Abstract
Sustainability and circular economy are increasingly pushing for the search of natural materials to foster antiparasitic treatments, especially in the case of economically relevant agricultural cultivations, such as grapevine. In this work, we propose to deliver neem oil, a natural biopesticide loaded into novel nanovectors (nanocapsules) which were fabricated using a scalable procedure starting from Kraft lignin and grapeseed tannins. The obtained formulations were characterized in terms of size and Zeta potential, showing that almost all the nanocapsules had size in the suitable range for delivery purposes (mean diameter 150–300 nm), with low polydispersity and sufficient stability to ensure long shelf life. The target microorganisms were three reference fungal pathogens of grapevine (Botrytis cinerea, Phaeoacremonium minimum, Phaeomoniella chlamydospora), responsible for recurrent diseases on this crop: grey mold or berry rot by B. cinerea and diseases of grapevine wood within the Esca complex of diseases. Results showed that grapeseed tannins did not promote inhibitory effects, either alone or in combination with Kraft lignin. On the contrary, the efficacy of neem oil against P. minimum was boosted by more than 1–2 orders of magnitude and the parasite growth inhibition was higher with respect to a widely used commercial pesticide, while no additional activity was detected against P. chlamydospora and B. cinerea.
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References
Baloyi MA, Mostert L, Halleen F (2018) Pathogenicity of ten Phaeoacremonium species associated with esca and Petri disease of grapevine. Phytopathol Mediterr 57(3):538–546. https://doi.org/10.14601/Phytopathol_Mediterr-23940
Benelli G, Canale A, Toniolo C, Higuchi A, Murugan K, Pavela R, Nicoletti M (2017) Neem (Azadirachta indica): towards the ideal insecticide? Nat Prod Res 31(4):369–386. https://doi.org/10.1080/14786419.2016.1214834
Bertsch C, Ramirez-Suero M, Magnin-Robert M, Larignon P, Chong J, Abou-Mansour E et al (2013) Grapevine trunk diseases: complex and still poorly understood. Plant Pathol 62(2):243–265. https://doi.org/10.1111/j.1365-3059.2012.02674.x
Cantrell CL, Dayan FE, Duke SO (2012) Natural products as sources for new pesticides. J Nat Prod 75:1231–1242
Chaudhary S, Kanwar RK, Sehgal A, Cahill DM, Barrow CJ, Sehgal R, Kanwar JR (2017) Progress on Azadirachta indica based biopesticides in replacing synthetic toxic pesticides. Front Plant Sci 108(6):1–10. https://doi.org/10.3389/fpls.2017.00610
Chhipa H (2017) Nanofertilizers and nanopesticides for agriculture. Environ Chem Lett 15:15–22. https://doi.org/10.1007/s10311-016-0600-4
Clemente I, Falsini S, Di Cola E, Fadda GC, Gonnelli C, Spinozzi F, Bacia-Verloop M, Grillo I, Ristori S (2019) Green nanovectors for phytodrug delivery: in-depth structural and morphological characterization. ACS Sustain Chem Eng 7(15):12838–12846. https://doi.org/10.1021/acssuschemeng.9b01748
Clemente I, Menicucci F, Colzi I, Sbraci L, Benelli C, Giordano C, Gonnelli C, Ristori S, Petruccelli R (2018) Unconventional and sustainable nanovectors for phytohormone delivery: insights on Olea europaea. ACS Sustainable Chem Eng 6(11):15022–15031. https://doi.org/10.1021/acssuschemeng.8b03489
Colzi I, Troyan AN, Perito B, Casalone E, Romoli R, Pieraccini G, Škalko-Basnet N, Adessi A, Rossi F, Gonnelli C, Ristori S (2015) Antibiotic delivery by liposomes from prokaryotic microorganisms: Similia cum similis works better. Eur J Pharm Biopharm 94:411–418. https://doi.org/10.1016/j.ejpb.2015.06.013
de Oliveira JL, Campos EVR, Fraceto LF (2018) Recent developments and challenges for nanoscale formulation of botanical pesticides for use in sustainable agriculture. J Agric Food Chem 66(34):8898–8913. https://doi.org/10.1021/acs.jafc.8b03183
Del Frari G, Gobbi A, Aggerbeck MR, Oliveira H, Hansen LH, Ferreira RB (2019) Fungicides and the grapevine wood mycobiome: a case study on tracheomycotic ascomycete Phaeomoniella chlamydospora reveals potential for two novel control strategies. Front Plant Sci 10:1405. https://doi.org/10.3389/fpls.2019.01405
Di Marco S, Metruccio EG, Moretti S, Nocentini M, Carella G, Pacetti A, Mugnai L (2022) Activity of Trichoderma asperellum strain ICC 012 and Trichoderma gamsii strain ICC 080 toward diseases of esca complex and associated pathogens. Front Microbiol 12:813410. https://doi.org/10.3389/fmicb.2021.813410
Díaz G A, Latorre B A (2014) Infection caused by Phaeomoniella chlamydospora associated with esca-like symptoms in grapevine in Chile. Plant Dis. https://doi.org/10.1094/pdis-12-12-1180-re
Ekambaram SP, Perumal SS, Balakrishnan A (2016) Scope of hydrolysable tannins as possible antimicrobial agent. Phytother Res 30:1035–1045
Falsini S, Clemente I, Papini A, Tani C, Schiff S, Salvatici MC, Petruccelli R, Benelli C, Giordano C, Gonnelli C, Ristori S (2019) When sustainable nanochemistry meets agriculture: lignin nanocapsules for bioactive compound delivery to plantlets. ACS Sustain Chem Eng 7(24):19935–19942. https://doi.org/10.1021/acssuschemeng.9b05462
Feliciano AJ, Gubler WD (2001) Histological investigations on infection of grape roots and shoots by Phaeoacremonium spp. Phytopathol Mediterr 40:387–393
Fischer J, Beckers SJ, Yiamsawas D, Thines E, Landfester K, Wurm FR (2019) Targeted drug delivery in plants: enzyme-responsive lignin nanocarriers for the curative treatment of the worldwide grapevine trunk disease esca. Adv Sci 6:1802315. https://doi.org/10.1002/advs.201802315
Glaive A-S, Modjinou T, Versace D-L, Abbad-Andaloussi S, Dubot P, Langlois V, Renard E (2017) Design of antibacterial and sustainable antioxidant networks based on plant phenolic derivatives used as delivery system of carvacrol or tannic acid. ACS Sustain Chem Eng 5(3):2320–2329. https://doi.org/10.1021/acssuschemeng.6b02655
Glazer I, Masaphy S, Marciano P, Bar-Ilan I, Holland D, Kerem Z, Partial AR (2012) Identification of antifungal compounds from Punica granatum peel extracts. J Agric Food Chem 60(19):4841–4848. https://doi.org/10.1021/jf300330y
Guerin-Dubrana L, Fontaine F, Mugnai L (2019). Grapevine trunk disease in European and Mediterranean vineyards: occurrence, distribution and associated disease-affecting cultural factors. Phytopathol Mediterr 58(1):49–71. https://doi.org/10.13128/Phytopathol_Mediterr-25153
Hashmat I, Azad H, Ahmed A (2012) Neem (Azadirachta indica A. Juss) - a nature's drugstore: an overview. Int Res J Biol Sci 1(6): 76–79.
Jacometti MA, Wratten SD, Walter M (2010) Review: alternatives to synthetic fungicides for Botrytis cinerea management in vineyards. Aust J Grape Wine Res 16(1):154–171. https://doi.org/10.1111/j.1755-0238.2009.0067.x
Jaspers MV (2001) Effect of fungicides, in vitro, on germination and growth of Phaeomoniella chlamydospora. Phytopathol Mediterr 40:S453–S458
Kah M, Kookana RS, Gogos A, Bucheli TD (2018) A critical evaluation of nanopesticides and nanofertilizers against their conventional analogues. Nat Nanotech 13:677–684. https://doi.org/10.1038/s41565-018-0131-1
Karny A, Zinger A, Kajal A et al (2018) Therapeutic nanoparticles penetrate leaves and deliver nutrients to agricultural crops. Sci Rep 8:7589. https://doi.org/10.1038/s41598-018-25197-y
Khan MR, Chonhenchob V, Huang C, Suwanamornlert P (2021) Antifungal activity of propyl disulfide from neem (Azadirachta indica) in vapor and agar diffusion assays against anthracnose pathogens (Colletotrichum gloeosporioides and Colletotrichum acutatum) in mango fruit. Microorganisms 9:839. https://doi.org/10.3390/microorganisms9040839
Kumar R, Mehta S, Pathak SR (2018) Bioactive constituents of neem. Synthesis of medicinal agents from plants 75-103https://doi.org/10.1016/B978-0-08-102071-5.00004-0
Lima PHC, Antunes DR, Forini MML, Pontes MS, Mattos BD, Grillo R (2021) Recent advances on lignocellulosic-based nanopesticides for agricultural applications. Front Nanotechnol 3:809329. https://doi.org/10.3389/fnano.2021.809329
Lowry GV, Avellan A, Gilbertson LM (2019) Opportunities and challenges for nanotechnology in the agri-tech revolution. Nat Nanotechnol 14:517–522. https://doi.org/10.1038/s41565-019-0461-7
Machado TO, Beckers SJ, Fischer J, Müller B, Sayer C, de Araújo PHH, Landfester K, Wurm FR (2020) Bio-based lignin nanocarriers loaded with fungicides as a versatile platform for drug delivery in plants. Biomacromol 21(7):2755–2763. https://doi.org/10.1021/acs.biomac.0c00487
Menicucci F, Michelozzi M, Raio A, Tredici M, Cencetti G, Clemente I, Ristori S (2021) Thymol-loaded lipid nanovectors from the marine microalga Nannochloropsis sp. as potential antibacterial agents. Biocatalysis Agric Biotechnol 32:101962. https://doi.org/10.1016/j.bcab.2021.101962
Niculescu A-G, Grumezescu AM (2021) Polymer-based nanosystems—a versatile delivery approach polymer-based nanosystems—a versatile delivery approach. Materials 14:6812. https://doi.org/10.3390/ma14226812
Nisbet AJ (2000) Azadirachtin from the neem tree Azadirachta indica: its action against insects. Anais Soc Entomol Bras 29:615–632. https://doi.org/10.1590/S0301-80592000000400001
Pascoli M, Jacques MT, Agarrayua DA, Avila DS, Lima R, Fraceto LF (2019) Neem oil and crop protection: from now to the future. Sci Total Environ 677:57–67. https://doi.org/10.3389/fpls.2016.01494
Peil S, Beckers SJ, Fischer J, Wurm FR (2020) Biodegradable, lignin-based encapsulation enables delivery of Trichoderma reesei with programmed enzymatic release against grapevine trunk diseases. Materials Today Bio 7:100061. https://doi.org/10.1016/j.mtbio.2020.100061
Pereira AES, de Oliveira JL, Savassa SM, Rogério CB, de Medeiros GA, Fraceto LF (2022) Lignin nanoparticles: new insights for a sustainable agriculture. J Clean Prod 345:131145. https://doi.org/10.1016/j.jclepro.2022.131145
Pertot I, Ca T, Rossi V, Mugnai L, Ho mann C, Grando M, Gary C, Lafond D, Duso C, Thiery D, (2017) A critical review of plant protection tools for reducing pesticide use on grapevine and new perspectives for the implementation of IPM in viticulture. Crop Prot 97:70–84. https://doi.org/10.1016/j.cropro.2016.11.025
Pizzi, A (2008) Chapter 8- tannins: major sources, properties and applications. Monomers, Polymers and Composites from Renewable Resources 179–199.
Rajput V D, Singh A, Minkina T M, Shende S S, Kumar P, Verma K K, Bauer T, Gorobtsova O, Deneva S, Sindireva A (2021) Potential applications of nanobiotechnology in plant nutrition and protection for sustainable agriculture, Chapter 5 Nanotechnology in plant growth promotion and protection: recent advances and impacts, first edition. Edited by Avinash P. Ingle. 2021 John Wiley & Sons Ltd.
Savy D, Cozzolino V (2022) Novel fertilising products from lignin and its derivatives to enhance plant development and increase the sustainability of crop production. J Clean Prod 366:132832. https://doi.org/10.1016/j.jclepro.2022.132832
Seibert JB, Viegas JSR, Almeida TC, Amparo TR, Rodrigues IV, Lanza JS, Frézard FJ, Soares RDOA, Teixeira LFM, de Souza GHB, Vieira PMA, Barichello JM, dos Santos ODH (2019) Nanostructured systems improve the antimicrobial potential of the essential oil from Cymbopogon densiflorus leaves. J Nat Prod 82:3208–3220. https://doi.org/10.1021/acs.jnatprod.8b00870
Shah FM, Razaq M, Ali A, Han P, Chen J (2017) Comparative role of neem seed extract, moringa leaf extract and imidacloprid in the management of wheat aphids in relation to yield losses in Pakistan. PLoS One, 12. https://doi.org/10.1371/journal.pone.0184639
Singh RP, Handa R, Manchanda G (2021) Nanoparticles in sustainable agriculture: an emerging opportunity. J Control Release 329:1234–1248. https://doi.org/10.1016/j.jconrel.2020.10.051
Singh UP, Singh HB, Singh RB (1980) The fungicidal effect of neem (Azadirachta Indica) extracts on some soil-borne pathogens of gram (Cicer Arietinum). Mycologia 72(6):1077–1093. https://doi.org/10.1080/00275514.1980.12021288
Sipponen MH, Lange H, Crestini C, Henn A, Österberg M (2019) Lignin for nano- and microscaled carrier systems: applications, trends, and challenges. Chemsuschem 12(10):2039–2054. https://doi.org/10.1002/cssc.201900480
Tripathi D K, Shweta, Singh S, Singh S, Pandey R, Singh V P, Sharma N C, Prasad SM, Dubey N K, Chauhan DK (2017) An overview on manufactured nanoparticles in plants: uptake, translocation, accumulation and phytotoxicity, Plant Physiology and Biochemistry 110:2-12, ISSN 0981-9428. https://doi.org/10.1016/j.plaphy.2016.07.030
Vanholme R, Demedts B, Morreel K, Ralph J, Boerjan W (2010) Lignin biosynthesis and structure. Plant Physiol 153:895–905. https://doi.org/10.1104/pp.110.155119
Weiss M, Fan J, Claudel M et al (2021) Density of surface charge is a more predictive factor of the toxicity of cationic carbon nanoparticles than zeta potential. J Nanobiotechnol 19:5. https://doi.org/10.1186/s12951-020-00747-7
Yu M, Sun C, Xue Y, Liu C, Qiu D, Cui B et al (2019) Tannic acid-based nanopesticides coating with highly improved foliage adhesion to enhance foliar retention. RSC Adv 9(46):27096–27104. https://doi.org/10.1039/C9RA05843E
Yeguerman, CA, Urrutia, R I, Jesser, E N et al. (2022) Essential oils loaded on polymeric nanoparticles: bioefficacy against economic and medical insect pests and risk evaluation on terrestrial and aquatic non-target organisms. Environ Sci Pollut Reshttps://doi.org/10.1007/s11356-022-20848-0
Zhu C, Lei M, Andargie M, Zeng J, Li J (2019) Antifungal activity and mechanism of action of tannic acid against Penicillium digitatum. Physiol Mol Plant Pathol 107:46–50
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Sara Falsini: Conceptualization, Methodology, Formal analysis, Investigation, Data curation, Writing—review & editing. Tommaso Nieri: Methodology, Formal analysis, Writing—review & editing. Aurora Paolini: Methodology, Formal analysis, Writing—review & editing. Silvia Schiff: Methodology, Formal analysis, Writing—review & editing. Alessio Papini: Data curation, Resources, Writing—review & editing. Laura Mugnai: Methodology, Resources, Supervision, Project administration, Funding acquisition. Cristina Gonnelli: Conceptualization, Methodology, Resources, Writing—original draft, Writing—review & editing, Supervision, Project administration, Funding acquisition. Sandra Ristori: Conceptualization, Methodology, Resources, Writing—review & editing, Supervision, Project administration, Funding acquisition.
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Highlights
Neem oil was loaded into novel nanocapsules formed by tannins and lignin.
Nanocapsules had mean diameter of 150–300 nm with low polydispersity.
Nanocapsules had a negative surface charge which guarantees good stability.
Lignin-based nanocapsules enhance the efficacy of neem oil by more than 1–2 order of magnitude on Phaeoacremonium minimum.
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Falsini, S., Nieri, T., Paolini, A. et al. Tannins-lignin mixed nanoformulations for improving the potential of neem oil as fungicide agent. Environ Sci Pollut Res 30, 39131–39141 (2023). https://doi.org/10.1007/s11356-022-24991-6
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DOI: https://doi.org/10.1007/s11356-022-24991-6