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Hydrogen peroxide alleviates salinity-induced damage through enhancing proline accumulation in wheat seedlings

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NADPH oxidase-mediated H2O2 maintains proline concentration under NaCl stress through regulating its biosynthesis and degradation, conferring salt tolerance to wheat plants.

Abstract

Considerable attention has been paid to the specific role of hydrogen peroxide (H2O2) in plant stress responses. Here, using microscopic, pharmacological and biochemical approaches, we explored H2O2 production and its roles in redox control under salt stress in wheat roots. Exogenous H2O2 pretreatment decreased salt-induced lipid peroxidation, while increased proline content in wheat roots. Salt stress led to a transient increase in NADPH oxidase activity accompanied by accumulation of H2O2 and proline in roots. The elevated proline accumulation in the presence of NaCl was significantly suppressed by diphenyleneiodonium, an inhibitor of NADPH oxidase, and dimethylthiourea, a scavenger of H2O2. The rate-limiting enzyme involved in proline biosynthesis, Δ1-pyrroline-5-carboxylate synthetase (P5CS), was induced by NaCl, whereas the house-keeping enzyme in proline degradation, proline dehydrogenase (ProDH), was inhibited. After 6 h, the activity of P5CS increased by 1.5-fold, whereas ProDH decreased by 13.9%. The levels of these enzymes, however, were restored by NADPH oxidase inhibitor or H2O2 scavenger. After treatment with H2O2, the effects of diphenyleneiodonium and or dimethylthiourea on proline content and activities of P5CS and ProDH were reversed. These results suggested that NADPH oxidase-mediated H2O2 alleviates oxidative damage induced by salt stress through regulating proline biosynthesis and degradation.

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References

  • Ashraf M, Foolad M (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216

    CAS  Google Scholar 

  • Rejeb KB, Lefebvre-De Vos D, Le Disquet I, Leprince AS, Bordenave M, Maldiney R, Jdey A, Abdelly C, Savoure A (2015) Hydrogen peroxide produced by NADPH oxidases increases proline accumulation during salt or mannitol stress in Arabidopsis thaliana. New Phytol 208:1138–1148

    PubMed  Google Scholar 

  • Chao YY, Chen CY, Huang WD, Kao CH (2010) Salicylic acid-mediated hydrogen peroxide accumulation and protection against Cd toxicity in rice leaves. Plant Soil 329:327–337

    CAS  Google Scholar 

  • Chung JS, Zhu JK, Bressan RA, Hasegawa PM, Shi H (2008) Reactive oxygen species mediate Na+-induced SOS1 mRNA stability in Arabidopsis. Plant J 53:554–565

    CAS  PubMed  Google Scholar 

  • de Campos MKF, de Carvalho K, de Souza FS, Marur CJ, Pereira LFP, Bespalhok Filho JC, Vieira LGE (2011) Drought tolerance and antioxidant enzymatic activity in transgenic ‘Swingle’ citrumelo plants over-accumulating proline. Environ Exp Bot 72:242–250

    Google Scholar 

  • de Sousa DPF, Braga BB, Gondim FA, Gomes-Filho MK, de Brito POB (2016) Increased drought tolerance in maize plants induced by H2O2 is closely related to an enhanced enzymatic antioxidant system and higher soluble protein a nd organic solutes contents. Theor Exp Plant Phys 28:297–306

    Google Scholar 

  • Di Martino C, Delfine S, Pizzuto R, Loreto F, Fuggi A (2003) Free amino acids and glycine betaine in leaf osmoregulation of spinach responding to increasing salt stress. New Phytol 158:455–463

    Google Scholar 

  • Forni C, Duca D, Glick BR (2017) Mechanisms of plant response to salt and drought stress and their alteration by rhizobacteria. Plant Soil 410:35–356

    Google Scholar 

  • Giberti S, Funck D, Forlani G (2014) Δ1-pyrroline-5-carboxylate reductase from Arabidopsis thaliana: stimulation or inhibition by chloride ions and feedback regulation by proline depend on whether NADPH or NADH acts as co-substrate. New Phytol 202:911–919

    CAS  PubMed  Google Scholar 

  • Gupta D, Pena L, Romero-Puertas M, Hernández A, Inouhe M, Sandalio L (2017) NADPH oxidases differentially regulate ROS metabolism and nutrient uptake under cadmium toxicity. Plant Cell Environ 40:509–526

    CAS  PubMed  Google Scholar 

  • Khedr AHA, Abbas MA, Wahid AAA, Quick WP, Abogadallah GM (2003) Proline induces the expression of salt-stress-responsive proteins and may improve the adaptation of Pancratium maritimum L. to salt-stress. J Exp Bot 54:2553–2562

    CAS  PubMed  Google Scholar 

  • Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JD, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623–2633

    CAS  PubMed  PubMed Central  Google Scholar 

  • López-Gómez M, Hidalgo-Castellanos J, Iribarne C, Lluch C (2014) Proline accumulation has prevalence over polyamines in nodules of Medicago sativa in symbiosis with Sinorhizobiummeliloti during the initial response to salinity. Plant Soil 374:149–159

    Google Scholar 

  • Marino D, Dunand C, Puppo A, Pauly N (2012) A burst of plant NADPH oxidases. Trends Plant Sci 17:9–15

    CAS  PubMed  Google Scholar 

  • Miller GA, Suzuki N, Ciftci-Yilmaz SU, Mittler RO (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    CAS  PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    CAS  PubMed  Google Scholar 

  • Molinari HBC, Marur CJ, Daros E, De Campos MKF, De Carvalho JFRP, Filho JCB, Pereira LFP, Vieira LGE (2007) Evaluation of the stress-inducible production of proline in transgenic sugarcane (Saccharum spp.): osmotic adjustment, chlorophyll fluorescence and oxidative stress. Physiol Plantarum 130:218–229

    CAS  Google Scholar 

  • Morgan RW, Christman MF, Jacobson FS, Storz G, Ames BN (1986) Hydrogen peroxide-inducible proteins in Salmonella typhimurium overlap with heat shock and other stress proteins. Proc Natl Acad Sci USA 83:8059–8063

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot 53:1237–1247

    CAS  PubMed  Google Scholar 

  • Rejeb KB, Abdelly C, Savouré A (2014) How reactive oxygen species and proline face stress together. Plant Physiol Bioc 80:278–284

    Google Scholar 

  • Rena AB, Splittstoesser WE (1975) Proline dehydrogenase and pyrroline-5-carboxylate reductase from pumpkin cotyledons. Phytochemistry 14:657–661

    CAS  Google Scholar 

  • Sharma S, Villamor JGC, Verslues PE (2011) Essential role of tissue specific proline synthesis and catabolism in growth and redox balance at low water potential. Plant Physiol 157:292–304

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sheldon AR, Dalal RC, Kirchhof G, Kopittke PM, Menzies NW (2017) The effect of salinity on plant-available water. Plant Soil 418:477–491

    CAS  Google Scholar 

  • Shin R, Schachtman DP (2004) Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proc Natl Acad Sci USA 101:8827–8832

    CAS  PubMed  Google Scholar 

  • Slama I, Abdelly C, Bouchereau A, Flowers T, Savoure A (2015) Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Ann Bot 115:433–447

    CAS  PubMed  PubMed Central  Google Scholar 

  • Smirnoff N, Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28:1057–1060

    CAS  Google Scholar 

  • Strizhov N, Ábrahám E, Ökrész L, Blickling S, Zilberstein A, Schell J, Koncz C, Szabados L (1997) Differential expression of two P5CS genes controlling proline accumulation during salt-stress requires ABA and is regulated by ABA1, ABI1 and AXR2 in Arabidopsis. Plant J 12:557–569

    CAS  PubMed  Google Scholar 

  • Sun C, Lu L, Liu L, Liu W, Yu Y, Liu X, Hu Y, Jin C, Lin X (2014) Nitrate reductase-mediated early nitric oxide burst alleviates oxidative damage induced by aluminum through enhancement of antioxidant defenses in roots of wheat (Triticum aestivum). New Phytol 201:1240–1250

    CAS  PubMed  Google Scholar 

  • Sun C, Liu L, Yu Y, Liu W, Lu L, Jin C, Lin X (2015) Nitric oxide alleviates aluminum-induced oxidative damage through regulating the ascorbate-glutathione cycle in roots of wheat. J Integr Plant Biol 57:550–561

    CAS  PubMed  Google Scholar 

  • Sun C, Liu L, Zhou W, Lu L, Jin C, Lin X (2017) Aluminum induces distinct changes in the metabolism of reactive oxygen and nitrogen species in the roots of two wheat genotypes with different aluminum resistance. J Agric Food Chem 65:9419–9427

    CAS  PubMed  Google Scholar 

  • Sun C, Liu L, Lu L, Jin C, Lin X (2018) Nitric oxide acts downstream of hydrogen peroxide in regulating aluminum-induced antioxidant defense that enhances aluminum resistance in wheat seedlings. Environ Exp Bot 145:95–103

    CAS  Google Scholar 

  • Szabados L, Savoure A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97

    CAS  Google Scholar 

  • Uchida A, Jagendorf AT, Hibino T, Takabe T, Takabe T (2002) Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci 163:515–523

    CAS  Google Scholar 

  • Vergara R, Parada F, Rubio S, Pérez FJ (2012) Hypoxia induces H2O2 production and activates antioxidant defence system in grapevine buds through mediation of H2O2 and ethylene. J Exp Bot 63:4123–4131

    CAS  PubMed  PubMed Central  Google Scholar 

  • Voothuluru P, Sharp RE (2012) Apoplastic hydrogen peroxide in the growth zone of the maize primary root under water stress. I. Increased levels are specific to the apical region of growth maintenance. J Exp Bot 64:1223–1233

    PubMed  Google Scholar 

  • Xia XJ, Wang YJ, Zhou YH, Tao Y, Mao WH, Shi K, Asami T, Chen Z, Yu JQ (2009) Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiol 150:801–814

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xia XJ, Gao CJ, Song LX, Zhou YH, Shi K, Yu JQ (2014) Role of H2O2 dynamics in brassinosteroid-induced stomatal closure and opening in Solanum lycopersicum. Plant Cell Environ 37:2036–2050

    CAS  PubMed  Google Scholar 

  • Xu J, Yin H, Li Y, Liu X (2010) Nitric oxide is associated with long-term Zn tolerance in Solanum nigrum. Plant Physiol 154:1319–1334

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang SL, Lan SS, Gong M (2009) Hydrogen peroxide-induced proline and metabolic pathway of its accumulation in maize seedlings. J Plant Physiol 166:1694–1699

    CAS  PubMed  Google Scholar 

  • Yang Y, Zhang Y, Lu J, Zhang H, Liu Y, Jiang Y, Shi R (2012) Exogenous H2O2 increased catalase and peroxidase activities and proline content in Nitraria tangutorum callus. Biol Plantarum 56:330–336

    CAS  Google Scholar 

  • Yang Z, Zheng H, Wei X, Song J, Wang B, Sui N (2018) Transcriptome analysis of sweet Sorghum inbred lines differing in salt tolerance provides novel insights into salt exclusion by roots. Plant Soil 430:423–439

    CAS  Google Scholar 

  • Yu L, Nie J, Cao C, Jin Y, Yan M, Wang F, Liu J, Xiao Y, Liang Y, Zhang W (2010) Phosphatidic acid mediates salt stress response by regulation of MPK6 in Arabidopsis thaliana. New Phytol 188:762–773

    CAS  PubMed  Google Scholar 

  • Zhang A, Jiang M, Zhang J, Ding H, Xu S, Hu X, Tan M (2007) Nitric oxide induced by hydrogen peroxide mediates abscisic acid-induced activation of the mitogen-activated protein kinase cascade involved in antioxidant defense in maize leaves. New Phytol 175:36–50

    CAS  PubMed  Google Scholar 

  • Zhang LP, Mehta SK, Liu ZP, Yang ZM (2008) Copper-induced proline synthesis is associated with nitric oxide generation in Chlamydomonas reinhardtii. Plant Cell Physiol 49:411–419

    CAS  PubMed  Google Scholar 

  • Zhao L, Zhang F, Guo J, Yang Y, Li B, Zhang L (2004) Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiol 134:849–857

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (31872167).

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Author notes

  1. Lijuan Liu and Lin Huang contributed equally to this work.

Authors and Affiliations

  1. MOE Key Laboratory of Environment Remediation and Ecological Health, College of Natural Resource and Environmental Sciences, Zhejiang University, Hangzhou, 310058, China

    Lijuan Liu, Lin Huang, Xianyong Lin & Chengliang Sun

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  1. Lijuan Liu
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  2. Lin Huang
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  3. Xianyong Lin
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  4. Chengliang Sun
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LL, LH and CS designed and performed the experiments; LL analyzed the data; LL, LH, CS and XL wrote the manuscript.

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Correspondence to Chengliang Sun.

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Communicated by Prakash Lakshmanan.

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Liu, L., Huang, L., Lin, X. et al. Hydrogen peroxide alleviates salinity-induced damage through enhancing proline accumulation in wheat seedlings. Plant Cell Rep 39, 567–575 (2020). https://doi.org/10.1007/s00299-020-02513-3

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