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Exogenous spermidine improves salt tolerance of pecan-grafted seedlings via activating antioxidant system and inhibiting the enhancement of Na+/K+ ratio

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Abstract

Salt stress is abiotic stress that negatively impacts plant growth. Exogenous spermidine (SPD) has been proposed as a priming agent that effectively alleviates various abiotic stresses in plants. To evaluate the alleviation role of exogenous SPD application against salt stress, we studied the physiological and biochemical changes, and the expression of gene encoding antioxidant enzymes and phytohormones in the SPD-treated pecan-grafted seedling. The results revealed that for the seedlings growing under salt stress environment, a drop in the total chlorophyll content and photosynthetic capability was observed. These effects subsided when the seedlings were treated with SPD. Moreover, the malondialdehyde level and Na+/K+ ratio, as well as the damage of the chloroplast ultrastructure in the seedlings, were markedly suppressed after SPD treatment. Compared with the non-SPD-treated counterparts, the exogenous SPD application promoted higher antioxidant enzyme activities and their corresponding gene expression. At the same time, the induction of abscisic acid and ethylene was suppressed. The results indicate that the exogenous SPD plays a vital role in alleviating salt-incurred phytotoxicity and oxidative damage in pecan-grafted seedlings. The remissive role of exogenous SPD is implicated by its interplay with the expression of the antioxidant enzymes and phytohormones in the pecan-grafted seedlings.

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Abbreviations

ABA:

Abscisic acid

CAT:

Catalase

Chl:

Chlorophyll

DAT:

Day after treatment

ETH:

Ethylene

Fv/Fm :

Maximum quantum yield of PSII photochemistry

MDA:

Malondialdehyde

PA:

Polyamine

Pn:

Net photosynthetic rate

POD:

Peroxidase

PVP:

Polyvinylpyrrolidone

SPD:

Spermidine

SPM:

Spermine

SOD:

Superoxide dismutase

TCA:

Trichloroacetic acid

TBA:

Thiobarbituric acid

References

  • Ahmed MZ, Shimazaki T, Gulzar S, Kikuchi A, Gul B, Khan MA (2013) The influence of genes regulating transmembrane transport of Na+ on the salt resistance of Aeluropus lagopoides. Funct Plant Biol 40:860–871

    CAS  PubMed  Google Scholar 

  • Antolín MC, Santesteban H, Santa María E, Aguirreolea J, Sánchez-díaz M (2008) Involvement of abscisic acid and polyamines in berry ripening of Vitis vinifera (L.) subjected to water deficit irrigation. Aust J Grape Wine Res 14:123–133

    Google Scholar 

  • Bleecker AB, Kende H (2000) Ethylene, a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16:1–18

    CAS  PubMed  Google Scholar 

  • Borzouei A, Jamali SS, Paknejad F (2015) Root characteristics, Na+/K+ ratio and grain yield of seven wheat genotypes under salinity stress. J Sci Tech Greenh Cult 5:165–175

    Google Scholar 

  • Cao W, Liu J, He X, Mu R, Zhou H, Chen S, Zhang J (2007) Modulation of ethylene responses affects plant salt-stress responses. Plant Physiol 143:707–719

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen J, Zhu C, Li LP, Sun ZY, Pan XB (2007) Effects of exogenous salicylic acid on growth and H2O2-metabolizing enzymes in rice seedlings under lead stress. J Environ Sci 19:44–49

    CAS  Google Scholar 

  • Childs AC, Mehta DJ, Gerner EW (2003) Polyamine-dependent gene expression. Cell Mol Life Sci 60:1394–1406

    CAS  PubMed  Google Scholar 

  • Choudhary SP, Kanwar M, Bhardwaj R, Yu JQ, Tran LS (2012) Chromium stress mitigation by polyamine-brassinosteroid application involves phytohormonal and physiological strategies in Raphanus sativus L. PLoS ONE 7:e33210

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ding S, Zhang B, Qin F (2015) Arabidopsis RZFP34/CHYR1, a Ubiquitin E3 ligase, regulates stomatal movement and drought tolerance via SnRK2.6-mediated phosphorylation. Plant Cell 27:3228–3244

    CAS  PubMed  PubMed Central  Google Scholar 

  • Evans PT, Malmberg RL (1989) Do polyamines have roles in plant development? Ann Rev Plant Physiolol 40:235–269

    CAS  Google Scholar 

  • Feng Y, Zhuang B (2017) Flame atomic absorption spectrometry for the determination of potassium and sodium in Yanhuning. Channel Pharm 29:58–60

    Google Scholar 

  • Gama PBS, Tanaka K, Ahmed Z, Siddig KE (2007) Salinity induced stress effects on biomass, photosynthetic rate, and ROS-scavenging enzymes accumulation of Phaseolus vulgaris L. Acta Hort 746:381–386

    CAS  Google Scholar 

  • Gómez-Pando LR, Álvarez-Castro R, Eguiluz-de la Barra A (2010) Effect of salt stress on peruvian germplasm of Chenopodium quinoa Willd, A promising crop. J Agron Crop Sci 196:391–396

    Google Scholar 

  • Guo H, Hong C, Chen X, Xu Y, Liu Y, Jiang D, Zheng B (2016) Different growth and physiological responses to cadmium of the three Miscanthus species. PLoS ONE 11:e0153475

    PubMed  PubMed Central  Google Scholar 

  • Hariadi Y, Marandon K, Tian Y, Jacobsen SE, Shabala S (2011) Ionic and osmotic relations in quinoa (Chenopodium quinoa Willd.) plants grown at various salinity levels. J Exp Bot 62:185–193

    CAS  PubMed  Google Scholar 

  • Hatami E (2018) Alleviating salt stress in almond rootstocks using of humic acid. Sci Hortic 237:296–302

    CAS  Google Scholar 

  • Hernández JA, Jiménezz MP, Sevilla F (2010) Tolerance of pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defences. Plant Cell Environ 23:853–862

    Google Scholar 

  • Hong C, Guo H, Fang J, Ren W, Wang T, Ji MC (2014) Physiological and biochemical responses of Miscanthus sacchariflorus to salt stress. Adv Mater Res 1051:333–340

    Google Scholar 

  • Hu L, Xiang L, Li S, Zou Z, Hu X (2015) Beneficial role of spermidine in chlorophyll metabolism and D1 protein content in tomato seedlings under salinity-alkalinity stress. Physiol Plant 156:468–477

    PubMed  Google Scholar 

  • Huang Y, Liu L, Huang JQ, Wang Z, Chen F, Zhang Q, Zheng B, Chen M (2013) Use of transcriptome sequencing to understand the pistillate flowering in hickory (Carya cathayensis Sarg.). BMC Genom 14:1–18

    Google Scholar 

  • Jampeetong A, Brix H (2009) Effects of NaCl salinity on growth morphology, photosynthesis and proline accumulation of Salvinia natans. Aquat Bot 91:181–186

    CAS  Google Scholar 

  • Javid MG, Sorooshzadeh A, Moradi F, Modarres SAM, Allahdadi I (2011) The role of phytohormones in alleviating salt stress in crop plants. Aust J Crop Sci 32:726–734

    Google Scholar 

  • Jungmyung L (2010) Current status of vegetable grafting, diffusion, grafting techniques, automation. Sci Hortic 127:93–105

    Google Scholar 

  • Katahata S, Naramoto M, Kakubari Y, Mukai Y (2007) Photosynthetic capacity and nitrogen partitioning in foliage of the evergreen shrub Daphniphyllum humile along a natural light gradient. Tree Physiol 27:199–208

    CAS  PubMed  Google Scholar 

  • Klein A, Hüsselmann L, Keyster M, Ludidi N (2018) Exogenous nitric oxide limits salt-induced oxidative damage in maize by altering superoxide dismutase activity. S Afr J Bot 115:44–49

    CAS  Google Scholar 

  • Kubis J (2005) The effect of exogenous spermidine on superoxide dismutase activity, H2O2 and superoxide radical level in barley leaves under water deficit conditions. Acta Physiol Plant 27:289–295

    Google Scholar 

  • Li Y, Shi G, Wang H, Zhao J, Yuan Q (2009) Exogenous spermidine can mitigate the poison of cadmium in Nymphoides peltatum. Chin Bull Bot 5:571–577

    Google Scholar 

  • Li B, Sang T, He L (2013) Exogenous spermidine inhibits ethylene production in leaves of cucumber seedlings under NaCl stress. J Am Soc Hortic Sci 138:108–113

    CAS  Google Scholar 

  • Liu H, Yu B, Zhang W, Liu Y (2005) Effect of osmotic stress on the activity of H+-ATPase and the levels of covalently and noncovalently conjugated polyamines in plasma membrane preparation from wheat seedling roots. Plant Sci 168:1599–1607

    CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real time quantitative PCR and the 2−∆∆CT method. Methods 25:402–408

    CAS  PubMed  Google Scholar 

  • Ma L, Zhang H, Sun L, Jiao YH, Zhang GZ, Miao C, Hao FS (2012a) NADPH oxidase AtrbohD and AtrbohF function in ROS-dependent regulation of Na+/K+ homeostasis in Arabidopsis under salt stress. J Exp Bot 63:305–317

    CAS  PubMed  Google Scholar 

  • Ma T, Chen HW, Xiong XW (2012b) Effects of stock and scion on graft survival rate and growth of Carya illinoensis. J Northwest For Univ 27:141–143

    CAS  Google Scholar 

  • Mansour MMF (2012) Plasma membrane permeability as an indicator of salt tolerance in plants. Biol Plant Biol Plant 57:1–10

    Google Scholar 

  • Margulies MM (1962) Effect of chloramphenicol on light dependent development of seedlings of phaseolus vulgaris var. black valentine, with particular reference to development of photosynthetic activity. Plant Physiol 37:473–480

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mehta RA, Cassol T, Li N (2002) Engineered polyamine accumulation in tomato enhances phytonutrient content, juice quality, and vine life. Nat Biotechnol 20:613–618

    CAS  PubMed  Google Scholar 

  • Metternicht G, Zinck A (2003) Remote sensing of soil salinity: potentials and constraints. Remote Sens Environ 85:1–20

    Google Scholar 

  • Minocha R (2014) Polyamines and abiotic stress in plants, a complex relationship. Front Plant Sci 5:175–192

    PubMed  PubMed Central  Google Scholar 

  • Moschou PN, Paschalidis KA, Delis ID, Andriopoulou AH, Lagiotis GD, Yakoumakis DI, Roubelakis-Angelakis KA (2008) Spermidine exodus and oxidation in the apoplast induced by abiotic stress is responsible for H2O2 signatures that direct tolerance responses in tobacco. Plant Cell 20:1708–1724

    CAS  PubMed  PubMed Central  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    CAS  PubMed  Google Scholar 

  • O'Neil CE (2010) Tree nut consumption improves nutrient intake and diet quality in US adults, an analysis of National Health and Nutrition Examination Survey (NHANES) 1999–2004. Asia Pac J Clin Nutr 19:142–150

    CAS  PubMed  Google Scholar 

  • Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants, a review. Ecotoxicol Environ Saf 60:324–349

    CAS  PubMed  Google Scholar 

  • Petronia C, Danila P, Pasqualina W, Giovanni P, Giuseppina M, Maria GA, Amodio F, Ronan S (2011) Salt-induced accumulation of glycine betaine is inhibited by high light in durum wheat. Funct Plant Biol 38:139–150

    Google Scholar 

  • Pottosin I, Shabala S (2014) Polyamines control of cation transport across plant membranes: implications for ion homeostasis and abiotic stress signaling. Front Plant Sci 5:1–16. https://doi.org/10.3389/fpls.2014.00154

    Article  Google Scholar 

  • 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 Sci 168:583–591

    CAS  Google Scholar 

  • Sanchez DH, Cuevas JC, Chiesa MA, Ruiz OA (2005) Free spermidine and spermine content in Lotus glaber under long-term salt stress. Plant Sci 168:541–546

    CAS  Google Scholar 

  • Shi H (2013) Comparative proteomic and physiological analyses reveal the protective effect of exogenous polyamines in the Bermudagrass (Cynodon dactylon) response to salt and drought stresses. J Proteome Res 12:4951–4964

    CAS  PubMed  Google Scholar 

  • Smadar H, Mee YG, Mattoo AK, Kieber JJ (2012) The formation of ACC and competition between polyamines and ethylene for SAM. Annu Plant Rev 44:53–81

    Google Scholar 

  • Stark F, Pfannstiel J, Klaiber I, Raabe T (2011) Protein kinase CK2 links polyamine metabolism to mapk signalling in drosophila. Cell Signal 23:876–882

    CAS  PubMed  Google Scholar 

  • Sudha G, Ravishankar GA (2002) Involvement and interaction of various signaling compounds on the plant metabolic events during defense response, resistance to stress factors, formation of secondary metabolites and their molecular aspects. Plant Cell Tissue Organ Cult 71:181–212

    CAS  Google Scholar 

  • Sun J, Zou DT, Luan FS, Zhao HW, Wang JG, Liu HL, Xie DW, Su DQ, Ma J, Liu ZL (2014) Dynamic QTL analysis of the Na+ content, K+ content, and Na+/K+ ratio in rice roots during the field growth under salt stress. Biol Plant 58:689–696

    CAS  Google Scholar 

  • Tabor CW, Tabor H (1984) Polyamines. Annu Rev Biochem 53:749–790

    CAS  PubMed  Google Scholar 

  • Tiwari JK, Munshi AD, Kumar R, Pandey RN, Arora A, Bhat JS, Sureja AK (2010) Effect of salt stress on cucumber: Na+–K+ ratio, osmolyte concentration, phenols and chlorophyll content. Acta Physiol Plant 32:103–114

    CAS  Google Scholar 

  • Wang R, Hua C, Luo Q, Liu Y (2002) Na+ and K+ accumulation in chloroplasts results in a decrease in net photosynthetic rate in rice leaves under salt stress. Acta Photophysiol Sinica 28:385–390

    CAS  Google Scholar 

  • Wang L, Liu J, Wang W, Sun Y (2016) Exogenous melatonin improves growth and photosynthetic capacity of cucumber under salinity-induce stress. Photosynthetica 54:19–27

    Google Scholar 

  • Wu J, Shu S, Li C (2018) Spermidine-mediated hydrogen peroxide signaling enhances the antioxidant capacity of salt-stressed cucumber roots. Plant Physiol Biochem 128:152–162

    CAS  PubMed  Google Scholar 

  • Xu Y, Wang J, Shan L, Dong X, Li M (2001) Effect of exogenous polyamines on glycolate oxidase activity and active oxygen species accumulation in wheat seedlings under osmotic stress. Isr J Plant Sci 49:173–178

    CAS  Google Scholar 

  • Xu J, Li Y, Wang Y, Liu H, Lei L, Yang H, Liu G, Ren D (2008) Activation of MAPK kinase 9 induces ethylene and camalexin biosynthesis and enhances sensitivity to salt stress in Arabidopsis. J Biol Chem 283:26996–27006

    CAS  PubMed  Google Scholar 

  • Xu Q, Wu J, Cao Y, Yang X, Wang Z, Huang J, Xia G, Zhang Q, Hu Y (2016) Photosynthetic characteristics of leaves and fruits of Hickory (Carya cathayensis Sarg.) and Pecan (Carya illinoensis K.Koch) during fruit development stages. Trees 30:1–12

    Google Scholar 

  • Yang L, Zhu Y, Hu C (2007) Effects of NaCl stress on polyamine contents in grafted cucumber leaves. Chin J Appl Ecol 18:831–836

    CAS  Google Scholar 

  • Zapata PJ, Serrano M, Pretel MT (2003) Changes in ethylene evolution and polyamine profiles of seedlings of nine cultivars of Lactuca sativa L. in response to salt stress during germination. Plant Sci 164:557–563

    CAS  Google Scholar 

  • Zeng Y, Zhang Y, Xiang J, Wu H, Chen H, Zhang Y (2016) Effects of chilling tolerance induced by spermidine pretreatment on antioxidative activity, endogenous hormones and ultrastructure of indica-japonica hybrid rices seedlings. J Integr Agric 15:295–308

    CAS  Google Scholar 

  • Zhang Z, Qu WP (2003) The experimental guide for plant physiology, 3rd edn. Higher Education Press, Beijing, pp 67–69

    Google Scholar 

  • Zhang J, Jia W, Yang J, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crops Res 97:111–119

    Google Scholar 

  • Zhang M, Yuan B, Leng P (2009) The role of ABA in triggering ethylene biosynthesis and ripening of tomato fruit. J Exp Bot 60:1579–1588

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao S, Xu C, Zou Q (1994) Improvements of method for measurement of malondialdchyde in plant tissues. Plant Physiol Commun 30:207–210

    CAS  Google Scholar 

  • Zhao F, Song CP, He J, Zhu H (2007) Polyamines improve K+/Na+ homeostasis in barley seedlings by regulating root ion channel activities. Plant Physiol 145:1061–1072

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao J, Sun F, Yao X (2012) Effects of salt stress on growth and photosynthetic characteristics of Carya Illinoemis. J Southwest China Norm Univ 37:93–97

    CAS  Google Scholar 

  • Zhu Z, Wei G, Li J, Qian Q, Yu J (2004) Silicon alleviates salt stress and increases antioxidant enzymes activity in leaves of salt-stressed cucumber (Cucumis sativus L.). Plant Sci 16:527–533

    Google Scholar 

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Acknowledgements

This study was supported by National Key Research and Development Program of China (2018YFD1000600, 2018YFD1000604); Key Project of Zhejiang Provincial Natural Science Foundation (LZ18C160001); Independent Research Project of State Key Laboratory of Subtropical Silviculture, Zhejiang A & F University (ZY20180208, ZY20180308); Key Research and Development Program of Zhejiang Province (2018C02004); National Natural Science Foundation of China (31470683, 31270716 and 31070604); National High Technology Research and Development Program of China (863 Program) (2013AA102605); Open Foundation of State Key Laboratory of Subtropical Silviculture, Zhejiang A & F University (KF201708); Fruit Innovation Team Project of Zhejiang Province (2016C02052-12); Key Agricultural New Varieties Breeding Projects founded by Zhejiang Province Science and Technology Department (2016C02052-13); Open Foundation of First-class Discipline of Forestry, Zhejiang Province (201703); National Undergraduate Innovation and Entrepreneurship Training Project (201610341010); Undergraduate Science and Technology Innovation Plan of Zhejiang Province (2017R412006); Undergraduate Research Training Program in Zhejiang A & F University (KX20180047, KX20180043, KX20180065).

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  1. Zhiwei Wu, Junfeng Wang, Daoliang Yan, and Huwei Yuan contributed equally in this study.

Authors and Affiliations

  1. State Key Laboratory of Subtropical Silviculture, Zhejiang A & F University, Linan, Hangzhou, 311300, China

    Zhiwei Wu, Junfeng Wang, Daoliang Yan, Huwei Yuan, Yang Wang, Yi He, Xiaofei Wang, Zhen Li, Jiaqi Mei, Mengyao Hu, Tingting Zhou, Sun-Li Chong & Bingsong Zheng

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  1. Zhiwei Wu
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Wu, Z., Wang, J., Yan, D. et al. Exogenous spermidine improves salt tolerance of pecan-grafted seedlings via activating antioxidant system and inhibiting the enhancement of Na+/K+ ratio. Acta Physiol Plant 42, 83 (2020). https://doi.org/10.1007/s11738-020-03066-4

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