Plant response to salinity: an analysis of ROS formation, signaling, and antioxidant defense

Reactive oxygen species (ROS) are byproducts of normal plant metabolism and their production is elevated under environmental stresses such as drought, extreme temperature, and salinity. Among these, salinity is a worldwide problem that impacts the fertility of arable lands and sustainability of food security, which is getting more attention due to climate change. Halophytes can survive and reproduce in soils containing high concentrations of salt and have developed adaptation mechanisms at physiological, biochemical, and molecular levels including maintenance of ROS metabolism. In this review, we aim to summarize findings related to ROS production, signaling, scavenging, and especially ROS avoidance mechanisms under salt stress. In addition, expressions of antioxidant genes in Arabidopsis thaliana and its close relative, the model halophyte Schrenkiella parvula, are compared. Moreover, time-course expression levels of genes encoding major antioxidant enzymes in the model plant A. thaliana are analyzed with publicly available data to understand rapid responses of antioxidant defense under salt stress. The role of ROS-Ca+2 interaction and involvement of NADPH oxidases in this process are also discussed in the context of the perception and signaling of salt stress.

___

  • Ali A, Yun DJ (2017). Salt stress tolerance; what do we learn from halophytes. Journal of Plant Biology 60 (5): 431-439.
  • Amor NB, Hamed KB, Debez A, Grignon C, Abdelly C (2005). Physiological and antioxidant responses of the perennial halophyte Crithmum maritimum to salinity. Plant Science 168 (4): 889-899.
  • Amor NB, Jiménez A, Megdiche W, Lundqvist M, Sevilla F et al. (2007). Kinetics of the anti-oxidant response to salinity in the halophyte Cakile maritima. Journal of Integrative Plant Biology 49 (7): 982-992.
  • Asada K (2006). Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiology 141 (2): 391-396. doi: 10.1104/pp.106.082040
  • Baxter A, Mittler R, Suzuki N (2013). ROS as key players in plant stress signalling. Journal of Experimental Botany 65 (5): 1229- 1240. doi: 10.1093/jxb/ert375
  • Benzarti M, Rejeb KB, Debez A, Messedi D, Abdelly C (2012). Photosynthetic activity and leaf antioxidative responses of Atriplex portulacoides subjected to extreme salinity. Acta Physiologiae Plantarum 34 (5): 1679-1688.
  • Bor M, Özdemir F, Türkan I (2003). The effect of salt stress on lipid peroxidation and antioxidants in leaves of sugar beet Beta vulgaris L. and wild beet Beta maritima L. Plant Science 164 (1): 77-84.
  • Bose J, Rodrigo-Moreno A, Shabala S (2014). ROS homeostasis in halophytes in the context of salinity stress tolerance. Journal of Experimental Botany 65 (5): 1241-1257.
  • Bromham L, Bennett TH (2014). Salt tolerance evolves more frequently in C4 grass lineages. Journal of Evolutionary Biology 27 (3): 653-659.
  • Carmo-Silva AE, Powers SJ, Keys AJ, Arrabaça MC, Parry MA (2008). Photorespiration in C4 grasses remains slow under drought conditions. Plant, Cell & Environment 31 (7): 925-940.
  • Costa JH, Svensson JT (2015). AOX gene diversity in Arabidopsis ecotypes. In: Gupta KJ, Mur LAJ, Neelwarne B (editors). Alternative Respiratory Pathways in Higher Plants. New York, NY, USA: Wiley, pp. 255-259.
  • Dassanayake M, Oh DH, Haas JS, Hernandez A, Hong H et al. (2011). The genome of the extremophile crucifer Thellungiella parvula. Nature Genetics 43 (9): 913.
  • Davenport R, James RA, Zakrisson-Plogander A, Tester M, Munns R (2005). Control of sodium transport in durum wheat. Plant Physiology 137 (3): 807-818.
  • Debez A, Rejeb KB, Ghars MA, Gandour M, Megdiche W et al. (2013). Ecophysiological and genomic analysis of salt tolerance of Cakile maritima. Environmental and Experimental Botany 92: 64-72.
  • Demidchik V, Cuin TA, Svistunenko D, Smith SJ, Miller AJ et al. (2010). Arabidopsis root K+-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. Journal of Cell Science 123 (9): 1468-1479.
  • Demidchik V, Shabala S (2018). Mechanisms of cytosolic calcium elevation in plants: the role of ion channels, calcium extrusion systems and NADPH oxidase-mediated ‘ROS-Ca2+ hub’. Functional Plant Biology 45 (2): 9-27.
  • Demiral T, Türkan I (2005). Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance. Environmental and Experimental Botany 53 (3): 247-257.
  • Edel KH, Marchadier E, Brownlee C, Kudla J, Hetherington AM (2017). The evolution of calcium-based signalling in plants. Current Biology 27 (13): R667-R679.
  • Ellouzi H, Ben Hamed K, Cela J, Munné-Bosch S, Abdelly C (2011). Early effects of salt stress on the physiological and oxidative status of Cakile maritima (halophyte) and Arabidopsis thaliana (glycophyte). Physiologia Plantarum 142 (2): 128-143.
  • Ellouzi H, Hamed KB, Hernández I, Cela J, Müller M et al. (2014). A comparative study of the early osmotic, ionic, redox and hormonal signaling response in leaves and roots of two halophytes and a glycophyte to salinity. Planta 240 (6): 1299- 1317.
  • Flowers TJ, Hajibagheri MA, Clipson NJW (1986). Halophytes. Quarterly Review of Biology 61 (3): 313-337.
  • Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H et al. (2003). Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422 (6930): 442.
  • Foyer CH, Noctor G (2011). Ascorbate and glutathione: the heart of the redox hub. Plant Physiology 155 (1): 2-18.
  • Ghosh S, Bagchi S, Majumder AL (2001). Chloroplast fructose-1, 6-bisphosphatase from Oryza differs in salt tolerance property from the Porteresia enzyme and is protected by osmolytes. Plant Science 160 (6): 1171-1181.
  • Glenn E, Miyamoto S, Moore D, Brown JJ, Thompson TL et al. (1997). Water requirements for cultivating Salicornia bigelovii Torr. with seawater on sand in a coastal desert environment. Journal of Arid Environments 36 (4): 711-730.
  • Gong Q, Li P, Ma S, Indu Rupassara S, Bohnert HJ (2005). Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. The Plant Journal 44 (5): 826-839
  • Greenway H, Munns R (1980). Mechanisms of salt tolerance in nonhalophytes. Annual Review of Plant Physiology 31 (1): 149-190.
  • Grigore MN (2019). Defining halophytes: a conceptual and historical approach in an ecological frame. In: Hasanuzzaman M, Shabala S, Fujita M (editors). Halophytes and Climate Change: Adaptive Mechanisms and Potential Uses. Wallingford, UK: CABI, pp. 3-18.
  • Gupta B, Huang B (2014). Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. International Journal of Genomics 2014: 701596.
  • Halliwell B, Gutteridge JM (2015). Free Radicals in Biology and Medicine. New York, NY, USA: Oxford University Press. Hu Y, Schmidhalter U (2005). Drought and salinity: a comparison of their effects on mineral nutrition of plants. Journal of Plant Nutrition and Soil Science 168 (4): 541-549.
  • Huang C, He W, Guo J, Chang X, Su P et al. (2005). Increased sensitivity to salt stress in an ascorbate-deficient Arabidopsis mutant. Journal of Experimental Botany 56 (422): 3041-3049.
  • Huang S, Jiang S, Liang J, Chen M (2019). Roles of plant CBL-CIPK systems in abiotic stress responses. Turkish Journal of Botany 43 (3): 271-280.
  • Jardim-Messeder D, Caverzan A, Rauber R, de Souza Ferreira E, Margis-Pinheiro M et al. (2015). Succinate dehydrogenase (mitochondrial complex II) is a source of reactive oxygen species in plants and regulates development and stress responses. New Phytologist 208 (3): 776-789.
  • Joshi R, Mangu VR, Bedre R, Sanchez L, Pilcher W et al. (2015). Salt adaptation mechanisms of halophytes: improvement of salt tolerance in crop plants. In: Pandey GK (editor). Elucidation of Abiotic Stress Signaling in Plants. New York, NY, USA: Springer, pp. 243-279.
  • Kangasjärvi S, Neukermans J, Li S, Aro EM, Noctor G (2012). Photosynthesis, photorespiration, and light signalling in defence responses. Journal of Experimental Botany 63 (4): 1619-1636.
  • Kärkönen A, Kuchitsu K (2015). Reactive oxygen species in cell wall metabolism and development in plants. Phytochemistry 112: 22-32.
  • Khan MA, Duke NC (2001). Halophytes–A resource for the future. Wetlands Ecology and Management 9 (6): 455-456.
  • Khan MA, Ungar IA, Showalter AM (2000). Effects of salinity on growth, water relations and ion accumulation of the subtropical perennial halophyte, Atriplex griffithii var. stocksii. Annals of Botany 85 (2): 225-232.
  • Kilian J, Whitehead D, Horak J, Wanke D, Weinl S et al. (2007). The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. The Plant Journal 50 (2): 347-363.
  • Krieger-Liszkay A, Feilke K (2016). The dual role of the plastid terminal oxidase PTOX: between a protective and a prooxidant function. Frontiers in Plant Science 6: 1147.
  • Ksouri R, Ksouri WM, Jallali I, Debez A, Magné C et al. (2012). Medicinal halophytes: potent source of health promoting biomolecules with medical, nutraceutical and food applications. Critical Reviews in Biotechnology 32 (4): 289- 326.
  • Kumari A, Das P, Parida AK, Agarwal PK (2015). Proteomics, metabolomics, and ionomics perspectives of salinity tolerance in halophytes. Frontiers in Plant Science 6: 537.
  • Mahajan S, Tuteja N (2005). Cold, salinity and drought stresses: an overview. Archives of Biochemistry and Biophysics 444 (2): 139-158.
  • Mano JI, Nagata M, Okamura S, Shiraya T, Mitsui T (2014). Identification of oxidatively modified proteins in salt-stressed Arabidopsis: a carbonyl-targeted proteomics approach. Plant and Cell Physiology 55 (7): 1233-1244.
  • Mazzucotelli E, Mastrangelo AM, Crosatti C, Guerra D, Stanca AM et al. (2008). Abiotic stress response in plants: when posttranscriptional and post-translational regulations control transcription. Plant Science 174 (4): 420-431.
  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004). Reactive oxygen gene network of plants. Trends in Plant Science 9 (10): 490-498.
  • Munns R, Day DA, Fricke W, Watt M, Arsova B et al. (2019). Energy costs of salt tolerance in crop plants. New Phytologist (in press). doi: 10.1111/nph.15864
  • Munns R, Tester M (2008). Mechanisms of salinity tolerance. Annual Reviews of Plant Biology 59: 651-681. doi: 10.1146/annurev. arplant.59.032607.092911
  • Nawrocki WJ, Tourasse NJ, Taly A, Rappaport F, Wollman FA (2015). The plastid terminal oxidase: its elusive function points to multiple contributions to plastid physiology. Annual Review of Plant Biology 66: 49-74. doi: 10.1146/annurevarplant-043014-114744
  • Oda T, Hashimoto H, Kuwabara N, Akashi S, Hayashi K et al. (2010). Structure of the N-terminal regulatory domain of a plant NADPH oxidase and its functional implications. Journal of Biological Chemistry 285 (2): 1435-1445.
  • Oh DH, Hong H, Lee SY, Yun DJ, Bohnert HJ et al. (2014). Genome structures and transcriptomes signify niche adaptation for the multiple-ion-tolerant extremophyte Schrenkiella parvula. Plant Physiology 164 (4): 2123-2138.
  • Osmond CB, Greenway H (1972). Salt responses of carboxylation enzymes from species differing in salt tolerance. Plant Physiology 49 (2): 260-263.
  • Ozfidan-Konakci C, Uzilday B, Ozgur R, Yildiztugay E, Sekmen AH et al. (2016). Halophytes as a source of salt tolerance genes and mechanisms: a case study for the Salt Lake area, Turkey. Functional Plant Biology 43 (7): 575-589.
  • Ozgur R, Uzilday B, Iwata Y, Koizumi N, Turkan I (2018). Interplay between the unfolded protein response and reactive oxygen species: a dynamic duo. Journal of Experimental Botany 69 (14): 3333-3345.
  • Ozgur R, Uzilday B, Sekmen AH, Turkan I (2013). Reactive oxygen species regulation and antioxidant defence in halophytes. Functional Plant Biology 40 (9): 832-847.
  • Pantoja O, Gelli A, Blumwald E (1992). Characterization of vacuolar malate and K+ channels under physiological conditions. Plant Physiology 100 (3): 1137-1141.
  • Papdi C, Abrahám E, Joseph MP, Popescu C, Koncz C et al. (2008). Functional identification of Arabidopsis stress regulatory genes using the controlled cDNA overexpression system. Plant Physiology 147 (2): 528-542.
  • Perez IB, Brown PJ (2014). The role of ROS signaling in crosstolerance: from model to crop. Frontiers in Plant Science 5: 754.
  • Petrov V, Hille J, Mueller-Roeber B, Gechev TS (2015). ROSmediated abiotic stress-induced programmed cell death in plants. Frontiers in Plant Science 6: 69.
  • Pottosin I, Velarde-Buendía AM, Bose J, Zepeda-Jazo I, Shabala S et al. (2014). Cross-talk between reactive oxygen species and polyamines in regulation of ion transport across the plasma membrane: implications for plant adaptive responses. Journal of Experimental Botany 65 (5): 1271-1283.
  • Qadir M, Quillérou E, Nangia V, Murtaza G, Singh M et al. (2014). Economics of salt-induced land degradation and restoration. Natural Resources Forum 38: 282-295. doi: 10.1111/1477- 8947.12054
  • Saha B, Borovskii G, Panda SK (2016). Alternative oxidase and plant stress tolerance. Plant Signaling & Behavior 11 (12): e1256530.
  • Schroeder JI, Kwak JM, Allen GJ (2001). Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature 410 (6826): 327.
  • Seckin B, Turkan I, Sekmen AH, Ozfidan C (2010). The role of antioxidant defense systems at differential salt tolerance of Hordeum marinum Huds. (sea barleygrass) and Hordeum vulgare L. (cultivated barley). Environmental and Experimental Botany 69 (1): 76-85.
  • Shabala S (2017). Signalling by potassium: another second messenger to add to the list? Journal of Experimental Botany 68 (15): 4003-4007. doi: 10.1093/jxb/erx238
  • Shabala S, Wu H, Bose J (2015). Salt stress sensing and early signalling events in plant roots: current knowledge and hypothesis. Plant Science 241: 109-119.
  • Shalata A, Mittova V, Volokita M, Guy M, Tal M (2001). Response of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii to salt-dependent oxidative stress: the root antioxidative system. Physiologia Plantarum 112 (4): 487- 494.
  • Smith CA, Melino VJ, Sweetman C, Soole KL (2009). Manipulation of alternative oxidase can influence salt tolerance in Arabidopsis thaliana. Physiologia Plantarum 137 (4): 459-472.
  • Srivastava AK, Srivastava S, Lokhande VH, D’Souza SF, Suprasanna P (2015). Salt stress reveals differential antioxidant and energetics responses in glycophyte (Brassica juncea L.) and halophyte (Sesuvium portulacastrum L.). Frontiers in Environmental Science 3: 19.
  • Steduto P, Albrizio R, Giorio P, Sorrentino G (2000). Gas-exchange response and stomatal and non-stomatal limitations to carbon assimilation of sunflower under salinity. Environmental and Experimental Botany 44 (3): 243-255.
  • Stepien P, Johnson GN (2009). Contrasting responses of photosynthesis to salt stress in the glycophyte Arabidopsis and the halophyte Thellungiella: role of the plastid terminal oxidase as an alternative electron sink. Plant Physiology 149 (2): 1154- 1165.
  • Suekawa M, Fujikawa Y, Inada S, Murano A, Esaka M (2016). Gene expression and promoter analysis of a novel tomato aldo-keto reductase in response to environmental stresses. Journal of Plant Physiology 200: 35-44.
  • Suzuki N, Koussevitzky S, Mittler R, Miller G (2012). ROS and redox signalling in the response of plants to abiotic stress. Plant, Cell & Environment 35 (2): 259-270.
  • Suzuki N, Miller G, Morales J, Shulaev V, Torres MA et al. (2011). Respiratory burst oxidases: the engines of ROS signaling. Current Opinion in Plant Biology 14 (6): 691-699. Swanson S, Gilroy S (2010). ROS in plant development. Physiologia Plantarum 138 (4): 384-392.
  • Turkan I, Uzilday B, Dietz KJ, Bräutigam A, Ozgur R (2018). Reactive oxygen species and redox regulation in mesophyll and bundle sheath cells of C4 plants. Journal of Experimental Botany 69 (14): 3321-3331.
  • Uzilday B, Ozgur R, Sekmen AH, Turkan I (2015). Redox regulation and antioxidant defence during abiotic stress: what have we learned from Arabidopsis and its relatives? In: Gupta DK (editor). Reactive Oxygen Species and Oxidative Damage in Plants Under Stress. Cham, Switzerland: Springer, pp. 83-113.
  • Uzilday B, Ozgur R, Sekmen AH, Turkan I (2018a). Endoplasmic reticulum stress regulates glutathione metabolism and activities of glutathione related enzymes in Arabidopsis. Functional Plant Biology 45 (2): 284-296.
  • Uzilday B, Ozgur R, Sekmen AH, Yildiztugay E, Turkan I (2014a). Changes in the alternative electron sinks and antioxidant defence in chloroplasts of the extreme halophyte Eutrema parvulum (Thellungiella parvula) under salinity. Annals of Botany 115 (3): 449-463.
  • Uzilday B, Ozgur R, Yalcinkaya T, Turkan I, Sekmen AH (2018b). Changes in redox regulation during transition from C3 to single cell C4 photosynthesis in Bienertia sinuspersici. Journal of Plant Physiology 220: 1-10.
  • Uzilday B, Turkan I, Ozgur R, Sekmen AH (2014b). Strategies of ROS regulation and antioxidant defense during transition from C3 to C4 photosynthesis in the genus Flaveria under PEG-induced osmotic stress. Journal of Plant Physiology 171 (1): 65-75.
  • Vemanna RS, Babitha KC, Solanki JK, Reddy VA, Sarangi SK et al. (2017). Aldo-keto reductase-1 (AKR1) protect cellular enzymes from salt stress by detoxifying reactive cytotoxic compounds. Plant Physiology and Biochemistry 113: 177-186.
  • Wang F, Chen ZH, Liu X, Shabala L, Yu M et al. (2019). The loss of RBOHD function modulates root adaptive responses to combined hypoxia and salinity stress in Arabidopsis. Environmental and Experimental Botany 158: 125-135.
  • Warwick NWM, Halloran GM (1992). Accumulation and excretion of sodium, potassium and chloride from leaves of two accessions of Diplachne fusca (L.) Beauv. New Phytologist 121 (1): 53-61.
  • Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV et al. (2007). An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS One 2 (8): e718.
  • Yaish MW (2015.) Proline accumulation is a general response to abiotic stress in the date palm tree (Phoenix dactylifera L.). Genetics and Molecular Research 14 (3): 9943-9950.
  • Yalcinkaya T, Uzilday B, Ozgur R, Turkan I (2019a). The roles of reactive carbonyl species in induction of antioxidant defence and ROS signalling in extreme halophytic model Eutrema parvulum and glycophytic model Arabidopsis thaliana. Environmental and Experimental Botany 160: 81-91.
  • Yalcinkaya T, Uzilday B, Ozgur R, Turkan I, Mano JI (2019b). Lipid peroxidation-derived reactive carbonyl species (RCS): their interaction with ROS and cellular redox during environmental stresses. Environmental and Experimental Botany 165: 139- 149.
  • Yang CW, Zhang ML, Liu J, Shi DC, Wang DL (2009). Effects of buffer capacity on growth, photosynthesis, and solute accumulation of a glycophyte (wheat) and a halophyte (Chloris virgata). Photosynthetica 47 (1): 55-60.
  • Yildiztugay E, Ozfidan-Konakci C, Kucukoduk M (2014). The role of antioxidant responses on the tolerance range of extreme halophyte Salsola crassa grown under toxic salt concentrations. Ecotoxicology and Environmental Safety 110: 21-30.
  • Zhu JK (2001) Plant salt tolerance. Trends in Plant Science 6 (2): 66-