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Improving performance of microbial biocontrol agents against plant diseases

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Abstract

Reducing dependence on chemical pesticides is considered as an essential challenge for sustainable crop production. The use of microbial biocontrol agents (MBCAs) is a key component of sustainable pest management. Numerous antagonistic microorganisms are known to suppress plant diseases, but their practical application and commercialization are still limited in part due to poor reliability of their efficacy in the field. Although promising MBCAs achieve remarkable disease control in the laboratory or greenhouse, field control is often unsatisfactory. Thus, for MBCAs to be integrated into crop production, their field performance must be improved to provide the cost-effectiveness and efficacy required by growers. In this review, we highlight recent approaches to enhance the field performance of MBCAs.

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References

  • Ab Rahman SFS, Singh E, Pieterse CMJ, Schenk PM (2018) Emerging microbial biocontrol strategies for plant pathogens. Plant Sci 267:102–111

    Article  CAS  Google Scholar 

  • Aeron A, Dubey RC, Maheshwari DK, Pandey P, Bajpai VK, Kang SC (2011) Multifarious activity of bioformulated Pseudomonas fluorescens PS1 and biocontrol of Sclerotinia sclerotiorum in Indian rapeseed (Brassica campestris L.). Eur J Plant Pathol 131:81–93

    Article  Google Scholar 

  • Angeli D, Saharan K, Segarra G, Sicher C, Pertot I (2017) Production of Ampelomyces quisqualis conidia in submerged fermentation and improvements in the formulation for increased shelf-life. Crop Prot 97:135–144

    Article  CAS  Google Scholar 

  • Anonymous (2005) The shipments of agricultural chemicals. In: Association Japan Plant Protection (ed) Agricultural chemicals handbook (in Japanese). Japan Plant Protection Association, Tokyo, pp 3–83

  • Anonymous (2017) The shipments of agricultural chemicals. In: Association Japan Plant Protection (ed) Agricultural chemicals handbook (in Japanese). Japan Plant Protection Association, Tokyo, pp 3–89

  • Barahona E, Navazo A, Martínez-Granero F, Zea-Bonilla T, Pérez-Jiménez RM, Martín M, Rivilla R (2011) Pseudomonas fluorescens F113 mutant with enhanced competitive colonization ability and improved biocontrol activity against fungal root pathogens. Appl Environ Microbiol 77:5412–5419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bardin M, Ajouz S, Comby M, Lopez-Ferber M, Graillot B, Siegwart M, Nicot PC (2015) Is the efficacy of biological control against plant diseases likely to be more durable than that of chemical pesticides? Front Plant Sci 6:566

    Article  PubMed  PubMed Central  Google Scholar 

  • Bashan N (2016) Inoculant formulations are essential for successful inoculation with plant growth-promoting bacteria and business opportunities. Indian Phytopathol 69:739–743

    Google Scholar 

  • Bejarano A, Sauer U, Preininger C (2017) Design and development of a workflow for microbial spray formulations including decision criteria. Appl Microbiol Biotechnol 101:7335–7346

    Article  CAS  PubMed  Google Scholar 

  • Berninger T, González López Ó, Bejarano A, Preininger C, Sessitsch A (2018) Maintenance and assessment of cell viability in formulation of non-sporulating bacterial inoculants. Microb Biotechnol 11:277–301

    Article  CAS  PubMed  Google Scholar 

  • Bilal M, Guo S, Iqbal HMN, Hu H, Wang W, Zhang X (2017) Engineering Pseudomonas for phenazine biosynthesis, regulation, and biotechnological applications: a review. World J Microbiol Biotechnol 33:191

    Article  CAS  PubMed  Google Scholar 

  • Bonanomi G, Lorito M, Vinale F, Woo SL (2018) Organic amendments, beneficial microbes, and soil microbiota: toward a unified framework for disease suppression. Annu Rev Phytopathol 56:1–20

    Article  CAS  PubMed  Google Scholar 

  • Bonaterra A, Badosa E, Cabrefiga J, Francés J, Montesinos E (2012) Prospects and limitations of microbial pesticides for control of bacterial and fungal pomefruit tree diseases. Trees 26:215–226

    Article  CAS  PubMed  Google Scholar 

  • Cabrefiga J, Francés J, Montesinos E, Bonaterra A (2011) Improvement of fitness and efficacy of a fire blight biocontrol agent via nutritional enhancement combined with osmoadaptation. Appl Environ Microbiol 77:3174–3181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cañamás TP, Viñas I, Abadias M, Usall J, Torres R, Teixidó N (2009) Acid tolerance response induced in the biocontrol agent Pantoea agglomerans CPA-2 and effect on its survival ability in acidic environments. Microbiol Res 164:438–450

    Article  CAS  PubMed  Google Scholar 

  • Carbó A, Torres R, Usall J, Fons E, Teixidó N (2017) Dry formulations of the biocontrol agent Candida sake CPA-1 using fluidised bed drying to control the main postharvest diseases on fruits. J Sci Food Agric 97:3691–3698

    Article  CAS  PubMed  Google Scholar 

  • Chemeltorit PP, Mutaqin KH, Widodo W (2017) Combining Trichoderma hamatum THSW13 and Pseudomonas aeruginosa BJ10–86: a synergistic chili pepper seed treatment for Phytophthora capsici infested soil. Eur J Plant Pathol 147:157–166

    Article  Google Scholar 

  • Cheng Z, Chi M, Li G, Chen H, Sui Y, Sun H, Wisniewski M, Liu Y, Liu J (2016) Heat shock improves stress tolerance and biocontrol performance of Rhodotorula mucilaginosa. Biol Control 95:49–56

    Article  CAS  Google Scholar 

  • Crozier J, Arroyo C, Morales H, Melnick RL, Strem MD, Vinyard BT, Bailey BA (2015) The influence of formulation on Trichoderma biological activity and frosty pod rot management in Theobroma cacao. Plant Pathol 64:1385–1395

    Article  CAS  Google Scholar 

  • Daranas N, Badosa E, Francés J, Montesinos E, Bonaterra A (2018) Enhancing water stress tolerance improves fitness in biological control strains of Lactobacillus plantarum in plant environments. PLoS ONE 13:e0190931

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Jaeger N, de la Providencia IE, Rouhier H, Declerck S (2011) Co-entrapment of Trichoderma harzianum and Glomus sp. within alginate beads: impact on the arbuscular mycorrhizal fungi life cycle. J Appl Microbiol 111:125–135

    Article  PubMed  Google Scholar 

  • Ding C, Shen Q, Zhang R, Chen W (2013) Evaluation of rhizosphere bacteria and derived bio-organic fertilizers as potential biocontrol agents against bacterial wilt (Ralstonia solanacearum) of potato. Plant Soil 366:453–466

    Article  CAS  Google Scholar 

  • Droby S, Wisniewski M, Teixidó N, Spadaro D, Jijakli MH (2016) The science, development, and commercialization of postharvest biocontrol products. Postharvest Biol Technol 122:22–29

    Article  Google Scholar 

  • Ehlers RU (ed) (2011) Regulation of biological control agents. Springer, Berlin

    Google Scholar 

  • European Commission (2019) EU pesticides database. European Commission, Brussels, Belgium. https://www.ec.europa.eu/food/plant/pesticides/eu-pesticidesdatabase/public/?event=homepage&language=EN. Acceessed 10 Mar 2019

  • Fravel DR (2005) Commercialization and implementation of biocontrol. Annu Rev Phytopathol 43:337–359

    Article  CAS  PubMed  Google Scholar 

  • Gava CAT, Pinto JM (2016) Biocontrol of melon wilt caused by Fusarium oxysporum Schlect f. sp. melonis using seed treatment with Trichoderma spp. and liquid compost. Biol Control 97:13–20

    Article  Google Scholar 

  • Glare T, Caradus J, Gelernter W, Jackson T, Keyhani N, Köhl J, Marrone P, Morin L, Stewart A (2012) Have biopesticides come of age? Trends Biotechnol 30:250–258

    Article  CAS  PubMed  Google Scholar 

  • Gotor-Vila A, Usall J, Torres R, Abadias M, Teixidó N (2017a) Formulation of the biocontrol agent Bacillus amyloliquefaciens CPA-8 using different approaches: liquid, freeze-drying and fluid-bed spray-drying. Biocontrol 62:545–555

    Article  CAS  Google Scholar 

  • Gotor-Vila A, Usall J, Torres R, Solsona C, Teixidó N (2017b) Biocontrol products based on Bacillus amyloliquefaciens CPA-8 using fluid-bed spray-drying process to control postharvest brown rot in stone fruit. LWT Food Sci Technol 82:274–282

    Article  CAS  Google Scholar 

  • Gramisci BR, Lutz MC, Lopes CA, Sangorrín MP (2018) Enhancing the efficacy of yeast biocontrol agents against postharvest pathogens through nutrient profiling and the use of other additives. Biol Control 121:151–158

    Article  Google Scholar 

  • Grosch R, Dealtry S, Schreiter S, Berg G, Mendonça-Hagler L, Smalla K (2012) Biocontrol of Rhizoctonia solani: complex interaction of biocontrol strains, pathogen and indigenous microbial community in the rhizosphere of lettuce shown by molecular methods. Plant Soil 361:343–357

    Article  CAS  Google Scholar 

  • Huang X, Chen L, Ran W, Shen Q, Yang X (2011) Trichoderma harzianum strain SQR-T37 and its bio-organic fertilizer could control Rhizoctonia solani damping-off disease in cucumber seedlings mainly by the mycoparasitism. Appl Microbiol Biotechnol 91:741–755

    Article  CAS  PubMed  Google Scholar 

  • Huang X, Zhang N, Yong X, Yang X, Shen Q (2012) Biocontrol of Rhizoctonia solani damping-off disease in cucumber with Bacillus pumilus SQR-N43. Microbiol Res 167:135–143

    Article  CAS  PubMed  Google Scholar 

  • Hyakumachi M, Takahashi H, Matsubara Y, Someya N, Shimizu M, Kobayashi K, Nishiguchi M (2014) Recent studies on biological control of plant diseases in Japan. J Gen Plant Pathol 80:287–302

    Article  Google Scholar 

  • Jambhulkar PP, Sharma P, Manokaran R, Lakshman DK, Rokadia P, Jambhulkar N (2018) Assessing synergism of combined applications of Trichoderma harzianum and Pseudomonas fluorescens to control blast and bacterial leaf blight of rice. Eur J Plant Pathol 152:747–757

    Article  Google Scholar 

  • Jing X, Cui Q, Li X, Yin J, Ravichandran V, Pan D, Fu J, Tu Q, Wang H, Bian X, Zhang Y (2018) Engineering Pseudomonas protegens Pf‐5 to improve its antifungal activity and nitrogen fixation. Microb Biotechnol. https://doi.org/10.1111/1751-7915.13335

    Article  PubMed  Google Scholar 

  • John RP, Tyagi RD, Brar SK, Surampalli RY, Prévost D (2011) Bio-encapsulation of microbial cells for targeted agricultural delivery. Crit Rev Biotechnol 31:211–226

    Article  CAS  PubMed  Google Scholar 

  • Kang BR (2011) Mannitol amendment as a carbon source in a bean-based formulation enhances biocontrol efficacy of a 2,4-diacetylphloroglucinol-producing Pseudomonas sp. nj134 against tomato Fusarium wilt. Plant Pathol J 27:390–395

    Article  CAS  Google Scholar 

  • Kavino M, Manoranjitham SK (2018) In vitro bacterization of banana (Musa spp.) with native endophytic and rhizospheric bacterial isolates: novel ways to combat Fusarium wilt. Eur J Plant Pathol 151:371–387

    Article  CAS  Google Scholar 

  • Kim YS, Jang BR, Chung IM, Sang MK, Ku HM, Kim KD, Chun SC (2008) Enhancement of biocontrol activity of antagonistic Chryseobacterium strain KJ1R5 by adding carbon sources against Phytophthora capsici. Plant Pathol J 24:164–170

    Article  CAS  Google Scholar 

  • Kim IY, Pusey PL, Zhao Y, Korban SS, Choi H, Kim KK (2012) Controlled release of Pantoea agglomerans E325 for biocontrol of fire blight disease of apple. J Control Release 161:109–115

    Article  CAS  PubMed  Google Scholar 

  • Kowsari M, Zamani MR, Motallebi M (2014) Enhancement of Trichoderma harzianum activity against Sclerotinia sclerotiorum by overexpression of Chit42. Iran J Biotechnol 12:26–31

    Article  Google Scholar 

  • Kwak MJ, Kong HG, Choi K, Kwon SK, Song JY, Lee J, Lee PA, Choi SY, Seo M, Lee HJ, Jung EJ (2018) Rhizosphere microbiome structure alters to enable wilt resistance in tomato. Nat Biotechnol 36:1100–1109

    Article  CAS  Google Scholar 

  • Li BQ, Tian SP (2006) Effects of trehalose on stress tolerance and biocontrol efficacy of Cryptococcus laurentii. J Appl Microbiol 100:854–861

    Article  CAS  PubMed  Google Scholar 

  • Li J, Liu W, Luo L, Dong D, Liu T, Zhang T, Lu C, Liu D, Zhang D, Wu H (2015) Expression of Paenibacillus polymyxa β-1,3-1,4-glucanase in Streptomyces lydicus A01 improves its biocontrol effect against Botrytis cinerea. Biol Control 90:141–147

    Article  CAS  Google Scholar 

  • Li M, Tshabalala MA, Buschle-Diller G (2016) Formulation and characterization of polysaccharide beads for controlled release of plant growth regulators. J Mater Sci 51:4609–4617

    Article  CAS  Google Scholar 

  • Liffourrena AS, Lucchesi GI (2018) Alginate-perlite encapsulated Pseudomonas putida A (ATCC 12633) cells: Preparation, characterization and potential use as plant inoculants. J Biotechnol 278:28–33

    Article  CAS  PubMed  Google Scholar 

  • Ling N, Zhang W, Tan S, Huang Q, Shen Q (2012) Effect of the nursery application of bioorganic fertilizer on spatial distribution of Fusarium oxysporum f. sp. niveum and its antagonistic bacterium in the rhizosphere of watermelon. Appl Soil Ecol 59:13–19

    Article  Google Scholar 

  • Liu J, Wisniewski M, Droby S, Norelli J, Hershkovitz V, Tian S, Farrell R (2012) Increase in antioxidant gene transcripts, stress tolerance and biocontrol efficacy of Candida oleophila following sublethal oxidative stress exposure. FEMS Microbiol Ecol 80:578–590

    Article  CAS  PubMed  Google Scholar 

  • Liu K, Hu H, Wang W, Zhang X (2016) Genetic engineering of Pseudomonas chlororaphis GP72 for the enhanced production of 2-hydroxyphenazine. Microb cell Fact 15:131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Locatelli GO, dos Santos GF, Botelho PS, Finkler CLL, Bueno LA (2018) Development of Trichoderma sp. formulations in encapsulated granules (CG) and evaluation of conidia shelf-life. Biol Control 117:21–29

    Article  CAS  Google Scholar 

  • Loján P, Demortier M, Velivelli SLS, Pfeiffer S, Suárez JP, De Vos P, Prestwich BD, Sessitsch A, Declerck S (2017) Impact of plant growth-promoting rhizobacteria on root colonization potential and life cycle of Rhizophagus irregularis following co-entrapment into alginate beads. J Appl Microbiol 122:429–440

    Article  CAS  PubMed  Google Scholar 

  • Ma X, Wang X, Cheng J, Nie X, Yu X, Zhao Y, Wang W (2015) Microencapsulation of Bacillus subtilis B99–2 and its biocontrol efficiency against Rhizoctonia solani in tomato. Biol Control 90:34–41

    Article  Google Scholar 

  • Ma L, Zheng SC, Zhang TK, Liu ZY, Wang XJ, Zhou XK, Yang CG, Duo JL, Mo MH (2018a) Effect of nicotine from tobacco root exudates on chemotaxis, growth, biocontrol efficiency, and colonization by Pseudomonas aeruginosa NXHG29. Antonie Van Leeuwenhoek 111:1237–1257

    Article  CAS  PubMed  Google Scholar 

  • Ma L, Zhang HY, Zhou XK, Yang CG, Zheng SC, Duo JL, Mo MH (2018b) Biological control tobacco bacterial wilt and black shank and root colonization by bio-organic fertilizer containing bacterium Pseudomonas aeruginosa NXHG29. Appl Soil Ecol 129:136–144

    Article  Google Scholar 

  • Maheshwari DK (ed) (2013) Bacteria in agrobiology: disease management. Springer, Berlin

    Google Scholar 

  • Manjukarunambika K, Ponmurugan P, Marimuthu S (2013) Efficacy of various fungicides and indigenous biocontrol agents against red root rot disease of tea plants. Eur J Plant Pathol 137:67–78

    Article  CAS  Google Scholar 

  • Marian M, Morita A, Koyama H, Suga H, Shimizu M (2019) Enhanced biocontrol of tomato bacterial wilt using the combined application of Mitsuaria sp. TWR114 and nonpathogenic Ralstonia sp. TCR112. J Gen Plant Pathol 85:142–154

    Article  Google Scholar 

  • Massart S, Martinez-Medina M, Jijakli MH (2015) Biological control in the microbiome era: challenges and opportunities. Biol Control 89:98–108

    Article  Google Scholar 

  • Melin P, Schnürer J, Håkansson S (2011) Formulation and stabilisation of the biocontrol yeast Pichia anomala. Antonie Van Leeuwenhoek 99:107–112

    Article  CAS  PubMed  Google Scholar 

  • Meng X, Yu J, Yu M, Yin X, Liu Y (2015) Dry flowable formulations of antagonistic Bacillus subtilis strain T429 by spray drying to control rice blast disease. Biol Control 85:46–51

    Article  CAS  Google Scholar 

  • Messing R, Brodeur J (2018) Current challenges to the implementation of classical biological control. Biocontrol 63:1–9

    Article  CAS  Google Scholar 

  • Narayanasamy P (ed) (2013) Biological management of diseases of crops. Springer, Dordrecht

    Google Scholar 

  • Nicot P (ed) (2011) Classical and augmentative biological control against diseases and pests: critical status analysis and review of factors influencing their success. International Organisation for Biological and Integrated Control of Noxious Animals and Plants, West Palaearctic Regional Section (IOBC-WPRS), Wageningen

    Google Scholar 

  • Nocker A, Fernández PS, Montijn R, Schuren F (2012) Effect of air drying on bacterial viability: a multiparameter viability assessment. J Microbiol Methods 90:86–95

    Article  CAS  PubMed  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

    Article  PubMed  PubMed Central  Google Scholar 

  • Pelaez V, Mizukawa G (2017) Diversification strategies in the pesticide industry: from seeds to biopesticides. Ciênc Rural. https://doi.org/10.1590/0103-8478cr20160007

    Article  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 3.1T8 and chitosan. Biol Control 48:301–309

    Article  Google Scholar 

  • Potts M (1994) Desiccation tolerance of prokaryotes. Microbiol Rev 58:755–805

    CAS  PubMed  PubMed Central  Google Scholar 

  • Puopolo G, Palmieri MC, Giovannini O, Pertot I (2015) Impact of temperature on the survival and the biocontrol efficacy of Lysobacter capsici AZ78 against Phytophthora infestans. Biocontrol 60:681–689

    Article  Google Scholar 

  • Pusey PL, Wend C (2012) Potential of osmoadaptation for improving Pantoea agglomerans E325 as biocontrol agent for fire blight of apple and pear. Biol Control 62:29–37

    Article  Google Scholar 

  • Rao MS, Kamalnath M, Umamaheswari R, Rajinikanth R, Prabu P, Priti K, Grace GN, Chaya MK, Gopalakrishnan C (2017) Bacillus subtilis IIHR BS-2 enriched vermicompost controls root knot nematode and soft rot disease complex in carrot. Sci Hortic 218:56–62

    Article  Google Scholar 

  • Ren X, Zhang N, Cao M, Wu K, Shen Q, Huang Q (2012) Biological control of tobacco black shank and colonization of tobacco roots by a Paenibacillus polymyxa strain C5. Biol Fertil Soils 48:613–620

    Article  Google Scholar 

  • Sartori M, Nesci A, Etcheverry M (2010) Impact of osmotic/matric stress and heat shock on environmental tolerance induction of bacterial biocontrol agents against Fusarium verticillioides. Res Microbiol 161:681–686

    Article  PubMed  Google Scholar 

  • Schisler DA, Slininger PJ, Olsen NL (2016) Appraisal of selected osmoprotectants and carriers for formulating Gram-negative biocontrol agents active against Fusarium dry rot on potatoes in storage. Biol Control 98:1–10

    Article  CAS  Google Scholar 

  • Schoebitz M, López MD, Roldán A (2013) Bioencapsulation of microbial inoculants for better soil–plant fertilization. A review. Agron Sustain Dev 33:751–765

    Article  CAS  Google Scholar 

  • Segarra G, Puopolo G, Giovannini O, Pertot I (2015) Stepwise flow diagram for the development of formulations of non spore-forming bacteria against foliar pathogens: the case of Lysobacter capsici AZ78. J Biotechnol 216:56–64

    Article  CAS  PubMed  Google Scholar 

  • Sennoi R, Singkham N, Jogloy S, Boonlue S, Saksirirat W, Kesmala T, Patanothai A (2013) Biological control of southern stem rot caused by Sclerotium rolfsii using Trichoderma harzianum and arbuscular mycorrhizal fungi on Jerusalem artichoke (Helianthus tuberosus L.). Crop Protect 54:148–153

    Article  Google Scholar 

  • Sharma RR, Singh D, Singh R (2009) Biological control of postharvest diseases of fruits and vegetables by microbial antagonists: a review. Biol Control 50:205–221

    Article  Google Scholar 

  • Singh PP, Shin YC, Park CS, Chung YR (1999) Biological control of Fusarium wilt of cucumber by chitinolytic bacteria. Phytopathology 89:92–99

    Article  CAS  PubMed  Google Scholar 

  • Sotoyama K, Akutsu K, Nakajima M (2017) Suppression of bacterial wilt of tomato by soil amendment with mushroom compost containing Bacillus amyloliquefaciens IUMC7. J Gen Plant Pathol 83:51–55

    Article  Google Scholar 

  • Streeter JG (2003) Effect of trehalose on survival of Bradyrhizobium japonicum during desiccation. J Appl Microbiol 95:484–491

    Article  CAS  PubMed  Google Scholar 

  • Strobel SA, Allen K, Roberts C, Jimenez D, Scher HB, Jeoh T (2018) Industrially-scalable microencapsulation of plant beneficial bacteria in dry cross-linked alginate matrix. Ind Biotechnol 14:138–147

    Article  CAS  Google Scholar 

  • Sui Y, Liu J (2014) Effect of glucose on thermotolerance and biocontrol efficacy of the antagonistic yeast Pichia guilliermondii. Biol Control 74:59–64

    Article  CAS  Google Scholar 

  • Sui Y, Liu J, Wisniewski M, Droby S, Norelli J, Hershkovitz V (2012) Pretreatment of the yeast antagonist, Candida oleophila, with glycine betaine increases oxidative stress tolerance in the microenvironment of apple wounds. Int J Food Microbiol 157:45–51

    Article  CAS  PubMed  Google Scholar 

  • Sun ZB, Sun MH, Zhou M, Li SD (2017) Transformation of the endochitinase gene Chi67-1 in Clonostachys rosea 67-1 increases its biocontrol activity against Sclerotinia sclerotiorum. AMB Express 7:1

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • Tomada S, Puopolo G, Perazzolli M, Musetti R, Loi N, Pertot I (2016) Pea broth enhances the biocontrol efficacy of Lysobacter capsici AZ78 by triggering cell motility associated with biogenesis of type IV pilus. Front Microbiol 7:1136

    Article  PubMed  PubMed Central  Google Scholar 

  • Tu L, He Y, Yang H, Wu Z, Yi L (2015) Preparation and characterization of alginate–gelatin microencapsulated Bacillus subtilis SL-13 by emulsification/internal gelation. J Biomater Sci Polym Ed 26:735–749

    Article  CAS  PubMed  Google Scholar 

  • Umashankar K, Chandralekha A, Dandavate T, Tavanandi HA, Raghavarao KSMS (2019) A nonconventional method for drying of Pseudomonas aeruginosa and its comparison with conventional methods. Dry Technol 37:839–853

    Article  CAS  Google Scholar 

  • Vemmer M, Patel AV (2013) Review of encapsulation methods suitable for microbial biological control agents. Biol Control 67:380–389

    Article  CAS  Google Scholar 

  • Wang Y, Luo Y, Sui Y, Xie Z, Liu Y, Jiang M, Liu J (2018) Exposure of Candida oleophila to sublethal salt stress induces an antioxidant response and improves biocontrol efficacy. Biol Control 127:109–115

    Article  CAS  Google Scholar 

  • Wei Z, Huang J, Yang C, Xu Y, Shen Q, Chen W (2015) Screening of suitable carriers for Bacillus amyloliquefaciens strain QL-18 to enhance the biocontrol of tomato bacterial wilt. Crop Protect 75:96–103

    Article  Google Scholar 

  • Wesche AM, Gurtler JB, Marks BP, Ryser ET (2009) Stress, sublethal injury, resuscitation, and virulence of bacterial foodborne pathogens. J Food Prot 72:1121–1138

    Article  CAS  PubMed  Google Scholar 

  • Wiyono S, Schulz DF, Wolf GA (2008) Improvement of the formulation and antagonistic activity of Pseudomonas fluorescens B5 through selective additives in the pelleting process. Biol Control 46:348–357

    Article  Google Scholar 

  • Wu Q, Bai L, Liu W, Li Y, Lu C, Li Y, Fu K, Yu C, Chen J (2013a) Construction of a Streptomyces lydicus A01 transformant with a chit42 gene from Trichoderma harzianum P1 and evaluation of its biocontrol activity against Botrytis cinerea. J Microbiol 51:166–173

    Article  CAS  PubMed  Google Scholar 

  • Wu Q, Bai L, Liu W, Li Y, Lu C, Li Y, Lin Z, Wang M, Xue C, Chen J (2013b) Construction of Streptomyces lydicus A01 transformant with the chit33 gene from Trichoderma harzianum CECT2413 and its biocontrol effect on Fusaria. China Sci Bull 58:3266–3273

    Article  CAS  Google Scholar 

  • Wu H, Li J, Dong D, Liu T, Zhang T, Zhang D, Liu W (2015a) Heterologous coexpression of Vitreoscilla hemoglobin and Bacillus megaterium glucanase in Streptomyces lydicus A02 enhanced its production of antifungal metabolites. Enzyme Microb Technol 81:80–87

    Article  CAS  PubMed  Google Scholar 

  • Wu K, Fang Z, Guo R, Pan B, Shi W, Yuan S, Guan H, Gong M, Shen B, Shen Q (2015b) Pectin enhances bio-control efficacy by inducing colonization and secretion of secondary metabolites by Bacillus amyloliquefaciens SQY 162 in the rhizosphere of tobacco. PLoS ONE 10:e0127418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu XM, Jeffries P, Pautasso M, Jeger MJ (2011) Combined use of biocontrol agents to manage plant diseases in theory and practice. Phytopathology 101:1024–1031

    Article  CAS  PubMed  Google Scholar 

  • Xu Z, Xie J, Zhang H, Wang D, Shen Q, Zhang R (2019) Enhanced control of plant wilt disease by a xylose-inducible degQ gene engineered into Bacillus velezensis strain SQR9XYQ. Phytopathology 109:36–43

    Article  PubMed  Google Scholar 

  • Yandigeri MS, Malviya N, Solanki MK, Shrivastava P, Sivakumar G (2015) Chitinolytic Streptomyces vinaceusdrappus S5MW2 isolated from Chilika lake, India enhances plant growth and biocontrol efficacy through chitin supplementation against Rhizoctonia solani. World J Microbiol Biotechnol 31:1217–1225

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Chen L, Yong X, Shen Q (2011) Formulations can affect rhizosphere colonization and biocontrol efficiency of Trichoderma harzianum SQR-T037 against Fusarium wilt of cucumbers. Biol Fertil Soils 47:239–248

    Article  Google Scholar 

  • Yang M, Mavrodi DV, Mavrodi OV, Thomashow LS, Weller DM (2017) Construction of a recombinant strain of Pseudomonas fluorescens producing both phenazine-1-carboxylic acid and cyclic lipopeptide for the biocontrol of take-all disease of wheat. Eur J Plant Pathol 149:683–694

    Article  CAS  Google Scholar 

  • Zembek P, Perlińska-Lenart U, Brunner K, Reithner B, Palamarczyk G, Mach RL, Kruszewska JS (2011) Elevated activity of dolichyl phosphate mannose synthase enhances biocontrol abilities of Trichoderma atroviride. Mol Plant-Microbe Interact 24:1522–1529

    Article  CAS  PubMed  Google Scholar 

  • Zhan Y, Xu Q, Yang MM, Yang HT, Liu HX, Wang YP, Guo JH (2012) Screening of freeze-dried protective agents for the formulation of biocontrol strains, Bacillus cereus AR156, Burkholderia vietnamiensis B418 and Pantoea agglomerans 2Re40. Lett Appl Microbiol 54:10–17

    Article  CAS  PubMed  Google Scholar 

  • Zhang C, Gao J, Han T, Tian X, Wang F (2017a) Integrated control of tobacco black shank by combined use of riboflavin and Bacillus subtilis strain Tpb55. Biocontrol 62:835–845

    Article  CAS  Google Scholar 

  • Zhang N, Pan R, Shen Y, Yuan J, Wang L, Luo X, Raza W, Ling N, Huang Q, Shen Q (2017b) Development of a novel bio-organic fertilizer for plant growth promotion and suppression of rhizome rot in ginger. Biol Control 114:97–105

    Article  Google Scholar 

  • Zhou TT, Li CY, Chen D, Wu K, Shen QR, Shen B (2014) phlF mutant of Pseudomonas fluorescens J2 improved 2,4-DAPG biosynthesis and biocontrol efficacy against tomato bacterial wilt. Biol Control 78:1–8

    Article  CAS  Google Scholar 

  • Zohar-Perez C, Chernin L, Chet I, Nussinovitch A (2003) Structure of dried cellular alginate matrix containing fillers provides extra protection for microorganisms against UVC radiation. Radiat Res 160:198–204

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The work was financially supported by JSPS KAKENHI (Grants JP24780317 and 15K07811).

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Correspondence to Masafumi Shimizu.

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Marian, M., Shimizu, M. Improving performance of microbial biocontrol agents against plant diseases. J Gen Plant Pathol 85, 329–336 (2019). https://doi.org/10.1007/s10327-019-00866-6

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