Effect of chitosan against to fungicide stress in tomato (Solanum lycopersicum L.)
Year 2023,
Volume: 9 Issue: 3, 499 - 510, 20.09.2023
Hüseyin Bulut
,
Halil İbrahim Öztürk
Abstract
Tomato is an important nutrient for humans in terms of its nutritional values, amount of use and variety. One of the important factors causing yield losses in tomato cultivation is fungal diseases. Fungicides are used as the fastest and most effective solution to combat these diseases. However, the stress and possible toxic risks resulting from the use of fungicides affect the food chain. In our study, the negative effects of fungicide and the use of chitosan to reduce stress in plant breeding were investigated. The level of stress caused by the fungicide containing 80% Mancozeb active substance on tomato, the effects of chitosan, changes in SOD, CAT and MDA expressions, single cell gel electrophoresis and damage on DNA were evaluated. As a result of the study, it was determined that the applied fungicide caused stress and changes in SOD, CAT and MDA enzyme values in tomato seedlings. In the comet assay analysis of the fungicide, it was determined that the tail length and tail DNA % value increased as a result of breakage
in the DNA strands. It was observed that the applied chitosan had a positive effect on enzyme values and DNA damage at some doses (100 ppm and 150 ppm). Chitosan can be used to support the defense mechanism against stress factors in plants.
Project Number
FBA-2021-765
References
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- Bohmdorfer, G., Schleiffer, A., Brunmeir, R., Ferscha, S., Nizhynska, V., Kozak, J., Angelis, K.J., Kreil, D.P., Schweizer, D. (2011). GMI1, a structural-maintenance-of-chromosomes-hinge domain-containing protein, is involved in somatic homologous recombination in Arabidopsis, Plant Journal, 67, pp. 420-433, DOI: 10.1111/j.1365-313X.2011.04604.x
- Bulut, H. (2020), Mısır (Zea mays L.)’ da Tuz Stresine Karşı Humik Asidin Etkisi, Manas Journal of Agriculture Veterinary and Life Sciences,Vol. 10-1, 11 – 18.
- Camargo Carniel, L.S., Niemeyer, J.C., Iuñes de Oliveira Filho, L.C., Alexandre, D., Gebler, L., Klauberg-Filho, O. (2019). The fungicide mancozeb affects soil invertebrates in two subtropical Brazilian soils, Chemosphere, 232, pp. 180-185, https://doi.org/10.1016/j.chemosphere.2019.05.179
- Chance, B., Maehly, A.C. (1955). Assay of catalases and peroxidases. Methods Enzymol. 2, 764–775.
Collins, A.R. (2004). The comet assay for DNA damage and repair: principles, applications, and limitations, Mol. Biotechnol., 26, pp. 249-261, DOI: 10.1385/MB:26:3:249
- Costa-Silva, D.Gd et al. (2018). N -acetylcysteine inhibits Mancozeb-induced impairments to the normal development of zebrafish embryos, J. Neurotoxicol. Teratol, 68, 1-12, https://doi.org/10.1016/j.ntt.2018.04.003
- Donà, M., Confalonieri, M., Minio, A., Biggiogera, M., Buttafava A., Raimondi, E., Delledonne M., Ventura, L., Sabatini, M.E., Macovei, A., Giraffa, G., Carbonera, D., Balestrazzi, A. (2013). RNA-Seq analysis discloses early senescence and nucleolar dysfunction triggered by Tdp1α depletion in Medicago truncatula, J. Exp. Bot. http://dx.doi.org/10.1093/jxb/ert063.
- Falcon-Rodriguez AB, Costales D, Cabrera JC, Martinez-Tellez MA (2011) Chitosan physico-chemical properties modulate and resistance in tobacco plants against the oomycete Phytophthora nicotianae. Pestic. Biochem. Phys. 100: 221-228.
- Feliziani E, Smilanick JL, Morgosan DA, Mansour MF, , Gu S, Gohil HL, Ames ZR (2013) Preharvest fungucide potassium sorbat or chitosan use on quality and storage decay of table grapes. Plant Dis. 97: 307-314.
- Hartung, F., Angelis, K.J., Meister, A., Schubert, I., Melzer, M., Puchta H. (2002). An archaebacterial topoisomerase homolog not present in other eukaryotes is indispensable for cell proliferation of plants, Curr. Biol., 12, pp. 1787-1791, DOI: 10.1016/s0960-9822(02)01218-6
- Heitzberg, F., Chen, I.-P., Hartung, F., Orel, N., Angelis, K.J., Puchta, H. (2004). The Rad17 homologue of Arabidopsis is involved in the regulation of DNA damage repair and homologous recombination, Plant J., 38, pp. 954-968, DOI: 10.1111/j.1365-313X.2004.02097.x
- Jeggo, P.A. (2010). A break is not the End; insight into the damage response to DNA double strand breaks, DNA Repair, 9, pp. 1217-1218, DOI: 10.1016/j.dnarep.2010.09.021
- Jennifer, R., Joan, F., Jeannie, E., Da L. (2017). A systematic review of Mancozeb as a reproductive and developmental hazard, J. Environ. Int., 99, DOI: 10.1016/j.envint.2016.11.006
- Kamisugi, Y., Schaefer, D.G., Kozak, J., Charlot, F., Vrielynck, N., Hola, M., Angelis, K.J., Cuming, A.C., Nogue, F. (2012). MRE11 and RAD50, but not NBS1 are essential for gene targeting in the moss Physcomitrella patens, Nucleic Acids Res., 40 pp. 3496-3510, doi: 10.1093/nar/gkr1272
- Kaushik G., Satya S., Naik S.N. (2009). Food processing a tool to pesticide residue dissipation – A review, Food Research International 42(1):26-40, DOI: 10.1016/j.foodres.2008.09.009
- Kleinkauf, N., Verweij, P.E., Arendrup, M.C., Donnelly, P.J., Cuenca-Estrella, M., Fraaije, B., et al. (2013). Risk assessment on the impact of environmental usage of triazoles on the development and spread of resistance to medical triazoles in Aspergillus species European Centre for Disease Prevention and Control Technical Report, ECDC, Stockholm, DOI: 10.2900/76274
- Kontou, S., Tsipi, D., Tzia, C. (2004). Stability of the dithiocarbamate pesticide maneb in tomato homogenates during cold storage and thermal processing, J. Food Addit. Contam.: Part A, 21, https://doi.org/10.1080/02652030400019372
- Kozak, J., West, C.E., White, C., Costa-Nunes, J.A. da, Angelis, K.J. (2009). Rapid repair of DNA double strand breaks in Arabidopsis is dependent on proteins involved in chromosome structure maintenance, DNA Repair, 8, pp. 413-419, DOI: 10.1016/j.dnarep.2008.11.012
- Lenucci, M. S., Cadinu, D., Taurino, M., Piro, G., Dalessandro, G. (2006). Antioxidant Composition in Cherry and High-Pigment Tomato Cultivars, J. Agric. Food Chem, 54, 7, 2606–2613, https://doi.org/10.1021/jf052920c
- Malerba, M., Cerana, R. (2016). Chitosan effects on plant systems, International journal of molecular sciences, 17(7), 996, DOI: 10.3390/ijms17070996
- Narasimhamurthy, K., Udayashankar, A. C., Britto, S.D., et al. (2022). Chitosan and chitosan-derived nanoparticles modulate enhanced immune response in tomato against bacterial wilt disease. International Journal of Biological Macromolecules, 220, 223-237. doi.org/10.1016/j.ijbiomac.2022.08.054
- Ong, K. (2011). Basic plant pathology training pathogenic agents. Agi Life Extension Texas, pp 1.
- Ostling, O., Johansons, K.J. (1984). Microelectrophoretic study of radiation-induced DNA damage in individual mammalian cells, BBRC, 123, pp. 291-298, DOI: 10.1016/0006-291x(84)90411-x
- Paoletti, F., Aldinucci, D., Mocali, A. et al.(1986). A sensitive spectrophotometric method for the determination of superoxide dismutase activity in tissue extracts, Anal. Biochem. 154, 536–541, DOI: 10.1016/0003-2697(86)90026-6
- Rakwal, R., Tamogami, S., Agrawal, G. K., & Iwahashi, H. (2002). Octadecanoid signaling component “burst” in rice (Oryza sativa L.) seedling leaves upon wounding by cut and treatment with fungal elicitor chitosan, Biochemical and Biophysical Research Communications, 295(5), 1041-1045, DOI: 10.1016/s0006-291x(02)00779-9
- Sathiyabana M, Balasubramanian R (1998) Chitosan induces resistance components in Arachis hypogaea against leaf rust caused by Puccinia arachidis, Speg. Crop Prot. 17: 307-313.
- Singh, N.P., McCoy, M.T., Tice, R.R., Schneider, E.L. (1988). A simple technique for quantitation of low levels of DNA damage in individual cells, Exp. Cell Res., 175, pp. 184-191, DOI: 10.1016/0014-4827(88)90265-0
- Stephenson, O.J., Trombetta L.D. (2020). Comparative effects of Mancozeb and Disulfiram-induced striated muscle myopathies in Long-Evans rats, Environ. Toxicol. Pharm., 74, Article 103300, DOI:10.1016/j.etap.2019.103300
- Sugeng, A.J., Beamer, P.I., Lutz, E.A., Rosales, C.B. (2013). Hazard-ranking of agricultural pesticides for chronic health effects in Yuma County, Arizona, J. Sci. Total Environ., pp. 463-464, doi: 10.1016/j.scitotenv.2013.05.051
- Tarimorman(2022)https://www.tarimorman.gov.tr/GKGM/Belgeler/DB_Bitki_Koruma _Urunleri/Istatistik/Yillar_Itibariyla_BKU_Kullanim_Miktar_2006-2021.pdf
- Tikhonov, V. E., Stepnova, E. A., Babak, V. G., Yamskov, I. A., Palma-Guerrero, J., Jansson, H. B., et al. (2006). Bactericidal and antifungal activities of a low molecular weight chitosan and its N-/2(3)-(dodec-2-enyl)succinoyl/- derivatives, Carbohydr. Polym. 64, 66–72. doi: 10.1016/j.carbpol.2005.10.021
- Trotel-Aziz, P., Couderchet, M., Vernet, G., and Aziz, A. (2006). Chitosan stimulates defense reactions in grapevine leaves and inhibits development of Botrytis cinerea, Eur. J. Plant Pathol. 114, 405–413. doi: 10.1007/s10658-006-0005-5
- TÜİK (2022) https://data.tuik.gov.tr/Bulten/Index?p=Bitkisel-Uretim-2.Tahmini-2022-45503
Vasconcelos, M. W. (2014). Chitosan and chitooligosaccharide utilization in phytoremediation and biofortification programs: current knowledge and future perspectives, Frontiers in plant science, 5, https://doi.org/10.3389/fpls.2014.00616
- Waterworth, W.M., Kozak, J., Provost, C.M., Bray, C.M., Angelis, K.J., West, C.E. (2009). DNA ligase 1 deficient plants display severe growth defects and delayed repair of both DNA single and double strand breaks, BMC Plant Biol., 9, p. 79, DOI: 10.1186/1471-2229-9-79
- Wise, K. A., Smith, D., Freije, A. S., Mueller, D., Kandel, Y., Allen, T., Bradley, C. A., et al. (2019). Meta-analysis of yield response of foliar fungicide-treated hybrid corn in the United States and Ontario, Canada, Plosone, Published: June 5, https://doi.org/10.1371/journal.pone.0217510
- Yang, M., Xi, X., Wu, X., Lu, R., Zhou, W., Zhang, S., Gao, H. (2015). Vortex-assisted magnetic β-cyclodextrin/attapulgite-linked ionic liquid dispersive liquid–liquid microextraction coupled with high-performance liquid chromatography for the fast determination of four fungicides in water samples, Journal of Chromatography A, Volume 1381, 13 Pages 37-47, https://doi.org/10.1016/j.chroma.2015.01.016
- Yin, H., Li, Y., Zhang, H. Y., Wang, W. X., Lu, H., Grevsen, K., ... & Du, Y. (2013). Chitosan oligosaccharides–triggered innate immunity contributes to oilseed rape resistance against Sclerotinia Sclerotiorum, International Journal of Plant Sciences, 174(4), 722-732, https://doi.org/10.1086/669721
- Zhang, C., Yi, X., Gao, X., Wang, M., Shao, C., Lv, Z., Chen, J., Liu, Z., Shen, C. (2020). Physiological and biochemical responses of tea seedlings (Camellia sinensis) to simulated acid rain conditions, Ecotoxicol. Environ. Saf.192, 110315, https://doi.org/10.1016/j.ecoenv.2020.110315
- Zhang, H., Zhao, X., Yang, J., Yin, H., Wang, W., Lu, H., & Du, Y. (2011). Nitric oxide production and its functional link with OIPK in tobacco defense response elicited by chitooligosaccharide, Plant cell reports, 30(6), 1153-1162, DOI: 10.1007/s00299-011-1024-z
- Zou, P., Tian, X., Dong, B., Zhang, C. (2017). Size effects of chitooligomers with certain degrees of polymerization on the chilling tolerance of wheat seedlings, Carbohydr. Polym. 160, 194–202, DOI: 10.1016/j.carbpol.2016.12.058
Domates (Solanum lycopersicum L.)’te Fungisit Stresine Karşı Kitosanın Etkisi
Year 2023,
Volume: 9 Issue: 3, 499 - 510, 20.09.2023
Hüseyin Bulut
,
Halil İbrahim Öztürk
Abstract
Domates içerdiği besin değerleri, kullanım miktarı ve çeşidi bakımından insanlar için önemli bir besin ögesidir. Domates yetiştiriciliğinde verim kayıplarına neden olan önemli faktörlerden birisi mantar hastalıklarıdır. Bu hastalıklarla mücadelede en hızlı ve etkili çözüm olarak fungisitler kullanılmaktadır. Ancak fungisitlerin kullanımı sonucu oluşan stres ve olası toksik riskler besin zincirini etkilemektedir. Çalışmamızda fungisitin olumsuz etkileri ve buna karşı kitosanın bitki yetiştiriciliğinde stresi azaltmak için kullanımı incelendi. % 80 Mancozeb aktif madde içeren
fungisitin domateste oluşturduğu stresin düzeyi, kitosanın etkileri SOD, CAT ve MDA ekspresyonlarındaki değişimleri tek hücre jel elektroforezi ve DNA üzerindeki hasarı değerlendirildi. Çalışma sonucunda uygulanan fungisitin domates fidelerinde strese, SOD, CAT ve MDA enzim değerlerinde değişime neden olduğu tespit edildi. Fungisitin comet assay analizinde DNA ipliklerinde kırılma sonucu oluşan kuyruk uzunluğu ve kuyruk DNA % değerinde artışa neden olduğu belirlendi. Uygulanan kitosanın enzim değerlerinde ve DNA hasarına karşı bazı dozlarda (100 ppm ve 150 ppm) olumlu etkisinin olduğu gözlendi. Kitosan bitkilerde stres etkenlerine karşı savunma mekanizmasını desteklemek için kullanılabilir.
Supporting Institution
Erzincan Binali Yıldırım Üniversitesi Bilimsel Araştırma Projeleri Koordinatörlüğü (BAP)
Project Number
FBA-2021-765
Thanks
Erzincan Binali Yıldırım Üniversitesi Bilimsel Araştırma Projeleri Koordinatörlüğü (BAP)
References
- Belpoggi, F., Soffritti, M., Guarino, M., Lambertini, L., Cevolani, D., Maltoni, C. (2010). Results of long-term experimental studies on the carcinogenicity of ethylene-bis-dithiocarbamate (Mancozeb) in rats, Ann N Y Acad Sci. 982:123–136, DOI: 10.1111/j.1749-6632.2002.tb04928.x
- Bohmdorfer, G., Schleiffer, A., Brunmeir, R., Ferscha, S., Nizhynska, V., Kozak, J., Angelis, K.J., Kreil, D.P., Schweizer, D. (2011). GMI1, a structural-maintenance-of-chromosomes-hinge domain-containing protein, is involved in somatic homologous recombination in Arabidopsis, Plant Journal, 67, pp. 420-433, DOI: 10.1111/j.1365-313X.2011.04604.x
- Bulut, H. (2020), Mısır (Zea mays L.)’ da Tuz Stresine Karşı Humik Asidin Etkisi, Manas Journal of Agriculture Veterinary and Life Sciences,Vol. 10-1, 11 – 18.
- Camargo Carniel, L.S., Niemeyer, J.C., Iuñes de Oliveira Filho, L.C., Alexandre, D., Gebler, L., Klauberg-Filho, O. (2019). The fungicide mancozeb affects soil invertebrates in two subtropical Brazilian soils, Chemosphere, 232, pp. 180-185, https://doi.org/10.1016/j.chemosphere.2019.05.179
- Chance, B., Maehly, A.C. (1955). Assay of catalases and peroxidases. Methods Enzymol. 2, 764–775.
Collins, A.R. (2004). The comet assay for DNA damage and repair: principles, applications, and limitations, Mol. Biotechnol., 26, pp. 249-261, DOI: 10.1385/MB:26:3:249
- Costa-Silva, D.Gd et al. (2018). N -acetylcysteine inhibits Mancozeb-induced impairments to the normal development of zebrafish embryos, J. Neurotoxicol. Teratol, 68, 1-12, https://doi.org/10.1016/j.ntt.2018.04.003
- Donà, M., Confalonieri, M., Minio, A., Biggiogera, M., Buttafava A., Raimondi, E., Delledonne M., Ventura, L., Sabatini, M.E., Macovei, A., Giraffa, G., Carbonera, D., Balestrazzi, A. (2013). RNA-Seq analysis discloses early senescence and nucleolar dysfunction triggered by Tdp1α depletion in Medicago truncatula, J. Exp. Bot. http://dx.doi.org/10.1093/jxb/ert063.
- Falcon-Rodriguez AB, Costales D, Cabrera JC, Martinez-Tellez MA (2011) Chitosan physico-chemical properties modulate and resistance in tobacco plants against the oomycete Phytophthora nicotianae. Pestic. Biochem. Phys. 100: 221-228.
- Feliziani E, Smilanick JL, Morgosan DA, Mansour MF, , Gu S, Gohil HL, Ames ZR (2013) Preharvest fungucide potassium sorbat or chitosan use on quality and storage decay of table grapes. Plant Dis. 97: 307-314.
- Hartung, F., Angelis, K.J., Meister, A., Schubert, I., Melzer, M., Puchta H. (2002). An archaebacterial topoisomerase homolog not present in other eukaryotes is indispensable for cell proliferation of plants, Curr. Biol., 12, pp. 1787-1791, DOI: 10.1016/s0960-9822(02)01218-6
- Heitzberg, F., Chen, I.-P., Hartung, F., Orel, N., Angelis, K.J., Puchta, H. (2004). The Rad17 homologue of Arabidopsis is involved in the regulation of DNA damage repair and homologous recombination, Plant J., 38, pp. 954-968, DOI: 10.1111/j.1365-313X.2004.02097.x
- Jeggo, P.A. (2010). A break is not the End; insight into the damage response to DNA double strand breaks, DNA Repair, 9, pp. 1217-1218, DOI: 10.1016/j.dnarep.2010.09.021
- Jennifer, R., Joan, F., Jeannie, E., Da L. (2017). A systematic review of Mancozeb as a reproductive and developmental hazard, J. Environ. Int., 99, DOI: 10.1016/j.envint.2016.11.006
- Kamisugi, Y., Schaefer, D.G., Kozak, J., Charlot, F., Vrielynck, N., Hola, M., Angelis, K.J., Cuming, A.C., Nogue, F. (2012). MRE11 and RAD50, but not NBS1 are essential for gene targeting in the moss Physcomitrella patens, Nucleic Acids Res., 40 pp. 3496-3510, doi: 10.1093/nar/gkr1272
- Kaushik G., Satya S., Naik S.N. (2009). Food processing a tool to pesticide residue dissipation – A review, Food Research International 42(1):26-40, DOI: 10.1016/j.foodres.2008.09.009
- Kleinkauf, N., Verweij, P.E., Arendrup, M.C., Donnelly, P.J., Cuenca-Estrella, M., Fraaije, B., et al. (2013). Risk assessment on the impact of environmental usage of triazoles on the development and spread of resistance to medical triazoles in Aspergillus species European Centre for Disease Prevention and Control Technical Report, ECDC, Stockholm, DOI: 10.2900/76274
- Kontou, S., Tsipi, D., Tzia, C. (2004). Stability of the dithiocarbamate pesticide maneb in tomato homogenates during cold storage and thermal processing, J. Food Addit. Contam.: Part A, 21, https://doi.org/10.1080/02652030400019372
- Kozak, J., West, C.E., White, C., Costa-Nunes, J.A. da, Angelis, K.J. (2009). Rapid repair of DNA double strand breaks in Arabidopsis is dependent on proteins involved in chromosome structure maintenance, DNA Repair, 8, pp. 413-419, DOI: 10.1016/j.dnarep.2008.11.012
- Lenucci, M. S., Cadinu, D., Taurino, M., Piro, G., Dalessandro, G. (2006). Antioxidant Composition in Cherry and High-Pigment Tomato Cultivars, J. Agric. Food Chem, 54, 7, 2606–2613, https://doi.org/10.1021/jf052920c
- Malerba, M., Cerana, R. (2016). Chitosan effects on plant systems, International journal of molecular sciences, 17(7), 996, DOI: 10.3390/ijms17070996
- Narasimhamurthy, K., Udayashankar, A. C., Britto, S.D., et al. (2022). Chitosan and chitosan-derived nanoparticles modulate enhanced immune response in tomato against bacterial wilt disease. International Journal of Biological Macromolecules, 220, 223-237. doi.org/10.1016/j.ijbiomac.2022.08.054
- Ong, K. (2011). Basic plant pathology training pathogenic agents. Agi Life Extension Texas, pp 1.
- Ostling, O., Johansons, K.J. (1984). Microelectrophoretic study of radiation-induced DNA damage in individual mammalian cells, BBRC, 123, pp. 291-298, DOI: 10.1016/0006-291x(84)90411-x
- Paoletti, F., Aldinucci, D., Mocali, A. et al.(1986). A sensitive spectrophotometric method for the determination of superoxide dismutase activity in tissue extracts, Anal. Biochem. 154, 536–541, DOI: 10.1016/0003-2697(86)90026-6
- Rakwal, R., Tamogami, S., Agrawal, G. K., & Iwahashi, H. (2002). Octadecanoid signaling component “burst” in rice (Oryza sativa L.) seedling leaves upon wounding by cut and treatment with fungal elicitor chitosan, Biochemical and Biophysical Research Communications, 295(5), 1041-1045, DOI: 10.1016/s0006-291x(02)00779-9
- Sathiyabana M, Balasubramanian R (1998) Chitosan induces resistance components in Arachis hypogaea against leaf rust caused by Puccinia arachidis, Speg. Crop Prot. 17: 307-313.
- Singh, N.P., McCoy, M.T., Tice, R.R., Schneider, E.L. (1988). A simple technique for quantitation of low levels of DNA damage in individual cells, Exp. Cell Res., 175, pp. 184-191, DOI: 10.1016/0014-4827(88)90265-0
- Stephenson, O.J., Trombetta L.D. (2020). Comparative effects of Mancozeb and Disulfiram-induced striated muscle myopathies in Long-Evans rats, Environ. Toxicol. Pharm., 74, Article 103300, DOI:10.1016/j.etap.2019.103300
- Sugeng, A.J., Beamer, P.I., Lutz, E.A., Rosales, C.B. (2013). Hazard-ranking of agricultural pesticides for chronic health effects in Yuma County, Arizona, J. Sci. Total Environ., pp. 463-464, doi: 10.1016/j.scitotenv.2013.05.051
- Tarimorman(2022)https://www.tarimorman.gov.tr/GKGM/Belgeler/DB_Bitki_Koruma _Urunleri/Istatistik/Yillar_Itibariyla_BKU_Kullanim_Miktar_2006-2021.pdf
- Tikhonov, V. E., Stepnova, E. A., Babak, V. G., Yamskov, I. A., Palma-Guerrero, J., Jansson, H. B., et al. (2006). Bactericidal and antifungal activities of a low molecular weight chitosan and its N-/2(3)-(dodec-2-enyl)succinoyl/- derivatives, Carbohydr. Polym. 64, 66–72. doi: 10.1016/j.carbpol.2005.10.021
- Trotel-Aziz, P., Couderchet, M., Vernet, G., and Aziz, A. (2006). Chitosan stimulates defense reactions in grapevine leaves and inhibits development of Botrytis cinerea, Eur. J. Plant Pathol. 114, 405–413. doi: 10.1007/s10658-006-0005-5
- TÜİK (2022) https://data.tuik.gov.tr/Bulten/Index?p=Bitkisel-Uretim-2.Tahmini-2022-45503
Vasconcelos, M. W. (2014). Chitosan and chitooligosaccharide utilization in phytoremediation and biofortification programs: current knowledge and future perspectives, Frontiers in plant science, 5, https://doi.org/10.3389/fpls.2014.00616
- Waterworth, W.M., Kozak, J., Provost, C.M., Bray, C.M., Angelis, K.J., West, C.E. (2009). DNA ligase 1 deficient plants display severe growth defects and delayed repair of both DNA single and double strand breaks, BMC Plant Biol., 9, p. 79, DOI: 10.1186/1471-2229-9-79
- Wise, K. A., Smith, D., Freije, A. S., Mueller, D., Kandel, Y., Allen, T., Bradley, C. A., et al. (2019). Meta-analysis of yield response of foliar fungicide-treated hybrid corn in the United States and Ontario, Canada, Plosone, Published: June 5, https://doi.org/10.1371/journal.pone.0217510
- Yang, M., Xi, X., Wu, X., Lu, R., Zhou, W., Zhang, S., Gao, H. (2015). Vortex-assisted magnetic β-cyclodextrin/attapulgite-linked ionic liquid dispersive liquid–liquid microextraction coupled with high-performance liquid chromatography for the fast determination of four fungicides in water samples, Journal of Chromatography A, Volume 1381, 13 Pages 37-47, https://doi.org/10.1016/j.chroma.2015.01.016
- Yin, H., Li, Y., Zhang, H. Y., Wang, W. X., Lu, H., Grevsen, K., ... & Du, Y. (2013). Chitosan oligosaccharides–triggered innate immunity contributes to oilseed rape resistance against Sclerotinia Sclerotiorum, International Journal of Plant Sciences, 174(4), 722-732, https://doi.org/10.1086/669721
- Zhang, C., Yi, X., Gao, X., Wang, M., Shao, C., Lv, Z., Chen, J., Liu, Z., Shen, C. (2020). Physiological and biochemical responses of tea seedlings (Camellia sinensis) to simulated acid rain conditions, Ecotoxicol. Environ. Saf.192, 110315, https://doi.org/10.1016/j.ecoenv.2020.110315
- Zhang, H., Zhao, X., Yang, J., Yin, H., Wang, W., Lu, H., & Du, Y. (2011). Nitric oxide production and its functional link with OIPK in tobacco defense response elicited by chitooligosaccharide, Plant cell reports, 30(6), 1153-1162, DOI: 10.1007/s00299-011-1024-z
- Zou, P., Tian, X., Dong, B., Zhang, C. (2017). Size effects of chitooligomers with certain degrees of polymerization on the chilling tolerance of wheat seedlings, Carbohydr. Polym. 160, 194–202, DOI: 10.1016/j.carbpol.2016.12.058