Exogenous spermidine improves drought tolerance in maize by enhancing the antioxidant defence system and regulating endogenous polyamine metabolism
Lijie Li A , Wanrong Gu A D , Congfeng Li B , Wenhua Li C , Caifeng Li A , Jing Li A and Shi Wei A
+ Author Affiliations
- Author Affiliations
A College of Agriculture, Northeast Agricultural University, Harbin 150030, Heilongjiang, China.
B Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, 10081, China.
C Institute of Maize Research, Heilongjiang Academy of Agricultural Sciences, Harbin 150030, Heilongjiang, China.
D Corresponding author. Email: wanronggu@163.com
Crop and Pasture Science 69(11) 1076-1091 https://doi.org/10.1071/CP18271
Submitted: 12 June 2018 Accepted: 15 September 2018 Published: 25 October 2018
Abstract
Drought stress is a primary abiotic constraint affecting crop production worldwide. In this study, the role of exogenous spermidine (Spd) in conferring drought-stress-tolerance in maize (Zea mays L.) seedlings was studied by analysing polyamine metabolism and the antioxidant defence system. Two maize cultivars, Xianyu 335 (drought resistant) and Fenghe 1 (drought susceptible), were subjected to drought stress (–0.8 MPa) induced by 15% polyethylene glycol 6000 with or without Spd (0.1 mm) application. Spd significantly reduced the inhibition of plant growth and decreased malondialdehyde and hydrogen peroxide contents and the generation rate of oxidised glutathione caused by drought stress, particularly in Fenghe 1. The activities of superoxide dismutase, ascorbate peroxidase and glutathione reductase further increased with the application of Spd to the stressed plants. Application of Spd significantly moderated the drought-induced reduction in activities of monodehydroascorbate reductase and dehydroascorbate and the ratio ascorbate : dehydroascorbate and reduced the ratio glutathione : oxidised glutathione. With the application of Spd, the contents of Spd and spermine and the activities of arginine decarboxylase, S-adenosyl methionine decarboxylase and diamine oxidase increased significantly in the stressed plants, and the increases were greater in Xianyu 335 than in Fenghe 1. Thus, exogenous Spd successfully reduced oxidative damage by enhancing the antioxidant components, raising the redox state of ascorbate and glutathione, and altering the polyamine pool, which play important roles in improving physiological characteristics and drought stress in maize.
Additional keywords: APX, endogenous polyamine pool, GSH, MDA, SOD.
References
Asthir B, Duffus CM, Smith RC, Spoor W (2002) Diamine oxidase is involved in H2O2 production in the chalazal cells during barley grain filling. Journal of Experimental Botany 53, 677–682.| Diamine oxidase is involved in H2O2 production in the chalazal cells during barley grain filling.Crossref | GoogleScholarGoogle Scholar |
Bai TH, Li CY, Ma FW, Feng FJ, Shu HR (2010) Responses of growth and antioxidant system to root-zone hypoxia stress in two Malus species. Plant and Soil 327, 95–105.
| Responses of growth and antioxidant system to root-zone hypoxia stress in two Malus species.Crossref | GoogleScholarGoogle Scholar |
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 |
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 |
Ceccarelli S, Grando S, Maatougui M, Michael M, Slash M, Haghparast R, Rahmanian M, Taheri A, Al-yassin A, Benbelkacem A, Labdi M, Mimoun H, Nachit M (2010) Plant breeding and climate changes. The Journal of Agricultural Science 148, 627–637.
| Plant breeding and climate changes.Crossref | GoogleScholarGoogle Scholar |
Chakraborty S, Newton AC (2011) Climate change, plant diseases and food security: An overview. Plant Pathology 60, 2–14.
| Climate change, plant diseases and food security: An overview.Crossref | GoogleScholarGoogle Scholar |
Chen F, Wang F, Wu F, Mao W, Zhang G, Zhou M (2010) Modulation of exogenous glutathione in antioxidant defense system against Cd stress in the two barley genotypes differing in Cd tolerance. Plant Physiology and Biochemistry 48, 663–672.
| Modulation of exogenous glutathione in antioxidant defense system against Cd stress in the two barley genotypes differing in Cd tolerance.Crossref | GoogleScholarGoogle Scholar |
Doulis AG, Debian N, Kingston-Smith AH, Foyer CH (1997) Differential localization of antioxidants in maize leaves. Plant Physiology 114, 1031–1037.
| Differential localization of antioxidants in maize leaves.Crossref | GoogleScholarGoogle Scholar |
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 |
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 |
Farooq M, Wahid A, Lee D (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 |
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 |
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry 48, 909–930.
| Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants.Crossref | GoogleScholarGoogle Scholar |
Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Analytical Biochemistry 106, 207–212.
| Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine.Crossref | GoogleScholarGoogle Scholar |
Guo WL, Chen RG, Gong ZH, Yin YX, Ahmed SS, He YM (2012) Exogenous abscisic acid increases antioxidant enzymes and related gene expression in pepper (Capsicum annuum) leaves subjected to chilling stress. Genetics and Molecular Research 11, 4063–4080.
| Exogenous abscisic acid increases antioxidant enzymes and related gene expression in pepper (Capsicum annuum) leaves subjected to chilling stress.Crossref | GoogleScholarGoogle Scholar |
Hodges DM, Delong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207, 604–611.
| Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds.Crossref | GoogleScholarGoogle Scholar |
Hodges JC, Harikrishnan LS, Ault-Justus S (2000) Preparation of designer resins via living free radical polymerization of functional monomers on solid support. Journal of Combinatorial Chemistry 2, 80–88.
| Preparation of designer resins via living free radical polymerization of functional monomers on solid support.Crossref | GoogleScholarGoogle Scholar |
Huang XX, Zhou GL, Yang WG, Wang AH, Hu ZH, Lin CF, Chen X (2014) Drought-inhibited ribulose-1, 5-bisphosphate carboxylase activity is mediated through increased release of ethylene and changes in the ratio of polyamines in pakchoi. Journal of Plant Physiology 171, 1392–1400.
| Drought-inhibited ribulose-1, 5-bisphosphate carboxylase activity is mediated through increased release of ethylene and changes in the ratio of polyamines in pakchoi.Crossref | GoogleScholarGoogle Scholar |
Hussain SS, Ali M, Ahmad M, Siddique KHM (2011) Polyamines: Natural and engineered abiotic and biotic stress tolerance in plants. Biotechnology Advances 29, 300–311.
| Polyamines: Natural and engineered abiotic and biotic stress tolerance in plants.Crossref | GoogleScholarGoogle Scholar |
Kim YH, Kim MD, Choi YI, Park SC, Yun DJ, Noh EW, Lee HS, Kwak SS (2011) Transgenic poplar expressing Arabidopsis NDPK2 enhances growth as well as oxidative stress tolerance. Plant Biotechnology Journal 9, 334–347.
| Transgenic poplar expressing Arabidopsis NDPK2 enhances growth as well as oxidative stress tolerance.Crossref | GoogleScholarGoogle Scholar |
Li Z, Zhou H, Peng Y, Zhang X, Ma X, Huang L, Yan Y (2015) 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, Zhang XQ, Peng Y, Merewitz E, Ma X, Huang L, Yan Y (2016) The alterations of endogenous polyamines and phytohormones induced by exogenous application of spermidine regulate antioxidant metabolism, metallothionein and relevant genes conferring drought tolerance in white clover. Environmental and Experimental Botany 124, 22–38.
| The alterations of endogenous polyamines and phytohormones induced by exogenous application of spermidine regulate antioxidant metabolism, metallothionein and relevant genes conferring drought tolerance in white clover.Crossref | GoogleScholarGoogle Scholar |
Li LL, Gu WR, Li J, Li CF, Xie TL, Qu DY, Meng Y, Li C, Wei S (2018) 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 |
Liu JH, Moriguchi T (2007) Changes in free polyamines and gene expression during peach flower development. Biologia Plantarum 51, 530–532.
| Changes in free polyamines and gene expression during peach flower development.Crossref | GoogleScholarGoogle Scholar |
Liu F, Stützel H (2004) Biomass partitioning, specific leaf area, and water use efficiency of vegetable amaranth (Amaranthus spp.) in response to drought stress. Scientia Horticulturae 102, 15–27.
| Biomass partitioning, specific leaf area, and water use efficiency of vegetable amaranth (Amaranthus spp.) in response to drought stress.Crossref | GoogleScholarGoogle Scholar |
Liu HP, Dong BH, Zhang YY, Liu ZP, Liu YL (2004) Relationship between osmotic stress and the levels of free, conjugated and bound polyamines in leaves of wheat seedlings. Plant Science 166, 1261–1267.
| Relationship between osmotic stress and the levels of free, conjugated and bound polyamines in leaves of wheat seedlings.Crossref | GoogleScholarGoogle Scholar |
Liu JH, Wang W, Wu H, Gong XQ, Moriguchi T (2015) 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 |
Liu B, Zhou XG, Li CX, Zhen B, Li HZ, Li ZY (2016) Foliar spraying polyamine improving waterlogging resistance of summer maize in early grain filling stage. Transactions of the Chinese Society of Agricultural Engineering 32, 122–128.
Matsuda H (1984) Some properties of arginine decarboxylase in Vicia faba leaves. Plant & Cell Physiology 25, 523–530.
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, Cell & Environment 33, 453–467.
| Reactive oxygen species homeostasis and signalling during drought and salinity stresses.Crossref | GoogleScholarGoogle Scholar |
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 |
Mo YL, Wang YQ, Yang RP, Zheng JX, Liu CM, Li H, Ma J, Zhang Y, Wei C, Zhang X (2016) Regulation of plant growth, photosynthesis, antioxidation and osmosis by an arbuscular mycorrhizal fungus in watermelon seedlings under well-watered and drought conditions. Frontiers in Plant Science 7, 644
| Regulation of plant growth, photosynthesis, antioxidation and osmosis by an arbuscular mycorrhizal fungus in watermelon seedlings under well-watered and drought conditions.Crossref | GoogleScholarGoogle Scholar |
Nahar K, Hasanuzzaman M, Alam MM, Fujita M (2015a) Glutathione-induced drought stress tolerance in mung bean: Coordinated roles of the antioxidant defence and methylglyoxal detoxification systems. AoB Plants 7, plv069
| Glutathione-induced drought stress tolerance in mung bean: Coordinated roles of the antioxidant defence and methylglyoxal detoxification systems.Crossref | GoogleScholarGoogle Scholar |
Nahar K, Hasanuzzaman M, Alam MM, Fujita M (2015b) Exogenous spermidine alleviates low temperature injury in mung bean (Vigna radiata L.) seedlings by modulating ascorbate-glutathione and glyoxalase pathway. International Journal of Molecular Sciences 16, 30117–30132.
| Exogenous spermidine alleviates low temperature injury in mung bean (Vigna radiata L.) seedlings by modulating ascorbate-glutathione and glyoxalase pathway.Crossref | GoogleScholarGoogle Scholar |
Noctor G, Mhamdi A, Foyer CH (2014) The roles of reactive oxygen metabolism in drought: Not so cut and dried. Plant Physiology 164, 1636–1648.
| The roles of reactive oxygen metabolism in drought: Not so cut and dried.Crossref | GoogleScholarGoogle Scholar |
Osakabe Y, Osakabe K, Shinozaki K, Tran LSP (2014) Response of plants to water stress. Frontiers in Plant Science 5, 86
| Response of plants to water stress.Crossref | GoogleScholarGoogle Scholar |
Pál M, Szalai G, Janda T (2015) Speculation: Polyamines are important in abiotic stress signaling. Plant Science 237, 16–23.
| Speculation: Polyamines are important in abiotic stress signaling.Crossref | GoogleScholarGoogle Scholar |
Pottosin I, Velarde-Buendía AM, Bose J, Fuglsang AT, Shabala S (2014) Polyamines cause plasma membrane depolarization, activate Ca2+-, and modulate H+-ATPase pump activity in pea roots. Journal of Experimental Botany 65, 2463–2472.
| Polyamines cause plasma membrane depolarization, activate Ca2+-, and modulate H+-ATPase pump activity in pea roots.Crossref | GoogleScholarGoogle Scholar |
Pyngrope S, Bhoomika K, Dubey RS (2013) Reactive oxygen species, ascorbate-glutathione pool, and enzymes of their metabolism in drought-sensitive and tolerant indica rice (Oryza sativa L.) seedlings subjected to progressing levels of water deficit. Protoplasma 250, 585–600.
| Reactive oxygen species, ascorbate-glutathione pool, and enzymes of their metabolism in drought-sensitive and tolerant indica rice (Oryza sativa L.) seedlings subjected to progressing levels of water deficit.Crossref | GoogleScholarGoogle Scholar |
Rao DE, Chaitanya KV (2016) Photosynthesis and antioxidative defense mechanisms in deciphering drought stress tolerance of crop plants. Biologia Plantarum 60, 201–218.
| Photosynthesis and antioxidative defense mechanisms in deciphering drought stress tolerance of crop plants.Crossref | GoogleScholarGoogle Scholar |
Ribaut JM, Betran J, Monneveux P, Setter T (2012) Drought tolerance in maize. In ‘Handbook of maize: its biology’. (Eds JL Bennetzen, SC Hake) pp. 311–344. (Springer: New York)
Sánchez-Rodríguez E, Romero L, Ruiz JM (2016) Accumulation of free polyamines enhances the antioxidant response in fruits of grafted tomato plants under water stress. Journal of Plant Physiology 190, 72–78.
| Accumulation of free polyamines enhances the antioxidant response in fruits of grafted tomato plants under water stress.Crossref | GoogleScholarGoogle Scholar |
Sapeta H, Costa JM, Lourenço T, Maroco J, van der Linde P, Oliveira MM (2013) Drought stress response in Jatropha curcas: Growth and physiology. Environmental and Experimental Botany 85, 76–84.
| Drought stress response in Jatropha curcas: Growth and physiology.Crossref | GoogleScholarGoogle Scholar |
Shao RX, Li LL, Zheng HF, Zhang JY, Yang SJ, Ma Y, Xin L, Su XY, Mao J, Zheng B, Yang Q (2016) Effects of exogenous nitric oxide on photosynthesis of maize seedlings under drought stress. Scientia Agricultura Sinica 49, 251–259.
Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Journal of Botany 2012, 1–26.
Shen WY, Nada K, Tachibana S (2000) Involvement of polyamines in the chilling tolerance of cucumber cultivars. Plant Physiology 124, 431–439.
| Involvement of polyamines in the chilling tolerance of cucumber cultivars.Crossref | GoogleScholarGoogle Scholar |
Shi HT, Chan ZL (2014) Improvement of plant abiotic stress tolerance through modulation of the polyamine pathway. Journal of Integrative Plant Biology 56, 114–121.
| Improvement of plant abiotic stress tolerance through modulation of the polyamine pathway.Crossref | GoogleScholarGoogle Scholar |
Shi H, Ye T, Chan Z (2013) Comparative proteomic and physiological analyses reveal the protective effect of exogenous polyamines in the Bermuda grass (Cynodon dactylon) response to salt and drought stresses. Journal of Proteome Research 12, 4951–4964.
| Comparative proteomic and physiological analyses reveal the protective effect of exogenous polyamines in the Bermuda grass (Cynodon dactylon) response to salt and drought stresses.Crossref | GoogleScholarGoogle Scholar |
Sofo A, Scopa A, Nuzzaci M, Vitti A (2015) Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses. International Journal of Molecular Sciences 16, 13561–13578.
| Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses.Crossref | GoogleScholarGoogle Scholar |
Talaat NB, Shawky BT, Ibrahim AS (2015) Alleviation of drought-induced oxidative stress in maize (Zea mays L.) plants by dual application of 24-epibrassinolide and spermine. Environmental and Experimental Botany 113, 47–58.
| Alleviation of drought-induced oxidative stress in maize (Zea mays L.) plants by dual application of 24-epibrassinolide and spermine.Crossref | GoogleScholarGoogle Scholar |
Tanou G, Ziogas V, Belghazi M, Christou A, Filippou P, Job D, Fotopoulos V, Molassiotis A (2014) Polyamines reprogram oxidative and nitrosative status and the proteome of citrus plants exposed to salinity stress. Plant, Cell & Environment 37, 864–885.
| Polyamines reprogram oxidative and nitrosative status and the proteome of citrus plants exposed to salinity stress.Crossref | GoogleScholarGoogle Scholar |
Yang H, Wu F, Cheng J (2011) Reduced chilling injury in cucumber by nitric oxide and the antioxidant response. Food Chemistry 127, 1237–1242.
| Reduced chilling injury in cucumber by nitric oxide and the antioxidant response.Crossref | GoogleScholarGoogle Scholar |
Yin ZP, Li S, Ren J, Song XS (2014) Role of spermidine and spermine in alleviation of drought-induced oxidative stress and photosynthetic inhibition in Chinese dwarf cherry (Cerasus humilis) seedlings. Plant Growth Regulation 74, 209–218.
| Role of spermidine and spermine in alleviation of drought-induced oxidative stress and photosynthetic inhibition in Chinese dwarf cherry (Cerasus humilis) seedlings.Crossref | GoogleScholarGoogle Scholar |
Zafar SA, Noor MA, Waqas MA, Wang X, Shaheen T, Raza M (2018)Temperature extremes in cotton production and mitigation strategies. In ‘Past, present and future trends in cotton breeding’. (Eds MR Rahman, Y Zafar) pp. 65–91. (IntertechOpen: London)
Zhao M, Running SW (2010) Drought-induced reduction in global terrestrial net primary production from 2000 through 2009. Science 329, 940–943.
| Drought-induced reduction in global terrestrial net primary production from 2000 through 2009.Crossref | GoogleScholarGoogle Scholar |
Zlatev Z, Lidon FC (2012) An overview on drought induced changes in plant growth, water relations and photosynthesis. Emirates Journal of Food and Agriculture 24, 57–72.
| An overview on drought induced changes in plant growth, water relations and photosynthesis.Crossref | GoogleScholarGoogle Scholar |
