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

Enhancing antioxidant systems by exogenous spermine and spermidine in wheat (Triticum aestivum) seedlings exposed to salt stress

Abdelaleim I. ElSayed A F , Mohammed S. Rafudeen B , Mohamed A. M. El-hamahmy C , Dennis C. Odero D and M. Sazzad Hossain E
+ Author Affiliations
- Author Affiliations

A Biochemistry Department, Faculty of Agriculture, Zagazig University, 44519 Zagazig, Egypt.

B Department of Molecular and Cell Biology, University of Cape Town, Private Bag, Rondebosch, 7701, South Africa.

C Department of Agricultural Botany, Faculty of Agriculture, Suez Canal University, 41522 Ismailia, Egypt.

D Everglades Research and Education Centre, University of Florida-IFAS, 3200 East Palm Beach Road, Belle Glade, FL 33430, USA.

E Department of Biochemistry and Physiology of Plants, Faculty of Biology, Bielefeld University, Universitätsstr.25, D-33615, Bielefeld, Germany.

F Corresponding author. Email: aelsayed@zu.edu.eg

Functional Plant Biology 45(7) 745-759 https://doi.org/10.1071/FP17127
Submitted: 30 April 2017  Accepted: 22 January 2018   Published: 13 February 2018

Abstract

Plants have evolved complex mechanisms to mitigate osmotic and ionic stress caused by high salinity. The effect of exogenous spermine (Spm) and spermidine (Spd) on defence responses of wheat seedlings under NaCl stress was investigated by measuring antioxidant enzyme activities and the transcript expression of corresponding genes. Exogenous Spm and Spd decreased the level of malondialdehyde, increased chlorophyll and proline contents, and modulated PSII activity in wheat seedlings under salt stress. Spermidine alleviated negative effects on CO2 assimilation induced by salt stress in addition to significantly increasing the activity and content of ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco). It appears Spd conferred salinity tolerance in wheat seedlings by enhancing photosynthetic capacity through regulation of gene expression and the activity of key CO2 assimilation enzymes. Exogenous Spm regulated activities of different antioxidant enzymes (catalase, glutathione reductase, dehydroascorbate reductase, ascorbate peroxidase, and superoxide dismutase) and efficiently modulate their transcription levels in wheat seedlings under salt stress. It is likely that Spm plays a key role in alleviating oxidative damage of salt stress by adjusting antioxidant enzyme activities in plants. In addition, exogenous Spd increased transcript level of spermine synthase under salt stress. Salinity stress also caused an increase in transcript levels of diamine oxidase (DAO) and polyamine oxidase (PAO). Exogenous Spd application resulted in a marked increase in free Spd and Spm contents under saline conditions. These results show that exogenous Spd and Spm effectively upregulated transcriptional levels of antioxidant enzyme genes and improved the defence response of plants under salt stress.

Additional keywords: antioxidant enzymes, gene expression, salt stress, spermine, spermidine, wheat.


References

Aebi H (1984) Catalase in vitro. Methods in Enzymology 105, 121–126.
Catalase in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXltVKis7s%3D&md5=d1e5efb5535f4cb3a03607981d55b43eCAS |

Alcázar R, Tiburcio AF (2014) Plant polyamines in stress and development: an emerging area of research in plant sciences. Frontiers in Plant Science 5, 319
Plant polyamines in stress and development: an emerging area of research in plant sciences.Crossref | GoogleScholarGoogle Scholar |

Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. Journal of Experimental Botany 53, 1331–1341.
Role of superoxide dismutases (SODs) in controlling oxidative stress in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktFSlsL4%3D&md5=18465929b02c9afefbe329067c011196CAS |

Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373–399.
Reactive oxygen species: metabolism, oxidative stress, and signal transduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvFeisL0%3D&md5=187985f9d8c4a6274567637eb1db143eCAS |

Baker NR (1991) A possible role for photosystem II in environmental perturbations of photosynthesis. Physiologia Plantarum 81, 563–570.
A possible role for photosystem II in environmental perturbations of photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXktVGisrw%3D&md5=ec2d194872bbc75186b2721dd05e5d1fCAS |

Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and applicable to acrylamide gels. Analytical Biochemistry 44, 276–287.
Superoxide dismutase: improved assays and applicable to acrylamide gels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38XjtFKhsg%3D%3D&md5=9884aea03cf87103d8d28e66b996629aCAS |

Bouchereau A, Aziz A, Larher F, Martin-Tanguy J (1999) Polyamines and environmental challenges: recent development. Plant Science 140, 103–125.
Polyamines and environmental challenges: recent development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXivVOisA%3D%3D&md5=5594cdb67e6c042b1d17e54062cebee4CAS |

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.
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=90b0b14534fb4b0d25711d896ae5505eCAS |

Cai G, Sobieszczuk-Nowicka E, Aloisi I, Fattorini L, Serafini-Fracassini D, Del Duca S (2015) Polyamines are common players in different facets of plant programmed cell death. Amino Acids 47, 27–44.
Polyamines are common players in different facets of plant programmed cell death.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvFGjurvK&md5=132f748adfe5b9fa8a6ede17403909a0CAS |

Chai YY, Jiang CD, Shi L, Shi TS, Gu WB (2010) Effects of exogenous spermine on sweet sorghum during germination under salinity. Biologia Plantarum 54, 145–148.
Effects of exogenous spermine on sweet sorghum during germination under salinity.Crossref | GoogleScholarGoogle Scholar |

Chattopadhayay MK, Tiwari BS, Chattopadhyay G, Bose A, Sengupta DN, Ghosh B (2002) Protective role of exogenous polyamines on salinity-stressed rice (Oryza sativa) plants. Physiologia Plantarum 116, 192–199.
Protective role of exogenous polyamines on salinity-stressed rice (Oryza sativa) plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnslSktbw%3D&md5=dd582e2c1404d33d414ced2f7f31dcccCAS |

Drolet G (1986) Radical scavenging properties of polyamines. Phytochemistry 25, 367–371.
Radical scavenging properties of polyamines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XhtVCmtr0%3D&md5=99a2bde04bb488bd268dd1a74915a108CAS |

Duan JJ, Li J, Guo SR, Kang YY (2008) Exogenous spermidine affects polyamine metabolism in salinity-stressed Cucumis sativus roots and enhances short-term salinity tolerance. Journal of Plant Physiology 165, 1620–1635.
Exogenous spermidine affects polyamine metabolism in salinity-stressed Cucumis sativus roots and enhances short-term salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlOqu7jF&md5=c6ca410ee5d64c5fe26c39bd451c7a4fCAS |

Dzung NA, Khanh VTP, Dzung TT (2011) Research on impact of chitosan oligomers on biophysical characteristics, growth, development and drought resistance of coffee. Carbohydrate Polymers 84, 751–755.
Research on impact of chitosan oligomers on biophysical characteristics, growth, development and drought resistance of coffee.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXitVSqsrw%3D&md5=86e5e12044275d8a6d97e5bbef4050e2CAS |

Eller MH, Warner AL, Knap HT (2006) Genomic organization and expression analyses of putrescine pathway genes in soybean. Plant Physiology and Biochemistry 44, 49–57.
Genomic organization and expression analyses of putrescine pathway genes in soybean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjtFGis74%3D&md5=8a453b1f8381b386bb9a05a0ffe354f8CAS |

Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiology 155, 2–18.
Ascorbate and glutathione: the heart of the redox hub.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXksFags7g%3D&md5=0deb50e8c4c5a48c8848d4890813c003CAS |

Groppa MD, Benavides MP (2008) Polyamines and abiotic stress: recent advances. Amino Acids 34, 35–45.
Polyamines and abiotic stress: recent advances.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlt1CltA%3D%3D&md5=5e5c0147f9a027fceb6c65cafd531266CAS |

Ha HC, Sirisoma NS, Kuppusamy P, Zweier JL, Woster PM, Casero RA (1998) The natural polyamine spermine functions directly as a free radical scavenger. Proceedings of the National Academy of Sciences of the United States of America 95, 11140–11145.
The natural polyamine spermine functions directly as a free radical scavenger.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmt1ajurk%3D&md5=a3eb611765b254efcd99e424d5b25c1bCAS |

Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regulation 21, 79–102.
Metabolic implications of stress-induced proline accumulation in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjs1amtLY%3D&md5=20f9a0ff9799edd387d3831b616d9916CAS |

Hellmann H, Funck D, Rentsch D, Frommer WB (2000) Hypersensitivity of an Arabidopsis sugar signaling mutant toward exogenous proline application. Plant Physiology 123, 779–789.
Hypersensitivity of an Arabidopsis sugar signaling mutant toward exogenous proline application.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3cvit1Ohuw%3D%3D&md5=e0df1c066cd89ebde0e97616c88b14d9CAS |

Hossain MS, ElSayed AI, Moore M, Dietz KJ (2017) Redox and reactive oxygen species network in acclimation for salinity tolerance in sugar beet. Journal of Experimental Botany 68, 1283–1298.
Redox and reactive oxygen species network in acclimation for salinity tolerance in sugar beet.Crossref | GoogleScholarGoogle Scholar |

Hsu YT, Kao CH (2007) Cadmium-induced oxidative damage in rice leaves is reduced by polyamines. Plant and Soil 291, 27–37.
Cadmium-induced oxidative damage in rice leaves is reduced by polyamines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjsFygtbo%3D&md5=ac727f2794625badc3014a1836bd928dCAS |

Jimenez MS, Gonzalez-Rodriguez AM, Morales D, Cid MC, Socorro AR, Caballero M (1997) Evaluation of chlorophyll fluorescence as a tool for salt stress detection in roses. Photosynthetica 33, 291–301.
Evaluation of chlorophyll fluorescence as a tool for salt stress detection in roses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXisV2ksbo%3D&md5=e73171e742fb4d2377c560347ef9232fCAS |

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 | 1:CAS:528:DC%2BD2cXltlWrtbg%3D&md5=f8f5d99a0f6fbc78f9cf26aaf07fb0c9CAS |

Kasukabe Y, He LX, Watakabe Y, Otani M, Shimada T, Tachibana S (2006) Improvement of environmental stress tolerance of sweet potato by introduction of genes for spermidine synthase. Plant Biotechnology Journal 23, 75–83.
Improvement of environmental stress tolerance of sweet potato by introduction of genes for spermidine synthase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XktFaqs7s%3D&md5=863995312f7f1f84cfeb7400b45fb835CAS |

Kusano T, Yamaguchi K, Berberich T, Takahashi Y (2007) Advances in polyamine research in 2007. Journal of Plant Research 120, 345–350.
Advances in polyamine research in 2007.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXltFSrsL0%3D&md5=2ae6a4b7598939bebdb5d1e3ccfe1d32CAS |

Larkin MA, Blackshileds G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X ver. 2.0. Bioinformatics 23, 2947–2948.
Clustal W and Clustal X ver. 2.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlaqsL%2FM&md5=ef281f9d8bef5b720fc8d77f6657b8abCAS |

Lee KO, Jang HH, Jung BG, Chi YH, Lee JY, Choi YO, Lee JR, Lim CO, Cho MJ, Lee SY (2000) Rice 1Cys-peroxiredoxin overexpressed in transgenic tobacco does not maintain dormancy but enhances antioxidant activity. FEBS Letters 486, 103–106.
Rice 1Cys-peroxiredoxin overexpressed in transgenic tobacco does not maintain dormancy but enhances antioxidant activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXoslGhsr8%3D&md5=72ae095fa6aef5a492606ddce623f02dCAS |

Li Sh, Jin H, Zhang Q (2016) The effect of exogenous spermidine concentration on polyamine metabolism and salt tolerance in zoysiagrass (Zoysia japonica steud) subjected to short-term salinity stress. Frontiers in Plant Science 7, 1221
The effect of exogenous spermidine concentration on polyamine metabolism and salt tolerance in zoysiagrass (Zoysia japonica steud) subjected to short-term salinity stress.Crossref | GoogleScholarGoogle Scholar |

Lichtenthaler HK (1987) Chlorophylls and carotenoids, the pigments of photosynthetic biomembranes. Methods in Enzymology 148, 350–382.
Chlorophylls and carotenoids, the pigments of photosynthetic biomembranes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXhs1Cgu78%3D&md5=99801d40c01e4b1b98dc9c06df6e4e16CAS |

Liu J, Kitashiba H, Wang J, Ban Y, Moriguchi T (2007) Polyamines and their ability to provide environmental stress tolerance to plants. Plant Biotechnology 24, 117–126.
Polyamines and their ability to provide environmental stress tolerance to plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkvFWnu7o%3D&md5=87a9be556245ddb7bf1cb0fd4bcc7166CAS |

Lu C, Jiang GM, Wang B, Kuang T (2003) Photosystem II photochemistry and photosynthetic pigment composition in salt-adapted halophyte Artimisia anethifolia grown under outdoor conditions. Journal of Plant Physiology 160, 403–408.
Photosystem II photochemistry and photosynthetic pigment composition in salt-adapted halophyte Artimisia anethifolia grown under outdoor conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXksVOjsrw%3D&md5=cf2843a6c11a7bf1ed43044ef0e37e9dCAS |

Lu KX, Cao BH, Feng XP, He Y, Jiang DA (2009) Photosynthetic response of salt-tolerant and sensitive soybean varieties. Photosynthetica 47, 381–387.
Photosynthetic response of salt-tolerant and sensitive soybean varieties.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlyqsbrM&md5=bb1131fc652e08d9ea19b3d5cedc2c87CAS |

M–STAT (1990) ‘A microcomputer program for the design, management and analysis of agronomic research experiments.’ (Michigan State University: East Lansing, MI, USA)

Madhava Rao KV, Sresty TVS (2000) Antioxidative parameters in the seedlings of pigeon pea (Cajanus cajan L. Millspaugh) in response to Zn and Ni stresses. Plant Science 157, 113–128.
Antioxidative parameters in the seedlings of pigeon pea (Cajanus cajan L. Millspaugh) in response to Zn and Ni stresses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsFCjtL4%3D&md5=76cee77421d67be126b437d02edee756CAS |

Mandhania S, Madan S, Sawhney V (2006) Antioxidant defense mechanism under salt stress in wheat seedlings. Biologia Plantarum 50, 227–231.
Antioxidant defense mechanism under salt stress in wheat seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjvFCitb4%3D&md5=e1394dcfe48f45e5cad6b5a98ee1bc01CAS |

Martin-Tanguy J (2001) Metabolism and function of polyamines in plants: recent development (new approaches). Plant Growth Regulation 34, 135–148.
Metabolism and function of polyamines in plants: recent development (new approaches).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXovVyrsLo%3D&md5=5f3311d5c1c45d8c4c02a27db0171469CAS |

Meloni DA, Oliva MA, Martinez CA, Cambraia J (2003) Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environmental and Experimental Botany 49, 69–76.
Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XpsFars7Y%3D&md5=8f4b5754c91dd94257518ca9d722d21eCAS |

Minocha R, Majumdar R, Minocha SC (2014) Polyamines and abiotic stress in plants: a complex relationship. Frontiers in Plant Science 5, 175
Polyamines and abiotic stress in plants: a complex relationship.Crossref | GoogleScholarGoogle Scholar |

Mishra P, Bhoomika K, Dubey RS (2013) Differential responses of antioxidative defense system to prolonged salinity stress in salt-tolerant and salt-sensitive Indica rice (Oryza sativa L.) seedlings. Protoplasma 250, 3–19.
Differential responses of antioxidative defense system to prolonged salinity stress in salt-tolerant and salt-sensitive Indica rice (Oryza sativa L.) seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVyqtLo%3D&md5=74ee43d5b961e48ab62dd9a9530cc53aCAS |

Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends in Plant Science 9, 490–498.
Reactive oxygen gene network of plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXotF2msrg%3D&md5=1bb7f852ef42e9acdce7db3cf0b3bdc0CAS |

Moustakas M, Sperdouli I, Kouna T, Antonopoulou CI, Therios I (2011) Exogenous proline induces soluble sugar accumulation and alleviates drought stress effects on photosystem II functioning of Arabidopsis thaliana leaves. Plant Growth Regulation 65, 315–325.
Exogenous proline induces soluble sugar accumulation and alleviates drought stress effects on photosystem II functioning of Arabidopsis thaliana leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtleru7fK&md5=853c9e3ab04bb63c0e916ddc2cf7b5afCAS |

Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology 49, 249–279.
Ascorbate and glutathione: keeping active oxygen under control.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjvVShtrc%3D&md5=0ee6e59d84de9561129285a5b1a7ceb9CAS |

Ohe M, Kobayashi M, Niitsu M, Bagni N, Matsuzaki S (2005) Analysis of polyamine metabolism in soybean seedlings using 15N-labelled putrescine. Phytochemistry 66, 523–528.
Analysis of polyamine metabolism in soybean seedlings using 15N-labelled putrescine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhsVyks7c%3D&md5=b7a6f28f53d3a662db55f463bdabe806CAS |

Peremarti A, Bassie L, Christou P, Capell T (2009) Spermine facilitates recovery from drought but does not confer drought tolerance in transgenic rice plants expressing Datura stramonium S-adenosylmethionine decarboxylase. Plant Molecular Biology 70, 253–264.
Spermine facilitates recovery from drought but does not confer drought tolerance in transgenic rice plants expressing Datura stramonium S-adenosylmethionine decarboxylase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltlygtbo%3D&md5=8076fc26dc1b94adb0341f83f8e7e916CAS |

Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, e45
A new mathematical model for relative quantification in real-time RT-PCR.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38nis12jtw%3D%3D&md5=15aa2bf3061ac5fcd9c20e8f4dae7ce5CAS |

Rouhier N, Jacquot JP (2002) Plant peroxiredoxins: alternative hydroperoxide scavenging enzymes. Photosynthesis Research 74, 259–268.
Plant peroxiredoxins: alternative hydroperoxide scavenging enzymes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XptFeiur0%3D&md5=b470ce427a8e90c95fa5bf11568b3b2bCAS |

Roy P, Niyogi K, SenGupta DN, Ghosh B (2005) Spermidine treatment to rice seedlings recovers salinity stress induced damage of plasma membrane and PM-bound H+ ATPase in salt-tolerant and salt-sensitive rice cultivars. Plant Science 168, 583–591.
Spermidine treatment to rice seedlings recovers salinity stress induced damage of plasma membrane and PM-bound H+ ATPase in salt-tolerant and salt-sensitive rice cultivars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXosVGjtg%3D%3D&md5=e39c3784a9a314b1921c8993a96950b8CAS |

Roychoudhury A, Basu S, Sengupta DN (2011) Amelioration of salinity stress by exogenously applied spermidine or spermine in three varieties of indica rice differing in their level of salt tolerance. Journal of Plant Physiology 168, 317–328.
Amelioration of salinity stress by exogenously applied spermidine or spermine in three varieties of indica rice differing in their level of salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXntVemtA%3D%3D&md5=ab0bde23682ea6a13be3e6377cc5cce2CAS |

Ruijter JM, Ramakers C, Hoogaars W, Bakker O, van den Hoff MJB, Karlen Y, Moorman AFM (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Research 37, e45
Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M3lslGhtA%3D%3D&md5=924b37c1a1013fc7381413d8d6c0ca24CAS |

Saha J, Brauer EK, Sengupta A, Popescu SC, Gupta K, Gupta B (2015) Polyamines as redox homeostasis regulators during salt stress in plants. Frontiers in Environmental Science 3, 21
Polyamines as redox homeostasis regulators during salt stress in plants.Crossref | GoogleScholarGoogle Scholar |

Sharma P, Rajam MV (1995) Spatial and temporal changes in endogenous polyamine levels associated with osmotic embryogenesis from different hypocotyls segments of eggplant (Solanum melongena L.). Journal of Plant Physiology 146, 658–664.
Spatial and temporal changes in endogenous polyamine levels associated with osmotic embryogenesis from different hypocotyls segments of eggplant (Solanum melongena L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXotlOnsr4%3D&md5=673b1847477af5e3faa67f1090608aeaCAS |

Shelp BJ, Bozzo GG, Trobacher CP, Zarei A, Deyman KL, Brikis CJ (2012) Hypothesis/review: contribution of putrescine to 4-aminobutyrate (GABA) production in response to abiotic stress. Plant Science 193–194, 130–135.
Hypothesis/review: contribution of putrescine to 4-aminobutyrate (GABA) production in response to abiotic stress.Crossref | GoogleScholarGoogle Scholar |

Shen WY, Nada K, Tachibana S (2000) Involvement of polyamines in the chilling tolerance of cucumber cultivars. Plant Physiology 124, 431–440.
Involvement of polyamines in the chilling tolerance of cucumber cultivars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmvVGhtbk%3D&md5=1ccb1caeaf56a534c18079376f106639CAS |

Shu S, Yuan L-Y, Guo S-R, Sun J, Liu C-J (2012) Effects of exogenous spermidine on photosynthesis, xanthophyll cycle and endogenous polyamines in cucumber seedlings exposed to salinity. African Journal of Biotechnology 11, 6064–6074.
Effects of exogenous spermidine on photosynthesis, xanthophyll cycle and endogenous polyamines in cucumber seedlings exposed to salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltlOjuro%3D&md5=b1135d629d1d41c8d41e5b11d1ee1529CAS |

Shu Sh, Chen L, Lu W, Sun J, Guo Sh, 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 | 1:CAS:528:DC%2BC2cXht1GksL%2FL&md5=0ba664a874e5722500cfbaab6b788164CAS |

Sivakumar P, Sharmila P, Pardha Saradhi P (2000) Proline alleviates salt-stress-induced enhancement in ribulose-1,5-bisphosphate oxygenase activity. Biochemical and Biophysical Research Communications 279, 512–515.
Proline alleviates salt-stress-induced enhancement in ribulose-1,5-bisphosphate oxygenase activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXovVCmsr4%3D&md5=3e46b9da53397e2a39b8f9f40c59b8f2CAS |

Spreitzer RJ (2003) Role of the small subunit in ribulose-1,5-bisphosphate carboxylase/oxygenase. Archives of Biochemistry and Biophysics 414, 141–149.
Role of the small subunit in ribulose-1,5-bisphosphate carboxylase/oxygenase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktFGjtrk%3D&md5=e32adb3e3b02dacb6fce7700fc3ebb62CAS |

Steel RGD, Torrie JH, Diskey DA (1997) ‘Principles and procedures of statistics: a biometrical approach.’ (3rd edn) (McGraw-Hill: New York)

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.
MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1eiu73K&md5=61a02c06ad66ae9e0d7acd1c8b402861CAS |

Tang W, Newton RJ (2005) Polyamines reduce salt-induced oxidative damage by increasing the activities of antioxidant enzymes and decreasing lipid peroxidation in Virginia pine. Plant Growth Regulation 46, 31–43.
Polyamines reduce salt-induced oxidative damage by increasing the activities of antioxidant enzymes and decreasing lipid peroxidation in Virginia pine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtVymt7w%3D&md5=f58d2968d3f26a03f9b85c358ef60e98CAS |

Tiburcio A, Altabella T, Bitrián M, Alcázar R (2014) The roles of polyamines during the lifespan of plants: from development to stress. Planta 240, 1–18.
The roles of polyamines during the lifespan of plants: from development to stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXkslemsbc%3D&md5=1ce775c3e2cff050c4465b3b8341a78bCAS |

Tuteja N, Ahmad P, Panda BB, Tuteja R (2009) Genotoxic stress in plants: shedding light on DNA damage, repair and DNA repair helicases. Mutation Research/Reviews in Mutation Research 681, 134–149.
Genotoxic stress in plants: shedding light on DNA damage, repair and DNA repair helicases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFOlt7o%3D&md5=cd46d25270c188a2f22aa35206abb58fCAS |

Verma S, Mishra SN (2005) Putrescine alleviation of growth in salt stressed Brassica juncea by inducing antioxidative defense system. Journal of Plant Physiology 162, 669–677.
Putrescine alleviation of growth in salt stressed Brassica juncea by inducing antioxidative defense system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXntVSmtL8%3D&md5=95bd7e68c3a73c4cbf48122ebc8f024aCAS |

Vicente O, Boscaiu M, Naranjo MA, Estrelles E, Belles JM, Soriano P (2004) Responses to salt stress in the halophyte Plantago crassifolia (Plantaginaceae). Journal of Arid Environments 58, 463–481.
Responses to salt stress in the halophyte Plantago crassifolia (Plantaginaceae).Crossref | GoogleScholarGoogle Scholar |

Walden R, Cordeiro A, Tiburcio AF (1997) Polyamines: small molecules triggering pathways in plant growth and development. Plant Physiology 113, 1009–1013.
Polyamines: small molecules triggering pathways in plant growth and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXis1Glsbc%3D&md5=9c5532d2af77034d847b4924e729f03cCAS |

Wang H, Gu M, Cui J, Shi K, Zhou Y, Yu J (2009) Effects of light quality on CO2 assimilation, chlorophyll-fluorescence quenching, expression of Calvin cycle genes and carbohydrate accumulation in Cucumis sativus. Journal of Photochemistry and Photobiology. B, Biology 96, 30–37.
Effects of light quality on CO2 assimilation, chlorophyll-fluorescence quenching, expression of Calvin cycle genes and carbohydrate accumulation in Cucumis sativus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXms1yhtr0%3D&md5=435cc50a6f8b8d25594e315a5c62eba4CAS |

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 | 1:CAS:528:DC%2BD28XptVertro%3D&md5=f164793b99ee6913dfba2828a6393b35CAS |

Woodward AJ, Bennett IJ (2005) The effect of salt stress and abscisic acid on proline production, chlorophyll content and growth of in vitro propagated shoots of Eucalyptus camaldulensis. Plant Cell, Tissue and Organ Culture 82, 189–200.
The effect of salt stress and abscisic acid on proline production, chlorophyll content and growth of in vitro propagated shoots of Eucalyptus camaldulensis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjvVKnsb4%3D&md5=a314225d961c0b5b07580f5025a4985bCAS |

Yue Y, Zhang M, Zhang J, Duan L, Li Z (2012) SOS1 gene overexpression increased salt tolerance in transgenic tobacco by maintaining a higher K+/Na+ ratio. Journal of Plant Physiology 169, 255–261.
SOS1 gene overexpression increased salt tolerance in transgenic tobacco by maintaining a higher K+/Na+ ratio.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XoslSqsw%3D%3D&md5=5e98c206242ab8a687169e301c6b2886CAS |

Zhang RH, Li J, Guo SR, Tezuka T (2009) Effects of exogenous putrescine on gas-exchange characteristics and chlorophyll fluorescence of NaCl-stressed cucumber seedlings. Photosynthesis Research 100, 155–162.
Effects of exogenous putrescine on gas-exchange characteristics and chlorophyll fluorescence of NaCl-stressed cucumber seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXotVKjs7Y%3D&md5=1312a7e41a327f3da90e433b90718757CAS |

Zou P, Li K, Liu S, He X, Zhang X, Xing R, Li P (2016) Effect of sulfated chitooligosaccharides on wheat seedlings (Triticum aestivum L.) under salt stress. Journal of Agricultural and Food Chemistry 64, 2815–2821.
Effect of sulfated chitooligosaccharides on wheat seedlings (Triticum aestivum L.) under salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xjt1OhtLk%3D&md5=b7c8d081191b9a70f00bbc1b001c533dCAS |