Abstract
Gibberellic acid (GA) and ethephon (ETH) can stimulate seed germination and seedling growth. However, uncertainties persist concerning the efficacy of GA or ETH priming in mitigating drought stress effects. This study aims to elucidate the underlying mechanisms of drought tolerance in rice seedlings induced by GA or ETH priming. Rice seeds were primed by water, GA, and ETH and sown under polyethylene glycol (PEG-6000)-induced stress. We set non-primed seeds under normal conditions as a control to investigate the effects of GA or ETH on seed germination and seedling growth under drought stress. Drought resistance mechanisms were characterized by osmoregulation, homeostasis of reactive oxygen species (ROS), antioxidants and transmission electron microscopy analysis. Drought significantly inhibited germination and seedling development. Nevertheless, GA or ETH priming enhanced rice emergence and establishment under water-deficient condition. Furthermore, hormonal priming enhanced chlorophyll content and osmolyte accumulation, ROS detoxification and antioxidant enzyme activity in rice seedlings (shoots and roots) during drought stress. Ultrastructural observations revealed GA or ETH priming’s protective role in leaf mesophyll integrity, chloroplast preservation, and mitigation of drought-induced damage in root tip cells. Nonetheless, distinct defense responses and mitigation mechanisms emerged post-GA or ETH priming. While ETH treatment affected shoot fresh weight and root volume, GA priming excelled in germination attributes, seedling length, soluble sugar, H2O2 reduction, electrolyte leakage, and ascorbate peroxidase activity under drought. GA and ETH priming promoted rice seed germination and seedling establishment under drought conditions by maintaining root conformation, attenuating oxidative stress, and maintaining cellular ultrastructure.
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References
Abdul-Baki AA, Anderson JD (1973) Vigor determination in soybean seed by multiple criteria 1. Crop Sci 13:630–633. https://doi.org/10.2135/cropsci1973.0011183X001300060013x
Abid M, Hakeem A, Shao Y, Liu Y, Zahoor R, Fan Y, Suyu J, Ata-Ul-Karim ST, Tian Z, Jiang D, Snider JL, Dai T (2018) Seed osmopriming invokes stress memory against post-germinative drought stress in wheat (Triticum aestivum L). Environ Exp Bot 145:12–20. https://doi.org/10.1016/j.envexpbot.2017.10.002
Al-Harthi MM, Bafeel SO, El-Zohri M (2021) Gibberellic Acid and Jasmonic Acid Improve Salt Tolerance in Summer Squash by modulating some physiological parameters symptomatic for oxidative stress and Mineral Nutrition. Plants-Basel 10:2768. https://doi.org/10.3390/plants10122768
Anjum SA, Wang L, Farooq M, Khan I, Xue L (2011) Methyl Jasmonate-Induced alteration in lipid peroxidation, Antioxidative Defence System and yield in soybean under Drought. J Agron Crop Sci 197:296–301. https://doi.org/10.1111/j.1439-037x.2011.00468.x
Anjum SA, Tanveer M, Hussain S, Bao M, Wang L, Khan I, Ullah E, Tung SA, Samad RA, Shahzad B (2015) Cadmium toxicity in Maize (Zea mays L.): consequences on antioxidative systems, reactive oxygen species and cadmium accumulation. Environ Sci Pollut Res 22:17022–17030. https://doi.org/10.1007/s11356-015-4882-z
AOSA (1990) Rules for testing seeds. J Seed Technol 12:1–12
Bewley JD (1997) Seed germination and dormancy. Plant Cell 9:1055. https://doi.org/10.1105/tpc.9.7.1055
Biju S, Fuentes S, Gupta D (2017) Silicon improves seed germination and alleviates drought stress in lentil crops by regulating osmolytes, hydrolytic enzymes and antioxidant defense system. Plant Physiol Biochem 119:250–264. https://doi.org/10.1016/j.plaphy.2017.09.001
Brocklehurst PA, Dearman J (1983) Interactions between seed priming treatments and nine seed lots of carrot, celery and onion. II. Seedling emergence and plant growth. Ann Appl Biol 102:585–593. https://doi.org/10.1111/j.1744-7348.1983.tb02730.x
Cai S, Wu L, Wang G, Liu J, Song J, Xu H, Luo J, Shen Y, Shen S (2022) DA-6 improves sunflower seed vigor under Al3+ stress by regulating Al3+ balance and ethylene metabolic. Ecotox Environ Safe 229:113048. https://doi.org/10.1016/j.ecoenv.2021.113048
Delauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4:215–223. https://doi.org/10.1046/j.1365-313X.1993.04020215.x
Dhillon BS, Kumar V, Sagwal P, Kaur N, Mangat GS, Singh S (2021) Seed priming with Potassium Nitrate and Gibberellic Acid enhances the performance of Dry Direct Seeded Rice (Oryza sativa L.) in North-Western India. Agronomy-Basel 11:849. https://doi.org/10.3390/agronomy11050849
Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135:1–9. https://doi.org/10.1016/S0168-9452(98)00025-9
El-Badri AM, Batool M, Mohamed IAA, Wang Z, Wang C, Tabl KM, Khatab A, Kuai J, Wang J, Wang B, Zhou G (2022) Mitigation of the salinity stress in rapeseed (Brassica napus L.) productivity by exogenous applications of bio-selenium nanoparticles during the early seedling stage. Environ Pollut 310:119815. https://doi.org/10.1016/j.envpol.2022.119815
Fan S, Wu H, Gong H, Guo J (2022) The salicylic acid mediates selenium-induced tolerance to drought stress in tomato plants. Sci Hortic 300:111092. https://doi.org/10.1016/j.scienta.2022.111092
Farooq M, Irfan M, Aziz T, Ahmad I, Cheema SA (2013) Seed priming with ascorbic acid improves Drought Resistance of Wheat. J Agron Crop Sci 199:12–22. https://doi.org/10.1111/j.1439-037X.2012.00521.x
Gautam H, Fatma M, Sehar Z, Iqbal N, Albaqami M, Khan NA (2022) Exogenously-sourced ethylene positively modulates photosynthesis, carbohydrate metabolism, and antioxidant defense to enhance heat tolerance in rice. Int J Mol Sci 23:1031. https://doi.org/10.3390/ijms23031031
Hasanuzzaman M, Nahar K, Anee TI, Khan MIR, Fujita M (2018) Silicon-mediated regulation of antioxidant defense and glyoxalase systems confers drought stress tolerance in Brassica napus L. S Afr J Bot 115:50–57. https://doi.org/10.1016/j.sajb.2017.12.006
Hussain S, Zheng M, Khan F, Khaliq A, Fahad S, Peng S, Huang J, Cui K, Nie L (2015) Benefits of rice seed priming are offset permanently by prolonged storage and the storage conditions. Sci Rep 5:8101. https://doi.org/10.1038/srep08101
Hussain S, Khan F, Hussain HA, Nie L (2016) Physiological and biochemical mechanisms of seed Priming-Induced Chilling Tolerance in Rice cultivars. Front Plant Sci 7:116. https://doi.org/10.3389/fpls.2016.00116
Hussain S, Bai Z, Huang J, Cao X, Zhu L, Zhu C, Khaskheli MA, Zhong C, Jin Q, Zhang J (2019) 1-Methylcyclopropene modulates physiological, biochemical, and antioxidant responses of rice to different salt stress levels. Front Plant Sci 10:124. https://doi.org/10.3389/fpls.2019.00124
Hussain S, Zhu C, Huang J, Huang J, Zhu L, Cao X, Nanda S, Khaskheli MA, Liang Q, Kong Y, Jin Q, Zhang J (2020) Ethylene response of salt stressed rice seedlings following Ethephon and 1-methylcyclopropene seed priming. Plant Growth Regul 92:219–231. https://doi.org/10.1007/s10725-020-00632-1
Iftikhar A, Ali S, Yasmeen T, Arif MS, Zubair M, Rizwan M, Alhaithloul HAS, Alayafi AAM, Soliman MH (2019) Effect of gibberellic acid on growth, photosynthesis and antioxidant defense system of wheat under zinc oxide nanoparticle stress. Environ Pollut 254:113109. https://doi.org/10.1016/j.envpol.2019.113109
Jisha KC, Vijayakumari K, Puthur JT (2013) Seed priming for abiotic stress tolerance: an overview. Acta Physiol Plant 35:1381–1396. https://doi.org/10.1007/s11738-012-1186-5
Kaur K, Kaur N, Gupta AK, Singh I (2013) Exploration of the antioxidative defense system to characterize chickpea genotypes showing differential response towards water deficit conditions. Plant Growth Regul 70:49–60. https://doi.org/10.1007/s10725-012-9777-0
Kavi Kishor PB, Hima Kumari P, Sunita M, Sreenivasulu N (2015) Role of proline in cell wall synthesis and plant development and its implications in plant ontogeny. Front Plant Sci 6:544. https://doi.org/10.3389/fpls.2015.00544
Khan MN, Zhang J, Luo T, Liu J, Rizwan M, Fahad S, Xu Z, Hu L (2019) Seed priming with melatonin coping drought stress in rapeseed by regulating reactive oxygen species detoxification: antioxidant defense system, osmotic adjustment, stomatal traits and chloroplast ultrastructure perseveration. Ind Crop Prod 140:111597. https://doi.org/10.1016/j.indcrop.2019.111597
Khan MIR, Jahan B, AlAjmi MF, Rehman MT, Khan NA (2020a) Ethephon mitigates nickel stress by modulating antioxidant system, glyoxalase system and proline metabolism in Indian mustard. Physiol Mol Biol Plants 26:1201–1213. https://doi.org/10.1007/s12298-020-00806-1
Khan MN, Khan Z, Luo T, Liu J, Rizwan M, Zhang J, Xu Z, Wu H, Hu L (2020b) Seed priming with gibberellic acid and melatonin in rapeseed: consequences for improving yield and seed quality under drought and non-stress conditions. Ind Crop Prod 156:112850. https://doi.org/10.1016/j.indcrop.2020.112850
Laxa M, Liebthal M, Telman W, Chibani K, Dietz K-J (2019) The role of the plant antioxidant system in drought tolerance. Antioxidants 8:94. https://doi.org/10.3390/antiox8040094
Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592. https://doi.org/10.1042/bst0110591
Luo L, Mei H, Yu X, Xia H, Chen L, Liu H, Zhang A, Xu K, Wei H, Liu G, Wang F, Liu Y, Ma X, Lou Q, Feng F, Zhou L, Chen S, Yan M, Liu Z, Bi J, Li T, Li M (2019) Water-saving and drought-resistance rice: from the concept to practice and theory. Mol Breed 39:145. https://doi.org/10.1007/s11032-019-1057-5
Meng JF, Xu TF, Wang ZZ, Fang YL, Xi ZM, Zhang ZW (2014) The ameliorative effects of exogenous melatonin on grape cuttings under water-deficient stress: antioxidant metabolites, leaf anatomy, and chloroplast morphology. J Pineal Res 57:200–212. https://doi.org/10.1111/jpi.12159
Muniandi SKM, Hossain MA, Abdullah MP, Ab Shukor NA (2018) Gibberellic acid (GA3) affects growth and development of some selected kenaf (Hibiscus cannabinus L.) cultivars. Ind Crop Prod 118:180–187. https://doi.org/10.1016/j.indcrop.2018.03.036
Nonogaki H, Bassel GW, Bewley JD (2010) Germination—still a mystery. Plant Sci 179:574–581. https://doi.org/10.1016/j.plantsci.2010.02.010
Ostonen I, Püttsepp Ü, Biel C, Alberton O, Bakker M, Lõhmus K, Majdi H, Metcalfe D, Olsthoorn A, Pronk A (2007) Specific root length as an indicator of environmental change. Plant Biosyst 141:426–442. https://doi.org/10.1080/11263500701626069
Paparella S, Araújo SS, Rossi G, Wijayasinghe M, Carbonera D, Balestrazzi A (2015) Seed priming: state of the art and new perspectives. Plant Cell Rep 34:1281–1293. https://doi.org/10.1007/s00299-015-1784-y
Rhaman MS, Imran S, Rauf F, Khatun M, Baskin CC, Murata Y, Hasanuzzaman M (2020) Seed priming with phytohormones: an Effective Approach for the mitigation of Abiotic Stress. Plants-Basel 10:37. https://doi.org/10.3390/plants10010037
Saddiq MS, Iqbal S, Afzal I, Ibrahim AMH, Bakhtavar MA, Hafeez MB, Jahanzaib, Maqbool MM (2019) Mitigation of salinity stress in wheat (Triticum aestivum L.) seedlings through physiological seed enhancements. J Plant Nutr 42:1192–1204. https://doi.org/10.1080/01904167.2019.1609509
Sasi M, Awana M, Samota MK, Tyagi A, Kumar S, Sathee L, Krishnan V, Praveen S, Singh A (2021) Plant growth regulator induced mitigation of oxidative burst helps in the management of drought stress in rice (Oryza sativa L). Environ Exp Bot 185:104413. https://doi.org/10.1016/j.envexpbot.2021.104413
Savaedi Z, Parmoon G, Moosavi SA, Bakhshande A (2019) The role of light and Gibberellic Acid on cardinal temperatures and thermal time required for germination of Charnushka (Nigella sativa) seed. Ind Crop Prod 132:140–149. https://doi.org/10.1016/j.indcrop.2019.02.025
Shaw AK, Ghosh S, Kalaji HM, Bosa K, Brestic M, Zivcak M, Hossain Z (2014) Nano-CuO stress induced modulation of antioxidative defense and photosynthetic performance of Syrian barley (Hordeum vulgare L). Environ Exp Bot 102:37–47. https://doi.org/10.1016/j.envexpbot.2014.02.016
Siddiqui MH, Al-Whaibi MH, Basalah MO (2011) Interactive effect of calcium and gibberellin on nickel tolerance in relation to antioxidant systems in Triticum aestivum L. Protoplasma 248:503–511. https://doi.org/10.1007/s00709-010-0197-6
Singh N, Bhardwaj RD (2016) Ascorbic acid alleviates water deficit induced growth inhibition in wheat seedlings by modulating levels of endogenous antioxidants. Biologia 71:402–413. https://doi.org/10.1515/biolog-2016-0050
Singh M, Kumar J, Singh S, Singh VP, Prasad SM (2015) Roles of osmoprotectants in improving salinity and drought tolerance in plants: a review. Rev Environ Sci Bio-Technol 14:407–426. https://doi.org/10.1007/s11157-015-9372-8
Sun C, Li X, Hu Y, Zhao P, Xu T, Sun J, Gao X (2015) Proline, sugars, and antioxidant enzymes respond to drought stress in the leaves of strawberry plants. Hortic Sci Technol 33:625–632. https://doi.org/10.7235/hort.2015.15054
Tuna AL, Kaya C, Dikilitas M, Higgs D (2008) The combined effects of gibberellic acid and salinity on some antioxidant enzyme activities, plant growth parameters and nutritional status in maize plants. Environ Exp Bot 62:1–9. https://doi.org/10.1016/j.envexpbot.2007.06.007
Wang KL-C, Li H, Ecker JR (2002) Ethylene Biosynthesis and Signaling Networks. Plant Cell 14:S131–S151. https://doi.org/10.1105/tpc.001768
Watanabe H, Honma K, Adachi Y, Fukuda A (2018) Effects of combinational treatment with ethephon and gibberellic acid on rice seedling growth and carbohydrate mobilization in seeds under flooded conditions. Plant Prod Sci 21:380–386. https://doi.org/10.1080/1343943x.2018.1520048
Yamaguchi S (2008) Gibberellin Metabolism and its regulation. Annu Rev Plant Biol 59:225–251. https://doi.org/10.1146/annurev.arplant.59.032607.092804
Yang H, Hu W, Zhao J, Huang X, Zheng T, Fan G (2021) Genetic improvement combined with seed ethephon priming improved grain yield and drought resistance of wheat exposed to soil water deficit at tillering stage. Plant Growth Regul 95:399–419. https://doi.org/10.1007/s10725-021-00749-x
Yu S, Ali J, Zhou S, Ren G, Xie H, Xu J, Yu X, Zhou F, Peng S, Ma L, Yuan D, Li Z, Chen D, Zheng R, Zhao Z, Chu C, You A, Wei Y, Zhu S, Gu Q, He G, Li S, Liu G, Liu C, Zhang C, Xiao J, Luo L, Li Z, Zhang Q (2022) From Green Super Rice to green agriculture: reaping the promise of functional genomics research. Mol Plant 15:9–26. https://doi.org/10.1016/j.molp.2021.12.001
Zhang N, Zhao B, Zhang H-J, Weeda S, Yang C, Yang Z-C, Ren S, Guo Y-D (2013) Melatonin promotes water-stress tolerance, lateral root formation, and seed germination in cucumber (Cucumis sativus L). J Pineal Res 54:15–23. https://doi.org/10.1111/j.1600-079x.2012.01015.x
Zhang M, Jin Z-Q, Zhao J, Zhang G, Wu F (2015) Physiological and biochemical responses to drought stress in cultivated and tibetan wild barley. Plant Growth Regul 75:567–574. https://doi.org/10.1007/s10725-014-0022-x
Zhang N, Han L, Xu L, Zhang X (2018) Ethephon seed treatment impacts on drought tolerance of kentucky bluegrass seedlings. HortTechnology 28:319–326. https://doi.org/10.21273/HORTTECH03976-18
Zhang J, Zhang Z, Liu W, Li L, Han L, Xu L, Zhao Y (2022a) Transcriptome analysis revealed a positive role of Ethephon on Chlorophyll Metabolism of Zoysia japonica under cold stress. Plants-Basel 11:442. https://doi.org/10.3390/plants11030442
Zhang K, Khan Z, Liu J, Luo T, Zhu K, Hu L, Bi J, Luo L (2022b) Germination and growth performance of water-saving and Drought-Resistant Rice enhanced by seed treatment with Wood Vinegar and Biochar under Dry Direct-Seeded System. Agronomy-Basel 12:1223. https://doi.org/10.3390/agronomy12051223
Zhang K, Khan Z, Wu H, Khan MN, Hu L (2022c) Gibberellic Acid Priming Improved Rapeseed Drought Tolerance by modulating Root morphology, ROS Homeostasis, and Chloroplast Autophagy. J Plant Growth Regul 42:5977–5990. https://doi.org/10.1007/s00344-022-10718-x
Zhang K, Han X, Fu Y, Zhou Y, Khan Z, Bi J, Hu L, Luo L (2023) Biochar Coating as a cost-effective Delivery Approach to promoting seed quality, Rice Germination, and Seedling Establishment. Plants-Basel 12:3896. https://doi.org/10.3390/plants12223896
Zhou H, Liang X, Feng N, Zheng D, Qi D (2021a) Effect of uniconazole to soybean seed priming treatment under drought stress at VC stage. Ecotox Environ Safe 224:112619. https://doi.org/10.1016/j.ecoenv.2021.112619
Zhou M, Hassan MJ, Peng Y, Liu L, Liu W, Zhang Y, Li Z (2021b) γ-Aminobutyric acid (GABA) priming improves seed germination and seedling stress tolerance Associated with enhanced antioxidant metabolism, DREB expression, and Dehydrin Accumulation in White Clover Under Water stress. Front Plant Sci 12:776939–776939. https://doi.org/10.3389/fpls.2021.776939
Acknowledgements
The authors would like to express their gratitude to Jianbo Cao and Limin He from Huazhong Agricultural University for their technical assistance with the TEM (transmission electron microscope) support during the experiment.
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This research was supported by the Technology System of Rice Industry in Shanghai: Grant NO. 2023(03).
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Conceptualization: [Liyong Hu and Lijun Luo]; Methodology: [Kangkang Zhang]; Formal analysis and investigation: [Kangkang Zhang]; Writing - original draft preparation: [Kangkang Zhang]; Writing - review and editing: [Mohammad Nauman Khan, Tao Luo and Junguo Bi]; Funding acquisition: [Junguo Bi]; Resources: [Liyong Hu and Lijun Luo]; Supervision: [Kangkang Zhang]
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Zhang, K., Khan, M.N., Luo, T. et al. Seed Priming with Gibberellic Acid and Ethephon Improved Rice Germination under Drought Stress via Reducing Oxidative and Cellular Damage. J Soil Sci Plant Nutr (2024). https://doi.org/10.1007/s42729-024-01691-3
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DOI: https://doi.org/10.1007/s42729-024-01691-3