Abstract
Bacterial blight, caused by Xanthomonas axonopodis pv. punicae, Xap is a serious threat to commercially successful pomegranate (Punica granatum L) crop. Owing to the non-availability of disease-resistant varieties of pomegranate, integrated disease management involving change of season, adequate nutrition, and preventive sprays of bactericides is used to control Xap. We undertook a systematic study to assess the efficacy of metal-based nanomaterials (Cu, CuO, ZnO, CaO, MgO) for the control of Xap. The antimicrobial effectiveness was in the order Cu > ZnO > MgO > CuO with MIC (minimum inhibitory concentration) 2.5, 20, 190, 200, and 1600 μg/ml. A time-to-kill curve indicated that Cu nanoparticles (CuNPs) killed Xap cells within 30 min at 2.5 μg/ml. Under controlled conditions (polyhouse), foliar application of CuNPs (400 μg/ml) resulted in ~ 90 and ~ 15% disease reduction in 6-month-old infected plants at early (disease severity 10%) and established (disease severity 40%) stages of infection, respectively. In a subsequent field study on severely infected 7-year-old plants, applications of nanoparticles reduced the disease incidence by ~ 20% as compared to untreated control. Microscopic observations revealed that CuNPs reduced the bacterial colonization of the leaf surface. Anti-Xap activity of foliar applied CuNPs was on par with conventionally used copper oxychloride (3000 μg/ml) albeit at 8-fold reduced copper concentration. Thus, early disease detection and application of effective dosage of copper nanoparticles can indeed help the farmer in achieving rapid infection control. Further studies on use of combinations of nanoparticles for management of bacterial blight are warranted.
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References
Avanzato CP, Follieri JM, Banerjee IA, Fath KR (2009) Biomimetic synthesis and antibacterial characteristics of magnesium oxide—germanium dioxide nanocomposite powders. J Compos Mater 43:897–910
Aysan Y, Sahin F (2003) First report of bacterial blight of anthurium caused by Xanthomonas axonopodis pv. dieffenbachiae in Turkey. Plant Pathol 52:783–783
Benagi VI, Ravikumar MR, Nargund VB (2012) Threat of bacterial blight on pomegranate in India—mitigation by an integrated approach. In: Melgarejo P, Valero D (eds) Options Méditerranéennes Series A: Mediterranean Seminars, II International Symposium on the Pomegranate, vol 103. CIHEAM, Zaragoza, pp 113–116
Benson DM, Hall JL, Moorman GW, Daughtrey ML, Chase AR, Lamour KH (2002) The history and diseases of poinsettia, the christmas flower. Plant Health Progress 3(1):18
Boro MC, Beriam LOS, Guzzo SD (2011) Induced resistance against Xanthomonas axonopodis pv. passiflorae in passion fruit plants. Trop Plant Pathol 36:74–80
Carabineiro SAC, Bogdanchikova N, Pestryakov A, Tavares PB, Fernandes LSG, Figueiredo JL (2011) Gold nanoparticles supported on magnesium oxide for CO oxidation. Nanoscale Res Lett 6(1):435
Carmo MGFD, Macagnan D, Carvalho ADOD (2001) Progress of bacterial leaf spot of pepper starting with different initial quantities of infected seedlings and treatment with the use or not of copper oxichloride. Hortic Bras 19:342–347
Chatterjee AK, Sarkar RK, Chattopadhyay AP, Aich P, Chakraborty R, Basu T (2012) A simple robust method for synthesis of metallic copper nanoparticles of high antibacterial potency against E. coli. Nanotechnology 23:085103
Chen X, Jing X, Wang J, Liu J, Song D, Liu L (2013) Self-assembly of ZnO nanoparticles into hollow microspheres via a facile solvothermal route and their application as gas sensor. CrystEngComm 15(36):7243
Christian T, Schneider RJ, Färber HA, Skutlarek D, Meyer MT, Goldbach HE (2003) Determination of antibiotic residues in manure, soil, and surface waters. Acta Hydrochim Hydrobiol 31:36–44
Dapkekar A, Deshpande P, Oak MD, Paknikar KM, Rajwade JM (2018) Zinc use efficiency is enhanced in wheat through nanofertilization. Sci Rep 8:6832
Degrassi G, Antisari LV, Venturi V, Carbone S, Gatti AM, Gambardella C, Falugi C, Vianello G (2014) Impact of Engineered Nanoparticles on Virulence of Xanthomonas oryzae pv oryzae and on Rice Sensitivity at its Infection. EQA-International. J Environ Qual 16:21–33
Deshpande P, Dapkekar A, Oak MD, Paknikar KM, Rajwade JM (2017) Zinc complexed chitosan/TPP nanoparticles: a promising micronutrient nanocarrier suited for foliar application. Carbohydr Polym 165:394–401
El-Hendawy HH, Osman ME, Sorour NM (2005) Biological control of bacterial spot of tomato caused by Xanthomonas campestris pv. vesicatoria by Rahnella aquatilis. Microbiol Res 160:343–352
Elmer WH, Ma C, White JC (2018) Nanoparticles for plant disease management. Curr Opin Environ Sci Heath 6:66–70
Espitia PJP, Soares NDFF, dos Reis Coimbra JS, de Andrade NJ, Cruz RS, Medeiros EAA (2012) Zinc oxide nanoparticles: synthesis, antimicrobial activity and food packaging applications. Food Bioprocess Technol 5:1447–1464
Fones H, Preston GM (2012) Reactive oxygen and oxidative stress tolerance in plant pathogenic Pseudomonas. FEMS Microbiol Lett 327:1–8
Gan N, Yang X, Xie D, Wu Y, Wen W (2010) A disposable organophosphorus pesticides enzyme biosensor based on magnetic composite nano-particles modified screen printed carbon electrode. Sensors 10:625–638
Graham JH, Gottwald TR, Cubero J, Achor DS (2004) Xanthomonas axonopodis pv. citri: factors affecting successful eradication of citrus canker. Mol Plant Pathol 5:1–15
Grass G, Rensing C, Solioz M (2011) Metallic copper as an antimicrobial surface. Appl Environ Microbiol 77:1541–1547
Guan H, Chi D, Yu J, Li X (2008) A novel photodegradable insecticide: preparation, characterization and properties evaluation of nano-Imidacloprid. Pestic Biochem Physiol 92:83–91
Hajipour MJ, Fromm KM, Ashkarran AA, de Aberasturi DJ, de Larramendi IR, Rojo T, Serpooshan V, Parak WJ, Mahmoudi M (2012) Antibacterial properties of nanoparticles. Trends Biotechnol 30:499–511
Horcas I, Fernández T (2007) WSXM: a software for scanning probe microscopy and a tool for nanotechnology. Rev Sci Instrum 78:013705
Horticultural Statistics of India (2017) http://www.mospi.gov.in/statistical-year-book-india/2017/178. Accessed 22 Oct 2018
Imtiaz A, Farrukh MA, Khaleeq-ur-Rahman M, Adnan R (2013) Micelle-assisted synthesis of Al O·CaO nanocatalyst: optical properties and their applications in photodegradation of 2, 4, 6-trinitrophenol. Sci World J Article ID 641420
Jain K, Desai N (2018) Pomegranate the cash crop of India: a comprehensive review on agricultural practices and diseases. Int J Health Sci Res 8:315–336
Johanningsmeier SD, Harris GK (2011) Pomegranate as a functional food and nutraceutical source. Ann Rev Food Sci Technol 2:181–201
Kasabe N (2015) Bacterial blight affects pomegranate quality in Maharashtra by up to 70%. https://www.financialexpress.com/market/commodities/bacterial-blight-affects-pomegranate-quality-in-maharashtra-by-up-to-70/109008/. Accessed 22 Oct 2018
Kathuria K, Bhargava R, Yadav PK, Gurjar K (2017) Molecular studies ascertaining the phylogenetic relationships in pomegranate (Punica granatum L.) cultivars using RAPD markers. Int J Curr Microbiol App Sci 6:1282–1291
Khiyami MA, Almoammar H, Awad YM, Alghuthaymi MA, Abd-Elsalam KA (2014) Plant pathogen nanodiagnostic techniques: forthcoming changes? Biotechnol Biotechnol Equip 28:775–785
Kim DY, Kadam A, Shinde S, Saratale RG, Patra J, Ghodake G (2018) Recent developments in nanotechnology transforming the agricultural sector: a transition replete with opportunities. J Sci Food Agric 98:849–864
Kirankumar KC, Khan ANA (2017) Performance of bactericides against bacterial blight of pomegranate. Environ Ecol 35:97–101
Knell M (2010) Nanotechnology and the sixth technological revolution. In: Cozzens SE, Wetmore JM (eds) Nanotechnology and the challenges of equity, equality and development. Springer, Dordrecht, pp 127–143
Koné D, Dao S, Tekete C, Doumbia I, Koita O, Abo K, Wicker E, Verdier V (2015) Confirmation of Xanthomonas axonopodis pv. manihotis causing cassava bacterial blight in Ivory Coast. Plant Dis 99:1445
Laha D, Pramanik A, Laskar A, Jana M, Pramanik P, Karmakar P (2014) Shape-dependent bactericidal activity of copper oxide nanoparticle mediated by DNA and membrane damage. Mater Res Bull 59:185–191
Lalithya KA, Manjunatha G, Raju B, Kulkarni MS, Lokesh V (2017) Plant growth regulators and signal molecules enhance resistance against bacterial blight disease of pomegranate. J Phytopathol 165:727–736
Lamichhane JR, Osdaghi E, Behlau F, Köhl J, Jones JB, Aubertot JN (2018) Thirteen decades of antimicrobial copper compounds applied in agriculture. A review. Agron Sustain Dev 38:28–46
Lansky EP, Newman RA (2007) Punica granatum (pomegranate) and its potential for prevention and treatment of inflammation and cancer. J Ethnopharmacol 109:177–206
Li B, Zhang Y, Yang Y, Qiu W, Wang X, Liu B, Wang Y, Sun G (2016) Synthesis, characterization, and antibacterial activity of chitosan/TiO nanocomposite against Xanthomonas oryzae pv. oryzae. Carbohydr Polym 152:825–831
Lisa M, Chouhan RS, Vinayaka AC, Manonmani HK, Thakur MS (2009) Gold nanoparticles based dipstick immunoassay for the rapid detection of dichlorodiphenyltrichloroethane: an organochlorine pesticide. Biosens Bioelectron 25:224–227
Lokesh R, Erayya KK, Chandrashekhar N, Khan ANA (2014) In vivo efficacy of some antibiotics against bacterial blight of pomegranate caused by Xanthomonas axonopodis pv. punicae. Int Res J Biol Sci 3:31–35
Majeed ZH, Taha MR (2013) A review of stabilization of soils by using nanomaterials. Aust J Basic Appl Sci 7(2):576–581
Mazzaglia A, Fortunati E, Kenny JM, Torre L, Balestra GM (2017) Nanomaterials in plant protection. In: MAV A, Voorde MV (eds) Nanotechnology in agriculture and food science. Wiley-VCH Verlag GmbH & Co, Weinheim, pp 113–134
Melgarejo P, Melgarejo-Sánchez P, Martínez JJ, Hernández F, Legua P, Martínez R (2013) The pomegranate tree in the world: new cultivars and uses. In: Yuan Z, Wilkins E, Wang D (eds) III International Symposium on Pomegranate and Minor Mediterranean Fruits Leuven, vol 1089. ISHS, Leuven, pp 327–332
Mondal KK, Mani C (2012) Investigation of the antibacterial properties of nanocopper against Xanthomonas axonopodis pv. punicae, the incitant of pomegranate bacterial blight. Ann Microbiol 62:889–893
Mondal KK, Rajendran TP, Phaneendra C, Mani C, Sharma J, Shukla R, Verma G, Kumar R, Singh D, Kumar A, Saxena AK (2012) The reliable and rapid polymerase chain reaction (PCR) diagnosis for Xanthomonas axonopodis pv. punicae in pomegranate. Afr J Microbiol Res 6:5950–5956
Mu C, He J (2011) Confined conversion of CuS nanowires to CuO nanotubes by annealing-induced diffusion in nanochannels. Nanoscale Res Lett 6(1):50
Mukherji S, Ruparelia J, Agnihotri S (2012) Antimicrobial activity of silver and copper nanoparticles: variation in sensitivity across various strains of bacteria and fungi. In: Cioffi N, Rai M (eds) Nano-Antimicrobials. Springer, Berlin, pp 225–251
Mukhopadhyay SS (2014) Nanotechnology in agriculture: prospects and constraints. Nanotechnol Sci Appl 7:63
Obradovic A, Jones JB, Momol MT, Balogh B, Olson SM (2004) Management of tomato bacterial spot in the field by foliar applications of bacteriophages and SAR inducers. Plant Dis 88:736–740
Ocsoy I, Paret ML, Ocsoy MA, Kunwar S, Chen T, You M, Tan W (2013) Nanotechnology in plant disease management: DNA-directed silver nanoparticles on graphene oxide as an antibacterial against Xanthomonas perforans. ACS Nano 7:8972–8980
Opio AF, Allen DJ, Teri JM (1996) Pathogenic variation in Xanthomonas campestris pv. phaseoli, the causal agent of common bacterial blight in Phaseolus beans. Plant Pathol 45:1126–1133
Owolade OF, Ogunleti DO, Adenekan MO (2008) Titanium dioxide affects disease development and yield of edible cowpea. Agri Food Chem 7:2942–2947
Paknikar KM, Nagpal V, Pethkar AV, Rajwade JM (2005) Degradation of lindane from aqueous solutions using iron sulfide nanoparticles stabilized by biopolymers. Sci Technol Adv Mater 6:370–374
Paret ML, Vallad GE, Averett DR, Jones JB, Olson SM (2013) Photocatalysis: effect of light-activated nanoscale formulations of TiO on and control of bacterial spot of tomato. Phytopathology 103(3):228–236
Petersen Y, Mansvelt EL, Venter E, Langenhoven WE (2010) Detection of Xanthomonas axonopodis pv. punicae causing bacterial blight on pomegranate in South Africa. Australas Plant Pathol 39:544–546
Raju J, Benagi VI, Jayalakshmi K, Nargund VB, Sonavane PS (2012) In vitro evaluation of chemicals, botanicals and bioagents against the bacterial blight of pomegranate caused by Xanthomonas axonopodis pv. punicae. Int J Plant Prot 5:315–318
Rastogi A, Zivcak M, Sytar O, Kalaji HM, He X, Mbarki S, Brestic M (2017) Impact of metal and metal oxide nanoparticles on plant: a critical review. Front Chem 5:78
Ravi V, Kulkarni SD, Samuel V, Kale SN, Mona J, Rajgopal R, Daundkar A, Lahoti PS, Joshee RS (2007) Synthesis of La Sr MnO at 800°C using citrate gel method. Ceram Int 33(6):1129–1132
Reidy B, Haase A, Luch A, Dawson K, Lynch I (2013) Mechanisms of silver nanoparticle release, transformation and toxicity: a critical review of current knowledge and recommendations for future studies and applications. Materials 6(6):2295–2350
Ruparelia JP, Chatterjee AK, Duttagupta SP, Mukherji S (2008) Strain specificity in antimicrobial activity of silver and copper nanoparticles. ActaBiomater 4:707–716
Santo CE, Quaranta D, Grass G (2012) Antimicrobial metallic copper surfaces kill Staphylococcus haemolyticus via membrane damage. Microbiol Open 1:46–52
Sarkar S, Datta SC, Biswas DR (2014) Synthesis and characterization of nanoclay–polymer composites from soil clay with respect to their water-holding capacities and nutrient-release behavior. J Appl Polym Sci 131:6
Sawai J (2003) Quantitative evaluation of antibacterial activities of metallic oxide powders (ZnO, MgO and CaO) by conductimetric assay. J Microbiol Methods 54:177–182
Servin A, Elmer W, Mukherjee A, De la Torre-Roche R, Hamdi H, White JC, Bindraban P, Dimkpa C (2015) A review of the use of engineered nanomaterials to suppress plant disease and enhance crop yield. J Nanopart Res 17(2)
Sharma KK, Jadhav VT, Sharma J (2011) Present status of pomegranate bacterial blight caused by Xanthomonas axonopodis pv. punicae and its management. Acta Hortic 890:513–522
Sharma J, Sharma KK, Kumar A, Mondal KK, Thalor S, Maity A, Gharate R, Chinchure S, Jadhav VT (2017) Pomegranate bacterial blight: symptomatology and rapid inoculation technique for Xanthomonas axonopodis pv. punicae. J Plant Pathol 99:109–119
Silva AT, Nguyen A, Ye C, Verchot J, Moon JH (2010) Conjugated polymer nanoparticles for effective siRNA delivery to tobacco BY-2 protoplasts. BMC Plant Biol 10:291
Slavin YN, Asnis J, Häfeli UO, Bach H (2017) Metal nanoparticles: understanding the mechanisms behind antibacterial activity. J Nanobiotechnol 15:65
Stall RE, Thayer PL (1962) Streptomycin resistance of the bacterial spot pathogen and control with streptomycin. Plant Dis Rep 46:389–392
Swings J, Van den Mooter M, Vauterin L, Hoste B, Gillis M, Mew TW, Kersters K (1990) Reclassification of the causal agents of bacterial blight (Xanthomonas campestris pv. oryzae) and bacterial leaf streak (Xanthomonas campestris pv. oryzicola) of rice as pathovars of Xanthomonas oryzae (ex Ishiyama 1922) sp. nov., nom. Rev. Int J Syst Evol Microbiol 40:309–311
Torney F, Trewyn BG, Lin VSY, Wang K (2007) Mesoporous silica nanoparticles deliver DNA and chemicals into plants. Nat Nanotechnol 2:295–300
Viuda-Martos M, Fernández-López J, Pérez-Álvarez JA (2010) Pomegranate and its many functional components as related to human health: a review. Compr Rev Food Sci Food Saf 9:635–654
Wang S, Chang LY, Wang YJ, Wang Q, Yang CH, Mei RH (2009) Nanoparticles affect the survival of bacteria on leaf surfaces. FEMS Microbiol Ecol 68:182–191
Xu Y, Zhu XF, Zhou MG, Kuang J, Zhang Y, Shang Y, Wang JX (2010) Status of streptomycin resistance development in Xanthomonas oryzae pv. oryzae and Xanthomonas oryzae pv. oryzicola in China and their resistance characters. J Phytopathol 158(9):601–608
Yao KS, Wang DY, Ho WY, Yan JJ, Tzeng KC (2007) Photocatalytic bactericidal effect of TiO thin film on plant pathogens. Surf Coat Technol 201(15):6886–6888
Yenjerappa ST, Byadagi AS, Ravikumar MR, Mokashi AN, Goud KB (2013) Biological management of bacterial blight of pomegranate caused by Xanthomonas axonopodis pv. punicae. Karnataka J Agrisci 26:561–562
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RGC is thankful to UGC, New Delhi for awarding the research fellowship.
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Chikte, R.G., Paknikar, K.M., Rajwade, J.M. et al. Nanomaterials for the control of bacterial blight disease in pomegranate: quo vadis?. Appl Microbiol Biotechnol 103, 4605–4621 (2019). https://doi.org/10.1007/s00253-019-09740-z
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DOI: https://doi.org/10.1007/s00253-019-09740-z