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Changes in Carbon Partitioning and Pattern of Antioxidant Enzyme Activity Induced by Arginine Treatment in the Green Microalga Dunaliella salina Under Long-Term Salinity

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Abstract

In this work, the effects of arginine (Arg) on biochemical responses and antioxidant enzyme activity in the green microalga Dunaliella salina grown at different salt concentrations were investigated. Suspensions adapted with the concentrations of 1, 2, and 3 M NaCl were treated at the exponential growth phase with a concentration of 5 mM Arg. Salt stress was associated with a large decrease in the number of cells and non-reducing sugar levels but accumulated higher amounts of chlorophyll, β-carotene, reducing sugar, starch, total protein, free amino acid, and glycerol. Increased levels of protein carbonylation, lipid peroxidation, proteolysis, hydrogen peroxide, and antioxidant enzyme activity also occurred during salinity. Arg treatment changed the pattern of biochemical responses in the cells grown at high salinity by directing carbon flow to the biosynthesis of non-reducing sugars instead of starch, lowering levels of hydrogen peroxide, and downregulating antioxidant enzyme activity, but the levels of lipid peroxidation, glycerol, and β-carotene remained nearly unchanged. These results suggest that Arg treatment alleviates salinity-induced oxidative stress in D. salina cells by modifying carbon partitioning and inducing signaling molecules rather than antioxidant enzymes.

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Data Availability

Data sharing is not applicable to this article as no datasets were generated or analyzed during the current study.

No conflicts, informed consent, human or animal rights are applicable to this study.

References

  1. Afify AEMMR, El-Beltagi HS, Abd El-Salam SM, Omran AA (2012) Protein solubility, digestibility and fractionation after germination of sorghum varieties. PLoS ONE 7(2):31154

    Article  CAS  Google Scholar 

  2. Ahmed AMA, El-Gohary AE, Osman SA, Khalid KA (2020) Arginine and salinity stress affect morphology and metabolism of Indian borage (Plectranthus amboinicus lour.). Acta Ecol Sin 40:417–424

    Article  Google Scholar 

  3. Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24:1337–1344

    Article  CAS  Google Scholar 

  4. Alisofi S, Einali A, Sangtarash MH (2020) Jasmonic acid-induced metabolic responses in bitter melon (Momordica charantia) seedlings under salt stress. J Hortic Sci Biotechnol 95:247–259

    Article  CAS  Google Scholar 

  5. Arnon D (1949) Copper enzymes in isolated chloroplasts: polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Avron M, Ben-Amotz A (1992) Dunaliella: physiology, biochemistry and biotechnology. CRC Press, Boca Raton

    Google Scholar 

  7. Azevedo Neto AD, Prisco JT, Eneas-Filho J, de Abrau CEB, Gomez-Filho E (2006) Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt sensitive maize genotypes. Environ Exp Bot 56:87–94

    Article  CAS  Google Scholar 

  8. Bahador E, Einali A, Azizian-Shermeh O, Sangtarash MH (2019) Metabolic responses of the green microalga Dunaliella salina to silver nanoparticles-induced oxidative stress in the presence of salicylic acid treatment. Aquat Toxicol 217:105356

  9. Behera B, Das AB, Mohanty P (2009) Changes of soluble proteins in leaf and thylakoid exposed in high saline condition of a mangrove taxa Bruguiera gymnorrhiza. Physiol Mol Biol Plants 15:53–59

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Ben-Amotz A, Avron M (1973) The role of glycerol in the osmotic regulation of the halophilic alga Dunaliella parva. Plant Physiol 51:875–878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Ben-Amotz A, Avron M (1983) On the factors which determine massive β-carotene accumulation in the halo-tolerant alga Dunaliella bardawil. Plant Physiol 72:593–597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Ben-Amotz A, Katz A, Avron M (1982) Accumulation of β-carotene in halotolerant algae: purification and characterization of β-carotene rich globules from Dunaliella bardawil (Chlorophyceae). J Phycol 18:529–537

    Article  CAS  Google Scholar 

  13. Bennoun P (2001) Chlororespiration and the process of carotenoid biosynthesis. Biochim Biophys Acta 1506:133–142

    Article  CAS  PubMed  Google Scholar 

  14. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  CAS  PubMed  Google Scholar 

  15. Bor M, Ozdemir F, Turkan I (2003) The effect of salt stress on lipid peroxidation and antioxidants in leaves of sugar beet (Beta vulgaris L.) and wild beet (Beta maritime L.) Plant Sci 164:77–84

  16. Borowitzka MA (2013) Dunaliella: biology, production, and markets. In: Richmond A, Hu Q (eds) Handbook of microalgal culture. John Wiley & Sons, Ltd, pp 359–368

  17. Borsani O, Valpuesta V, Botella MA (2001) Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol 126:1024–1030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Bradford M (1976) A rapid and sensitive method for the quantitation of microgramquantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  19. Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560

    Article  CAS  PubMed  Google Scholar 

  20. Chen G, Asada K (1992) Inactivation of ascorbate peroxidase by thoils requires hydrogen peroxide. Plant Cell Physiol 33:117–123

    CAS  Google Scholar 

  21. Chen H, Jiang JG, Wu GH (2009) Effect of salinity changes on the growth of Dunaliella salina and its isozyme activates of glycerol-3-phosphate dehydrogenase. J Agr Food Chem 57:6178–6182

    Article  CAS  Google Scholar 

  22. Chung YC, Chen SJ, Hsu CK, Chang CT, Chou ST (2005) Studies on the antioxidative activity of Graptopetalum paraguayense E. Walther Food Chem 91:419–424

    Article  CAS  Google Scholar 

  23. Cowan AK, Rose PD, Horne LG (1992) Dunaliella salina—a model system for studying the response of plant cells to stress. J Exp Bot 43:1535–1547

    Article  CAS  Google Scholar 

  24. Das U, Hariprasad G, Ethayathulla AS, Manral P, Das TK, Pasha S, et al. (2007) Inhibition of protein aggregation: supramolecular assemblies of arginine hold the key. PLoS One 2:e1176

  25. Dean RT, Fu S, Stocker R, Davies MJ (1997) Biochemistry and pathology of radical-mediated protein oxidation. Biochem J 324:1–18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Debska K, Krasuska U, Budnicka K, Bogatek R, Gniazdowska A (2013) Dormancy removal of apple seeds by cold stratification is associated with fluctuation in H2O2, NO production and protein carbonylation level. J Plant Physiol 170:480–488

    Article  CAS  PubMed  Google Scholar 

  27. Ebert S, Gibis M, Terjung N, Weiss J (2020) Survey of aqueous solubility, appearance, and pH of plant protein powders from carbohydrate and vegetable oil production. LWT 133:110078

  28. Einali A (2018) The induction of salt stress tolerance by propyl gallate treatment in green microalga Dunaliella bardawil, through enhancing ascorbate pool and antioxidant enzymes activity. Protoplasma 255:601–611

    Article  CAS  PubMed  Google Scholar 

  29. Einali A, Azizian-Shermeh O, Ghasemi A (2018) Phytochemical screening and antimicrobial activities of Periploca aphylla Decne, Persian walnut (Juglans regia L.) and oleander (Nerium indicum mill.) leaf extracts. J Food Meas Charact 12:1350–1359

    Article  Google Scholar 

  30. Einali A, Valizadeh J (2017) Storage reserve mobilization, gluconeogenesis, and oxidative pattern in dormant pistachio (Pistacia vera L.) seeds during cold stratification. Trees 31:659–671

    Article  CAS  Google Scholar 

  31. Einali A, Valizadeh J (2015) Propyl gallate promotes salt stress tolerance in green microalga Dunaliella salina by reducing free radical oxidants and enhancing b-carotene production. Acta Physiol Plant 37:83

    Article  CAS  Google Scholar 

  32. Fanciullino AL, Bidel LPR, Urban L (2014) Carotenoid responses to environmental stimuli: integrating redox and carbon controls into a fruit model. Plant Cell Environ 37:273–289

    Article  CAS  PubMed  Google Scholar 

  33. Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55:307–319

    Article  CAS  PubMed  Google Scholar 

  34. Foyer CH, Noctor G (2003) Redox sensing and signaling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119:355–364

    Article  CAS  Google Scholar 

  35. Fukuchi S, Yoshimune K, Wakayama M, Moriguchi M, Nishikawa K (2003) Unique amino acid composition of proteins in halophilic bacteria. J Mol Biol 327:347–357

    Article  CAS  PubMed  Google Scholar 

  36. Galvan-Ampudia CS, Testerink C (2011) Salt stress signals shape the plant root. Curr Opin Plant Biol 14:296–302

    Article  CAS  PubMed  Google Scholar 

  37. Gapinska M, Skiodowska M, Gabara B (2008) Effect of short and long term salinity on the activities of antioxidative enzymes and lipid peroxidation in tomato roots. Acta Physiol Plant 30:11–18

    Article  CAS  Google Scholar 

  38. Garcia F, Freile-Pelegrin Y, Robledo D (2007) Physiological characterization of Dunaliella sp. (Chlorophyta, Volvocales) from Yucatan. Mexico Bioresour Technol 98:1359–1365

    Article  CAS  PubMed  Google Scholar 

  39. Garcia-Gomez C, Parages ML, Jimenez C, Palma A, Mata MT, Segovia M (2012) Cell survival after UV radiation stress in the unicellular chlorophyte Dunaliella tertiolecta is mediated by DNA repair and MAPK phosphorylation. J Exp Bot 63:5259–5274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  41. Gong B, Wen D, Bloszies S, Li X, Wei M, Yang F, Shi Q, Wang X (2014) Comparative effects of NaCl and NaHCO3 stresses on respiratory metabolism, antioxidant system, nutritional status, and organic acid metabolism in tomato roots. Acta Physiol Plant 36:2167–2181

    Article  CAS  Google Scholar 

  42. Gould KS, Markham KR, Smith RH, Goris JJ (2000) Functional role of anthocyanins in the leaves of Quintinia serrata A. Cunn J Exp Bot 51:1107–1115

    Article  CAS  PubMed  Google Scholar 

  43. Goyal A (2007) Osmoregulation in Dunaliella, part II: photosynthesis and starch contribute carbon for glycerol synthesis during a salt stress in Dunaliella tertiolecta. Plant Physiol Biochem 45:705–710

    Article  CAS  PubMed  Google Scholar 

  44. Haghjou MM, Colville L, Smirnoff N (2014) The induction of menadione stress tolerance in the marine microalga, Dunaliella viridis, through cold pretreatment and modulation of the ascorbate and glutathione pools. Plant Physiol Biochem 84:96–104

    Article  CAS  Google Scholar 

  45. Haghjou MM, Shariati M, Smirnoff N (2009) The effect of acute high light and low temperature stresses on the ascorbate-glutathione cycle and superoxide dismutase activity in two Dunaliella salina strains. Physiol Plant 135:272–280

    Article  CAS  PubMed  Google Scholar 

  46. Handel EV (1968) Direct micro determination of sucrose. Anal Biochem 22:280–283

    Article  PubMed  Google Scholar 

  47. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  CAS  PubMed  Google Scholar 

  48. Hildebrandt TM (2018) Synthesis versus degradation: directions of amino acid metabolism during Arabidopsis abiotic stress response. Plant Mol Biol 98:121–135

    Article  CAS  PubMed  Google Scholar 

  49. Hildebrandt TM, Nunes Nesi A, Araujo WL, Braun H (2015) Amino acid catabolism in plants. Mol Plant 8:1563–1579

    Article  CAS  PubMed  Google Scholar 

  50. Huang T, Jander G (2017) Abscisic acid-regulated protein degradation causes osmotic stress-induced accumulation of branched chain amino acids in Arabidopsis thaliana. Planta 246:737–747

    Article  CAS  PubMed  Google Scholar 

  51. Jahnke LS, White AL (2003) Long-term hyposaline and hypersaline stresses produce distinct antioxidant responses in the marine alga Dunaliella tertiolecta. J Plant Physiol 160:1193–1202

    Article  CAS  PubMed  Google Scholar 

  52. Jeong JC, Lee IY, Kim SW, Park YH (1999) Stimulation of β-carotene synthesis by hydrogen peroxide in Blakeslea trispora. Biotech Lett 21:683–686

    Article  CAS  Google Scholar 

  53. Jimenez C, Pick U (1993) Differential reactivity of β-carotene isomers from Dunaliella bardawil toward oxygen radicals. Plant Physiol 101:385–390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Kakkar RK, Bhaduri S, Rai VK, Kumar S (2000) Amelioration of NaCl stress by arginine in rice seedlings: changes in endogenous polyamines. Biol Plantarum 43:419–422

    Article  CAS  Google Scholar 

  55. Kaplan A, Schreiber U, Avron M (1980) Salt-induced metabolic changes in Dunaliella salina. Plant Physiol 65:810–813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. 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

    Article  CAS  PubMed  Google Scholar 

  57. Kobayashi M, Kakizono T, Nagai S (1993) Enhanced carotenoid biosynthesis by oxidative stress in acetate-induced cyst cells of a green unicellular alga, Haematococcus pluvialis. Appl Environ Microbiol 59:867–873

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, Ahn BW, Shaltiel S, Stadtman ER (1990) Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 186:464–478

    Article  CAS  PubMed  Google Scholar 

  59. Levine RL, Williams JA, Stadtman ER, Shacker E (1994) Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 233:346–357

    Article  CAS  PubMed  Google Scholar 

  60. Liska AJ, Shevchenko A, Pick U, Katz A (2004) Enhanced photosynthesis and redox energy production contribute to salinity tolerance in Dunaliella as revealed by homology-based proteomics. Plant Physiol 136:2806–2817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Liu JH, Nada K, Honda C, Kitashiba H, Wen XP, Pang XM, Moriguchi T (2006) Polyamine biosynthesis of apple callus under salt stress: importance of the arginine decarboxylase pathway in stress response. J Exp Bot 57:2589–2599

    Article  CAS  PubMed  Google Scholar 

  62. Liu YS, Wu JY (2006) Hydrogen peroxide-induced astaxanthin biosynthesis and catalase activity in X. dendrorhous. Appl Microbiol Biotechnol 73:663–668

    Article  CAS  PubMed  Google Scholar 

  63. Luck H (1965) Catalase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Verlage Chemie, Weinheim, pp 885–894

    Chapter  Google Scholar 

  64. Ma J, Zhu X, Shi L, Ni C, Hou J, Cheng J (2019) Enhancement of soluble protein, polypeptide production and functional properties of heat-denatured soybean meal by fermentation of Monascus purpureus 04093. CYTA J Food 17:1014–1022

    Article  CAS  Google Scholar 

  65. Majumdar R, Barchi B, Turlapati SA, Gagne M, Minocha R, Long S, Minocha SC (2016) Glutamate, ornithine, arginine, proline, and polyamine metabolic interactions: the pathway is regulated at the post-transcriptional level. Front Plant Sci 7:78

    Article  PubMed  PubMed Central  Google Scholar 

  66. Markwell MAK, Hass SM, Tolbert NE, Bieber LL (1981) Protein determination in membrane and lipoprotein samples: manual and automated procedures. Meth Enzymol 72:296–303

    Article  CAS  Google Scholar 

  67. McCready RM, Guggolz J, Silviera V, Owens HS (1950) Determination of starch and amylose in vegetables. Anal Chem 22:1156–1158

    Article  CAS  Google Scholar 

  68. Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugars. Anal Chem 31:426–428

    Article  CAS  Google Scholar 

  69. Mirshekari M, Einali A, Valizadeh J (2019) Metabolic changes and activity pattern of antioxidant enzymes induced by salicylic acid treatment in green microalga Dunaliella salina under nitrogen deficiency. J Appl Phycol 31:1709–1719

    Article  CAS  Google Scholar 

  70. Mishra A, Jha B (2011) Antioxidant response of the microalga Dunaliella salina under salt stress. Bot Mar 54:195–199

  71. Mishra A, Mandoli A, Jha B (2008) Physiological characterization and stress-induced metabolic responses of Dunaliella salina isolated from salt pan. J Ind Microbiol Biotechnol 35:1093–1101

    Article  CAS  PubMed  Google Scholar 

  72. Moller IM, Jensen PE, Hansson A (2007) Oxidative modification to cellular components in plants. Annu Rev Plant Biol 58:459–481

    Article  PubMed  CAS  Google Scholar 

  73. Munne-Bosch S, Penuelas J (2003) Photo- and antioxidative protection, and a role for salicylic acid during drought and recovery in field grown Phillyrea angustifolia plants. Planta 217:758–766

    Article  CAS  PubMed  Google Scholar 

  74. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 9:651–681

    Article  CAS  Google Scholar 

  75. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  76. Naliwajski M, Sklodowska M (2021) The relationship between the antioxidant system and proline metabolism in the leaves of cucumber plants acclimated to salt stress. Cells 10:609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Nasibi F, Heidari T, Asrar Z, Mansoori H (2013) Effect of arginine pre-treatment on nickel accumulation and alleviation of the oxidative stress in Hyoscyamus niger. J Soil Sci Plant Nutr 13:680–689

    Google Scholar 

  78. Nasibi F, Yaghoobi MM, Manouchehri Kalantari Kh (2011) Effect of exogenous arginine on alleviation of oxidative damage in tomato plant under water stress. J Plant Interact 6:291–296

    Article  CAS  Google Scholar 

  79. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    Article  CAS  PubMed  Google Scholar 

  80. Ozturk ZN, Talame V, Deyholos M, Michalowski CB, Galbraith DW, Gozukirmizi N, Tuberosa R, Bohnert HJ (2002) Monitoring large scale changes in transcript abundance in drought- and salt-stressed barley. Plant Mol Biol 48:551–573

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  82. Pena LB, Pausini LA, Tomaro ML, Gallego SM (2006) Proteolytic system in sunflower (Helianthus annuus L.) leaves under cadmium stress. Plant Sci 171:531–537

    Article  CAS  PubMed  Google Scholar 

  83. Peoples MB, Dalling MJ (1978) Degradation of ribulose 1,5-bisphosphate carboxylase by proteolytic enzymes from crude extracts of wheat leaves. Planta 138:153–160

    Article  CAS  PubMed  Google Scholar 

  84. Ramadan AA, Abd Elhamid EM, Sadak MS (2019) Comparative study for the effect of arginine and sodium nitroprusside on sunflower plants grown under salinity stress conditions. Bull Natl Res Cent 43:118

    Article  Google Scholar 

  85. Sairam RK, Tyagi A (2004) Physiology and molecular biology of salinity stress tolerance in plants. Curr Sci 86:407–421

    CAS  Google Scholar 

  86. Salguero A, de la Morena B, Vigara J, Vega JM, Vilchez C, Leon R (2003) Carotenoids as protective response against oxidative damage in Dunaliella bardawil. Biomol Eng 20:249–253

    Article  CAS  PubMed  Google Scholar 

  87. Schoen M (1988) Cell counting. In: Lobban C, Champan D, Kermer BP (eds) Experimental phycology. Cambridge University Press, Cambridge

  88. Shaish A, Avron M, Pick U, Benamotz A (1993) Are active oxygen species involved in induction of β-carotene in Dunaliella bardawil. Planta 190:363–368

    Article  CAS  Google Scholar 

  89. Sharma P, Bhatt D, Zaidi MG, Saradhi PP, Khanna PK, Arora S (2012) Silver nanoparticle-mediated enhancement in growth and antioxidant status of Brassica juncea. Appl Biochem Biotechnol 167:2225–2233

    Article  CAS  PubMed  Google Scholar 

  90. Shu P, Min D, Ai W, Li J, Zhou J, Li Z, Zhang X, Shi Z, Sun Y, Jiang Y, Li F, Li X, Guo Y (2020) L-Arginine treatment attenuates postharvest decay and maintains quality of strawberry fruit by promoting nitric oxide synthase pathway. Postharvest Biol Technol 168:111253

  91. Stoop JMH, Pharr DM (1994) Growth substrate and nutrient salt environment after mannitol to hexose partitioning in celery petioles. J Am Soc Hortic Sci 119:237–242

    Article  CAS  Google Scholar 

  92. TakagiKarseno M, Yoshida T (2006) Effect of salt concentration on intracellular accumulation of lipids and triacylglyceride in marine microalgae Dunaliella cells. J Biosci Bioeng 101:223–226

    Article  CAS  Google Scholar 

  93. Tawfik MM, Badr EA, Ibrahim OM, Abd Elhamid EM, Sadak MS (2017) Biomass and some physiological aspects of Spartina patens grown under salt affected environment in South Sinai, inter. J Agric Res 12(1):17–26

    Google Scholar 

  94. Tian JY, Yu J (2009) Changes in ultrastructure and responses of antioxidant systems of algae (Dunaliella salina) during acclimation to enhanced ultraviolet-B radiation. J Photochem Photobiol B Biol 97:152–160

    Article  CAS  Google Scholar 

  95. Trevino SR, Scholtz JM, Pace CN (2007) Amino acid contribution to protein solubility: Asp, Glu, and Ser contribute more favorably than the other hydrophilic amino acids in RNase Sa. J Mol Biol 366:449–460

    Article  CAS  PubMed  Google Scholar 

  96. Trivellini A, Gordillo B, Rodríguez-Pulido FJ, Borghesi E, Ferrante A, Vernieri P, Quijada-Morin N, González-Miret ML, Heredia FJ (2014) Effect of salt stress in the regulation of anthocyanins and color of hibiscus flowers by digital image analysis. J Agri Food Chem 62:6966–6974

    Article  CAS  Google Scholar 

  97. Vanita J, Werner K, Huber SC (2008) Cytokinin inhibits the proteasome-mediated degradation of carbonylated proteins in Arabidopsis leaves. Plant Cell Physiol 49:843–852

    Article  CAS  Google Scholar 

  98. Walia H, Wilson C, Condamine P, Liu X, Ismail AM, Close TJ (2007) Large-scale expression profiling and physiological characterization of jasmonic acid-mediated adaptation of barley to salinity stress. Plant Cell Environ 30:410–421

    Article  CAS  PubMed  Google Scholar 

  99. Winter G, Todd CD, Trovato M, Forlani G, Funck D (2015) Physiological implications of arginine metabolism in plants. Front Plant Sci 6:534

    Article  PubMed  PubMed Central  Google Scholar 

  100. Wu G, Morris SM (1998) Arginine metabolism: nitric oxide and beyond. Biochem J 336:1–17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Xia BB, Wang SH, Duan JB, Bai LH (2014) The relationship of glycerol and glycolysis metabolism pathway under hyperosmotic stress in Dunaliella salina. Cent Eur J Biol 9:901–908

    CAS  Google Scholar 

  102. Xu Y, Harvey PJ (2019) Carotenoid production by Dunaliella salina under red light. Antioxidants 8:123

    Article  CAS  PubMed Central  Google Scholar 

  103. Yang M, Sun F, Wang S, Qi W, Wang Q, Dong X, Yang J, Luo X (2013) Down-regulation of OsPDCD5, a homolog of the mammalian PDCD5, increases rice tolerance to salt stress. Mol Breed 31:333–346

    Article  CAS  Google Scholar 

  104. Yemm EW, Cocking EC (1955) The determination of amino acids with Ninhydrin. Analyst 80:209–213

    Article  CAS  Google Scholar 

  105. Yilancioglu K, Cokol M, Pastirmaci I, Erman B, Cetiner S (2014) Oxidative stress is a mediator for increased lipid accumulation in a newly isolated Dunaliella salina strain. PLoS One 9:e91957

  106. Zeid IM (2009) Effect of arginine and urea on polyamines content and growth of bean under salinity stress. Acta Physiol Plant 31:65–70

    Article  CAS  Google Scholar 

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Acknowledgements

We thank the USB Deputy of Research for monetary contributions in the form of a grant to Z.B. for the M.Sc. research project.

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This work was supported by the University of Sistan and Baluchestan.

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Zahra Bamary: Laboratory investigation. Alireza Einali: Supervision, conceptualization, writing—original draft preparation, funding acquisition, experimental design, data curation, formal analysis, project administration, writing—reviewing and editing. All authors have read and approved the submitted manuscript.

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Correspondence to Alireza Einali.

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Bamary, Z., Einali, A. Changes in Carbon Partitioning and Pattern of Antioxidant Enzyme Activity Induced by Arginine Treatment in the Green Microalga Dunaliella salina Under Long-Term Salinity. Microb Ecol 84, 198–212 (2022). https://doi.org/10.1007/s00248-021-01843-3

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