Seed priming with ZnO nanoparticles promotes early growth and bioactive compounds of Moringa oleifera

Authors

  • Carlos A. GARZA-ALONSO Universidad Autónoma Agraria Antonio Narro, Doctorado en Ciencias en Agricultura Protegida, Calzada Antonio Narro 1923, Buenavista, Saltillo, Coahuila (MX)
  • Yolanda GONZÁLEZ-GARCÍA Universidad Autónoma Agraria Antonio Narro, Doctorado en Ciencias en Agricultura Protegida, Calzada Antonio Narro 1923, Buenavista, Saltillo, Coahuila (MX)
  • Gregorio CADENAS-PLIEGO Centro de Investigación en Química Aplicada, Enrique Reyna H. 140, San José de los Cerritos, 25294, Saltillo, Coahuila (MX)
  • Emilio OLIVARES-SÁENZ Universidad Autónoma de Nuevo León, Facultad de Agronomía, Francisco Villa s/n, ExHacienda el Canadá, Gral. Escobedo, Nuevo León (MX)
  • Libia I. TREJO-TÉLLEZ Colegio de Postgraduados, Programa de Edafología, Carretera México-Texcoco km 36.5, Montecillo, Texcoco, Estado de México (MX)
  • Adalberto BENAVIDES-MENDOZA Universidad Autónoma Agraria Antonio Narro, Departamento de Horticultura, Calzada Antonio Narro 1923, Buenavista, Saltillo, Coahuila (MX)

DOI:

https://doi.org/10.15835/nbha49412546

Keywords:

Antioxidants, germination, hormesis, nanomaterials

Abstract

DOI: 10.15835/nbha49412546

Nanotechnology has gained importance in agricultural production systems, with various applications such as pesticides or fertilizers. The application of nanomaterials (NMs) as a pretreatment to seeds (seed priming) has positively affected plant growth and development. On the other hand, Moringa oleifera is a plant appreciated for its multiple nutraceutical properties. Therefore, the objective of this study was to evaluate the effect of pretreatment of M. oleifera seeds with ZnO nanoparticles (NZnO) (0, 0.5, 2.5, 5, 7.5, and 10 mg L-1). The study was divided into two experimental phases: the first phase consisted of evaluating germination under laboratory conditions (25 °C) at 15 DAS, while in the second phase, vegetative growth and bioactive compounds were evaluated at 45 DAS under greenhouse conditions. For phase one, the percentage of germination, length, and dry weight of the plumule and radicle were considered, and the vigor indices of seeds were determined. In phase two, we measured the plant height, stem diameter, fresh and dry biomass of aerial and root parts, and the concentration of photosynthetic pigments, phenolic compounds, flavonoids, vitamin C, glutathione (GSH), and antioxidant capacity (DPPH), such as the activity of antioxidant enzymes such as ascorbate peroxidase (APX), catalase (CAT), glutathione peroxidase (GPX), and phenylalanine ammonium lyase (PAL). The results showed an increase in some variables related to seed germination, with an increase of between 30 and 25% in the vigor of the seeds subjected to 2.5 and 10 mg L-1 NZnO. The photosynthetic pigments resulted in increases of between 23 and 49% for the 7.5-10 mg L-1 NZnO treatments. Regarding bioactive compounds, the increase in phenols, flavonoids and vitamin C stands out, mainly at the levels of 7.5-10 mg L-1 NZnO, where increases of up to 543% were observed with respect to the control. The enzymatic activity showed different responses to the application of NZnO, where a biphasic response (hormesis) was observed on the activity of APX and CAT activities as the levels of NZnO increased. The results show that it is possible to promote the initial growth and bioactive compounds of M. oleifera by pretreatment of seeds mainly with 10 mg L-1 NZnO.

Metrics

Metrics Loading ...

References

Abbasi KM, Moameri M, Asgari LB, Astatkie T (2021). Influence of nano-priming on seed germination and plant growth of forage and medicinal plants. Plant Growth Regulation 93:13-28. https://doi.org/10.1007/s10725-020-00670-9

Abdel Latef AAH, Abu Alhmad MF, Abdelfattah KE (2017). The possible roles of priming with ZnO nanoparticles in mitigation of salinity stress in lupine (Lupinus termis) Plants. Plant Growth Regulation 36:60-70. https://doi.org/10.1007/s00344-016-9618-x

Abdel-Aziz HMM, Hasaneen MNA, Omer AM (2019). Impact of engineered nanomaterials either alone or loaded with NPK on growth and productivity of french bean plants: Seed priming vs foliar application. South African Journal of Botany 125:102-108. https://doi.org/10.1016/j.sajb.2019.07.005

Adhikari T, Kundu S, Rao AS (2016). Zinc delivery to plants through seed coating with nano-zinc oxide particles. Journal of Plant Nutrition 39:136-146. https://doi.org/10.1080/01904167.2015.1087562

Agathokleous E, Feng ZZ, Iavicoli I, Calabrese EJ (2019). The two faces of nanomaterials: A quantification of hormesis in algae and plants. Environment International 131:105044. https://doi.org/10.1016/j.envint.2019.105044

Akdemir H (2021). Evaluation of transcription factor and aquaporin gene expressions in response to Al2O3 and ZnO nanoparticles during barley germination. Plant Physiology and Biochemistry 166:466-476. https://doi.org/10.1016/j.plaphy.2021.06.018

Alcántar GG, Sandoval VM (1999). Handbook Chemical Analysis of Vegetal Tissue. Especial Publication No. 10; Mexican Society of Soil Science, Chapingo, Mexico.

Arvouet-Grand A, Vennat B, Pourrat A, Legret P (1994). Standardization of a propolis extract and identification of the main constituents. Journal de Pharmacie de Belgique 49:462-468.

Bose B, Kumar M, Singhal R, Mondal S (2018). Impact of seed priming on the modulation of physico-chemical and molecular processes during germination, growth, and development of crops. In: Rakshit A, Singh HB (Eds). Advances in Seed Priming. Springer Nature Singapore, pp 23-40. https://doi.org/10.1007/978-981-13-0032-5_2

Bradford MM (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72:248-254. https://doi.org/10.1016/0003-2697(76)90527-3

Brand-Williams W, Cuvelier ME, Berset C (1995). Use of a free radical method to evaluate antioxidant activity. Food Science and Technology 28(1):25–30. https://doi.org/10.1016/S0023-6438(95)80008-5

Carballo-Méndez FJ, Olivares-Sáenz E, Bolívar-Duarte M, Antonio-Bautista A, Vázquez-Badillo ME, Niño-Medina G (2019). Effect of silicon on germination of Moringa oleifera Lam. in different types of salts. Fresenius Environmental 28:8823-8830.

Caverzan A, Giacomin R, Müller M, Biazus C, Lângaro NC, Chavarria G (2018). How does seed vigor affect soybean yield components? Agronomy Journal 110:1318-1327. https://doi.org/10.2134/agronj2017.11.0670

Chen K, Arora R (2013). Priming memory invokes seed stress-tolerance. Environmental and Experimental Botany 94:33-45. https://doi.org/10.1016/j.envexpbot.2012.03.005

Dhindsa RS, Plumb-Dhindsa P, Thorpe TA (1981). Leaf senescence: Correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. Journal of Experimental Botany 32:93-101. https://doi.org/10.1093/jxb/32.1.93

Doğaroğlu ZG, Köleli N (2017). TiO2 and ZnO nanoparticles toxicity in barley (Hordeum vulgare L.). Clean - Soil, Air, Water 45:1700096. https://doi.org/10.1002/clen.201700096

Flohé L, Günzler WA (1984). Assays of glutathione peroxidase. Methods in Enzymology 105:114-120. https://doi.org/10.1016/S0076-6879(84)05015-1

García-López JI, Zavala-García F, Olivares-Saénz E, Lira-Saldívar RH, Barriga-Castro ED, Ruiz-Torres NA, … Niño-Medina G, (2018). Zinc Oxide nanoparticles boosts phenolic compounds and antioxidant activity of Capsicum annuum L. during germination. Agronomy 8:215. https://doi.org/10.3390/agronomy8100215

Ghosh M, Jana A, Sinha S, Jothiramajayam M, Nag A, Chakraborty A, Mukherjee A, Mukherjee A (2016). Effects of ZnO nanoparticles in plants: Cytotoxicity, genotoxicity, deregulation of antioxidant defenses, and cell-cycle arrest. Mutation Research/Genetic Toxicology and Environmental Mutagenesis 807:25-32. https://doi.org/10.1016/j.mrgentox.2016.07.006

Hajra A, Mondal NK (2017). Effects of ZnO and TiO2 nanoparticles on germination, biochemical and morphoanatomical attributes of Cicer arietinum L. Energy, Ecology and Environment 2:277-288. https://doi.org/10.1007/s40974-017-0059-6

Hoe PT, Mai NC, Lien LQ, Ban NK, Van Minh C, Chau NH, … Linh TM (2018). Germination responses of soybean seeds under Fe, ZnO, Cu and Co nanoparticle treatments. International Journal of Agriculture and Biology 20(7):1562–1568. https://doi.org/10.17957/IJAB/15.0670

Hussein MM, Abou-Baker NH (2018). The contribution of nano-zinc to alleviate salinity stress on cotton plants. Royal Society Open Science 5:171809. https://doi.org/10.1098/rsos.171809

Itroutwar PD, Kasivelu G, Raguraman V, Malaichamy K, Sevathapandian SK (2020). Effects of biogenic zinc oxide nanoparticles on seed germination and seedling vigor of maize (Zea mays). Biocatalysis and Agricultural Biotechnology 29:101778. https://doi.org/10.1016/j.bcab.2020.101778

Juárez-Maldonado A, González-Morales S, Cabrera-De la Fuente M, Medrano-Macías J, Benavides-Mendoza A (2018). Nanometals as promoters of nutraceutical quality in crop plants. In: Grumezescu AM, Holban AM (Eds). Impact of Nanoscience in the Food Industry. Elsevier Inc., pp 277-310. https://doi.org/10.1016/c2016-0-00498-9

Juárez-Maldonado A, Ortega-Ortíz H, Cadenas-Pliego G, Valdés-Reyna J, Pinedo-Espinoza JM, López-Palestina CU, Hernández-Fuentes AD (2018). Foliar application of Cu nanoparticles modified the content of bioactive compounds in Moringa oleifera Lam. Agronomy 8:167. https://doi.org/10.3390/agronomy8090167

Juárez-Maldonado A, Ortega-Ortíz H, Morales-Díaz AB, González-Morales S, Morelos-Moreno Á, Cabrera-De la Fuente M, … Benavides-Mendoza A (2019). Nanoparticles and nanomaterials as plant biostimulants. International Journal of Molecular Sciences 20:162. https://doi.org/10.3390/ijms20010162

Juárez-Maldonado A, Tortella G, Rubilar O, Fincheira P, Benavides-Mendoza A (2021). Biostimulation and toxicity: The magnitude of the impact of nanomaterials in microorganisms and plants. Journal of Advanced Research 31:113-126. https://doi.org/10.1016/j.jare.2020.12.011

Klein BP, Perry AK (1982). Ascorbic acid and vitamin A activity in selected vegetables from different geographical areas of the United States. Journal of Food Science 47:941-945. https://doi.org/10.1111/j.1365-2621.1982.tb12750.x

Kondhare KR, Farrell AD, Kettlewell PS, Hedden P, Monaghan JM (2015). Pre-maturity α-amylase in wheat: The role of abscisic acid and gibberellins. Journal of Cereal Science 63:95-108. https://doi.org/10.1016/j.jcs.2015.03.004

Li Y, Liang L, Li W, Ashraf U, Ma L, Tang X, Pan S, Tian H, Mo Z (2021). ZnO nanoparticle-based seed priming modulates early growth and enhances physio-biochemical and metabolic profiles of fragrant rice against cadmium toxicity. Journal of Nanobiotechnology 19:75. https://doi.org/10.1186/s12951-021-00820-9

Liu R, Zhang H, Lal R (2016). Effects of stabilized nanoparticles of copper, zinc, manganese, and iron oxides in low concentrations on lettuce (Lactuca sativa) seed germination: nanotoxicants or nanonutrients? Water, Air, & Soil Pollution 227:42. https://doi.org/10.1007/s11270-015-2738-2

López-Vargas ER, González-García Y, Pérez-Álvarez M, Cadenas-Pliego G, González-Morales S, Benavides-Mendoza A, … Juárez-Maldonado A (2020). Seed priming with carbon nanomaterials to modify the germination, growth, and antioxidant status of tomato seedlings. Agronomy 10:639. https://doi.org/10.3390/agronomy10050639

Ma ZF, Ahmad J, Zhang H, Khan I, Muhammad S (2020). Evaluation of phytochemical and medicinal properties of Moringa (Moringa oleifera) as a potential functional food. South African Journal of Botany 129:40-46. https://doi.org/10.1016/j.sajb.2018.12.002

Majeed A, Muhammad Z, Islam S, Ahmad H (2019). Salinity imposed stress on principal cereal crops and employing seed priming as a sustainable management approach. Acta Ecologica Sinica 39(4):280-283. https://doi.org/10.1016/j.chnaes.2018.09.004

Mallhi ZI, Rizwan M, Mansha A, Ali Q, Asim S, Ali S, Hussain A, Alrokayan SH, Khan HA, Alam P, Ahmad P (2019). Citric acid enhances plant growth, photosynthesis, and phytoextraction of lead by alleviating the oxidative stress in castor beans. Plants 8:525. https://doi.org/10.3390/plants8110525

Meza-Carranzo Z, Olivares-Sáenz E, Gutiérrez-Ornelas E, Bernal-Barragán H, Aranda-Ruíz J, Vázquez-Alvarado RE, Carranza-de la Rosa R (2016). Crecimiento y producción de biomasa de moringa (Moringa oleifera Lam.) bajo las condiciones climáticas del Noreste de México. Tecnociencia Chihuahua 10:143-153.

Molnár Á, Rónavári A, Bélteky P, Szőllősi R, Valyon E, Oláh D, Rázga Z, Ördög A, Kónya Z, Kolbert Z (2020). ZnO nanoparticles induce cell wall remodeling and modify ROS/ RNS signalling in roots of Brassica seedlings. Ecotoxicology and Environmental Safety 206:111158. https://doi.org/10.1016/j.ecoenv.2020.111158

Munir T, Rizwan M, Kashif M, Shahzad A, Ali S, Amin N, Zahid R, Alam MFE, Imran M (2018). Effect of zinc oxide nanoparticles on the growth and Zn uptake in wheat (Triticum aestivum L.) by seed priming method. Digest Journal of Nanomaterials and Biostructures 13:315-323.

Nagata M, Yamashita I (1992). Simple method for simultaneous determination of chlorophyll and carotenoids in tomato fruit. Journal of Japanese Society Food Science and Technology 39:925-928. https://doi.org/10.3136/nskkk1962.39.925

Nakano Y, Asada K (1987). Purification of ascorbate peroxidase in spinach chloroplasts; its inactivation in ascorbate-depleted medium and reactivation by monodehydroascorbate radical. Plant Cell Physiology 28:131-140. https://doi.org/10.1093/oxfordjournals.pcp.a077268

Neto ME, Britt DW, Lara LM, Cartwright A, Dos Santos RF, Inoue TT, Batista MA (2020). Initial development of corn seedlings after seed priming with nanoscale synthetic zinc oxide. Agronomy 10:307. https://doi.org/10.3390/agronomy10020307

Pandey P, Singh J, Achary VMM, Mallireddy Reddy K (2015). Redox homeostasis via gene families of ascorbate-glutathione pathway. Frontiers in Environmental Science 3:25. https://doi.org/10.3389/fenvs.2015.00025

Patil SA, Shinde DV, Ahn DY, Patil DV, Tehare KK, Jadhav VV, Lee JK, Mane RS, Shrestha NK, Han SH (2014). A simple, room temperature, solid-state synthesis route for metal oxide nanostructures. Journal of Materials Chemistry A 33:13519-13526. https://doi.org/10.1039/c4ta02267j

Patterson BD, MacRae EA, Ferguson IB (1984). Estimation of hydrogen peroxide in plant extracts using titanium (IV). Analytical Biochemistry 139(2):487-492. https://doi.org/10.1016/0003-2697(84)90039-3

Pereira ADES, Oliveira HC, Fraceto LF, Santaella C (2021). Nanotechnology potential in seed priming for sustainable agriculture. Nanomaterials 11:1-29. https://doi.org/10.3390/nano11020267

Rai-Kalal P, Jajoo A (2021). Priming with zinc oxide nanoparticles improve germination and photosynthetic performance in wheat. Plant Physiology and Biochemistry 160:341-351. https://doi.org/10.1016/j.plaphy.2021.01.032

Rajjou L, Duval M, Gallardo K, Catusse J, Bally J, Job C, Job D (2012). Seed germination and vigor. Annual Reviews of Plant Biology 63:507-533. https://doi.org/10.1146/annurev-arplant-042811-105550

Rao MJ, Hussain S, Anjum MA, Saqib M, Ahmad R, Khalid MF, … Ahmad S (2019). Effect of Seed Priming on Seed Dormancy and Vigor. In: Hasanuzzaman M, Fotopolus V (Eds). Priming and Pretreatment of Seeds and Seedlings. Springer Nature Singapore, pp 135-145. https://doi.org/10.1007/978-981-13-8625-1_6

Reis S, Pavia I, Carvalho A, Moutinho-Pereira J, Correia C, Lima-Brito J (2018). Seed priming with iron and zinc in bread wheat: effects in germination, mitosis and grain yield. Protoplasma 255:1179-1194. https://doi.org/10.1007/s00709-018-1222-4

Rochaix JD, Bassi R (2019). LHC-like proteins involved in stress responses and biogenesis/repair of the photosynthetic apparatus. Biochemistry Journal 476:581-593. https://doi.org/10.1042/BCJ20180718

Ruiz-Torres N, Flores-Naveda A, Barriga-Castro ED, Camposeco-Montejo N, Ramírez-Barrón S, Borrego-Escalante F, … García-López JI (2021). Zinc oxide nanoparticles and zinc sulfate impact physiological parameters and boosts lipid peroxidation in soil grown coriander plants (Coriandrum sativum). Molecules 26:1998. https://doi.org/10.3390/molecules26071998

Savassa SM, Duran NM, Rodrigues ES, De Almeida E, Van Gestel CAM, Bompadre TFV, De Carvalho HWP (2018). Effects of ZnO nanoparticles on Phaseolus vulgaris germination and seedling development determined by X-ray spectroscopy. ACS Applied Nano Materials 1:6414-6426. https://doi.org/10.1021/acsanm.8b01619

Seyyedi SM, Khajeh-Hosseini M, Moghaddam PR, Shahandeh H (2015). Effects of phosphorus and seed priming on seed vigor, fatty acids composition and heterotrophic seedling growth of black seed (Nigella sativa L.) grown in a calcareous soil. Industrial Crops and Products 74:939-949. https://doi.org/10.1016/j.indcrop.2015.05.082

Sharma A, Patni B, Shankhdhar D, Shankhdhar SC (2013). Zinc - an indispensable micronutrient. Physiology and Molecular Biology of Plants 19:11-20. https://doi.org/10.1007/s12298-012-0139-1

Sher A, Sarwar T, Nawaz A, Ijaz M, Sattar A, Ahmad S (2019). Methods of seed priming. In: Hasanuzzaman M, Fotopoulos V (Eds). Priming and Pretreatment of Seeds and Seedlings. Springer, Singapore, pp 1-10. https://doi.org/10.1007/978-981-13-8625-1_1

Singh A, Singh NB, Hussain I, Singh H, Yadav V, Singh SC (2016). Green synthesis of nano zinc oxide and evaluation of its impact on germination and metabolic activity of Solanum lycopersicum. Journal of Biotechnology 233:84-94. https://doi.org/10.1016/j.jbiotec.2016.07.010

Singleton VL, Orthofer R, Lamuela-Raventos RM (1999). Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin Ciocalteau reagent. Methods in Enzymology 299:152-178.

Smirnoff N (2018). Ascorbic acid metabolism and functions: A comparison of plants and mammals. Free Radical Biology and Medicine 122:116-129. https://doi.org/10.1016/j.freeradbiomed.2018.03.033

Solanki P, Laura JS (2018). Effect of ZnO nanoparticles on seed germination and seedling growth in wheat (Triticum aestivum). Journal of Pharmacognosy and Phytochemistry 7(5):2048-2052.

Steiner AA (1961). A universal method for preparing nutrient solutions of a certain desired composition. Plant and Soil 15(2):134-154. https://doi.org/10.1007/BF01347224

Sturikova H, Krystofova O, Huska D, Adam V (2018). Zinc, zinc nanoparticles and plants. Journal of Hazardous Materials 349:101-110. https://doi.org/10.1016/j.jhazmat.2018.01.040

Suekawa M, Fujikawa Y, Esaka M (2018). Physiological role of ascorbic acid recycling enzymes in plants. In: Hossain MA, Munné-Bosch S, Burrit DJ, Díaz-Vivancos P, Fujita P, Lorence M (Eds). Ascorbic Acid in Plant Growth, Development and Stress Tolerance. Springer Nature Singapore, pp 355-373. https://doi.org/10.1007/978-3-319-74057-7_14

Sykłowska-Baranek K, Pietrosiuk A, Naliwajski MR, Kawiak A, Jeziorek M, Wyderska S, Łojkowska E, Chinou I (2012). Effect of l-phenylalanine on PAL activity and production of naphthoquinone pigments in suspension cultures of Arnebia euchroma (Royle) Johnst. In Vitro Cellular & Developmental Biology – Plant 48:555-564. https://doi.org/10.1007/s11627-012-9443-2

Tondey M, Kalia A, Singh A, Dheri GS, Taggar MS, Nepovimova E, Krejcar O, Kuca K (2021). Seed priming and coating by nano-scale zinc oxide particles improved vegetative growth, yield, and quality of fodder maize (Zea mays). Agronomy 11:729. https://doi.org/10.3390/agronomy11040729

Tymoszuk A, Wojnarowicz J (2020). Zinc oxide and zinc oxide nanoparticles impact on in vitro germination and seedling growth in Allium cepa L. Materials 13:2784. https://doi.org/10.3390/ma13122784

Uarrota VG, Stefen DLV, Leolato LS, Gindri DM, Nerling D (2018). Revisiting carotenoids and their role in plant stress responses: From biosynthesis to plant signaling mechanisms during stress. In: Gupta DK, Palma JM, Corpas F (Eds). Antioxidants and Antioxidant Enzymes in Higher Plants. Springer International Publishing AG, pp 207-32. https://doi.org/10.1007/978-3-319-75088-0_10

Wang P, Grimm B (2021). Connecting chlorophyll metabolism with accumulation of the photosynthetic apparatus. Trends in Plant Sciences. 26:484-495. https://doi.org/10.1016/j.tplants.2020.12.005

Waqas M, Korres NE, Khan MD, Nizami AS, Deeba F, Ali I, Hussain H (2019). Advances in the concept and methods of seed priming. In: Hasanuzzaman M, Fotopoulos V (Eds). Priming and Pretreatment of Seeds and Seedlings. Springer, Singapore, pp 11-41. https://doi.org/10.1007/978-981-13-8625-1_2

Xue T, Hartikainen H, Piironen V (2001). Antioxidative and growth-promoting effect of selenium on senescing lettuce. Plant Soil 237:55-61. https://doi.org/10.1023/A:1013369804867

Zhang J, Wang S, Song S, Xu F, Pan Y, Wang H (2019). Transcriptomic and proteomic analyses reveal new insight into chlorophyll synthesis and chloroplast structure of maize leaves under zinc deficiency stress. Journal of Proteomics 199:123-134. https://doi.org/10.1016/j.jprot.2019.03.001

Downloads

Published

2021-11-30

How to Cite

GARZA-ALONSO, C. A., GONZÁLEZ-GARCÍA, Y., CADENAS-PLIEGO, G., OLIVARES-SÁENZ, E., TREJO-TÉLLEZ, L. I., & BENAVIDES-MENDOZA, A. (2021). Seed priming with ZnO nanoparticles promotes early growth and bioactive compounds of Moringa oleifera. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 49(4), 12546. https://doi.org/10.15835/nbha49412546

Issue

Section

Research Articles
CITATION
DOI: 10.15835/nbha49412546

Most read articles by the same author(s)