Effects of Sodium Nitroprusside and Gibberellic Acid Applications on Direct Germination of Fully Mature Grapevine Seeds and Seedling Growth

Abstract

Seeds are widely used in grapevine breeding to obtain new genotypes, however, physical, and physiological constraints in seeds reduce the germination rate and slow down breeding programs. The germination rate of matured grapevine seeds and in vitro methodologies that shorten the process of obtaining seedlings have been described, but the early germination of fully matured seeds in vivo has not been adequately studied. In this study, the effects of Sodium nitroprusside (SNP) and GA3 on germination stimulation were examined. At the same time, fresh (F) and dried (D) seeds were used to determine the drying effect of the seeds separated from the fruit flesh. The effects of control (pure water), SNP (100–500 µM) and GA3 (1–5 gL-1) 24-hours immersion applications on seed germination, vegetative development and seedling development were evaluated. While SNP (F-500 µM SNP in cv. Gök Üzüm, 77.94%) and GA3 (F-GA3 1 g L-1 in cv. Royal 70.87%) applications increased germination and plant transformation rates, dose effects were relatively limited. GA3 treatments promoted germination more in cv. Royal and SNP in cv. Gök Üzüm. GA3 (2.5 gL-1) and SNP (500 µM) applications also increased shoot growth and leaf chlorophyll contents. This technique can contribute and accelerate breeding programs carried out with seed-producing vines, as it provides higher germination rates and seed germination and seedling production immediately after the fully mature clusters harvested.

Keywords

• Vine
• fully matured seed
• seedling
• germination

References

1. Ahlfors R, Brosché M, Kangasjär J (2009). Ozone and nitric oxide interaction in Arabidopsis thaliana, a role for ethylene? A role for ethylene?. Plant Signaling & Behavior, 4(9):878-879. https://doi.org/10.4161/psb.4.9.9428
2. Arif İ, Kaya MD, Gürbüz B (2008). Çemen Trigonella foenum-graecum L. ve kimyon Cuminum cyminum L. tohumlarının çimlenmesi üzerine tohum yaşı ve ga3 uygulamalarının etkileri. Tarım Bilimleri Dergisi, 14(01):57-61. Arteca RN (1996). Plant growth substances: principles and applications. Springer Science & Business Media.
3. Bailly C, El-Maarouf-Bouteau H, Corbineau F (2008). From intracellular signaling networks to cell death: the dual role of reactive oxygen species in seed physiology. Comptes Rendus Biologies, 331(10):806-814. https://doi.org/10.1016/j.crvi.2008.07.022
4. Beligni M, Lamattina L (2002). Nitric oxide interferes with plant photo‐oxidative stress by detoxifying reactive oxygen species. Plant Cell Environ, 25(6):737-748. https://doi.org/10.1046/j.1365-3040.2002.00857.x
5. Beligni MV, Fath A, Bethke PC, Lamattina L, Jones RL (2002). Nitric oxide acts as an antioxidant and delays programmed cell death in barley aleurone layers. Plant Physiology, 129(4):1642-1650. https://doi.org/10.1104/pp.002337
6. Cardemil L, Reinero A (1982). Changes of Araucaria araucana seed reserves during germination and early seedling growth. Canadian Journal of Botany, 60(9):1629-1638. https://doi.org/10.1139/b82-211
7. Chohan G, Dhillon B (1976). Seed dormancy and endogenous growth substances in Anab-e-Shahi grapes. Vitis, 15(1):5-10.
8. Conner PJ (2008). Effects of stratification, germination temperature, and pretreatment with gibberellic acid and hydrogen peroxide on germination of ‘Fry’muscadine (Vitis rotundifolia) seed. HortScience, 43(3):853-856. https://doi.org/10.21273/HORTSCI.43.3.853

9. Çelik M (2014). The effects of stratification periods and GA3 (Gibberellic acid) applications on germination of seeds of some grape cultivars. Turkish Journal of Agricultural and Natural Sciences, (Özel Sayı-1):1118-1122.
10. da Costa Júnior OD, Carvalho VS, Generoso AL, da Silva LM, de Sales RA, Viana AP (2022). Overcoming germination barriers through in vitro culture of mature zygotic embryos of grapevine cultivars. Plant Cell Culture & Micropropagation, 18(18):e182-118. https://doi.org/10.46526/pccm.2022.v18.182
11. Delledonne M, Xia Y, Dixon RA, Lamb C (1998). Nitric oxide functions as a signal in plant disease resistance. Nature, 394(6693):585-588. https://doi.org/10.1038/29087
12. do Brasil F, Brasília D (2016). Ministério da agricultura, pecuária e abastecimento. Secretaria de Defesa Agropecuária. Disponível em: Acesso em, 5(10):2016.
13. dos Santos PR, Viana A, Santos, EA, de Barros Walter FH, Riaz S, Walker AM (2019). Molecular genetic diversity in segregates of Vitis: implications for the breeding of grapevine aiming at resistance to Pratylenchus brachyurus. Euphytica, 215:1-10. https://doi.org/10.1007/s10681-019-2403-8
14. Duan X, You Y, Su X, Qu H, Joyce D, Jiang Y (2007). Influence of the nitric oxide donor, sodium nitroprusside, on lipid peroxidation and anti-oxidant activity in pericarp tissue of longan fruit. The Journal of Horticultural Science and Biotechnology, 82(3):467-473. https://doi.org/10.1080/14620316.2007.11512260
15. Durner J, Klessig DF (1999). Nitric oxide as a signal in plants. Current Opinion in Plant Biology, 2(5):369-374. https://doi.org/10.1016/S1369-5266(99)00007-2
16. Ellis R, Hong T, Roberts E (1983). A note on the development of a practical procedure for promoting the germination of dormant seed of grape (Vitis spp.). Vitis, 22(3):211-219.
17. Ergenoglu F, Tangolar S, Gök S (1996). The effects of some pre-treatments for promoting germination of grape seeds. V Temperate Zone Fruit in the Tropics and Subtropics, 441:207-212. https://doi.org/10.17660/ActaHortic.1997.441.27
18. Eriş A, Düring H (1978). Hamburg misketi üzüm çeşidi çekirdeklerinde katlama uygulamalan ile değişen absizik asit (ABA) miktannın yüksek basınçlı sıvı Kromotografi cihazı ile saptanması. Ankara Üniversitesi Ziraat Fakültesi Yıllığı, 27(3-4):489-498.
19. García MJ, Suárez V, Romera FJ, Alcántara E, Pérez-Vicente R (2011). A new model involving ethylene, nitric oxide and Fe to explain the regulation of Fe-acquisition genes in Strategy I plants. Plant Physiology and Biochemistry 49(5):537-544. https://doi.org/10.1016/j.plaphy.2011.01.019
20. Garcia-Mata C, Graziano M, Pagnussat G (2003). Nitric oxide: the versatility of an extensive signal molecule. Annual Review Plant Biology, 54:109-136. https://doi.org/10.1146/annurev.arplant.54.031902.134752
21. Garcı́a-Mata C, Lamattina L (2001). Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiology, 126(3):1196-1204. https://doi.org/10.1104/pp.126.3.1196
22. Generoso AL, Viana AP, Carvalho VS, Costa Júnior ODd (2019). In vitro germination to overcome dormancy in seeds of ‘Red Globe’,‘Italia’and ‘Niagara Rosada’grapes. Revista Brasileira de Fruticultra, 41:e-495. https://doi.org/10.1590/0100-29452019495
23. Gniazdowska A, Dobrzyńska U, Babańczyk T, Bogatek R (2007). Breaking the apple embryo dormancy by nitric oxide involves the stimulation of ethylene production. Planta, 225(4):1051-1057. https://doi.org/10.1007/s00425-006-0384-z
24. Gniazdowska A, Krasuska U, Bogatek R (2010a). Dormancy removal in apple embryos by nitric oxide or cyanide involves modifications in ethylene biosynthetic pathway. Planta, 232(6):1397-1407. https://doi.org/10.1007/s00425-010-1262-2
25. Gniazdowska A, Krasuska U, Dębska K, Andryka P, Bogatek R (2010b). The beneficial effect of small toxic molecules on dormancy alleviation and germination of apple embryos is due to NO formation. Planta, 232(4):999-1005. https://doi.org/10.1007/s00425-010-1214-x
26. Hayat S, Yadav S, Alyemeni M, Ahmad A (2014). Effect of sodium nitroprusside on the germination and antioxidant activities of tomato (Lycopersicon esculentum Mill). Bulgarian Journal of Agricultural Sciences, 20(1):140-144.
27. Hopkins W (1995). Introduction to Plant Physiology. John Wiley and Sons, Inc, USA.
28. Hummel SG, Fischer AJ, Martin SM, Schafer Q, Buettner GR (2006). Nitric oxide as a cellular antioxidant: a little goes a long way. Free Radical Biology & Medicine, 40(3):501-506. https://doi.org/10.1016/-j.freeradbiomed.2005.08.047
29. Hung KT, Kao CH (2004). Nitric oxide acts as an antioxidant and delays methyl jasmonate-induced senescence of rice leaves. Journal of Plant Physiology, 161(1):43-52. https://doi.org/10.1078/0176-1617-01178
30. Kachru R (1969). Physiological studies on dormancy in grape seeds (Vitis vinifera) 1. On the naturally occurring growth substances in grapes and their changes during low temperature after ripening. Vitis, 8:12-18.
31. Kang Y (1968). Effect of low temperature and growth regulators on germination of seeds of 'Tokay grapes' grapes. Proceedings of the American Society for Horticultural Science, 323-330. https://doi.org/10.6964/JCSHS.196712.0066
32. Kara Z, Yazar K, Doğan O, Vergili E (2020). Sodium nitroprusside and gibberellin effects on seed germination and seedling development of grapevine (Vitis vinifera L.) cvs. Ekşi Kara and Gök Üzüm. Erwerbs-Obstbau, 62:61-68. https://doi.org/10.1007/s10341-020-00497-8
33. Lee S, Kim SG, Park CM (2010). Salicylic acid promotes seed germination under high salinity by modulating antioxidant activity in Arabidopsis. New Phytologist, 188(2):626-637. https://doi.org/10.1111/j.1469-8137.2010.03378.x
34. Leymarie J, Vitkauskaité G, Hoang HH, Gendreau E, Chazoule V, Meimoun P, Corbineau F, El-Maarouf-Bouteau H, Bailly C (2012). Role of reactive oxygen species in the regulation of Arabidopsis seed dormancy. Plant & Cell Physiology, 53(1):96-106. https://doi.org/10.1093/pcp/pcr129
35. Li J, Wang X, Wang X, Wang Y (2015). Embryo rescue technique and its applications for seedless breeding in grape. Plant Cell Tissue and Organ Culture, 120:861-880. https://doi.org/10.1007/s11240-014-0656-4
36. Li S, Li Z, Zhao Y, Zhao J, Luo Q, Wang Y (2020). New disease-resistant, seedless grapes are developed using embryo rescue and molecular markers, 3 Biotech, 10:1-12. https://doi.org/10.1007/s13205-019-1993-0
37. Lin Y, Wang J, Zu Y, Tang Z (2012). Ethylene antagonizes the inhibition of germination in Arabidopsis induced by salinity by modulating the concentration of hydrogen peroxide. Acta Physiolologiae Plantarum, 34(5):1895-1904. https://doi.org/10.1007/s11738-012-0989-8
38. Liu Y, Ye N, Liu R, Chen M, Zhang J (2010). H2O2 mediates the regulation of ABA catabolism and GA biosynthesis in Arabidopsis seed dormancy and germination. Journal of Experimental Botany, 61(11):2979-2990. https://doi.org/10.1093/jxb/erq125
39. Maeda JA, Pereira MdFDA, Terra MM (1985). Effect of storage conditions on the viability and dormancy of grape seeds. Bragantia, 44:245-254. https://doi.org/10.1590/S0006-87051985000100023
40. Manivel L, Weaver R (1974). Effect of growth regulators and heat on germination of Tokay grape seeds. Vitis, 12(4):286-290.
41. Mbi KT, Tonfack LB, Ntsefong GN, Mir BA, Ebongue GFN, Ngaha D, Njembele C, Namuene KS, Youmbi E (2016). Mature zygotic embryo rescue improves in vitro germination and seedling production in high value oil palm (Elaeis guineensis Jacq.) cultivars. Industrial Crops and Products, 94:445-453. https://doi.org/10.1016/j.indcrop.2016.09.002
42. Moreno D, Berli FJ, Piccoli PN, Bottini R (2011). Gibberellins and abscisic acid promote carbon allocation in roots and berries of grapevines. Journal of Plant Growth Regulation, 30:220–228. https://doi.org/10.1007/s00344-010-9186-4
43. Olmo H (1934). Empty-seededness in varieties of Vitis vinifera. Proceedings of the American Society for Horticultural Science, 376-385.
44. Özen H, Onay A (1999). Bitki büyüme ve gelişme fizyolojisi. Dicle Üniversitesi Basımevi. Diyarbakır, 166.
45. Pal R, Singh R (1976). Effect of gibberellins GA3, GA+7 and GA13 on seed germination and subsequent seedling growth in Early Muscat grape (Vitis vinifera). Vitis, 14(4):265-268.
46. Pandey S, Singh R (1988). Germination of seeds extracted from immature berries of grapes. Indian Journal of Horticulture, 45(1 and 2):56-60.
47. Pommer CV, Maeda JA, Ribeiro IJA (1988). Capacidade de germinação e quebra de dormência em sementes de cultivares de videira. Bragantia, 47:143-157. https://doi.org/10.1590/S0006-87051988000200001
48. Rajasekaran K, Vine J, Mullins M (1982). Dormancy in somatic embryos and seeds of Vitis: changes in endogenous abscisic acid during embryogeny and germination. Planta, 154:139-144. https://doi.org/10.1007/BF00387907
49. Ritschel P, Maia JDG, Camargo UA, Zanus MC, Souza RTd, Fajardo TVM (2014). 'BRS MAGNA'-a novel grape cultivar for juice making, with wide climatic adaptation. Crop Breeding and Applied Biotechnology, 14:266-269. https://doi.org/10.1590/1984-70332014v14n4c42
50. Selim H, Ibrahim F, Fayek M, El-Deen SS, Gamal N (2016). Effect of different treatments on germination of Romi red grape seeds. Vitis, 20(2):115-121.
51. Sharpe MA, Robb SJ, Clark JB (2003). Nitric oxide and Fenton/Haber–Weiss chemistry: nitric oxide is a potent antioxidant at physiological concentrations. Journal of Neurochemistry, 87(2):386-394. https://doi.org/10.1046/j.1471-4159.2003.02001.x
52. Shi S, Wang G, Wang Y, Zhang L, Zhang L (2005). Protective effect of nitric oxide against oxidative stress under ultraviolet-B radiation. Nitric Oxide, 13(1):1-9. https://doi.org/10.1016/j.niox.2005.04.006
53. Soltys D, Rudzińska-Langwald A, Gniazdowska A, Wiśniewska A, Bogatek R (2012). Inhibition of tomato (Solanum lycopersicum L.) root growth by cyanamide is due to altered cell division, phytohormone balance and expansin gene expression. Planta, 236(5):1629-1638. https://doi.org/10.1007/s00425-012-1722-y
54. Tang D, Wang Y, Cai J, Zhao R (2009). Effects of exogenous application of plant growth regulators on the development of ovule and subsequent embryo rescue of stenospermic grape (Vitis vinifera L.). Scientia Horticulturae, 120(1):51-57. https://doi.org/10.1016/j.scienta.2008.09.018
55. Tian L, Wang Y, Niu L, Tang D (2008). Breeding of disease-resistant seedless grapes using Chinese wild Vitis spp.: I. In vitro embryo rescue and plant development. Scientia Horticulturae, 117(2):136-141. https://doi.org/10.1016/j.scienta.2008.03.024
56. Ünal O, Gökceoğlu M, Topçuoğlu ŞF (2004). Antalya endemiği Origanum türlerinin tohum çimlenmesi ve çelikle çoğaltılması üzerinde araştırmalar. Akdeniz University Journal of the Faculty of Agriculture 17(2):135-147.
57. Val ADBd, Motoike SY, Alvarenga EM, Cecon PR (2010). Breaking the dormancy of Niagara Rosada seeds without stratification. Revista Ceres, 57:234-238. https://doi.org/10.1590/S0034-737X2010000200015
58. Walter R, Carvalho VS, Generoso AL, Rodrigues R, Gravina GdA (2018). Cultivation of immature Capsicum spp. embryos for incompatible-crossing embryo rescue. Acta Scientiarum Agronomy, 40. https://doi.org/10.4025/actasciagron.v40i1.39474
59. Wang H, Liang X, Wan Q, Wang X, Bi Y (2009). Ethylene and nitric oxide are involved in maintaining ion homeostasis in Arabidopsis callus under salt stress. Planta, 230(2):293-307. https://doi.org/10.1007/s00425-009-0946-y
60. Wang Z-L, Hui M, Shi, X-Q, Wu D, Wang Y, Han X, Cao X, Yao F, Li H, Wang H (2022). Characteristics of the seed germination and seedlings of six grape varieties (V. vinifera). Plants, 11(4):479. https://doi.org/10.3390/plants11040479
61. Wurzburger J, Leshem Y, Koller D (1974). The role of gibberellin and the hulls in the control of germination in Aegilops kotschyi caryopses. Canadian Journal of Botany, 52(7):1597-1601. https://doi.org/10.1139/b74-209
62. Yang D, Li W, Li S, Yang X, Wu J, Cao Z (2007). In vitro embryo rescue culture of F1 progenies from crosses between diploid and tetraploid grape varieties. Plant Growth Regulation, 51:63–71. https://doi.org/10.1007/s10725-006-9148-9
63. Zhang J, Wu J, Hao X, Xie Y, Lv K, Xu W (2023). Establishment of a stable grape immature zygotic embryo-based genetic transformation system. Scientia Horticulturae, 316:112009. https://doi.org/10.1016/j.scienta.2023.112009
64. Zhao L, Zhang F, Guo J, Yang Y, Li B, Zhang L (2004). Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiology, 134(2):849-857. https://doi.org/10.1104/pp.103.030023
65. Zhao MG, Tian Q-Y, Zhang WH (2007). Nitric oxide synthase-dependent nitric oxide production is associated with salt tolerance in Arabidopsis. Plant Physiology, 144(1):206-217. https://doi.org/10.1104/pp.107.096842