Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Exogenous application of spermidine mitigates the adverse effects of drought stress in faba bean (Vicia faba L.)

Ghassen Abid https://orcid.org/0000-0001-7120-9547 A * , Rim Nefissi Ouertani https://orcid.org/0000-0003-4999-2453 B , Emna Ghouili A , Yordan Muhovski C , Salwa Harzalli Jebara A , Souhir Abdelkarim A , Oumaima Chaieb A , Yosr Ben Redjem A , Mohamed El Ayed D , Fathi Barhoumi A , Fatma Souissi A and Moez Jebara A
+ Author Affiliations
- Author Affiliations

A Laboratory of Legumes and Sustainable Agrosystems, Centre of Biotechnology of Borj Cedria, BP 901, Hammam-Lif 2050, Tunisia.

B Laboratory of Plant Molecular Physiology, Centre of Biotechnology of Borj Cedria, BP 901, Hammam-Lif 2050, Tunisia.

C Department of Life Sciences, Walloon Agricultural Research Centre, Chaussée de Charleroi, BP 234, Gembloux 5030, Belgium.

D Laboratory of Bioactive Substances, Centre of Biotechnology of Borj Cedria, BP 901, Hammam-Lif 2050, Tunisia.

* Correspondence to: gha_abid@yahoo.fr

Handling Editor: Ismail Turkan

Functional Plant Biology 49(4) 405-420 https://doi.org/10.1071/FP21125
Submitted: 23 April 2021  Accepted: 1 February 2022   Published: 25 February 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

In Tunisia, drought stress is a major environmental factor limiting crop production and causing relatively low and unstable faba bean yields. In the present study, we explored the putative role of spermidine (0.5, 1, 1.5 and 2 mM) in ameliorating the effects of drought stress induced by polyethylene glycol (PEG-6000, −0.58 MPa) in faba bean seedlings. Drought stress reduced photosynthetic performance, chlorophyll and relative water content in leaves of faba bean variety Badii. Moreover, drought increased proline, electrolyte leakage and malondialdehyde content by inducing reactive oxygen species (hydrogen peroxide) generation in leaves. However, applying spermidine increased the activities of catalase, superoxide dismutase, ascorbate peroxidase and guaiacol peroxidase. The results show that the application of spermidine especially at a rate of 1.5 mM effectively reduces oxidative damage and alleviates negative effects caused by drought stress. In addition, exogenous spermidine increased the expression of polyamine biosynthetic enzymes’ genes (VfADC, VfSAMDC and VfSPDS), and reduced the expression of VfSPMS suggesting that exogenous spermidine can regulate polyamines’ metabolic status under drought challenge, and consequently may enhance drought stress tolerance in faba bean. Real-time quantitative polymerase chain reaction analysis revealed that some drought responsive genes (VfNAC, VfHSP, VfNCED, VfLEA, VfCAT, VfAPX, VfRD22, VfMYB, VfDHN, VfERF, VfSOD and VfWRKY) from various metabolic pathways were differentially expressed under drought stress. Overall, these genes were more abundantly transcribed in the spermidine-treated plants compared to untreated suggesting an important role of spermidine in modulating faba bean drought stress response and tolerance.

Keywords: drought responsive genes, drought stress, faba bean, gene expression, oxidative damage, polyamine biosynthetic enzymes, spermidine, qRT-PCR.


References

Abid G, Hessini K, Aouida M, Aroua I, Baudoin JP, Muhovski Y, Mergeai G, Sassi K, Machraoui M, Souissi F, Jebara M (2017) Agro-physiological and biochemical responses of faba bean (Vicia faba L. var. ‘minor’) genotypes to water deficit stress. Biotechnology, Agronomy, Society and Environment 21, 146–159.
Agro-physiological and biochemical responses of faba bean (Vicia faba L. var. ‘minor’) genotypes to water deficit stress.Crossref | GoogleScholarGoogle Scholar |

Abid G, Ouertani RN, Muhovski Y, Jebara SH, Hidri Y, Ghouili E, Abdelkarim S, Chaieb O, Souissi F, Zribi F, Jebara M (2021) Variation in antioxidant metabolism of faba bean (Vicia faba) under drought stress induced by polyethylene glycol reveals biochemical markers associated with antioxidant defense. Plant Biosystems – An International Journal Dealing with all Aspects of Plant Biology 155, 797–806.
Variation in antioxidant metabolism of faba bean (Vicia faba) under drought stress induced by polyethylene glycol reveals biochemical markers associated with antioxidant defense.Crossref | GoogleScholarGoogle Scholar |

Aduse Poku S, Nkachukwu Chukwurah P, Aung HH, Nakamura I (2020) Over-expression of a melon Y3SK2-type LEA gene confers drought and salt tolerance in transgenic tobacco plants. Plants 9, 1749
Over-expression of a melon Y3SK2-type LEA gene confers drought and salt tolerance in transgenic tobacco plants.Crossref | GoogleScholarGoogle Scholar |

Alcázar R, Bitrián M, Bartels D, Koncz C, Altabella T, Tiburcio AF (2011) Polyamine metabolic canalization in response to drought stress in Arabidopsis and the resurrection plant Craterostigma plantagineum. Plant Signaling & Behavior 6, 243–250.
Polyamine metabolic canalization in response to drought stress in Arabidopsis and the resurrection plant Craterostigma plantagineum.Crossref | GoogleScholarGoogle Scholar |

Alcázar R, Bueno M, Tiburcio AF (2020) Polyamines: small amines with large effects on plant abiotic stress tolerance. Cells 9, 2373
Polyamines: small amines with large effects on plant abiotic stress tolerance.Crossref | GoogleScholarGoogle Scholar |

Amede T, Schubert S (2003) Mechanisms of drought resistance in seed legumes. I. Osmotic adjustment. SINET Ethiopian Journal of Science 26, 37–46.

Aneja B, Yadav NR, Kumar N, Yadav RC (2015) Hsp transcript induction is correlated with physiological changes under drought stress in Indian mustard. Physiology and Molecular Biology of Plants 21, 305–316.
Hsp transcript induction is correlated with physiological changes under drought stress in Indian mustard.Crossref | GoogleScholarGoogle Scholar | 26261395PubMed |

Awan SA, Khan I, Rizwan M, Zhang X, Brestic M, Khan A, El-Sheikh MA, Alyemeni MN, Ali S, Huang L (2021) Exogenous abscisic acid and jasmonic acid restrain polyethylene glycol-induced drought by improving the growth and antioxidative enzyme activities in pearl millet. Physiologia Plantarum 172, 809–819.
Exogenous abscisic acid and jasmonic acid restrain polyethylene glycol-induced drought by improving the growth and antioxidative enzyme activities in pearl millet.Crossref | GoogleScholarGoogle Scholar | 33094486PubMed |

Bae H, Kim S-H, Kim MS, Sicher RC, Lary D, Strem MD, Natarajan S, Bailey BA (2008) The drought response of Theobroma cacao (cacao) and the regulation of genes involved in polyamine biosynthesis by drought and other stresses. Plant Physiology and Biochemistry 46, 174–188.
The drought response of Theobroma cacao (cacao) and the regulation of genes involved in polyamine biosynthesis by drought and other stresses.Crossref | GoogleScholarGoogle Scholar | 18042394PubMed |

Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Australian Journal of Biological Sciences 15, 413–428.
A re-examination of the relative turgidity technique for estimating water deficits in leaves.Crossref | GoogleScholarGoogle Scholar |

Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant and Soil 39, 205–207.
Rapid determination of free proline for water-stress studies.Crossref | GoogleScholarGoogle Scholar |

Blum A, Ebercon A (1981) Cell membrane stability as a measure of drought and heat tolerance in wheat. Crop Science 21, 43–47.
Cell membrane stability as a measure of drought and heat tolerance in wheat.Crossref | GoogleScholarGoogle Scholar |

Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 722, 248–254.
A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar |

Capell T, Bassie L, Christou P (2004) Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proceedings of the National Academy of Sciences of the United States of America 101, 9909–9914.
Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress.Crossref | GoogleScholarGoogle Scholar | 15197268PubMed |

Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Molecular Biology Reporter 11, 113–116.
A simple and efficient method for isolating RNA from pine trees.Crossref | GoogleScholarGoogle Scholar |

Chen D, Shao Q, Yin L, Younis A, Zheng B (2019) Polyamine function in plants: metabolism, regulation on development, and roles in abiotic stress responses. Frontiers in Plant Science 9, 1945
Polyamine function in plants: metabolism, regulation on development, and roles in abiotic stress responses.Crossref | GoogleScholarGoogle Scholar | 30687350PubMed |

Cheng L, Sun R, Wang F, Peng Z, Kong F, Wu J, Cao J, Lu G (2012) Spermidine affects the transcriptome responses to high temperature stress in ripening tomato fruit. Journal of Zhejiang University-SCIENCE B 13, 283–297.
Spermidine affects the transcriptome responses to high temperature stress in ripening tomato fruit.Crossref | GoogleScholarGoogle Scholar | 22467370PubMed |

Dhindsa RS, Dhindsa PP, 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.
Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase.Crossref | GoogleScholarGoogle Scholar |

DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Analytical Chemistry 28, 350–356.
Colorimetric method for determination of sugars and related substances.Crossref | GoogleScholarGoogle Scholar |

Ebeed HT, Hassan NM, Aljarani AM (2017) Exogenous applications of polyamines modulate drought responses in wheat through osmolytes accumulation, increasing free polyamine levels and regulation of polyamine biosynthetic genes. Plant Physiology and Biochemistry 118, 438–448.
Exogenous applications of polyamines modulate drought responses in wheat through osmolytes accumulation, increasing free polyamine levels and regulation of polyamine biosynthetic genes.Crossref | GoogleScholarGoogle Scholar | 28743037PubMed |

Fang Y, Xiong L (2015) General mechanisms of drought response and their application in drought resistance improvement in plants. Cellular and Molecular Life Sciences 72, 673–689.
General mechanisms of drought response and their application in drought resistance improvement in plants.Crossref | GoogleScholarGoogle Scholar | 25336153PubMed |

FAO (2018) FAOSTAT database: Food and Agriculture Organization of the United Nations. Available at http://www.fao.org/faostat/en/#data/QC.

Farooq M, Wahid A, Lee D-J (2009) Exogenously applied polyamines increase drought tolerance of rice by improving leaf water status, photosynthesis and membrane properties. Acta Physiologiae Plantarum 31, 937–945.
Exogenously applied polyamines increase drought tolerance of rice by improving leaf water status, photosynthesis and membrane properties.Crossref | GoogleScholarGoogle Scholar |

Fu XZ, Huang Y, Xing F, Chun CP, Ling LL, Cao L, Peng LZ (2016) Changes in free polyamines and expression of polyamine metabolic genes under drought and high-temperature in Citrus sinensis. Biologia Plantarum 60, 793–798.
Changes in free polyamines and expression of polyamine metabolic genes under drought and high-temperature in Citrus sinensis.Crossref | GoogleScholarGoogle Scholar |

Gao H, Wang Y, Xu P, Zhang Z (2018) Overexpression of a WRKY transcription factor TaWRKY2 enhances drought stress tolerance in transgenic wheat. Frontiers in Plant Science 9, 997
Overexpression of a WRKY transcription factor TaWRKY2 enhances drought stress tolerance in transgenic wheat.Crossref | GoogleScholarGoogle Scholar | 30131813PubMed |

Guo X, Zhang L, Wang X, Zhang M, Xi Y, Wang A, Zhu J (2019) Overexpression of Saussurea involucrata dehydrin gene SiDHN promotes cold and drought tolerance in transgenic tomato plants. PLoS ONE 14, e0225090
Overexpression of Saussurea involucrata dehydrin gene SiDHN promotes cold and drought tolerance in transgenic tomato plants.Crossref | GoogleScholarGoogle Scholar | 31738789PubMed |

Gupta K, Sengupta A, Chakraborty M, Gupta B (2016) Hydrogen peroxide and polyamines act as double edged swords in plant abiotic stress responses. Frontiers in Plant Science 7, 1343
Hydrogen peroxide and polyamines act as double edged swords in plant abiotic stress responses.Crossref | GoogleScholarGoogle Scholar | 27672389PubMed |

Harshavardhan VT, Van Son L, Seiler C, Junker A, Weigelt-Fischer K, Hlukas C, Altmann T, Sreenivasulu N, Bäumlein H, Kuhlmann M (2014) AtRD22 and AtUSPL1, members of the plant-specific BURP domain family involved in Arabidopsis thaliana drought tolerance. PLoS ONE 9, e110065
AtRD22 and AtUSPL1, members of the plant-specific BURP domain family involved in Arabidopsis thaliana drought tolerance.Crossref | GoogleScholarGoogle Scholar | 25333723PubMed |

Hasan MM, Skalicky M, Jahan MS, Hossain MN, Anwar Z, Nie Z-F, Alabdallah NM, Brestic M, Hejnak V, Fang X-W (2021) Spermine: its emerging role in regulating drought stress responses in plants. Cells 10, 261
Spermine: its emerging role in regulating drought stress responses in plants.Crossref | GoogleScholarGoogle Scholar | 33525668PubMed |

Hasheminasab H, Assad MT, Aliakbari A, Sahhafi SR (2012) Influence of drought stress on oxidative damage and antioxidant defense system in tolerant and susceptible wheat genotypes. Journal of Agricultural Science 4, 8–30.
Influence of drought stress on oxidative damage and antioxidant defense system in tolerant and susceptible wheat genotypes.Crossref | GoogleScholarGoogle Scholar |

Hendawey MH, Abdel Raheem EA, Kamel HA, Khalfallah GM, Mahmoud NE (2018) Assessment of the contribution of exogenous polyamines for water stress tolerance in faba bean. Bioscience Resarch 15, 956–966.

Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. California Agricultural Experiment Station 347, 1–32.

Hu L, Xiang L, Li S, Zou Z, Hu X-H (2016) Beneficial role of spermidine in chlorophyll metabolism and D1 protein content in tomato seedlings under salinity-alkalinity stress. Physiologia Plantarum 156, 468–477.
Beneficial role of spermidine in chlorophyll metabolism and D1 protein content in tomato seedlings under salinity-alkalinity stress.Crossref | GoogleScholarGoogle Scholar | 26477612PubMed |

Jiang D, Hou J, Gao W, Tong X, Li M, Chu X, Chen G (2021) Exogenous spermidine alleviates the adverse effects of aluminum toxicity on photosystem II through improved antioxidant system and endogenous polyamine contents. Ecotoxicology and Environmental Safety 207, 111265
Exogenous spermidine alleviates the adverse effects of aluminum toxicity on photosystem II through improved antioxidant system and endogenous polyamine contents.Crossref | GoogleScholarGoogle Scholar | 32920313PubMed |

Karkanis A, Ntatsi G, Lepse L, Fernández JA, Vågen IM, Rewald B, Alsiņa I, Kronberga A, Balliu A, Olle M, Bodner G, Dubova L, Rosa E, Savvas D (2018) Faba bean cultivation – revealing novel managing practices for more sustainable and competitive European cropping systems. Frontiers in Plant Science 9, 1115
Faba bean cultivation – revealing novel managing practices for more sustainable and competitive European cropping systems.Crossref | GoogleScholarGoogle Scholar | 30116251PubMed |

Kasukabe Y, He L, Nada K, Misawa S, Ihara I, Tachibana S (2004) Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana. Plant and Cell Physiology 45, 712–722.
Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 15215506PubMed |

Kharrat M, Ouchari H (2011) Faba bean status and prospects in Tunisia. Grain Legume 56, 11–12.

Khoshbakht D, Asghari MR, Haghighi M (2018) Influence of foliar application of polyamines on growth, gas-exchange characteristics, and chlorophyll fluorescence in Bakraii citrus under saline conditions. Photosynthetica 56, 731–742.
Influence of foliar application of polyamines on growth, gas-exchange characteristics, and chlorophyll fluorescence in Bakraii citrus under saline conditions.Crossref | GoogleScholarGoogle Scholar |

Kubiś J, Floryszak-Wieczorek J, Arasimowicz-Jelonek M (2014) Polyamines induce adaptive responses in water deficit stressed cucumber roots. Journal of Plant Research 127, 151–158.
Polyamines induce adaptive responses in water deficit stressed cucumber roots.Crossref | GoogleScholarGoogle Scholar | 23934013PubMed |

Li Z, Peng Y, Zhang X-Q, Pan M-H, Ma X, Huang L-K, Yan Y-H (2014) Exogenous spermidine improves water stress tolerance of white clover (Trifolium repens L.) involved in antioxidant defence, geneexpression and proline metabolism. Plant Omics Journal 7, 517–526.

Li Z, Zhou H, Peng Y, Zhang X, Ma X, Huang L, Yan Y (2015a) Exogenously applied spermidine improves drought tolerance in creeping bentgrass associated with changes in antioxidant defense, endogenous polyamines and phytohormones. Plant Growth Regulation 76, 71–82.
Exogenously applied spermidine improves drought tolerance in creeping bentgrass associated with changes in antioxidant defense, endogenous polyamines and phytohormones.Crossref | GoogleScholarGoogle Scholar |

Li Z, Zhang Y, Peng D, Wang X, Peng Y, He X, Zhang X, Ma X, Huang L, Yan Y (2015b) Polyamine regulates tolerance to water stress in leaves of white clover associated with antioxidant defense and dehydrin genes via involvement in calcium messenger system and hydrogen peroxide signaling. Frontiers in Physiology 6, 280
Polyamine regulates tolerance to water stress in leaves of white clover associated with antioxidant defense and dehydrin genes via involvement in calcium messenger system and hydrogen peroxide signaling.Crossref | GoogleScholarGoogle Scholar | 26528187PubMed |

Li L, Gu W, Li C, Li W, Li C, Li J, Wei S (2018a) Exogenous spermidine improves drought tolerance in maize by enhancing the antioxidant defence system and regulating endogenous polyamine metabolism. Crop & Pasture Science 69, 1076–1091.
Exogenous spermidine improves drought tolerance in maize by enhancing the antioxidant defence system and regulating endogenous polyamine metabolism.Crossref | GoogleScholarGoogle Scholar |

Li L, Gu W, Li J, Li C, Xie T, Qu D, Meng Y, Li C, Wei S (2018b) Exogenously applied spermidine alleviates photosynthetic inhibition under drought stress in maize (Zea mays L.) seedlings associated with changes in endogenous polyamines and phytohormones. Plant Physiology and Biochemistry 129, 35–55.
Exogenously applied spermidine alleviates photosynthetic inhibition under drought stress in maize (Zea mays L.) seedlings associated with changes in endogenous polyamines and phytohormones.Crossref | GoogleScholarGoogle Scholar | 29793181PubMed |

Li Y, Zhang S, Zhang N, Zhang W, Li M, Liu B, Shi Z (2019) MYB-CC transcription factor, TaMYBsm3, cloned from wheat is involved in drought tolerance. BMC Plant Biology 19, 143
MYB-CC transcription factor, TaMYBsm3, cloned from wheat is involved in drought tolerance.Crossref | GoogleScholarGoogle Scholar | 30987595PubMed |

Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochemical Society Transactions 11, 591–592.
Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents.Crossref | GoogleScholarGoogle Scholar |

Liu M, Chu M, Ding Y, Wang S, Liu Z, Tang S, Ding C, Li G (2015a) Exogenous spermidine alleviates oxidative damage and reduce yield loss in rice submerged at tillering stage. Frontiers in Plant Science 6, 919
Exogenous spermidine alleviates oxidative damage and reduce yield loss in rice submerged at tillering stage.Crossref | GoogleScholarGoogle Scholar | 26583021PubMed |

Liu J-H, Wang W, Wu H, Gong X, Moriguchi T (2015b) Polyamines function in stress tolerance: from synthesis to regulation. Frontiers in Plant Science 6, 827
Polyamines function in stress tolerance: from synthesis to regulation.Crossref | GoogleScholarGoogle Scholar | 26528300PubMed |

Marcińska I, Dziurka K, Waligórski P, Janowiak F, Skrzypek E, Warchoł M, Juzon K, Kapłoniak K, Czyczyło-Mysza IM (2020) Exogenous polyamines only indirectly induce stress tolerance in wheat growing in hydroponic culture under polyethylene glycol-induced osmotic stress. Life 10, 151
Exogenous polyamines only indirectly induce stress tolerance in wheat growing in hydroponic culture under polyethylene glycol-induced osmotic stress.Crossref | GoogleScholarGoogle Scholar |

Marco F, Alcázar R, Tiburcio AF, Carrasco P (2011) Interactions between polyamines and abiotic stress pathway responses unraveled by transcriptome analysis of polyamine overproducers. OMICS: A Journal of Integrative Biology 15, 775–781.
Interactions between polyamines and abiotic stress pathway responses unraveled by transcriptome analysis of polyamine overproducers.Crossref | GoogleScholarGoogle Scholar | 22011340PubMed |

Marco F, Busó E, Lafuente T, Carrasco P (2019) Spermine confers stress resilience by modulating abscisic acid biosynthesis and stress responses in arabidopsis plants. Frontiers in Plant Science 10, 972
Spermine confers stress resilience by modulating abscisic acid biosynthesis and stress responses in arabidopsis plants.Crossref | GoogleScholarGoogle Scholar | 31417589PubMed |

Michel BE, Kaufmann MR (1973) The osmotic potential of polyethylene glycol 6000. Plant Physiology 51, 914–916.
The osmotic potential of polyethylene glycol 6000.Crossref | GoogleScholarGoogle Scholar | 16658439PubMed |

Misra N, Gupta AK (2005) Effect of salt stress on proline metabolism in two high yielding genotypes of green gram. Plant Science 169, 331–339.

Mustafavi SH, Shekari F, Maleki HH (2016) Influence of exogenous polyamines on antioxidant defence and essential oil production in valerian (Valeriana officinalis L.) plants under drought stress. Acta agriculturae Slovenica 107, 81–91.
Influence of exogenous polyamines on antioxidant defence and essential oil production in valerian (Valeriana officinalis L.) plants under drought stress.Crossref | GoogleScholarGoogle Scholar |

Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology 22, 867–880.
Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts.Crossref | GoogleScholarGoogle Scholar |

Parkash V, Singh S (2020) A review on potential plant-based water stress indicators for vegetable crops. Sustainability 12, 3945
A review on potential plant-based water stress indicators for vegetable crops.Crossref | GoogleScholarGoogle Scholar |

Parvin S, Lee OR, Sathiyaraj G, Khorolragchaa A, Kim Y-J, Yang D-C (2014) Spermidine alleviates the growth of saline-stressed ginseng seedlings through antioxidative defense system. Gene 537, 70–78.
Spermidine alleviates the growth of saline-stressed ginseng seedlings through antioxidative defense system.Crossref | GoogleScholarGoogle Scholar | 24365592PubMed |

Paul S, Roychoudhury A (2017) Seed priming with spermine and spermidine regulates the expression of diverse groups of abiotic stress-responsive genes during salinity stress in the seedlings of indica rice varieties. Plant Gene 11, 124–132.

Qin L, Zhang X, Yan J, Fan L, Rong C, Mo C, Zhang M (2019) Effect of exogenous spermidine on floral induction, endogenous polyamine and hormone production, and expression of related genes in ‘Fuji’ apple (Malus domestica Borkh.). Scientific Reports 9, 12777
Effect of exogenous spermidine on floral induction, endogenous polyamine and hormone production, and expression of related genes in ‘Fuji’ apple (Malus domestica Borkh.).Crossref | GoogleScholarGoogle Scholar | 31484948PubMed |

Rong W, Qi L, Wang A, Ye X, Du L, Liang H, Xin Z, Zhang Z (2014) The ERF transcription factor TaERF3 promotes tolerance to salt and drought stresses in wheat. Plant Biotechnology Journal 12, 468–479.
The ERF transcription factor TaERF3 promotes tolerance to salt and drought stresses in wheat.Crossref | GoogleScholarGoogle Scholar | 24393105PubMed |

Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In ‘Bioinformatics methods and protocols: methods in molecular biology’. (Eds S Krawetz, S Misener) pp. 365–386. (Humana Press: Totowa)

Sagor GHM, Berberich T, Takahashi Y, Niitsu M, Kusano T (2013) The polyamine spermine protects Arabidopsis from heat stress-induced damage by increasing expression of heat shock-related genes. Transgenic Research 22, 595–605.
The polyamine spermine protects Arabidopsis from heat stress-induced damage by increasing expression of heat shock-related genes.Crossref | GoogleScholarGoogle Scholar |

Satish L, Rency AS, Ramesh M (2018) Spermidine sprays alleviate the water deficit-induced oxidative stress in finger millet (Eleusine coracana L. Gaertn.) plants. 3 Biotech 8, 63
Spermidine sprays alleviate the water deficit-induced oxidative stress in finger millet (Eleusine coracana L. Gaertn.) plants.Crossref | GoogleScholarGoogle Scholar | 29354374PubMed |

Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nature Protocols 3, 1101–1108.
Analyzing real-time PCR data by the comparative CT method.Crossref | GoogleScholarGoogle Scholar | 18546601PubMed |

Shu S, Chen L, Lu W, Sun J, Guo S, Yuan Y, Li J (2014) Effects of exogenous spermidine on photosynthetic capacity and expression of Calvin cycle genes in salt-stressed cucumber seedlings. Journal of Plant Research 127, 763–773.
Effects of exogenous spermidine on photosynthetic capacity and expression of Calvin cycle genes in salt-stressed cucumber seedlings.Crossref | GoogleScholarGoogle Scholar | 25069716PubMed |

Sohag AAM, Tahjib-Ul-Arif M, Brestič M, Afrin S, Sakil MA, Hossain MT, Hossain MA, Hossain MA (2020) Exogenous salicylic acid and hydrogen peroxide attenuate drought stress in rice. Plant, Soil and Environment 66, 7–13.
Exogenous salicylic acid and hydrogen peroxide attenuate drought stress in rice.Crossref | GoogleScholarGoogle Scholar |

Talaat NB, Shawky BT (2016) Dual application of 24-epibrassinolide and spermine confers drought stress tolerance in maize (Zea mays L.) by modulating polyamine and protein metabolism. Journal of Plant Growth Regulation 35, 518–533.
Dual application of 24-epibrassinolide and spermine confers drought stress tolerance in maize (Zea mays L.) by modulating polyamine and protein metabolism.Crossref | GoogleScholarGoogle Scholar |

Tavladoraki P, Cona A, Federico R, Tempera G, Viceconte N, Saccoccio S, Battaglia V, Toninello A, Agostinelli E (2012) Polyamine catabolism: target for antiproliferative therapies in animals and stress tolerance strategies in plants. Amino Acids 42, 411–426.
Polyamine catabolism: target for antiproliferative therapies in animals and stress tolerance strategies in plants.Crossref | GoogleScholarGoogle Scholar | 21874532PubMed |

Torabian S, Shakiba MR, Dabbagh Mohammadi Nasab A, Toorchi M (2018) Leaf gas exchange and grain yield of common bean exposed to spermidine under water stress. Photosynthetica 56, 1387–1397.
Leaf gas exchange and grain yield of common bean exposed to spermidine under water stress.Crossref | GoogleScholarGoogle Scholar |

Urbanek H, Kuzniak-Gebarowska E, Herka K (1991) Elicitation of defense responses in bean leaves by Botrytis cinerea polygalacturonase. Acta Physiologiae Plantarum (Poland) 13, 43–50.

Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Protective role of exogenous polyamines. Plant Science 151, 59–66.
Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Protective role of exogenous polyamines.Crossref | GoogleScholarGoogle Scholar |

Wi SJ, Kim WT, Park KY (2006) Overexpression of carnation S-adenosylmethionine decarboxylase gene generates a broad-spectrum tolerance to abiotic stresses in transgenic tobacco plants. Plant Cell Reports 25, 1111–1121.
Overexpression of carnation S-adenosylmethionine decarboxylase gene generates a broad-spectrum tolerance to abiotic stresses in transgenic tobacco plants.Crossref | GoogleScholarGoogle Scholar | 16642382PubMed |

Wu J, Shu S, Li C, Sun J, Guo S (2018) Spermidine-mediated hydrogen peroxide signaling enhances the antioxidant capacity of salt-stressed cucumber roots. Plant Physiology and Biochemistry 128, 152–162.
Spermidine-mediated hydrogen peroxide signaling enhances the antioxidant capacity of salt-stressed cucumber roots.Crossref | GoogleScholarGoogle Scholar | 29778839PubMed |

Xiang J, Chen X, Hu W, Xiang Y, Yan M, Wang J (2018) Overexpressing heat-shock protein OsHSP50.2 improves drought tolerance in rice. Plant Cell Reports 37, 1585–1595.
Overexpressing heat-shock protein OsHSP50.2 improves drought tolerance in rice.Crossref | GoogleScholarGoogle Scholar | 30099612PubMed |

Xue G-P, Way HM, Richardson T, Drenth J, Joyce PA, McIntyre CL (2011) Overexpression of TaNAC69 leads to enhanced transcript levels of stress upregulated genes and dehydration tolerance in bread wheat. Molecular Plant 4, 697–712.
Overexpression of TaNAC69 leads to enhanced transcript levels of stress upregulated genes and dehydration tolerance in bread wheat.Crossref | GoogleScholarGoogle Scholar | 21459832PubMed |