Browse > Article
http://dx.doi.org/10.1080/12298093.2022.2136333

Biological Control of Oomycete Soilborne Diseases Caused by Phytophthora capsici, Phytophthora infestans, and Phytophthora nicotianae in Solanaceous Crops  

Elena Volynchikova (Laboratory of Plant Disease and Biocontrol, Department of Plant Biotechnology, Korea University)
Ki Deok Kim (Laboratory of Plant Disease and Biocontrol, Department of Plant Biotechnology, Korea University)
Publication Information
Mycobiology / v.50, no.5, 2022 , pp. 269-293 More about this Journal
Abstract
Oomycete pathogens that belong to the genus Phytophthora cause devastating diseases in solanaceous crops such as pepper, potato, and tobacco, resulting in crop production losses worldwide. Although the application of fungicides efficiently controls these diseases, it has been shown to trigger negative side effects such as environmental pollution, phytotoxicity, and fungicide resistance in plant pathogens. Therefore, biological control of Phytophthora-induced diseases was proposed as an environmentally sound alternative to conventional chemical control. In this review, progress on biological control of the soilborne oomycete plant pathogens, Phytophthora capsici, Phytophthora infestans, and Phytophthora nicotianae, infecting pepper, potato, and tobacco is described. Bacterial (e.g., Acinetobacter, Bacillus, Chryseobacterium, Paenibacillus, Pseudomonas, and Streptomyces) and fungal (e.g., Trichoderma and arbuscular mycorrhizal fungi) agents, and yeasts (e.g., Aureobasidium, Curvibasidium, and Metschnikowia) have been reported as successful biocontrol agents of Phytophthora pathogens. These microorganisms antagonize Phytophthora spp. via antimicrobial compounds with inhibitory activities against mycelial growth, sporulation, and zoospore germination. They also trigger plant immunity-inducing systemic resistance via several pathways, resulting in enhanced defense responses in their hosts. Along with plant protection, some of the microorganisms promote plant growth, thereby enhancing their beneficial relations with host plants. Although the beneficial effects of the biocontrol microorganisms are acceptable, single applications of antagonistic microorganisms tend to lack consistent efficacy compared with chemical analogues. Therefore, strategies to improve the biocontrol performance of these prominent antagonists are also discussed in this review.
Keywords
Biocontrol; oomycete; Phytophthora capsici; Phytophthora infestans; Phytophthora nicotianae; solanaceous crop;
Citations & Related Records
Times Cited By KSCI : 18  (Citation Analysis)
연도 인용수 순위
1 Bae SJ, Mohanta TK, Chung JY, et al. Trichoderma metabolites as biological control agents against Phytophthora pathogens. Biol Control. 2016;92:128-138.
2 Nguyen X-H, Naing K-W, Lee Y-S, et al. Biocontrol potential of Streptomyces griseus H7602 against root rot disease (Phytophthora capsici) in pepper. Plant Pathol J. 2012;28(3):282-289.   DOI
3 Zohara F, Akanda MA, Paul NC, et al. Inhibitory effects of Pseudomonas spp. on plant pathogen Phytophthora capsici in vitro and in planta. Biocatal. 2016;5:69-77.
4 Cheng W, Lin M, Qiu M, et al. Chitin synthase is involved in vegetative growth, asexual reproduction and pathogenesis of Phytophthora capsici and Phytophthora sojae. Environ Microbiol. 2019;21(12):4537-4547.   DOI
5 de Vrieze M, Varadarajan AR, Schneeberger K, et al. Linking comparative genomics of nine potato-associated Pseudomonas isolates with their differing biocontrol potential against late blight. Front Microbiol. 2020;11:857.
6 Kruijt M, Tran H, Raaijmakers JM. Functional, genetic and chemical characterization of biosurfactants produced by plant growth-promoting Pseudomonas putida 267. J Appl Microbiol. 2009;107(2):546-556.   DOI
7 Robles-Yerena L, Rodriguez-Villarreal RA, Ortega-Amaro MA, et al. Characterization of a new fungal antagonist of Phytophthora capsici. Sci Hortic. 2010;125(3):248-255.
8 El-Sayed AS, Ali GS. Aspergillus flavipes is a novel efficient biocontrol agent of Phytophthora parasitica. Biol Control. 2020;140:104072.
9 Han T, You C, Zhang L, et al. Biocontrol potential of antagonist Bacillus subtilis Tpb55 against tobacco black shank. BioControl. 2016;61(2):195-205.   DOI
10 Abbasi S, Safaie N, Sadeghi A, et al. Tissue-specific synergistic bio-priming of pepper by two Streptomyces species against Phytophthora capsici. PLoS One. 2020;15(3):e0230531.
11 Xu S, Kim BS. Evaluation of Paenibacillus polymyxa strain SC09-21 for biocontrol of phytophthora blight and growth stimulation in pepper plants. Trop Plant Pathol. 2016;41(3):162-168.   DOI
12 Macias-Rodriguez L, Guzman-Gomez A, Garcia-Juarez P, et al. Trichoderma atroviride promotes tomato development and alters the root exudation of carbohydrates, which stimulates fungal growth and the biocontrol of the phytopathogen Phytophthora cinnamomi in a tripartite interaction system. FEMS Microbiol. 2018;94:fiy137.
13 Jiang Z, Guo Y, Li S, et al. Evaluation of biocontrol efficiency of different Bacillus preparations and field application methods against phytophthora blight of bell pepper. Biol Control. 2006;36(2):216-223.   DOI
14 Rajaofera MJN, Jin PF, Fan YM, et al. Antifungal activity of the bioactive substance from Bacillus atrophaeus strain HAB-5 and its toxicity assessment on Danio rerio. Pestic Biochem Physiol. 2018;147:153-161.   DOI
15 Syed-Ab-Rahman SF, Carvalhais LC, Chua E, et al. Identification of soil bacterial isolates suppressing different Phytophthora spp. and promoting plant growth. Front Plant Sci. 2018;871:1502.
16 Abbasi S, Spor A, Sadeghi A, et al. Streptomyces strains modulate dynamics of soil bacterial communities and their efficacy in disease suppression caused by Phytophthora capsici. Sci Rep. 2021;11:1-14.   DOI
17 Ozyilmaz U, Benlioglu K. Enhanced biological control of Phytophthora blight of pepper by biosurfactant-producing Pseudomonas. Plant Pathol J. 2013;29(4):418-426.
18 de Vrieze M, Germanier F, Vuille N, et al. Combining different potato-associated Pseudomonas strains for improved biocontrol of Phytophthora infestans. Front Microbiol. 2018;9(2573):2573.
19 Sang MK, Jeong JJ, Kim J, et al. Growth promotion and root colonisation in pepper plants by phosphate-solubilising Chryseobacterium sp. strain ISE14 that suppresses Phytophthora blight. Ann Appl Biol. 2018;172(2):208-223.   DOI
20 Sharma R, Chauhan A, Shirkot CK. Characterization of plant growth promoting Bacillus strains and their potential as crop protectants against Phytophthora capsici in tomato. Biol Agric Hortic. 2015;31(4):230-244.   DOI
21 Ma L, Zhang HY, Zhou XK, et al. Biological control tobacco bacterial wilt and black shank and root colonization by bio-organic fertilizer containing bacterium Pseudomonas aeruginosa NXHG29. Appl Soil Ecol. 2018;129:136-144.   DOI
22 Hausbeck MK, Lamour KH. Phytophthora capsici on vegetable crops: research progress and management challenges. Plant Dis. 2004;88(12):1292-1303.   DOI
23 Aravind R, Kumar A, Eapen SJ, et al. Endophytic bacterial flora in root and stem tissues of black pepper (Piper nigrum L.) genotype: isolation, identification and evaluation against Phytophthora capsici. Lett Appl Microbiol. 2009;48(1):58-64.   DOI
24 Ngo VA, Wang SL, Nguyen VB, et al. Phytophthora antagonism of endophytic bacteria isolated from roots of black pepper (Piper nigrum L.). Agronomy. 2020;10(2):286.
25 Yang MM, Xu LP, Xue QY, et al. Screening potential bacterial biocontrol agents towards Phytophthora capsici in pepper. Eur J Plant Pathol. 2012;134(4):811-820.   DOI
26 Yang R, Fan X, Cai X, et al. The inhibitory mechanisms by mixtures of two endophytic bacterial strains isolated from Ginkgo biloba against pepper Phytophthora blight. Biol Control. 2015;85:59-67.   DOI
27 Kim HS, Sang MK, Jung HW, et al. Identification and characterization of Chryseobacterium wanjuense strain KJ9C8 as a biocontrol agent of phytophthora blight of pepper. Crop Prot. 2012;32:129-137.   DOI
28 Arseneault T, Goyer C, Filion M. Pseudomonas fluorescens LBUM223 increases potato yield and reduces common scab symptoms in the field. Phytopathology. 2015;105(10):1311-1317.   DOI
29 Bhusal B, Mmbaga MT. Biological control of phytophthora blight and growth promotion in sweet pepper by Bacillus species. Biol Control. 2020;150:104373.
30 Yu X, Ai C, Xin L, et al. The siderophore-producing bacterium, Bacillus subtilis CAS15, has a biocontrol effect on Fusarium wilt and promotes the growth of pepper. Eur J Soil Biol. 2011;47(2):138-145.   DOI
31 Sang MK, Shrestha A, Kim DY, et al. Biocontrol of Phytophthora blight and anthracnose in pepper by sequentially selected antagonistic rhizobacteria against Phytophthora capsici. Plant Pathol J. 2013;29(2):154-167.   DOI
32 Caulier S, Gillis A, Colau G, et al. Versatile antagonistic activities of soil-borne Bacillus spp. and Pseudomonas spp. against Phytophthora infestans and other potato pathogens. Front Microbiol. 2018;9(143):143.
33 Zhang M, Li J, Shen A, et al. Isolation and identification of Bacillus amyloliquefaciens IBFCBF-1 with potential for biological control of Phytophthora blight and growth promotion of pepper. J Phytopathol. 2016;164(11-12):1012-1021.   DOI
34 Liu CH, Chen X, Liu TT, et al. Study of the antifungal activity of Acinetobacter baumannii LCH001 in vitro and identification of its antifungal components. Appl Microbiol Biotechnol. 2007;76(2):459-466.   DOI
35 Syed-Ab-Rahman SF, Carvalhais LC, Chua ET, et al. Soil bacterial diffusible and volatile organic compounds inhibit Phytophthora capsici and promote plant growth. Sci Total Environ. 2019;692:267-280.   DOI
36 Zhao Z, Wang Q, Wang K, et al. Study of the antifungal activity of Bacillus vallismortis ZZ185 in vitro and identification of its antifungal components. Bioresour Technol. 2010;101(1):292-297.   DOI
37 Wang Q, Ma Y, Wang G, et al. Integration of biofumigation with antagonistic microorganism can control Phytophthora blight of pepper plants by regulating soil bacterial community structure. Eur J Soil Biol. 2014;61:58-67.   DOI
38 Wang Z, Wang Y, Zheng L, et al. Isolation and characterization of an antifungal protein from Bacillus licheniformis HS10. Biochem Biophys Res Commun. 2014;454(1):48-52.   DOI
39 Sid Ahmed A, Ezziyyani M, Perez Sanchez C, et al. Effect of chitin on biological control activity of Bacillus spp. and Trichoderma harzianum against root rot disease in pepper (Capsicum annuum) plants. Eur J Plant Pathol. 2003;109:633-637. Effect   DOI
40 Sopheareth M, Chan S, Naing K, et al. Biocontrol of late blight (Phytophthora capsici) disease and growth promotion of pepper by Burkholderia cepacia MPC-7. Plant Pathol J. 2013;29(1):67-76.   DOI
41 Kim YC, Jung H, Kim KY, et al. An effective biocontrol bio-formulation against Phytophthora blight of pepper using growth mixtures of combined chitinolytic bacteria under different field conditions. Eur J Plant Pathol. 2008;120(4):373-382.   DOI
42 Jeong JJ, Sang MK, Lee DW, et al. Chryseobacterium phosphatilyticum sp. nov., a phosphate-solubilizing endophyte isolated from cucumber (Cucumis sativus L.) root. Int J Syst Evol Microbiol. 2019;69(3):610-615.   DOI
43 Jeong J, Sajidah S, Oh J, et al. Complete genome sequence data of Flavobacterium anhuiense strain GSE09, a volatile-producing biocontrol bacterium isolated from cucumber (Cucumis sativus) root. Data Brief. 2019;25:104270.
44 Sheoran N, Nadakkakath A, Munjal V, et al. Genetic analysis of plant endophytic Pseudomonas putida BP25 and chemo-profiling of its antimicrobial volatile organic compounds. Microbiol Res. 2015;173:66-78.   DOI
45 Sang MK, Kim JD, Kim BS, et al. Root treatment with rhizobacteria antagonistic to Phytophthora blight affects anthracnose occurrence, ripening, and yield of pepper fruit in the plastic house and field. Phytopathology. 2011;101(6):666-678.   DOI
46 Paul D, Sarma YR. Antagonistic effects of metabolites of Pseudomonas fluorescens strains on the different growth phases of Phytophthora capsici, foot rot pathogen of black pepper (Piper nigrum L.). Arch Phytopathol Pflanzenschutz. 2006;39(2):113-118.   DOI
47 Agisha VN, Kumar A, Eapen SJ, et al. Broad-spectrum antimicrobial activity of volatile organic compounds from endophytic Pseudomonas putida BP25 against diverse plant pathogens. Biocontrol Sci Technol. 2019;29(11):1069-1089.   DOI
48 Thampi A, Bhai RS. Rhizosphere actinobacteria for combating Phytophthora capsici and Sclerotium rolfsii, the major soil borne pathogens of black pepper (Piper nigrum L.). Biol Control. 2017;109:1-13.   DOI
49 Tomah AA, Alamer IAS, Li B, et al. A new species of Trichoderma and gliotoxin role: a new observation in enhancing biocontrol potential of T. virens against Phytophthora capsici on chili pepper. Biol Control. 2020;145:104261.
50 Ezziyyani MM, Requena ME, Egea-Gilabert C, et al. Biological control of Phytophthora root rot of pepper using Trichoderma harzianum and Streptomyces rochei in combination. J Phytopathol. 2007;155(6):342-349.   DOI
51 Li H, Cai X, Gong J, et al. Long-term organic farming manipulated rhizospheric microbiome and Bacillus antagonism against pepper blight. (Phytophthora capsici) Front Microbiol. 2019;10(342):342.
52 Lim JH, Kim SD. Induction of drought stress resistance by multi-functional PGPR Bacillus licheniformis K11 in pepper. Plant Pathol J. 2013;29(2):201-208.   DOI
53 Glick BR, Li J, Shah S, et al. ACC deaminase is central to the functioning of plant growth promoting rhizobacteria. In Biology and biotechnology of the plant hormone ethylene II. Dordrecht: Springer; 1999. p. 293-298.
54 Lee KJ, Kamala-Kannan S, Sub HS, et al. Biological control of Phytophthora blight in red pepper (Capsicum annuum L.) using Bacillus subtilis. World J Microbiol Biotechnol. 2008;24(7):1139-1145.   DOI
55 Lim JH, Kim SD. Biocontrol of phytophthora blight of red pepper caused by Phytophthora capsici using Bacillus subtilis AH18 and B. licheniformis K11 formulations. JKSABC. 2010;53(6):766-773.   DOI
56 Arrebola E, Jacobs R, Korsten L. Iturin a is the principal inhibitor in the biocontrol activity of Bacillus amyloliquefaciens PPCB004 against postharvest fungal pathogens. J Appl Microbiol. 2010;108(2):386-395.   DOI
57 Ben Abdallah D, Frikha-Gargouri O, Tounsi S. Bacillus amyloliquefaciens strain 32a as a source of lipopeptides for biocontrol of Agrobacterium tumefaciens strains. J Appl Microbiol. 2015;119(1):196-207.   DOI
58 Shan H, Zhao M, Chen D, et al. Biocontrol of rice blast by the phenaminomethylacetic acid producer of Bacillus methylotrophicus strain BC79. Crop Prot. 2013;44:29-37.   DOI
59 Chae DH, De Jin R, Hwangbo H, et al. Control of late blight (Phytophthora capsici) in pepper plant with a compost containing multitude of chitinase-producing bacteria. BioControl. 2006;51(3):339-351.   DOI
60 Passari AK, Mishra VK, Gupta VK, et al. In vitro and in vivo plant growth promoting activities and DNA fingerprinting of antagonistic endophytic actinomycetes associates with medicinal plants. PLoS One. 2015;10(9):e0139468.
61 la Spada F, Stracquadanio C, Riolo M, et al. Trichoderma counteracts the challenge of Phytophthora nicotianae infections on tomato by modulating plant defense mechanisms and the expression of crinkler, necrosis-inducing phy-ophthora protein 1, and cellulose-binding elicitor lectin pathogenic effectors. Front Plant Sci. 2020;11:583539.
62 Qin S, Miao Q, Feng W, et al. Biodiversity and plant growth promoting traits of culturable endophytic actinobacteria associated with Jatropha curcas L. growing in Panxi dry-hot valley soil. Appl Soil Ecol. 2015;93:47-55.   DOI
63 Hwang J, Chilton W, Benson DM. Pyrrolnitrin production by Burkholderia cepacia and biocontrol of rhizoctonia stem rot of poinsettia. Biol Control. 2002;25(1):56-63.
64 Szczech M, Shoda M. Biocontrol of rhizoctonia damping-off of tomato by Bacillus subtilis combined with Burkholderia cepacia. J Phytopathol. 2004;152(10):549-556.   DOI
65 Zhang X, Gao Z, Zhang X, et al. Control effects of Bacillus siamensis G-3 volatile compounds on raspberry postharvest diseases caused by Botrytis cinerea and Rhizopus stolonifer. Biol Control. 2020;141:104135.
66 Adams TB, Doull J, Feron VJ, et al. The FEMA GRAS assessment of pyrazine derivatives used as flavor ingredients. Food Chem Toxicol. 2002;40(4):429-451.   DOI
67 Sharifi R, Ryu CM. Are bacterial volatile compounds poisonous odors to a fungal pathogen Botrytis cinerea, alarm signals to Arabidopsis seedlings for eliciting induced resistance, or both? Front Microbiol. 2016;7:196.
68 Kim YJ, Hwang BK. Pepper gene encoding a basic pathogenesis-related 1 protein is pathogen and ethylene inducible. Physiol Plant. 2000;108:51-60.   DOI
69 Park CJ, Shin R, Park JM, et al. A hot pepper cDNA encoding a pathogenesis-related protein 4 is induced during the resistance response to tobacco mosaic virus. Mol Cells. 2001;11:122-127.
70 Ojaghian MR, Jiang H, Xie G-L, et al. In vitro biofumigation of Brassica tissues against potato stem rot caused by Sclerotinia sclerotiorum. Plant Pathol J. 2012;28(2):185-190.
71 Brown PD. Control of soil-borne plant pests using glucosinolate-containing plants. Adv Agron. 1997;61:168-231.
72 de Vrieze M, Gloor R, Codina JM, et al. Biocontrol activity of three Pseudomonas in a newly assembled collection of Phytophthora infestans isolates. Phytopathology. 2019;109(9):1555-1565.   DOI
73 de Vrieze M, Pandey P, Bucheli TD, et al. Volatile organic compounds from native potato-associated Pseudomonas as potential anti-oomycete agents. Front Microbiol. 2015;6:1295.
74 Guyer A, de Vrieze M, Bonisch D, et al. The anti-Phytophthora effect of selected potato-associated Pseudomonas strains: from the laboratory to the field. Front Microbiol. 2015;6:1309.
75 Hunziker L, Bonisch D, Groenhagen U, et al. Pseudomonas strains naturally associated with potato plants produce volatiles with high potential for inhibition of Phytophthora infestans. Appl Environ Microbiol. 2015;81(3):821-830.
76 Morrison CK, Arseneault T, Novinscak A, et al. Phenazine-1-carboxylic acid production by Pseudomonas fluorescens LBUM636 alters Phytophthora infestans growth and late blight development. Phytopathology. 2017;107(3):273-279.   DOI
77 Hultberg M, Bengtsson T, Liljeroth E. Late blight on potato is suppressed by the biosurfactant-producing strain Pseudomonas koreensis 2.74 and its biosurfactant. BioControl. 2010;55(4):543-550.   DOI
78 Linkies A, Jacob S, Zink P, et al. Characterization of cultural traits and fungicidal activity of strains belonging to the fungal genus Chaetomium. J Appl Microbiol. 2021;131(1):375-391.   DOI
79 Shanthiyaa V, Saravanakumar D, Rajendran L, et al. Use of Chaetomium globosum for biocontrol of potato late blight disease. Crop Prot. 2013;52:33-38.   DOI
80 Park JH, Choi GJ, Jang KS, et al. Antifungal activity against plant pathogenic fungi of chaetoviridins isolated from Chaetomium globosum. FEMS Microbiol Lett. 2005;252(2):309-313.   DOI
81 Alaux PL, Cesar V, Naveau F, et al. Impact of Rhizophagus irregularis MUCL 41833 on disease symptoms caused by Phytophthora infestans in potato grown under field conditions. Crop Prot. 2018;107:26-33.   DOI
82 Di Francesco A, Milella F, Mari M, et al. A preliminary investigation into Aureobasidium pullulans as a potential biocontrol agent against Phytophthora infestans of tomato. Biol Control. 2017;114:144-149.   DOI
83 Hadwiger LA, McDonel H, Glawe D. Wild yeast strains as prospective candidates to induce resistance against potato late blight (Phytophthora infestans). Am J Potato Res. 2015;92(3):379-386.   DOI
84 Gachango E, Kirk W, Schafer R, et al. Evaluation and comparison of biocontrol and conventional fungicides for control of postharvest potato tuber diseases. Biol Control. 2012;63(2):115-120.   DOI
85 Stephan D, Schmitt A, Martins Carvalho S, et al. Evaluation of biocontrol preparations and plant extracts for the control of Phytophthora infestans on potato leaves. Eur J Plant Pathol. 2005;112(3):235-246.   DOI
86 Driscoll JA, Brody SL, Kollef MH. The epidemiology, pathogenesis and treatment of Pseudomonas aeruginosa infections. Drugs. 2007;67(3):351-368.   DOI
87 Afek U, Rinaldelli E, Menge JA, et al. Mycorrhizal species, root age, and position of mycorrhizal inoculum influence colonization of cotton, onion, and pepper seedlings. JASHS. 1990;115(6):938-942.   DOI
88 Zhang C, Gao J, Han T, et al. Integrated control of tobacco black shank by combined use of riboflavin and Bacillus subtilis strain Tpb55. BioControl. 2017;62(6):835-845.   DOI
89 Soytong K, Kanokmedhakul S, Kukongviriyapa V, et al. Application of Chaetomium species (Ketomium) as a new broad spectrum biological fungicide for plant disease control. Fungal Divers. 2001;7:1-15.
90 Rajkumar M, Lee WH, Lee KJ. Screening of bacterial antagonists for biological control of Phytophthora blight of pepper. J Basic Microbiol. 2005;45(1):55-63.   DOI
91 Wu L, Huang Z, Li X, et al. Stomatal closure and SA-, JA/ET-signaling pathways are essential for Bacillus amyloliquefaciens FZB42 to restrict leaf disease caused by Phytophthora nicotianae in Nicotiana benthamiana. Front Microbiol. 2018;9(847):847.
92 Ding H, Mo W, Yu S, et al. Whole genome sequence of Bacillus velezensis strain GUMT319: a potential biocontrol agent against tobacco black shank disease. Front Microbiol. 2021;12(1607):658113.
93 Guo D, Yuan C, Luo Y, et al. Biocontrol of tobacco black shank disease (Phytophthora nicotianae) by Bacillus velezensis Ba168. Pestic Biochem Physiol. 2020;165:104523.
94 Ren X, Zhang N, Cao M, et al. Biological control of tobacco black shank and colonization of tobacco roots by a Paenibacillus polymyxa strain C5. Biol Fertil Soils. 2012;48(6):613-620.   DOI
95 Ma L, Zheng SC, Zhang TK, et al. Effect of nicotine from tobacco root exudates on chemotaxis, growth, biocontrol efficiency, and colonization by Pseudomonas aeruginosa NXHG29. Antonie Van Leeuwenhoek. 2018;111(7):1237-1257.   DOI
96 Cordier C, Pozo MJ, Barea JM, et al. Cell defense responses associated with localized and systemic resistance to Phytophthora parasitica induced in tomato by an arbuscular mycorrhizal fungus. MPMI. 1998;11(10):1017-1028.   DOI
97 Shishido M, Breuil C, Chanway CP. Endophytic colonization of spruce by plant growth-promoting rhizobacteria. FEMS Microbiol Ecol. 1999;29(2):191-196.   DOI
98 Pozo M, Cordier C, Dumas-Gaudot E, et al. Localized versus systemic effect of arbuscular mycorrhizal fungi on defence responses to Phytophthora infection in tomato plants. J Exp Bot. 2002;53(368):525-534.
99 Vigo C, Norman JR, Hooker JE. Biocontrol of the pathogen Phytophthora parasitica by arbuscular mycorrhizal fungi is a consequence of effects on infection loci. Plant Pathol. 2000;49(4):509-514.   DOI
100 Garbeva P, Overbeek LS, Vuurde JWL, et al. Analysis of endophytic bacterial communities of potato by plating and denaturing gradient gel electrophoresis (DGGE) of 16S rDNA based PCR fragments. Microb Ecol. 2001;41(4):369-383.   DOI
101 Broeckling CD, Broz AK, Bergelson J, et al. Root exudates regulate soil fungal community composition and diversity. Appl Environ Microbiol. 2008;74(3):738-744.   DOI
102 Ros M, Raut I, Santisima-Trinidad AB, et al. Relationship of microbial communities and suppressiveness of Trichoderma fortified composts for pepper seedlings infected by Phytophthora nicotianae. PLoS One. 2017;12(3):e0174069.
103 Li XG, Zhang TL, Wang XX, et al. The composition of root exudates from two different resistant peanut cultivars and their effects on the growth of soil-borne pathogen. Int J Biol Sci. 2013;9(2):164-173.   DOI
104 Norman J, Hooker JE. Sporulation of Phytophthora fragariae shows greater stimulation by exudates of non-mycorrhizal than by mycorrhizal strawberry roots. Mycol Res. 2000;104(9):1069-1073.   DOI
105 Steinkellner S, Mammerler R, Vierheilig H. Microconidia germination of the tomato pathogen Fusarium oxysporum in the presence of root exudates. J Plant Interact. 2005;1(1):23-30.   DOI
106 Daura-Pich O, Hernandez I, Pinyol-Escala L, et al. No antibiotic and toxic metabolites produced by the biocontrol agent Pseudomonas putida strain B2017. FEMS Microbiol Lett. 2020;367:fnaa075.
107 Nishad R, Ahmed T, Rahman VJ, et al. Modulation of plant defense system in response to microbial interactions. Front Microbiol. 2020;11(1298):1298.
108 You C, Zhang C, Kong F, et al. Comparison of the effects of biocontrol agent Bacillus subtilis and fungicide metalaxyl-mancozeb on bacterial communities in tobacco rhizospheric soil. Ecol Eng. 2016;91:119-125.
109 Fiers M, Edel-Hermann V, Chatot C, et al. Potato soil-borne diseases. A review. Agron Sustain Dev. 2012;32(1):93-132.   DOI
110 Griffin K, Gambley C, Brown P, et al. Copper-tolerance in Pseudomonas syringae pv. tomato and Xanthomonas spp. and the control of diseases associated with these pathogens in tomato and pepper. Crop Prot. 2017;96:144-150.   DOI
111 Panno S, Davino S, Caruso A, et al. A review of the most common and economically important diseases that undermine the cultivation of tomato crop in the Mediterranean basin. Agronomy. 2021;11(11):2188.
112 Thines M. Oomycetes. Curr Biol. 2018;28(15):R812-R813.   DOI
113 Latijnhouwers M, de Wit PJ, Govers F. Oomycetes and fungi: similar weaponry to attack plants. Trends Microbiol. 2003;11:462-469.   DOI
114 Judelson HS, Blanco FA. The spores of Phytophthora: weapons of the plant destroyer. Nat Rev Microbiol. 2005;3(1):47-58.   DOI
115 Rossman AY, Palm ME. Why are Phytophthora and other oomycota not true fungi? Outlook Pest Man. 2006;17(5):217-219.   DOI
116 Taxvig C, Hass U, Axelstad M, et al. Endocrine-disrupting activities in vivo of the fungicides tebuconazole and epoxiconazole. Toxicol Sci. 2007;100(2):464-473.   DOI
117 Thind TS, Hollomon DW. Thiocarbamate fungicides: reliable tools in resistance management and future outlook. Pest Manag Sci. 2018;74(7):1547-1551.   DOI
118 Zubrod JP, Bundschuh M, Feckler A, et al. Ecotoxicological impact of the fungicide tebuconazole on an aquatic decomposer-detritivore system. Environ Toxicol Chem. 2011;30(12):2718-2724.   DOI
119 Singh M, Mersie W, Brlansky RH. Phytotoxicity of the fungicide metalaxyl and its optical isomers. Plant Dis. 2003;87(9):1144-1147.   DOI
120 Lamour KH, Hausbeck MK. Mefenoxam insensitivity and the sexual stage of Phytophthora capsici in Michigan cucurbit fields. Phytopathology. 2000;90(4):396-400.   DOI
121 Lamour KH, Hausbeck MK. The dynamics of mefenoxam insensitivity in a recombining population of Phytophthora capsici characterized with amplified fragment length polymorphism markers. Phytopathology. 2001;91(6):553-557.   DOI
122 Chemeltorit PP, Mutaqin KH, Widodo W. Combining Trichoderma hamatum THSW13 and Pseudomonas aeruginosa BJ10-86: a synergistic chili pepper seed treatment for Phytophthora capsici infested soil. Eur J Plant Pathol. 2017;147(1):157-166.   DOI
123 Hu H, Li XS, He H. Characterization of an antimicrobial material from a newly isolated Bacillus amyloliquefaciens from mangrove for biocontrol of Capsicum bacterial wilt. Biol Control. 2010;54(3):359-365.   DOI
124 Chen Y-Y, Chen P-C, Tsay T-T. Biocontrol efficacy and antibiotic activity of Streptomyces plicatus on the oomycete Phytophthora capsici. Biol Control. 2016;98:34-42.
125 Khabbaz SE, Zhang L, Caceres LA, et al. Characterisation of antagonistic Bacillus and Pseudomonas strains for biocontrol potential and suppression of damping-off and root rot diseases. Ann Appl Biol. 2015;166(3):456-471.   DOI
126 Segarra G, Aviles M, Casanova E, et al. Effectiveness of biological control of Phytophthora capsici in pepper by Trichoderma asperellum strain T34. Phytopathology. 2013;52:77-83.
127 Li Y, Feng X, Wang X, et al. Inhibitory effects of Bacillus licheniformis BL06 on Phytophthora capsici in pepper by multiple modes of action. Biol Control. 2020;144:104210.
128 Lim S, Yoon M, Choi G, et al. Diffusible and volatile antifungal compounds produced by an antagonistic Bacillus velezensis G341 against various phytopathogenic fungi. Plant Pathol J. 2017;33(5):488-498.   DOI
129 Munjal V, Nadakkakath AV, Sheoran N, et al. Genotyping and identification of broad spectrum antimicrobial volatiles in black pepper root endophytic biocontrol agent, Bacillus megaterium BP17. Biol Control. 2016;92:66-76.   DOI
130 Sang MK, Kim KD. The volatile-producing Flavobacterium johnsoniae strain GSE09 shows biocontrol activity against Phytophthora capsici in pepper. J Appl Microbiol. 2012;113(2):383-398.   DOI
131 Sang MK, Kim KD. Biocontrol activity and root colonization by Pseudomonas corrugata strains CCR04 and CCR80 against Phytophthora blight of pepper. BioControl. 2014;59(4):437-448.   DOI