Polyamines effectively mitigate senescence in persistent leaves of Berginia ciliata – a novel model system
Foziya Altaf A , Shazia Parveen A , Sumira Farooq A , Aehsan ul Haq A , Mohammad Lateef Lone A , Inayatullah Tahir A * , Prashant Kaushik B and Hamed A. El-Serehy CA Plant Physiology and Biochemistry Research Laboratory, Department of Botany, University of Kashmir, Srinagar 190006, India.
B Instituto de Conservación y Mejora de la Agrodiversidad Valenciana, Universitat Politècnica de València, 46022 Valencia, Spain.
C Department of Zoology, College of Science, King Saud University, Riyadh 11451, Saudi Arabia.
Functional Plant Biology - https://doi.org/10.1071/FP21273
Submitted: 7 September 2021 Accepted: 10 January 2022 Published online: 11 February 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Plant leaves provide a unique insight into the changes that occur in organs, tissues and cells as they approach senescence. As part of the parental outlay, plants instigate leaf senescence to reallocate resources from older tissues to new organs towards the termination of the growing season. The aim of crop breeding initiatives is to optimize senescence for specific species. Considering hormonal regulation and their crosstalk during leaf senescence through integration of developmental signals, this work examines the efficacy of polyamines (PAs) in modulating several biochemical and physiological aspects with an ultimate aim to delay leaf senescence in leaf discs of Berginia ciliata (Haw.) sternb. Leaf discs were treated with putrescine (Put), spermidine (Spd) and spermine (Spm) at 20 μM, 20 μM and 15 μM concentration, respectively. A set of leaf discs kept in distilled water served as the control. Leaf discs treated with PAs were green and fresh by about 4 days compared to the control, thus exhibited delayed senescence. This delayed leaf senescence corroborated with the maintenance of high activity of reactive oxygen species (ROS) scavenging antioxidant enzymes viz, superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX) and higher content of chlorophylls. A marked increase was also observed in membrane stability and soluble proteins in leaf discs treated with PAs. Exogenous PAs reduced oxidative stress in the leaf discs, as revealed by lower malondialdehyde (MDA) level, which is manifested as reduced lipid peroxidation (LPO). Improved membrane stability was proportional to lower LPO, as measured by the membrane stability index (MSI).
Keywords: Berginia ciliata, chlorophyll, oxidative stress, putrescine, ROS, senescence, spermidine, spermine.
References
Aebi H (1984) [13] Catalase in vitro. In ‘Methods in enzymology. Vol. 105’. (Ed. E Beutler) pp. 121–126. (Academic Press)Agami RA (2016) Pre-soaking in indole-3-acetic acid or spermidine enhances copper tolerance in wheat seedlings. South African Journal of Botany 104, 167–174.
| Pre-soaking in indole-3-acetic acid or spermidine enhances copper tolerance in wheat seedlings.Crossref | GoogleScholarGoogle Scholar |
Ahmad A, Ali A (2019) Improvement of postharvest quality, regulation of antioxidants capacity and softening enzymes activity of cold-stored carambola in response to polyamines application. Postharvest Biology and Technology 148, 208–217.
| Improvement of postharvest quality, regulation of antioxidants capacity and softening enzymes activity of cold-stored carambola in response to polyamines application.Crossref | GoogleScholarGoogle Scholar |
Ahmad P, Jaleel CA, Salem MA, Nabi G, Sharma S (2010) Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress. Critical Reviews in Biotechnology 30, 161–175.
| Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress.Crossref | GoogleScholarGoogle Scholar | 20214435PubMed |
Ahmad P, Tripathi DK, Deshmukh R, Pratap Singh V, Corpas FJ (2019) Revisiting the role of ROS and RNS in plants under changing environment. Environmental and Experimental Botany 161, 1–3.
| Revisiting the role of ROS and RNS in plants under changing environment.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 |
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology 24, 1–15.
| Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris.Crossref | GoogleScholarGoogle Scholar | 16654194PubMed |
Aronova EE, Shevyakova NI, Stetsenko LA, Kuznetsov VV (2005) Cadaverine-induced induction of superoxide dismutase gene expression in Mesembryanthemum crystallinum L. Doklady Biological Sciences 403, 257–259.
| Cadaverine-induced induction of superoxide dismutase gene expression in Mesembryanthemum crystallinum L.Crossref | GoogleScholarGoogle Scholar | 16358565PubMed |
Arora A, Sairam R, Srivastava G (2002) Oxidative stress and antioxidative system in plants. Current Science 82, 1227–1238.
Axerold B, Chesbrough T, Laakso S (1981) Lipoxygenase from soybeans. In ‘Methods in enzymology’. (Ed. JM Lowenstein) pp. 441–451. (Academic Press: New York)
Banerjee A, Roychoudhury A (2016) Group II late embryogenesis abundant (LEA) proteins: structural and functional aspects in plant abiotic stress. Plant Growth Regulation 79, 1–17.
| Group II late embryogenesis abundant (LEA) proteins: structural and functional aspects in plant abiotic stress.Crossref | GoogleScholarGoogle Scholar |
Baniasadi F, Saffari VR, Maghsoudi Moud AA (2018) Physiological and growth responses of Calendula officinalis L. plants to the interaction effects of polyamines and salt stress. Scientia Horticulturae 234, 312–317.
| Physiological and growth responses of Calendula officinalis L. plants to the interaction effects of polyamines and salt stress.Crossref | GoogleScholarGoogle Scholar |
Bano C, Amist N, Singh NB (2020) Role of polyamines in plants abiotic stress tolerance: advances and future prospects. In ‘Plant life under changing environment’. (Eds DK Tripathi, DK Chauhan, SM Prasad, N Ramawat) pp. 481–496. (Academic Press)
Besford RT, Richardson CM, Campos JL, Tiburcio AF (1993) Effect of polyamines on stabilization of molecular complexes in thylakoid membranes of osmotically stressed oat leaves. Planta 189, 201–206.
| Effect of polyamines on stabilization of molecular complexes in thylakoid membranes of osmotically stressed oat leaves.Crossref | GoogleScholarGoogle Scholar |
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 | 942051PubMed |
Breeze E, Harrison E, McHattie S, et al. (2011) High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. The Plant Cell 23, 873–894.
| High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation.Crossref | GoogleScholarGoogle Scholar | 21447789PubMed |
Che-Husin N-M, Joyce DC, Irving DE (2018) Gel xylem occlusions decrease hydraulic conductance of cut Acacia holosericea foliage stems. Postharvest Biology and Technology 135, 27–37.
| Gel xylem occlusions decrease hydraulic conductance of cut Acacia holosericea foliage stems.Crossref | GoogleScholarGoogle Scholar |
Chen G-X, Asada K (1989) Ascorbate peroxidase in tea leaves: occurrence of two isozymes and the differences in their enzymatic and molecular properties. Plant and Cell Physiology 30, 987–998.
| Ascorbate peroxidase in tea leaves: occurrence of two isozymes and the differences in their enzymatic and molecular properties.Crossref | GoogleScholarGoogle Scholar |
Chen D, Wang S, Qi L, Yin L, Deng X (2018) Galactolipid remodeling is involved in drought-induced leaf senescence in maize. Environmental and Experimental Botany 150, 57–68.
| Galactolipid remodeling is involved in drought-induced leaf senescence in maize.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 |
Dhindsa RS, Plumb-Dhindsa P, 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 |
Doganlar ZB, Demir K, Basak H, Gul I (2010) Effects of salt stress on pigment and total soluble protein contents of three different tomato cultivars. African Journal of Agricultural Research 5, 2056–2065.
| Effects of salt stress on pigment and total soluble protein contents of three different tomato cultivars.Crossref | GoogleScholarGoogle Scholar |
Ezhilmathi K, Singh VP, Arora A, Sairam RK (2007) Effect of 5-sulfosalicylic acid on antioxidant activity in relation to vase life of Gladiolus cut flowers. Plant Growth Regulation 51, 99–108.
| Effect of 5-sulfosalicylic acid on antioxidant activity in relation to vase life of Gladiolus cut flowers.Crossref | GoogleScholarGoogle Scholar |
Gao F, Mei X, Li Y, Guo J, Shen Y (2021) Update on the roles of polyamines in fleshy fruit ripening, senescence, and quality. Frontiers in Plant Science 12, 140
| Update on the roles of polyamines in fleshy fruit ripening, senescence, and quality.Crossref | GoogleScholarGoogle Scholar |
Ghadakchiasl A, Mozafari A-a, Ghaderi N (2017) Mitigation by sodium nitroprusside of the effects of salinity on the morpho-physiological and biochemical characteristics of Rubus idaeus under in vitro conditions. Physiology and Molecular Biology of Plants 23, 73–83.
| Mitigation by sodium nitroprusside of the effects of salinity on the morpho-physiological and biochemical characteristics of Rubus idaeus under in vitro conditions.Crossref | GoogleScholarGoogle Scholar | 28250585PubMed |
Ghassemi S, Farhangi-Abriz S, Faegi-Analou R, Ghorbanpour M, Lajayer BA (2018) Monitoring cell energy, physiological functions and grain yield in field-grown mung bean exposed to exogenously applied polyamines under drought stress. Journal of Soil Science and Plant Nutrition 18, 1108–1125.
| Monitoring cell energy, physiological functions and grain yield in field-grown mung bean exposed to exogenously applied polyamines under drought stress.Crossref | GoogleScholarGoogle Scholar |
Girondé A, Poret M, Etienne P, Trouverie J, Bouchereau A, Le Cahérec F, Leport L, Niogret M-F, Avice J-C (2016) A comparative study of proteolytic mechanisms during leaf senescence of four genotypes of winter oilseed rape highlighted relevant physiological and molecular traits for NRE improvement. Plants 5, 1
| A comparative study of proteolytic mechanisms during leaf senescence of four genotypes of winter oilseed rape highlighted relevant physiological and molecular traits for NRE improvement.Crossref | GoogleScholarGoogle Scholar |
Gomez FM, Carrión CA, Costa ML, Desel C, Kieselbach T, Funk C, Krupinska K, Guiamet J (2019) Extra-plastidial degradation of chlorophyll and photosystem I in tobacco leaves involving ‘senescence-associated vacuoles’. The Plant Journal 99, 465–477.
| Extra-plastidial degradation of chlorophyll and photosystem I in tobacco leaves involving ‘senescence-associated vacuoles’.Crossref | GoogleScholarGoogle Scholar | 30985038PubMed |
Guo Y, Gan S (2005) Leaf senescence: signals, execution, and regulation. In ‘Current topics in developmental biology. Vol. 71’. (Ed. G Schatten) pp. 83–112. (Academic Press)
Guo P, Li Z, Huang P, Li B, Fang S, Chu J, Guo H (2017) A tripartite amplification loop involving the transcription factor WRKY75, salicylic acid, and reactive oxygen species accelerates leaf senescence. The Plant Cell 29, 2854–2870.
| A tripartite amplification loop involving the transcription factor WRKY75, salicylic acid, and reactive oxygen species accelerates leaf senescence.Crossref | GoogleScholarGoogle Scholar | 29061866PubMed |
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125, 189–198.
| Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation.Crossref | GoogleScholarGoogle Scholar | 5655425PubMed |
James M, Poret M, Masclaux-Daubresse C, Marmagne A, Coquet L, Jouenne T, Chan P, Trouverie J, Etienne P (2018) SAG12, a major cysteine protease involved in nitrogen allocation during senescence for seed production in Arabidopsis thaliana. Plant and Cell Physiology 59, 2052–2063.
| SAG12, a major cysteine protease involved in nitrogen allocation during senescence for seed production in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 29982633PubMed |
Jibran R, Donald AH, Paul PD (2013) Hormonal regulation of leaf senescence through integration of developmental and stress signals. Plant Molecular Biology 82, 547–561.
| Hormonal regulation of leaf senescence through integration of developmental and stress signals.Crossref | GoogleScholarGoogle Scholar | 23504405PubMed |
Joshi S, Choukimath A, Isenegger D, Panozzo J, Spangenberg G, Kant S (2019) Improved wheat growth and yield by delayed leaf senescence using developmentally regulated expression of a cytokinin biosynthesis gene. Frontiers in Plant Science 10, 1285
| Improved wheat growth and yield by delayed leaf senescence using developmentally regulated expression of a cytokinin biosynthesis gene.Crossref | GoogleScholarGoogle Scholar | 31681380PubMed |
Kamiab F, Tavassolian I, Hosseinifarahi M (2020) Biologia futura: the role of polyamine in plant science. Biologia Futura 71, 183–194.
| Biologia futura: the role of polyamine in plant science.Crossref | GoogleScholarGoogle Scholar | 34554509PubMed |
Kaur-Sawhney R, Shih L-m, Cegielska T, Galston AW (1982) Inhibition of protease activity by polyamines: relevance for control of leaf senescence. FEBS Letters 145, 345–349.
| Inhibition of protease activity by polyamines: relevance for control of leaf senescence.Crossref | GoogleScholarGoogle Scholar |
Killiny N, Nehela Y (2020) Citrus polyamines: structure, biosynthesis, and physiological functions. Plants 9, 426
| Citrus polyamines: structure, biosynthesis, and physiological functions.Crossref | GoogleScholarGoogle Scholar |
Kim H-S, Jin C-D (2006) Polyamines as antioxidant protectors against paraquat damage in radish (Raphanus sativus L.) cotyledons. Journal of Plant Biology 49, 237–246.
| Polyamines as antioxidant protectors against paraquat damage in radish (Raphanus sativus L.) cotyledons.Crossref | GoogleScholarGoogle Scholar |
Kim J, Kim JH, Lyu JI, Woo HR, Lim PO (2018) New insights into the regulation of leaf senescence in Arabidopsis. Journal of Experimental Botany 69, 787–799.
| New insights into the regulation of leaf senescence in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 28992051PubMed |
Kohli SK, Khanna K, Bhardwaj R, Abd_Allah EF, Ahmad P, Corpas FJ (2019) Assessment of subcellular ROS and NO metabolism in higher plants: multifunctional signaling molecules. Antioxidants 8, 641
| Assessment of subcellular ROS and NO metabolism in higher plants: multifunctional signaling molecules.Crossref | GoogleScholarGoogle Scholar |
Kubiś J (2008) Exogenous spermidine differentially alters activities of some scavenging system enzymes, H2O2 and superoxide radical levels in water-stressed cucumber leaves. Journal of Plant Physiology 165, 397–406.
| Exogenous spermidine differentially alters activities of some scavenging system enzymes, H2O2 and superoxide radical levels in water-stressed cucumber leaves.Crossref | GoogleScholarGoogle Scholar | 17658660PubMed |
Kumar P, Dey SR, Komal JY, Siddique A (2019) Effect of polyamines and endo-mycorrhiza on chlorophyll a, b ratio and total carotenoids in leaves of Sorghum grown under cadmium toxicity. International Journal of Conservation Sciences 7, 2402–2406.
Legocka J, Zajchert I (1999) Role of spermidine in the stabilization of the apoprotein of the light-harvesting chlorophyll a/b-protein complex of photosystem II during leaf senescence process. Acta Physiologiae Plantarum 21, 127–132.
| Role of spermidine in the stabilization of the apoprotein of the light-harvesting chlorophyll a/b-protein complex of photosystem II during leaf senescence process.Crossref | GoogleScholarGoogle Scholar |
Lei W, Li Y, Yao X, Qiao K, Wei L, Liu B, Zhang D, Lin H (2020) NAP is involved in GA-mediated chlorophyll degradation and leaf senescence by interacting with DELLAs in Arabidopsis. Plant Cell Reports 39, 75–87.
| NAP is involved in GA-mediated chlorophyll degradation and leaf senescence by interacting with DELLAs in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 31646371PubMed |
Liang D, Shen Y, Ni Z, Wang Q, Lei Z, Xu N, Deng Q, Lin L, Wang J, Lv X, Xia H (2018) Exogenous melatonin application delays senescence of kiwifruit leaves by regulating the antioxidant capacity and biosynthesis of flavonoids. Frontiers in Plant Science 9, 426
| Exogenous melatonin application delays senescence of kiwifruit leaves by regulating the antioxidant capacity and biosynthesis of flavonoids.Crossref | GoogleScholarGoogle Scholar | 29675031PubMed |
Lim PO, Kim HJ, Gil Nam H (2007) Leaf senescence. Annual Review of Plant Biology 58, 115–136.
| Leaf senescence.Crossref | GoogleScholarGoogle Scholar | 17177638PubMed |
Lone ML, Haq Au, Farooq S, Altaf F, Tahir I (2021) Nitric oxide effectively curtails neck bending and mitigates senescence in isolated flowers of Calendula officinalis L. Physiology and Molecular Biology of Plants 27, 835–845.
| Nitric oxide effectively curtails neck bending and mitigates senescence in isolated flowers of Calendula officinalis L.Crossref | GoogleScholarGoogle Scholar | 33967466PubMed |
Martínez DE, Costa ML, Gomez FM, Otegui MS, Guiamet JJ (2008) Senescence-associated vacuoles’ are involved in the degradation of chloroplast proteins in tobacco leaves. The Plant Journal 56, 196–206.
| Senescence-associated vacuoles’ are involved in the degradation of chloroplast proteins in tobacco leaves.Crossref | GoogleScholarGoogle Scholar | 18564383PubMed |
Mattoo AK, Sobieszczuk-Nowicka E (2019) Chapter 8 - Polyamine as signaling molecules and leaf senescence. In ‘Senescence signalling and control in plants’. (Eds M Sarwat, N Tuteja) pp. 125–138. (Academic Press)
Mellidou I, Karamanoli K, Constantinidou H-IA, Roubelakis-Angelakis KA (2020) Antisense-mediated S-adenosyl-l-methionine decarboxylase silencing affects heat stress responses of tobacco plants. Functional Plant Biology 47, 651–658.
| Antisense-mediated S-adenosyl-l-methionine decarboxylase silencing affects heat stress responses of tobacco plants.Crossref | GoogleScholarGoogle Scholar | 32375995PubMed |
Mohammadi H, Ghorbanpour M, Brestic M (2018) Exogenous putrescine changes redox regulations and essential oil constituents in field-grown Thymus vulgaris L. under well-watered and drought stress conditions. Industrial Crops and Products 122, 119–132.
| Exogenous putrescine changes redox regulations and essential oil constituents in field-grown Thymus vulgaris L. under well-watered and drought stress conditions.Crossref | GoogleScholarGoogle Scholar |
Mostafaei E, Zehtab-Salmasi S, Salehi-Lisar Y, Ghassemi-Golezani K (2018) Changes in photosynthetic pigments, osmolytes and antioxidants of Indian mustard by drought and exogenous polyamines. Acta Biologica Hungarica 69, 313–324.
| Changes in photosynthetic pigments, osmolytes and antioxidants of Indian mustard by drought and exogenous polyamines.Crossref | GoogleScholarGoogle Scholar | 30257583PubMed |
Mustafavi SH, Naghdi Badi H, Sękara A, Mehrafarin A, Janda T, Ghorbanpour M, Rafiee H (2018) Polyamines and their possible mechanisms involved in plant physiological processes and elicitation of secondary metabolites. Acta Physiologiae Plantarum 40, 102
| Polyamines and their possible mechanisms involved in plant physiological processes and elicitation of secondary metabolites.Crossref | GoogleScholarGoogle Scholar |
Nahar K, Hasanuzzaman M, Suzuki T, Fujita M (2017) Polyamines-induced aluminum tolerance in mung bean: a study on antioxidant defense and methylglyoxal detoxification systems. Ecotoxicology 26, 58–73.
| Polyamines-induced aluminum tolerance in mung bean: a study on antioxidant defense and methylglyoxal detoxification systems.Crossref | GoogleScholarGoogle Scholar | 27819117PubMed |
Nahed GAA, Lobna ST, Soad MI (2009) Some studies on the effect of putrescine, ascorbic acid and thiamine on growth, flowering and some chemical constituents of gladiolus plants at Nubaria. Ozean Journal of Applied Sciences 2, 169–179.
Napieraj N, Reda M, Janicka M (2020) The role of NO in plant response to salt stress: interactions with polyamines. Functional Plant Biology 47, 865–879.
| The role of NO in plant response to salt stress: interactions with polyamines.Crossref | GoogleScholarGoogle Scholar | 32522331PubMed |
Nisar S, Tahir I, Ahmad SS (2015) Modulation of flower senescence in Nicotiana plumbaginifolia L. by polyamines. Indian Journal of Plant Physiology 20, 186–190.
| Modulation of flower senescence in Nicotiana plumbaginifolia L. by polyamines.Crossref | GoogleScholarGoogle Scholar |
Pal M, Szalai G, Gondor OK, Janda T (2021) Unfinished story of polyamines: role of conjugation, transport and light-related regulation in the polyamine metabolism in plants. Plant Science 308, 110923
| Unfinished story of polyamines: role of conjugation, transport and light-related regulation in the polyamine metabolism in plants.Crossref | GoogleScholarGoogle Scholar | 34034871PubMed |
Peerzada YY, Iqbal M (2021) Leaf senescence and ethylene signaling. In ‘Plant growth regulators: signaling under stress conditions. Vol. 153’. (Eds T Aftab, KR Hakeem) (Springer)
Poret M, Chandrasekar B, Van der Hoorn RA, Coquet L, Jouenne T, Avice J-C (2017) Proteomic investigations of proteases involved in cotyledon senescence: a model to explore the genotypic variability of proteolysis machinery associated with nitrogen remobilization efficiency during the leaf senescence of oilseed rape. Proteomes 5, 29
| Proteomic investigations of proteases involved in cotyledon senescence: a model to explore the genotypic variability of proteolysis machinery associated with nitrogen remobilization efficiency during the leaf senescence of oilseed rape.Crossref | GoogleScholarGoogle Scholar |
Procházková D, Wilhelmová N (2007) Leaf senescence and activities of the antioxidant enzymes. Biologia Plantarum 51, 401–406.
| Leaf senescence and activities of the antioxidant enzymes.Crossref | GoogleScholarGoogle Scholar |
Promyou S, Ketsa S, van Doorn WG (2012) Salicylic acid alleviates chilling injury in anthurium (Anthurium andraeanum L.) flowers. Postharvest Biology and Technology 64, 104–110.
| Salicylic acid alleviates chilling injury in anthurium (Anthurium andraeanum L.) flowers.Crossref | GoogleScholarGoogle Scholar |
Qiu K, Li Z, Yang Z, Chen J, Wu S, Zhu X, Gao S, Gao J, Ren G, Kuai B, Zhou X (2015) EIN3 and ORE1 accelerate degreening during ethylene-mediated leaf senescence by directly activating chlorophyll catabolic genes in Arabidopsis. PLoS Genetics 11, e1005399
| EIN3 and ORE1 accelerate degreening during ethylene-mediated leaf senescence by directly activating chlorophyll catabolic genes in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 26218222PubMed |
Qu Y, Jiang L, Wuyun T, Mu S, Xie F, Chen Y, Zhang L (2020) Effects of exogenous putrescine on delaying senescence of cut foliage of Nephrolepis cordifolia. Frontiers in Plant Science 11, 1395
| Effects of exogenous putrescine on delaying senescence of cut foliage of Nephrolepis cordifolia.Crossref | GoogleScholarGoogle Scholar |
Quirino BF, Noh Y-S, Himelblau E, Amasino RM (2000) Molecular aspects of leaf senescence. Trends in Plant Science 5, 278–282.
| Molecular aspects of leaf senescence.Crossref | GoogleScholarGoogle Scholar | 10871899PubMed |
Radhakrishnan R, Lee I-J (2013) Spermine promotes acclimation to osmotic stress by modifying antioxidant, abscisic acid, and jasmonic acid signals in soybean. Journal of Plant Growth Regulation 32, 22–30.
| Spermine promotes acclimation to osmotic stress by modifying antioxidant, abscisic acid, and jasmonic acid signals in soybean.Crossref | GoogleScholarGoogle Scholar |
Radhakrishnan R, Lee I-J (2014) Endogenous antioxidants and phytohormonal regulation induced by spermidine improve cucumber plant growth. Pakistan Journal of Botany 46, 2151–2156.
Rady MM, Hemida KA (2015) Modulation of cadmium toxicity and enhancing cadmium-tolerance in wheat seedlings by exogenous application of polyamines. Ecotoxicology and Environmental Safety 119, 178–185.
| Modulation of cadmium toxicity and enhancing cadmium-tolerance in wheat seedlings by exogenous application of polyamines.Crossref | GoogleScholarGoogle Scholar | 26004358PubMed |
Rai S, Sindhu V, Sarkar RK, Santhoshkumar G (2020) Role of polyamines in vegetable crop production: a review. Journal of Pharmacognosy and Phytochemistry 9, 466–476.
| Role of polyamines in vegetable crop production: a review.Crossref | GoogleScholarGoogle Scholar |
Rasool S, Ahmad A, Siddiqi TO, Ahmad P (2013) Changes in growth, lipid peroxidation and some key antioxidant enzymes in chickpea genotypes under salt stress. Acta Physiologiae Plantarum 35, 1039–1050.
| Changes in growth, lipid peroxidation and some key antioxidant enzymes in chickpea genotypes under salt stress.Crossref | GoogleScholarGoogle Scholar |
Reis RS, Vale EdM, Heringer AS, Santa-Catarina C, Silveira V (2016) Putrescine induces somatic embryo development and proteomic changes in embryogenic callus of sugarcane. Journal of Proteomics 130, 170–179.
| Putrescine induces somatic embryo development and proteomic changes in embryogenic callus of sugarcane.Crossref | GoogleScholarGoogle Scholar | 26435420PubMed |
Rezvanypour S, Osfoori M (2011) Effect of chemical treatments and sucrose on vase life of three cut rose cultivars. Journal of Research in Agricultural Science 7, 133–139.
Sairam R (1994) Effect of moisture-stress on physiological activities of two contrasting wheat genotypes. Indian Journal of Experimental Biology 32, 594–597.
Sánchez-Rodríguez E, Romero L, Ruiz JM (2016) Accumulation on free polyamines enhances the antioxidant response in fruit of grafting tomato plants under water stress. Journal of Plant Physiology 190, 72–78.
| Accumulation on free polyamines enhances the antioxidant response in fruit of grafting tomato plants under water stress.Crossref | GoogleScholarGoogle Scholar | 26687637PubMed |
Shah AA, Ahmed S, Ali A, Yasin NA (2020) 2-Hydroxymelatonin mitigates cadmium stress in cucumis sativus seedlings: modulation of antioxidant enzymes and polyamines. Chemosphere 243, 125308
| 2-Hydroxymelatonin mitigates cadmium stress in cucumis sativus seedlings: modulation of antioxidant enzymes and polyamines.Crossref | GoogleScholarGoogle Scholar | 31722261PubMed |
Sharma A, Slathia S, Choudhary SP, Sharma YP, Langer A (2014) Role of 24-epibrassinolide, putrescine and spermine in salinity stressed Adiantum capillus-veneris leaves. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences 84, 183–192.
Sharma S, Pareek S, Sagar NA, Valero D, Serrano M (2017) Modulatory effects of exogenously applied polyamines on postharvest physiology, antioxidant system and shelf life of fruits: a review. International Journal of Molecular Sciences 18, 1789
| Modulatory effects of exogenously applied polyamines on postharvest physiology, antioxidant system and shelf life of fruits: a review.Crossref | GoogleScholarGoogle Scholar |
Shin N-H, Trang DT, Hong W-J, Kang K, Chuluuntsetseg J, Moon J-K, Yoo Y-H, Jung K-H, Yoo S-C (2020) Rice senescence-induced receptor-like kinase (OsSRLK) is involved in phytohormone-mediated chlorophyll degradation. International Journal of Molecular Sciences 21, 260
| Rice senescence-induced receptor-like kinase (OsSRLK) is involved in phytohormone-mediated chlorophyll degradation.Crossref | GoogleScholarGoogle Scholar |
Singh P, Basu S, Kumar G (2018) Polyamines metabolism: a way ahead for abiotic stress tolerance in crop plants. In ‘Biochemical, physiological and molecular avenues for combating abiotic stress tolerance in plants’. (Ed. SH Wani) pp. 39–55. (Academic Press)
Skutnik E, Rabiza-Świder J, Wachowicz M, Łukaszewska AJ (2004) Senescence of cut leaves of Zantedeschia aethiopica and Z. elliottiana. Part I. Chlorophyll degradation. Acta Scientiarum Polonorum Hortorum Cultus 3, 57–65.
Soares C, Carvalho MEA, Azevedo RA, Fidalgo F (2019) Plants facing oxidative challenges—a little help from the antioxidant networks. Environmental and Experimental Botany 161, 4–25.
| Plants facing oxidative challenges—a little help from the antioxidant networks.Crossref | GoogleScholarGoogle Scholar |
Sobieszczuk-Nowicka E (2017) Polyamine catabolism adds fuel to leaf senescence. Amino Acids 49, 49–56.
| Polyamine catabolism adds fuel to leaf senescence.Crossref | GoogleScholarGoogle Scholar | 28039518PubMed |
Sobieszczuk-Nowicka E, Kubala S, Zmienko A, Małecka A, Legocka J (2016) From accumulation to degradation: reprogramming polyamine metabolism facilitates dark-induced senescence in barley leaf cells. Frontiers in Plant Science 6, 1198
| From accumulation to degradation: reprogramming polyamine metabolism facilitates dark-induced senescence in barley leaf cells.Crossref | GoogleScholarGoogle Scholar | 26779231PubMed |
Spormann S, Soares C, Teixeira J, Fidalgo F (2021) Polyamines as key regulatory players in plants under metal stress—a way for an enhanced tolerance. Annals of Applied Biology 178, 209–226.
| Polyamines as key regulatory players in plants under metal stress—a way for an enhanced tolerance.Crossref | GoogleScholarGoogle Scholar |
Stewart TM, Dunston TT, Woster PM, Casero RA (2018) Polyamine catabolism and oxidative damage. Journal of Biological Chemistry 293, 18736–18745.
| Polyamine catabolism and oxidative damage.Crossref | GoogleScholarGoogle Scholar |
Sun X, Xie L, Han L (2019) Effects of exogenous spermidine and spermine on antioxidant metabolism associated with cold-induced leaf senescence in zoysiagrass (Zoysia japonica Steud.). Horticulture, Environment, and Biotechnology 60, 295–302.
| Effects of exogenous spermidine and spermine on antioxidant metabolism associated with cold-induced leaf senescence in zoysiagrass (Zoysia japonica Steud.).Crossref | GoogleScholarGoogle Scholar |
Sun X, Li X, Zhu J, Huang N, Bian X, Li H, Wang L, Han L (2020) Polyamines and ethylene metabolism during cold acclimation in zoysiagrass (Zoysia Japonica Steud.). Acta Physiologiae Plantarum 42, 138
| Polyamines and ethylene metabolism during cold acclimation in zoysiagrass (Zoysia Japonica Steud.).Crossref | GoogleScholarGoogle Scholar |
Süssenbacher I, Menghini D, Scherzer G, Salinger K, Erhart T, Moser S, Vergeiner C, Hörtensteiner S, Kräutler B (2019) Cryptic chlorophyll breakdown in non-senescent green Arabidopsis thaliana leaves. Photosynthesis Research 142, 69–85.
| Cryptic chlorophyll breakdown in non-senescent green Arabidopsis thaliana leaves.Crossref | GoogleScholarGoogle Scholar | 31172355PubMed |
Taie HAA, Seif El-Yazal MA, Ahmed SMA, Rady MM (2019) Polyamines modulate growth, antioxidant activity, and genomic DNA in heavy metal–stressed wheat plant. Environmental Science and Pollution Research 26, 22338–22350.
| Polyamines modulate growth, antioxidant activity, and genomic DNA in heavy metal–stressed wheat plant.Crossref | GoogleScholarGoogle Scholar | 31154641PubMed |
Takács Z, Poór P, Szepesi Á, Tari I (2017) In vivo inhibition of polyamine oxidase by a spermine analogue, MDL-72527, in tomato exposed to sublethal and lethal salt stress. Functional Plant Biology 44, 480–492.
| In vivo inhibition of polyamine oxidase by a spermine analogue, MDL-72527, in tomato exposed to sublethal and lethal salt stress.Crossref | GoogleScholarGoogle Scholar | 32480581PubMed |
Takács Z, Poór P, Tari I (2021) Interaction between polyamines and ethylene in the response to salicylic acid under normal photoperiod and prolonged darkness. Plant Physiology and Biochemistry 167, 470–480.
| Interaction between polyamines and ethylene in the response to salicylic acid under normal photoperiod and prolonged darkness.Crossref | GoogleScholarGoogle Scholar | 34419831PubMed |
Tan X-L, Fan Z-q, Kuang J-f, Lu W-j, Reiter RJ, Lakshmanan P, Su X-g, Zhou J, Chen J-y, Shan W (2019) Melatonin delays leaf senescence of Chinese flowering cabbage by suppressing ABFs-mediated abscisic acid biosynthesis and chlorophyll degradation. Journal of Pineal Research 67, e12570
| Melatonin delays leaf senescence of Chinese flowering cabbage by suppressing ABFs-mediated abscisic acid biosynthesis and chlorophyll degradation.Crossref | GoogleScholarGoogle Scholar | 30897243PubMed |
Tang S, Zhang H, Li L, Liu X, Chen L, Chen W, Ding Y (2018) Exogenous spermidine enhances the photosynthetic and antioxidant capacity of rice under heat stress during early grain-filling period. Functional Plant Biology 45, 911–921.
| Exogenous spermidine enhances the photosynthetic and antioxidant capacity of rice under heat stress during early grain-filling period.Crossref | GoogleScholarGoogle Scholar | 32291055PubMed |
Tang C, Zhang R, Hu X, Song J, Li B, Ou D, Hu X, Zhao Y (2019) Exogenous spermidine elevating cadmium tolerance in Salix matsudana involves cadmium detoxification and antioxidant defense. International Journal of Phytoremediation 21, 305–315.
| Exogenous spermidine elevating cadmium tolerance in Salix matsudana involves cadmium detoxification and antioxidant defense.Crossref | GoogleScholarGoogle Scholar | 30648425PubMed |
Tassoni A, Accettulli P, Bagni N (2006) Exogenous spermidine delays senescence of Dianthus caryophyllus flowers. Plant Biosystems - An International Journal Dealing with all Aspects of Plant Biology 140, 107–114.
| Exogenous spermidine delays senescence of Dianthus caryophyllus flowers.Crossref | GoogleScholarGoogle Scholar |
Tayyab S, Qamar S (1992) A look into enzyme kinetics: some introductory experiments. Biochemical Education 20, 116–118.
| A look into enzyme kinetics: some introductory experiments.Crossref | GoogleScholarGoogle Scholar |
Teerarak M, Laosinwattana C (2019) Essential oil from ginger as a novel agent in delaying senescence of cut fronds of the fern (Davallia solida (G. Forst.) Sw.). Postharvest Biology and Technology 156, 110927
| Essential oil from ginger as a novel agent in delaying senescence of cut fronds of the fern (Davallia solida (G. Forst.) Sw.).Crossref | GoogleScholarGoogle Scholar |
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 |
Walters DR (2003) Polyamines and plant disease. Phytochemistry 64, 97–107.
| Polyamines and plant disease.Crossref | GoogleScholarGoogle Scholar | 12946408PubMed |
Wang C, Dai S, Zhang Z-L, Lao W, Wang R, Meng X, Zhou X (2021) Ethylene and salicylic acid synergistically accelerate leaf senescence in Arabidopsis. Journal of Integrative Plant Biology 63, 828–833.
| Ethylene and salicylic acid synergistically accelerate leaf senescence in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 33501715PubMed |
Woo HR, Kim HJ, Lim PO, Nam HG (2019) Leaf senescence: systems and dynamics aspects. Annual Review of Plant Biology 70, 347–376.
| Leaf senescence: systems and dynamics aspects.Crossref | GoogleScholarGoogle Scholar | 30811218PubMed |
Xu L, Xing S, Sun X (2014) Effects of polyamines on hormones contents and the relationship with the flower bud differentiation in chrysanthemum. Plant Physiology Journal 50, 1195–1202.
Yu Y, Zhou W, Zhou K, Liu W, Liang X, Chen Y, Sun D, Lin X (2018) Polyamines modulate aluminum-induced oxidative stress differently by inducing or reducing H2O2 production in wheat. Chemosphere 212, 645–653.
| Polyamines modulate aluminum-induced oxidative stress differently by inducing or reducing H2O2 production in wheat.Crossref | GoogleScholarGoogle Scholar | 30173111PubMed |
Yu X, Xu Y, Yan S (2021) Salicylic acid and ethylene coordinately promote leaf senescence. Journal of Integrative Plant Biology 63, 823–827.
| Salicylic acid and ethylene coordinately promote leaf senescence.Crossref | GoogleScholarGoogle Scholar | 33501782PubMed |
Zhang W, Jiang B, Li W, Song H, Yu Y, Chen J (2009) Polyamines enhance chilling tolerance of cucumber (Cucumis sativus L.) through modulating antioxidative system. Scientia Horticulturae 122, 200–208.
| Polyamines enhance chilling tolerance of cucumber (Cucumis sativus L.) through modulating antioxidative system.Crossref | GoogleScholarGoogle Scholar |
Zhang C, Teng X-D, Zheng Q-Q, Zhao Y-Y, Lu J-Y, Wang Y, Guo H, Yang Z-N (2018a) Ethylene signaling is critical for synergid cell functional specification and pollen tube attraction. The Plant Journal 96, 176–187.
| Ethylene signaling is critical for synergid cell functional specification and pollen tube attraction.Crossref | GoogleScholarGoogle Scholar | 30003612PubMed |
Zhang Y, Li Z, Li Y-P, Zhang X-Q, Ma X, Huang L-K, Yan Y-H, Peng Y (2018b) Chitosan and spermine enhance drought resistance in white clover, associated with changes in endogenous phytohormones and polyamines, and antioxidant metabolism. Functional Plant Biology 45, 1205–1222.
| Chitosan and spermine enhance drought resistance in white clover, associated with changes in endogenous phytohormones and polyamines, and antioxidant metabolism.Crossref | GoogleScholarGoogle Scholar | 32291011PubMed |
Zhang W, Peng K, Cui F, Wang D, Zhao J, Zhang Y, Yu N, Wang Y, Zeng D, Wang Y, Cheng Z, Zhang K (2021) Cytokinin oxidase/dehydrogenase OsCKX11 coordinates source and sink relationship in rice by simultaneous regulation of leaf senescence and grain number. Plant Biotechnology Journal 19, 335–350.
| Cytokinin oxidase/dehydrogenase OsCKX11 coordinates source and sink relationship in rice by simultaneous regulation of leaf senescence and grain number.Crossref | GoogleScholarGoogle Scholar | 33448635PubMed |
Zhu C, Xiaoyu L, Junlan G, Yun X, Jie R (2020) Integrating transcriptomic and metabolomic analysis of hormone pathways in Acer rubrum during developmental leaf senescence. BMC Plant Biology 20, 410
| Integrating transcriptomic and metabolomic analysis of hormone pathways in Acer rubrum during developmental leaf senescence.Crossref | GoogleScholarGoogle Scholar | 32883206PubMed |