% effective concentration (EC50) values of 0.037, 0.81, and 2.44 μg ml−1, respectively. Xcn1 also reduced zoospore motility. In vivo, Xcn1 efficiently controlled the Phytophthora blight of pepper with a disease reduction of 99% at a concentration of 5 μg ml−1 assessed on the third day after incubation of wound stem plants. In addition, Xcn1-treated P. capsici mycelia exhibited increased mycelial branch spacing, evident plasmolysis, and leakage of intracellular components. In conclusion, in the presence of Xcn1, several stages in the life cycle of P. capsici were inhibited, and the hyphae exhibited obvious morphological changes.
Similar content being viewed by others
References
Andrieu N, Jaworska G, Genet JL, Bompeix G (2001) Biological mode of action of famoxadone on Plasmopara viticola and Phytophthora infestans. Crop Prot 20:253–260
Anke T (1995) The antifungal strobilurins and their possible ecological role. Can J Bot 73:940–945
Cohen Y, Coffey MD (1986) Systemic fungicides and the control of oomycetes. Annu Rev Phytopathol 24:311–338
Cray JA, Bell AN, Bhaganna P, Mswaka AY, Timson DJ, Hallsworth JE (2013) The biology of habitat dominance; can microbes behave as weeds? Microb Biotechnol 6:453–492
Cray JA, Stevenson A, Ball P, Bankar SB, Eleutherio EC, Ezeji TC, Singhal RS, Thevelein JM, Timson DJ, Hallsworth JE (2015) Chaotropicity: a key factor in product tolerance of biofuel-producing microorganisms. Curr Opin Biotechnol 33:228–259
Davidse LC, Hofman AE, Velthuis GCM (1983) Specific interference of metalaxyl with endogenous RNA polymerase activity in isolated nuclei from Phytophthora megasperma f. sp. medicaginis. Exp Mycol 7:344–361
De Lima Alves F, Stevenson A, Baxter E, Gillion JL, Hejazi F, Hayes S, Morrison IE, Prior BA, McGenity TJ, Rangel DE, Magan N, Timmis KN, Hallsworth JE (2015) Concomitant osmotic and chaotropicity-induced stresses in Aspergillus wentii: compatible solutes determine the biotic window. Curr Genet 61:457–477
Deising HB, Reimann S, Peil A, Weber WE (2002) Disease management of rusts and powdery mildews. In: Kempken F (ed) The mycota XI. Application in Agriculture. Springer, Berlin, pp 243–269
Duniway JM (1983) Role of physical factors in the development of Phytophthora diseases. In: Erwin DC, Bartnicki-Garcia S, Tsao PH (eds) Phytophthora: its biology, taxonomy, ecology, and pathology. APS, St Paul, MN, pp 175–187
Dynesen J, Nielsen J (2003) Branching is coordinated with mitosis in growing hyphae of Aspergillus nidulans. Fung Genet Biol 40:15–24
Erwin DC, Ribeiro OK (1996) Phytophthora diseases worldwide. APS, St Paul, MN
Fiddy C, Trinci AP (1976) Mitosis, septation, branching, and the duplication cycle in Aspergillus nidulans. J Genet Microbiol 97:169–184
Gregory PH (1983) Some major epidemics caused by Phytophthora. In: Erwin DC, Bartnicki-Garcia S, Tsao PH (eds) Phytophthora: its biology, taxonomy, ecology, and pathology. St Paul, MN, APS, pp 271–278
Hallsworth JE, Heim S, Timmis KN (2003) Chaotropic solutes cause water stress in Pseudomonas putida. Environ Microbiol 5:1270–1280
Hausbeck MK, Lamour KH (2004) Phytophthora capsici on vegetable crops: research progress and management challenges. Plant Dis 88:1292–1303
Hickman C (1970) Biology of Phytophthora zoospores. Phytopathology 60:1128–1135
Huang W, Zhu C, Yang X, Yang H, Xu H, Xie Y, Jian H (2005) Isolation and structural indentification of main component CB6-1 produced by Xenorhabdus nematophila var. pekingensis. Chin J Antibiot 30:513–515
Huang W, Yang X, Yang H, Liu Z, Yuan J (2006) Identification and activity of antibacterial substance from Xenorhabdus nematophila var. Pekingense. Nat Prod Res Dev 18:25–28
Judelson HS, Blanco FA (2005) The spores of Phytophthora: weapons of the plant destroyer. Nat Rev Microbiol 3:47–58
Kuhn PJ, Pitt D, Lee SA, Wakley G, Sheppard AN (1991) Effects of dimethomorph on the morphology and ultrastructure of Phytophthora. Mycol Res 95:333–340
Lozowicka B, Hrynko I, Kaczynski P, Jankowska M, Rutkowska E (2016) Long-term investigation and health risk assessment of multi-class fungicide residues in fruits. Pol J Environ Stud 25:681–697
Matheron ME, Porchas M (2000) Impact of azoxystrobin, dimethomorph, fluazinam, fosetyl-Al, and metalaxyl on growth, sporulation, and zoospore cyst germination of three Phytophthora spp. Plant Dis 84:454–458
McInerney BV, Taylor WC, Lacey MJ, Akhurst RJ, Gregson RP (1991) Biologically active metabolites from Xenorhabdus spp, Part 2. Benzpyran-1-one derivatives with gastroprotective activity. J Nat Prod 54:785–795
Muri SD, van der Voet H, Boon PE, van Klaveren JD, Bruschweiler BJ (2009) Comparison of human health risks resulting from exposure to fungicides and mycotoxins via food. Food Chem Toxicol 47:2963–2974
Park H (2003) Isolation and anti-oomycete activity of nyasol from Anemarrhena asphodeloides rhizomes. Phytochemistry 64:997–1001
Ristaino JB, Johnston SA (1999) Ecologically based approaches to management of Phytophthora blight on bell pepper. Plant Dis 83:1080–1089
Schlub RL (1983) Epidemiology of Phytophthora capsici on bell pepper. J Agric Sci Camb 100:7–11
Schwinn F, Staub T (1995) Oomycetes fungicides. In: Lyr H (ed) Modern selective fungicides: properties, applications, mechanisms of action. Gustav Fischer Verlag, New York, pp 323–346
van der Auwera G, De Baere R, van de Peer Y, De Rijk P, van den Broeck I, De Wachter R (1995) The phylogeny of the Hyphochytriomycota as deduced from ribosomal RNA sequences of Hyphochytrium catenoides. Mol Biol Evol 12:671–678
Walker GM (2011) Pichia anomala: cell physiology and biotechnology relative to other yeasts. Antonie van Leeuwenhoek 99:25–34
Yan XJ, Qin WC, Sun LP, Qi SH, Yang DB, Qin ZH, Yuan HZ (2010) Study of inhibitory effects and action mechanism of the novel fungicide pyrimorph against Phytophthora capsici. J Agric Food Chem 58:2720–2725
Yang XF, Yang HW, Jian H, Luan XQ (1998) The antibiosis of Xenorhabdus spp. against Phytophthora boehmeriae. Chin J Biol Control 14:21–24
Yang HW, Zhang ZM, Yang XF, Jian H (2000) Antibiosis of metabolite of Xenorhabdus nematophilus against Phytophthora infestans. Chin J Biol Control 16:111–113
Yang XF, Yang HW, Jian H (2002) Antibiotic activity of metabolites from Xenorhabdus nematophilus against Phytophthora sojae. Soybean Sci 21:52–55
Yang XF, Qiu DW, Yang HW, Liu Z, Zeng HM, Yuan JJ (2011) Antifungal activity of xenocoumacin 1 from Xenorhabdus nematophilus var. pekingensis against Phytophthora infestans. World J Microbiol Biotechnol 27:523–528
Zheng YL, Zhu LM, Yao ST (2006) Study on the yield loss induced by Phytophthora capsici Leonian and its controlling index. Acta Agric Zhejiangensis 18:179–182
Zhou TT, Zeng HM, Qiu DW, Yang XF, Wang BN, Chen MJ, Guo LH, Wang SC (2011) Global transcriptional responses of Bacillus subtilis to xenocoumacin 1. J Appl Microbiol 111:652–662
Acknowledgements
We thank Ms. Hongjing Hao (Institute of Agro-food Science and Technology, Chinese Academy of Agricultural Sciences, China) for technical assistance in transmission electron microscopy. This work was supported by the Special Fund for Agro-Scientific Research in the Public Interest (No. 200903052).
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Jesus Mercado Blanco
Rights and permissions
About this article
Cite this article
Zhou, T., Yang, X., Qiu, D. et al. Inhibitory effects of xenocoumacin 1 on the different stages of Phytophthora capsici and its control effect on Phytophthora blight of pepper. BioControl 62, 151–160 (2017). https://doi.org/10.1007/s10526-016-9779-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10526-016-9779-3