Effect of Putrescine and Nitric Oxide on Morphological, Biochemical and Postharvest Characteristics of Rose ‘Avalanche’

علوم باغبانی

Article 14, Volume 36, Issue 1 - Serial Number 53, March 2022, Pages 193-212   

Document Type: Research Article

DOI: 10.22067/jhs.2021.69604.1036

Authors

R. Abdi; Z. Jabbarzadeh^*

Department of Horticultural Science, Faculty of Agriculture, Urmia University, Urmia, Iran

Abstract

Introduction
 The genus Rosa from the family Rosaceae with over 150 species is one of the most important ornamental plants in the world. From a commercial point of view, cut roses play a key role in trade of cut flowers. Nitric oxide regulates key physiological processes that depend on the concentration of this compound such as hypocotyls growth, defensive responses, growth and development, photosynthesis, and phytoalexin generation in stressful conditions. Polyamines are key biomolecules that have a role to play in the regulation of many plants’ growth and development processes and their responses to different environmental stimuli. This study was performed to investigate the effect of foliar application of sodium nitroprusside (as a NO donor) and putrescine (as a polyamine) on ‘Avalanche’ rose in hydroponic conditions.
Materials and Methods
 This study was conducted in the research and production greenhouses of Urmia University and the research laboratory of the Department of Horticultural Sciences of the Faculty of Agriculture in 2019-2020 on rose (Rosa hybrida ‘Avalanche). This experiment was conducted as a factorial trial based on completely randomized design with two factors including sodium nitroprusside in four concentrations of 0, 50, 100 and 200 μM and putrescine in four concentrations of 0, 1, 2 and 4 mM with 3 replications as a foliar application under hydroponic conditions in greenhouses and in pots. The treatments were applied two weeks after transplantation, every 15 day-interval for 4 months. In order to investigate the effects of putrescine and sodium nitroprusside on some morphological and physiological characteristics of plants, two weeks after the end of treatments, sampling was performed to measure morphological and physiological characteristics. The measured indicators included: fresh and dry weight of flowering stem, chlorophyll a, b and total chlorophyll, carotenoids and also in the postharvest stage were guaiacol peroxidase and ascorbate peroxidase enzymes activity and bending of flowering stem. The SAS software version 9.2 was used to analyze the variance and compare the mean of the studied traits. Comparison of means was performed using the Tukey’s range test method at a probability level of 1 and 5%. Also, Excel (2016) software was used to draw the graph.
Results
 According to the means comparison of measured parameters, sodium nitroprusside along with putrescine increase the flowering stem fresh and dry weight, photosynthetic pigments of leaves and antioxidant enzymes activities at the postharvest stages. Sodium nitroprusside at a concentration of 50 μM with 4 mM putrescine increased the fresh and dry weight of the flowering stem. Also, the concentration of 100 μM sodium nitroprusside with 4 mM putrescine significantly increased chlorophyll a, b, total chlorophyll and carotenoid content compared to control. It should be noted that preharvest application of sodium nitroprusside along with putrescine cause to improve postharvest characteristics of rose. In this research, application of 100 and 200 μM SNP alone or with different concentrations of putrescine increased guaiacol peroxidase and ascorbate peroxidase activity and reduced bending of flowering stem of rose ‘Avalanche’ at the postharvest stage. Probably polyamines (such as putrescine) and nitric oxide increase photosynthesis potential with increasing photosynthetic pigments and protecting cell membranes thus increase growth and flowering traits of plants such as increasing the flowering stem weight of rose in this research. At postharvest stage, senescence of flowers is an inevitable phenomenon that cause to produce free radicles in plants. Free radicles injure the plant membranes lipids and change the antioxidant enzymes activities. This despite the fact that nitric oxide and putrescine protect antioxidant enzymes against free radicles as a result can improve vase life of rose.   
Conclusion
 Based on the results of the present study, it can be concluded that putrescine, with SNP, improves growth characteristics as well as increases the postharvest traits and quality of cut flowers of rose.  According to the results, it is observed that among the different concentrations of putrescine, the concentration of 4 mM had the greatest effect on the growth and physiological parameters of rose while the concentration of 100 and 200 μM sodium nitroprusside had a greatest effect on physiological characteristics and postharvest traits of rose. In general, both SNP and putrescine had a positive and favorable effects on improving growth and postharvest indices, but the effective concentration varied depending on the type of parameter.

Keywords

Antioxidant enzymes; Polyamine; Sodium nitroprusside; Stem neck

References

1. Abdel Aziz N.G., Taha Lobna S., and Ibrahim Soad M.M. Some studies on the effect of putrescine, ascorbic acid and thiamine on growth, flowering and some chemical constituent of Gladiolous plants at Nuberia. Ozean. Journal of Applied Sciences 2(2): 169-179.
2. Arab S., Baradaran Firoz Abadi M., Asghari A., and Rahimi M. The effect of foliar application of ascorbic acid and sodium nitroprusside on grain protein content, yield and some agronomic traits of safflower under water deficit stress. Journal of Crop Production 38(4): 93-104.
3. Asghari M. Hormones and New (Non-Classic) Plants Growth Regulators. Urmia University press. (In Persian)
4. Asna Ashari M., and Zokai Khosroshahi M. Polyamines and Horticultural Sciences. Bu-Ali Sina University, 163 p. (In Persian)
5. Ataii D., Khandan-Mirkohi A., and Naderi R. Exogenous putrescine delays senescence of Lisianthus cut flowers. Journal of Ornamental Plants 3: 167-174.
6. Badawy E.M., Kandil M.M., Mahgoub M., Shanan N., and Hegazi N. Chemical constituents of Celosia argentea var. cristata L. plants as affected by foliar application of putrescine and alpha-tocopherol. International Journal of ChemTech Research 8(12): 464-470.
7. Bani Assadi F., Safari V.R., and Maghsoudi A.A. 2015. Effect of putrescine and salinity on the morphological, biochemical, and pigments of English marigold plant (Calendula officinalis). Journal of Science and Technology of Greenhouse Cultures 6(21): 125–133. (In Persian with English abstract)
8. Bhattacharjee S.K., and Banerji B.K. 2010. The Complete Book of Roses. Jaipur 302 003 (Raj.) India. 531 p.
9. Chen D., Shao Q., Yin L., Younis A., and Zheng B. 2019. Polyamine function in plants: metabolism, regulation on development, and roles in abiotic stress responses. Frontiers in Plant Science 9: 1945. https://doi.org/10.3389/fpls.2018.01945.
10. ‏Danaee E., and Abdossi V. 2018. Effect of different concentration and application methods of polyamines (Putrescine, Spermine, Spermidine) on some morphological, physiological, and enzymatic characteristics and vase life of Rosa hybrida Dolce Vita cut flower. Journal of Ornamental Plants 8(3): 171-182.
11. Dastyaran M., and Hosseini Farahi M. 2014. The effect of humic acid and putrescin on vegetative properties and vase life of rose in a soilless system. Journal of Science and Technology of Greenhouse Cultures 20: 243–252. (In Persian with English abstract)
12. Deng Y., Wang C., Huo J., Hu W., and Liao W. 2019. The involvement of NO in ABA-delayed the senescence of cut roses by maintaining water content and antioxidant enzymes activity. Scientia Horticulturae 247: 35-41. https://doi.org/10.1016/j.scienta.2018.12.006.
13. Duan X., Su X., You Y., Qu H., Li Y., and Jiang Y. 2007. Effect of nitric oxide on pericarp browning of harvested longan fruit in relation to phenolic metabolism. Food Chemistry 104(2): 571-576. https://doi.org/10.1016/j.foodchem.2006.12.007.
14. Eslami M., Nasibi F., Manouchehri Kalantari K., Khezri M., and Oloumi H. 2019. Effect of exogenous application of L-arginine and sodium nitroprusside on fruit abscission and physiological disorders of pistachio (Pistacia vera) Scions. International Journal of Horticultural Science and Technology 6(1): 51-62.
15. Fan H.F., Du C.X., Ding L., and Xu Y.L. 2014. Exogenous nitric oxide promotes waterlogging tolerance as related to the activities of antioxidant enzymes in cucumber seedlings. Russian Journal of Plant Physiology 61(3): 366-373. https://doi.org/1134/S1021443714030042.
16. Ferrante A., Alberici A., Antonacci S., and Serra G. 2007. Effect of promoter and inhibitors of phenylalanine ammonia-lyase enzyme on stem bending of cut gerbera flowers. In International Conference on Quality Management in Supply Chains of Ornamental 755: 471-476.
17. Fraser P.D., and Bramley P.M. 2004. The biosynthesis and nutritional uses of carotenoids. Progress in Lipid Research 43(3): 228-265. https://doi.org/10.1016/j.plipres.2003.10.002.
18. Gohari G., Alavi Z., Esfandiari E., Panahirad S., Hajihoseinlou S., and Fotopoulos V. 2020. Interaction between hydrogen peroxide and sodium nitroprusside following chemical priming of Ocimum basilicum against salt stress. Physiologia Plantarum 168(2): 361-373.‏ https://doi.org/10.1111/ppl.13020.
19. Gomez-Ros L.V., Gabaldon C., Nunez-Flores M.J.L., Gutierrez J., Herrero J., Zapata J.M., Sottomayor M., Cuello J., and Barcelo A.R. 2012. The promoter region of the Zinnia elegans basic peroxidase isoenzyme gene contains cis-elements responsive to nitric oxide and hydrogen peroxide. Planta 236(2): 327-342. https://doi.org/1007/s00425-012-1604-3. 
20. Gupta D.K., Palma J.M., and Corpas F.J. 2019. Nitric Oxide and Hydrogen Peroxide Signaling in Higher Plants. Springer, 275p.
21. Hemati E., Daneshvar M.H., and Heidari M. 2019. The roles of sodium nitroprusside, salicylic acid, and methyl jasmonate as hold solutions on vase life of Gerbera jamesonii ‘Sun Spot’. Advances in Horticultural Science 33(2): 187-195. https://doi.org/10.13128/ahs-24261.
22. Hosseini Farahi M., Khalighi A., Kholdbarin B., Mashhadi Akbar-Boojar M., and Eshghi S. 2013. Morphological responses and vase life of Rosa hybrida Dolce Vita to polyamines spray in hydroponic system. World Applied Sciences Journal 21(11): 1681-1686. https://doi.org/10.5829/idosi.wasj.2013.21.11.1868.
23. Hosseini H., and Rezaei Nezhad A. 2016. Effects of foliar application of sodium nitroprusside on drought tolerance of Marigold. Iranian Journal of Horticulture Science and Technology 17(3): 285-298. (In Persian with English abstract)
24. Jabbarzadeh M., Tehranifar A., Amiri J., and Abedi B. 2016. Investigation on the protective role of nitric oxide in reducing damages induced by salinity stress in Calendula officinalis Journal of Horticultural Science 30(2): 185-191. (In Persian with English abstract)
25. Jalili Marandi R. 2010. Physiology of Environmental Stresses and Resistance Mechanisms in Garden Plants. Jahad Daneshghahi of Urmia press, 636P. (In Persian)
26. Kahrobaiyan M., Nemati S.H., Rahemi M., Kholdebarin B., and Tehranifar A. 2019. Morphological responses of ornamental sunflower to putrescine treatment under drought conditions. Applied Ecology and Environmental Research 17(3): 6117-6127.
27. Kakkar, R.K., and Sawhney, V.K. 2003. Polyamine research in plants- a changing perspective. Physiolgia Plantarium 116:281-292. https://doi.org/1034/J.1399-3054.2002.1160302.X.
28. Kamiab F., and Zamani Bahramabadi E. 2016. The effect of different polyamines on some physiological traits as ACC oxidase and superoxide dismutase enzymes activity in Chrysanthemum morifolium Bright Golden Ann. Journal of Ornamental Plants 6(2): 83-91.
29. Kandil M.M., Soad M.M., Lbrahaim S.H., El-Hanafy S.H., and El-Sabwah M.M. 2015. Effect of putrescine and uniconazole on some flowering characteristics and some chemical constituents of Saliva splendens plant. Journal of Chemical Technology and Biotechnology 8(9): 178-186. https://doi.org/10.21608/ejarc.2012.214880.
30. Kang H.M., and Saltveit M.E. 2002. Chilling tolerance of maize, cucumber and rice seedling leaves and roots and differentially affected by salicylic acid. Plant Physiology 115: 571-576. https://doi.org/10.1034/j.1399-3054.2002.1150411.x.
31. Karamiyan R. 2019. Study of the effects of salicylic acid, sodium nitroprusside and ethanol on vase life and flower quality of cut flowers of two gerbera varieties. Journal of Plant Research 32(3): 635-646.
32. Kazemzadeh-Beneh H., Samsampour D., and Zarbakhsh S. 2018. Biochemical, physiological changes and antioxidant responses of cut gladiolus flower 'White Prosperity' induced by nitric oxide. Advances in Horticultural Science 32(3): 421-431. https://doi.org/10.13128/ahs-23361.
33. Khosh-Khui M., Sheybani B., Rohani E., and Tafazoli A. 2010. Principles of Horticulture. Shiraz University press. (In Persian)
34. Kumar S., Yadav P., Jain V., and Malhotra S.P. 2014. Isozymes of antioxidative enzymes during ripening and storage of ber (Ziziphus mauritiana ). Food Science and Technology 51: 329-334. https://doi.org/10.1007/s13197-011-0489-7.
35. Li X., Yang Y., Yao J., Chen G., Li X., Zhang Q., and Wu C. 2009. Flexible culm encoding a cinnamyl-alcohol dehydrogenase controls culm mechanical strength in rice. Plant Molecular Biology 69(6): 685-697. https://doi.org/10.1007/s11103-008-9448-8.
36. Lichtenthaler H.K. 1987. Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. Methods in Enzymology 148: 350-382. https://doi.org/10.1016/0076-6879(87)48036-1.
37. Mahgoub M.H., El-Aziz N.A., and Mazhar A.M.A. 2011. Response of Dahlia pinnata plant to foliar spray with putrescine and thiamine on growth, flowering and photosynthetic pigments. American-Eurasian Journal of Agricultural and Environmental Sciences 10(5): 769-775.
38. Mohammadi H., Ghorbanpour M., and Brestic M. 2018. Exogenous putrescine changes redox regulations and essential oil constituents in field-grown Thymus vulgaris under well-watered and drought stress conditions. Industrial Crops and Products 122: 119-132. https://doi.org/10.1016/j.indcrop.2018.05.064.
39. Monzon G.C., Pinedo M., Di Rienzo J., Novo-Uzal E., Pomar F., Lamattina L., and de la Canal L. 2014. Nitric oxide is required for determining root architecture and lignin composition in sunflower. Supporting evidence from microarray analyses. Nitric Oxide 39: 20-28. https://doi.org/1016/j.niox.2014.04.004.
40. Mostafaei E., Zehtab-Salmasi S., Salehi-Lisar Y., and Ghassemi-Golezani K. 2018. Changes in photosynthetic pigments, osmolytes and antioxidants of Indian Mustard by drought and exogenous polyamines. Acta Biologica Hungarica 69(3): 313-324. https://doi.org/1556/018.68.2018.3.7.
41. Mostofi Y., Rasouli P., Naderi R., Bagheri Marandi G., and Shafiei M. 2010. Effect of nitric oxide and thidiazuron on vase life and some qualitative characteristics of cut carnation flower (Dianthus caryophyllus Nelson). Iranin Journal of Horticulture Science 41: 301-308. (In Persian with English abstract)
42. Nakano Y., and Asada K. 1981. Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Journal of Plant Cell Physiology 22: 867-880. https://doi.org/10.1093/oxfordjournals.pcp.a076232.
43. Neily M.H., Matsukura C., Maucourt M., Bernillon S., Deborde C., Moing A., Yin Y., Saito T., Mori K., Asamizu E., Rolin D., Moriguchi T., and Ezura H. 2011. Enhanced polyamine accumulation alters carotenoid metabolism at the transcriptional level in tomato fruit over-expressing spermidine synthase. Journal of Plant Physiology 168: 242-252. https://doi.org/1016/j.jplph.2010.07.003.
44. Perik R.R., Razé D., Harkema H., Zhong Y., and Van Doorn W.G. 2012. Bending in cut Gerbera jamesonii flowers relates to adverse water relations and lack of stem sclerenchyma development, not to expansion of the stem central cavity or stem elongation. Postharvest Biology and Technology 74: 11-18. https://doi.org/10.1016/j.postharvbio.2012.06.009.
45. Pirzad A.R., and Mohammadzadeh S. 2018. Crop Physiology. Urmia University Press. (In Persian)
46. Salachna P., and Zawadzińska A. 2018. Effect of nitric oxide on growth, flowering and bulb yield of Eucomis autumnalis. In VII International Conference on Managing Quality in Chains (MQUIC2017) and II International Symposium on Ornamentals in 1201: 635-640.
47. Sadeghi J., Farahmand H., Nasibi F., and Hosseini F. 2016. Effect of nitric oxide on physiological and antioxidant responses and reducing stem neck of gerbera cut flower. Iranian Journal of Horticultural Sciences and Technologies 17(2): 193-208. (In Persian with English abstract)
48. Salachna P., Zawadzińska A., Wierzbiński Ł., and Senderek W. 2016. Enhancing growth in Eucomis autumnalis (Mill.) Chitt. seedlings with exogenous application of nitric oxide. Journal of Horticultural Research 24(2): 13-17.
49. Sami F., Faizan M., Faraz A., Siddiqui H., Yusuf M., and Hayat S. 2017. Nitric oxide-mediated integrative alterations in plant metabolism to confer abiotic stress tolerance, NO crosstalk with phytohormones and NO-mediated post translational modifications in modulating diverse plant stress. Nitric Oxide 73: 22-38. https://doi.org/1016/j.niox.2017.12.005.
50. Shabanian, S., Esfahani, M.N., Karamian, R., and Tran, L.S.P. 2018. Physiological and biochemical modifications by postharvest treatment with sodium nitroprusside extend vase life of cut flowers of two gerbera cultivars. Postharvest Biology and Technology 137: 1-8. https://doi.org/10.1016/j.postharvbio.2017.11.009.
51. Shi H., Liu W., Wei Y., and Ye T. 2017. Integration of auxin/indole-3-acetic acid 17 and RGA-LIKE3 confers salt stress resistance through stabilization by nitric oxide in Arabidopsis. Journal of Experimental Botany 68: 1239–1249. https://doi.org/1093/jxb/erw508.
52. Singh S., Kumar V., Kapoor D., Kumar S., Singh S., Dhanjal D.S., and Singh J. 2020. Revealing on hydrogen sulfide and nitric oxide signals co‐ordination for plant growth under stress conditions. Physiologia Plantarum 168(2): 301-317.‏ https://doi.org/1111/ppl.13002.
53. Talebi F. 2011. The effects of nitric oxide and thidiazuron on qualitative traits and shelf life of cut roses (Rosa hybrida Sensiro) (M.Sc. Thesis). Zanjan University. (In Persian)
54. Upadhyaya A., Sankhla D., Davis T.D., Sankhla N., and Smith B.N. 1985. Effect of paclobutrazol on the activities of some enzymes of activated oxygen metabolism and lipid peroxidation in senescing soybean leaves. Journal of Plant Physiology 121(5): 453-461. https://doi.org/10.1016/S0176-1617(85)80081-X.
55. Vuosku J., Karppinen K., Muilu-Mäkelä R., Kusano T., Sagor G.H.M., and Avia K. 2018. Scot’s pine aminopropyl transferases shed new light on evolution of the polyamine biosynthesis pathway in seed plants. Annals of Botany 121: 1243–1256. https://doi.org/10.1093/aob/mcy012.
56. Wang M., Li B., Zhu Y.C., Niu L.J., Jin X., Xu Q.Q., and Liao W.B. 2015. Effect of exogenous nitric oxide on vegetative and reproductive growth of oriental lily ‘Siberia’. Horticulture, Environment and Biotechnology 56(5): 677-686. https://doi.org/1007/s13580-015-0051-z.
57. Yousefi F., Jabbarzadeh Z., Amiri J., and Rasouli-Sadaghiani M.H. 2019. Response of Roses (Rosa hybrida ‘Herbert Stevens’) to foliar application of polyamines on root development, flowering, photosynthetic pigments, antioxidant enzymes activity and NPK. Scientific Reports 9(16025): 1-11. 025. https://doi.org/10.1038/s41598-019-52547-1.
58. Zeng C.L., Liu L., and Xu G.Q. 2011. The physiological responses of carnation cut flowers to exogenous nitric oxide. Scientia Horticulturae 127(3): 424-430. https://doi.org/10.1016/j.scienta.2010.10.024.
59. Zhou R., Li Y., Yan L., and Xie J. 2011. Effect of edible coatings on enzymes, cell membrane integrity, and cell-wall constituents in relation to brittleness and firmness of Huanghua pears (Pyrus pyrifolia Huanghua) during storage. Food Chemistry 124: 569-575. https://doi.org/10.1016/j.foodchem.2010.06.075.