Advertisement

Physiology and Molecular Biology of Plants

, Volume 24, Issue 6, pp 1017–1033 | Cite as

Effect of salinity on osmotic adjustment, proline accumulation and possible role of ornithine-δ-aminotransferase in proline biosynthesis in Cakile maritima

  • Dorsaf Hmidi
  • Chedly Abdelly
  • Habib-ur-Rehman AtharEmail author
  • Muhammad Ashraf
  • Dorsaf MessediEmail author
Research Article

Abstract

The short time response to salt stress was studied in Cakile maritima. Plants were exposed to different salt concentrations (0, 100, 200 and 400 mM NaCl) and harvested after 4, 24, 72 and 168 h of treatment. Before harvesting plants, tissue hydration, osmotic potential, inorganic and organic solute contents, and ornithine-δ-aminotransferase activity were measured. Plants of C. maritima maintained turgor and tissue hydration at low osmotic potential mainly at 400 mM NaCl. The results showed that, in leaves and stems, Na+ content increased significantly after the first 4 h of treatment. However, in roots, the increase of Na+ content remained relatively unchanged with increasing salt. The K+ content decreased sharply at 200 and 400 mM NaCl with treatment duration. This decrease was more pronounced in roots. The content of proline and amino acids increased with increasing salinity and treatment duration. These results indicated that the accumulation of inorganic and organic compounds was a central adaptive mechanism by which C. maritima maintained intracellular ionic balance under saline conditions. However, their percentage contribution to total osmotic adjustment varies from organ to organ; for example, Na+ accumulation mainly contributes in osmotic adjustment of stem tissue (60%). Proline contribution to osmotic adjustment reached 36% in roots. In all organs, proline as well as δ-OAT activity increased with salt concentration and treatment duration. Under normal growth conditions, δ-OAT is mainly involved in the mobilization of nitrogen required for plant growth. However, the highly significant positive correlation between proline and δ-OAT activity under salt-stress conditions suggests that ornithine pathway contributed to proline synthesis.

Keywords

Halophyte Organic solutes Osmoregulation δ-OAT activity Salt stress 

Notes

Acknowledgements

This work was supported by the Tunisian Ministry of Higher Education and Scientific Research (LR15CBBC02).

Author’s contribution

DH: PhD Scholar conducted the experiment; CA: Professor, Design the experiment and finalize the manuscript; HA: Professor, editing and finalizing manuscript, submission to the Journal on behalf of Drosaf Messedi, handle the manuscript and will responsible for submission of responses to any query; MA: Professor, Editing and finalizing the manuscript; DM: Assistant Professor, conceive and design the experiment, writing the manuscript, the person who won the research grant for this project, corresponding author.

References

  1. AbdElgawad H, De Vos D, Zinta G, Domagalska MA, Beemster GTS, Asard H (2015) Grassland species differentially regulate proline concentrations under future climate conditions: an integrated biochemical and modelling approach. New Phytol 208:354–369CrossRefGoogle Scholar
  2. Adams E, Frank L (1980) Metabolism of proline and the hydroxyprolines. Annu Rev Biochem 49:1005–1061CrossRefGoogle Scholar
  3. Albacete A, Ghanem ME, Martínez-Andújar C, Acosta M, Sánchez-Bravo J, Martínez V, Lutts S, Dodd IC, Pérez-Alfocea F (2008) Hormonal changes in relation to biomass partitioning and shoot growth impairment in salinized tomato (Solanum lycopersicum L.) plants. J Exp Bot 59:4119–4131CrossRefGoogle Scholar
  4. Amtmann A (2009) Learning from evolution: Thellungiella generates new knowledge on essential and critical components of abiotic stress tolerance in plants. Mol Plant 2:3–12CrossRefGoogle Scholar
  5. Armengaud P, Thiery L, Buhot N, Grenier-de March G, Savoure A (2004) Transcriptional regulation of proline biosynthesis in Medicago truncatula reveals developmental and environmental specific features. Physiol Plant 120:442–450CrossRefGoogle Scholar
  6. Ashraf M (2004) Some important physiological selection criteria for salt tolerance in plants. Flora Morphol Distrib Funct Ecol Plants 199:361–376CrossRefGoogle Scholar
  7. Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216CrossRefGoogle Scholar
  8. Ashraf M, Harris PJC (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166:3–16CrossRefGoogle Scholar
  9. Ashraf M, Athar HR, Harris PJC, Kwon TR (2008) Some prospective strategies for improving crop salt tolerance. Adv Agron 97:45–110CrossRefGoogle Scholar
  10. Athar H-u-R, Zafar ZU, Ashraf M (2015) Glycinebetaine improved photosynthesis in canola under salt stress: evaluation of chlorophyll fluorescence parameters as potential indicators. J Agron Crop Sci 201:428–442CrossRefGoogle Scholar
  11. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207CrossRefGoogle Scholar
  12. Belkheiri O, Mulas M (2013) The effects of salt stress on growth, water relations and ion accumulation in two halophyte Atriplex species. Environ Exp Bot 86:17–28CrossRefGoogle Scholar
  13. Bressan RA, Zhang CQ, Zhang H, Hasegawa PM, Bohnert HJ, Zhu JK (2001) Learning from the Arabidopsis experience. The next gene search paradigm. Plant Physiol 127:1354–1360CrossRefGoogle Scholar
  14. da Rocha IM, Vitorello VA, Silva JS, Ferreira-Silva SL, Viegas RA, Silva EN, Silveira JA (2012) Exogenous ornithine is an effective precursor and the delta-ornithine amino transferase pathway contributes to proline accumulation under high N recycling in salt-stressed cashew leaves. J Plant Physiol 169:41–49CrossRefGoogle Scholar
  15. Debez A, Saadaoui D, Ramani B, Ouerghi Z, Koyro H-W, Huchzermeyer B, Abdelly C (2006a) Leaf H+-ATPase activity and photosynthetic capacity of Cakile maritima under increasing salinity. Environ Exp Bot 57:285–295CrossRefGoogle Scholar
  16. Debez A, Taamalli W, Saadaoui D, Ouerghi Z, Zarrouk M, Huchzermeyer B, Abdelly C (2006b) Salt effect on growth, photosynthesis, seed yield and oil composition of the potential crop halophyte Cakile maritima. In: Öztürk M, Waisel Y, Khan MA, Görk G (eds) Biosaline agriculture and salinity tolerance in plants. Birkhäuser, Basel, pp 55–63CrossRefGoogle Scholar
  17. Debez A, Saadaoui D, Slama I, Huchzermeyer B, Abdelly C (2010) Responses of Batis maritima plants challenged with up to two-fold seawater NaCl salinity. J Plant Nutr Soil Sci/Zeitschrift für Pflanzenernährung und Bodenkunde 173:291CrossRefGoogle Scholar
  18. Delauney AJ, Hu CA, Kishor PB, Verma DP (1993) Cloning of ornithine delta-aminotransferase cDNA from Vigna aconitifolia by trans-complementation in Escherichia coli and regulation of proline biosynthesis. J Biol Chem 268:18673–18678PubMedGoogle Scholar
  19. Demiral T, Turkan I (2005) Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance. Environ Exp Bot 53:247–257CrossRefGoogle Scholar
  20. Funck D, Stadelhofer B, Koch W (2008) Ornithine-δ-aminotransferase is essential for arginine catabolism but not for proline biosynthesis. BMC Plant Biol 8:40CrossRefGoogle Scholar
  21. Gagneul D, Aïnouche A, Duhazé C, Lugan R, Larher FR, Bouchereau A (2007) A reassessment of the function of the so-called compatible solutes in the halophytic plumbaginaceae Limonium latifolium. Plant Physiol 144:1598–1611CrossRefGoogle Scholar
  22. Glenn E, Brown J (1998) Effects of soil salt levels on the growth and water use efficiency of Atriplex canescens (Chenopodiaceae) varieties in drying soil. Am J Bot 85:10CrossRefGoogle Scholar
  23. Harrouni MC, Daoud S, Koyro H-W (2003) Effect of seawater irrigation on biomass production and ion composition of seven halophytic species in Morocco. In: Lieth H, Mochtchenko M (eds) Cash crop halophytes: recent studies: 10 years after Al Ain Meeting. Springer, Dordrecht, pp 59–70CrossRefGoogle Scholar
  24. Hewitt EJ (1966) Sand and water culture methods used in the study of plant nutrition, 2nd edn. Commonwealth Agricultural Bureaux, Farnham RoyalGoogle Scholar
  25. Inan G, Zhang Q, Li P, Wang Z, Cao Z, Zhang H, Zhang C, Quist TM, Goodwin SM, Zhu J, Shi H, Damsz B, Charbaji T, Gong Q, Ma S, Fredricksen M, Galbraith DW, Jenks MA, Rhodes D, Hasegawa PM, Bohnert HJ, Joly RJ, Bressan RA, Zhu JK (2004) Salt cress. A halophyte and cryophyte Arabidopsis relative model system and its applicability to molecular genetic analyses of growth and development of extremophiles. Plant Physiol 135:1718–1737CrossRefGoogle Scholar
  26. Kim HR, Rho HW, Park JW, Park BH, Kim JS, Lee MW (1994) Assay of ornithine aminotransferase with ninhydrin. Anal Biochem 223:205–207CrossRefGoogle Scholar
  27. Kishor PK, Sangam S, Amrutha R, Laxmi PS, Naidu K, Rao K, Rao S, Reddy K, Theriappan P, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr Sci 88:424–438Google Scholar
  28. Krell A, Funck D, Plettner I, John U, Dieckmann G (2007) Regulation of proline metabolism under salt stress in the psychrophilic diatom Fragilariopsis Cylindrus (Bacillariophyceae). J Phycol 43(4):753–762CrossRefGoogle Scholar
  29. Lee G, Carrow RN, Duncan RR, Eiteman MA, Rieger MW (2008) Synthesis of organic osmolytes and salt tolerance mechanisms in Paspalum vaginatum. Environ Exp Bot 63:19–27CrossRefGoogle Scholar
  30. Lehmann S, Gumy C, Blatter E, Boeffel S, Fricke W, Rentsch D (2011) In planta function of compatible solute transporters of the AtProT family. J Exp Bot 62:787–796CrossRefGoogle Scholar
  31. Li Z, Peng D, Zhang X, Peng Y, Chen M, Ma X, Huang L, Yan Y (2017) Na+ induces the tolerance to water stress in white clover associated with osmotic adjustment and aquaporins-mediated water transport and balance in root and leaf. Environ Exp Bot 144:11–24CrossRefGoogle Scholar
  32. Lohaus G, Hussmann M, Pennewiss K, Schneider H, Zhu JJ, Sattelmacher B (2000) Solute balance of a maize (Zea mays L.) source leaf as affected by salt treatment with special emphasis on phloem retranslocation and ion leaching. J Exp Bot 51:1721–1732CrossRefGoogle Scholar
  33. Maggio A, Miyazaki S, Veronese P, Fujita T, Ibeas JI, Damsz B, Narasimhan ML, Hasegawa PM, Joly RJ, Bressan RA (2002) Does proline accumulation play an active role in stress-induced growth reduction? Plant J 31:699–712CrossRefGoogle Scholar
  34. Maggio A, Raimondi G, Martino A, De Pascale S (2007) Salt stress response in tomato beyond the salinity tolerance threshold. Environ Exp Bot 59:276–282CrossRefGoogle Scholar
  35. Mansour MMF, Ali EF (2017) Evaluation of proline functions in saline conditions. Phytochemistry 140:52–68CrossRefGoogle Scholar
  36. Martinez JP, Lutts S, Schanck A, Bajji M, Kinet JM (2004) Is osmotic adjustment required for water stress resistance in the Mediterranean shrub Atriplex halimus L? J Plant Physiol 161:1041–1051CrossRefGoogle Scholar
  37. Messedi D, Slama I, Laabidi N, Ghnaya T, Savoure A, Soltani A, Abdelly C (2006) Effect of nitrogen deficiency, salinity and drought on proline metabolism in Sesuvium portulacastrum. In: Öztürk M, Waisel Y, Khan MA, Görk G (eds) Biosaline agriculture and salinity tolerance in plants. Birkhäuser, Basel, pp 65–72CrossRefGoogle Scholar
  38. Messedi D, Farhani F, Hamed KB, Trabelsi N, Ksouri R, Athar H-u-R, Abdelly C (2016) Highlighting the mechanisms by which proline can confer tolerance to salt stress in Cakile maritima. Pak J Bot 48:417–427Google Scholar
  39. Molinari HBC, Marur CJ, Daros E, de Campos MKF, de Carvalho J, Bespalhok JC, 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 Plant 130:218–229CrossRefGoogle Scholar
  40. Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167:645–663CrossRefGoogle Scholar
  41. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681CrossRefGoogle Scholar
  42. Nguyen HT, Meir P, Sack L, Evans JR, Oliveira RS, Ball MC (2017) Leaf water storage increases with salinity and aridity in the mangrove Avicennia marina: integration of leaf structure, osmotic adjustment and access to multiple water sources. Plant Cell Environ 40:1576–1591CrossRefGoogle Scholar
  43. Olías R, Eljakaoui Z, Li J, de Morales PA, Marin-Manzano MC, Pardo JM, Belver A (2009) The plasma membrane Na+/H+ antiporter SOS1 is essential for salt tolerance in tomato and affects the partitioning of Na+ between plant organs. Plant Cell Environ 32:904–916CrossRefGoogle Scholar
  44. Rayapati PJ, Stewart CR (1991) Solubilization of a proline dehydrogenase from maize (Zea mays L.) mitochondria. Plant Physiol 95:787–791CrossRefGoogle Scholar
  45. Rodrigues CRF, Silva EN, da Mata Moura R, dos Anjos DC, Hernandez FFF, Viégas RA (2014) Physiological adjustment to salt stress in R. communis seedlings is associated with a probable mechanism of osmotic adjustment and a reduction in water lost by transpiration. Ind Crops Prod 54:233–239CrossRefGoogle Scholar
  46. Roosens NHCJ, Thu TT, Iskandar HM, Jacobs M (1998) Isolation of the ornithine-δ-aminotransferase cDNA and effect of salt stress on its expression in Arabidopsis thaliana. Plant Physiol 117:263–271CrossRefGoogle Scholar
  47. Roosens NH, Al Bitar F, Loenders K, Angenon G, Jacobs M (2002) Overexpression of ornithine-delta-aminotransferase increases proline biosynthesis and confers osmotolerance in transgenic plants. Mol Breed 9:73–80CrossRefGoogle Scholar
  48. Ruiz JM, Sánchez E, García PC, López-Lefebre LR, Rivero RM, Romero L (2002) Proline metabolism and NAD kinase activity in greenbean plants subjected to cold-shock. Phytochemistry 59:473–478CrossRefGoogle Scholar
  49. Sanchez E, Lopez-Lefebre LR, Garcia PC, Rivero RM, Ruiz JM, Romero L (2001) Proline metabolism in response to highest nitrogen dosages in green bean plants (Phaseolus vulgaris L. cv. Strike). J Plant Physiol 158:593–598CrossRefGoogle Scholar
  50. Silveira JAG, Araújo SAM, Lima JPMS, Viégas RA (2009) Roots and leaves display contrasting osmotic adjustment mechanisms in response to NaCl-salinity in Atriplex nummularia. Environ Exp Bot 66:1–8CrossRefGoogle Scholar
  51. Slama I, Messedi D, Ghnaya T, Savoure A, Abdelly C (2006) Effects of water deficit on growth and proline metabolism in Sesuvium portulacastrum. Environ Exp Bot 56:231–238CrossRefGoogle Scholar
  52. Slama I, Ghnaya T, Savouré A, Abdelly C (2008) Combined effects of long-term salinity and soil drying on growth, water relations, nutrient status and proline accumulation of Sesuvium portulacastrum. C R Biol 331:442–451CrossRefGoogle Scholar
  53. Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97CrossRefGoogle Scholar
  54. Taffouo V, Kenne M, Fotsop OW, Sameza M, Ndomou M, Amougou A (2006) Salinity effects on growth, ionic distribution and water content in salt-tolerant species: Gossypium hirsutum (Malvaceae). J Cam Acad Sci 6:167–174Google Scholar
  55. Ueda A, Shi WM, Sanmiya K, Shono M, Takabe T (2001) Functional analysis of salt-inducible proline transporter of barley roots. Plant Cell Physiol 42:1282–1289CrossRefGoogle Scholar
  56. Ueda A, Shi W, Nakamura T, Takabe T (2002) Analysis of salt-inducible genes in barley roots by differential display. J Plant Res 115:0119–0130CrossRefGoogle Scholar
  57. Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35:753–759CrossRefGoogle Scholar
  58. Woodrow P, Ciarmiello LF, Annunziata MG, Pacifico S, Iannuzzi F, Mirto A, D’Amelia L, Dell’Aversana E, Piccolella S, Fuggi A, Carillo P (2017) Durum wheat seedling responses to simultaneous high light and salinity involve a fine reconfiguration of amino acids and carbohydrate metabolism. Physiol Plant 159:290–312CrossRefGoogle Scholar
  59. Wu Y, Wang Q, Ma Y, Chu C (2005) Isolation and expression analysis of salt up-regulated ESTs in upland rice using PCR-based subtractive suppression hybridization method. Plant Sci 168:847–853CrossRefGoogle Scholar
  60. Xue X, Liu A, Hua X (2009) Proline accumulation and transcriptional regulation of proline biothesynthesis and degradation in Brassica napus. BMB Rep 42:28–34CrossRefGoogle Scholar
  61. Yang Y, Zhang Y, Wei X, You J, Wang W, Lu J, Shi R (2011) Comparative antioxidative responses and proline metabolism in two wheat cultivars under short term lead stress. Ecotoxicol Environ Saf 74:733–740CrossRefGoogle Scholar
  62. Yao X, Horie T, Xue S, Leung H-Y, Katsuhara M, Brodsky DE, Wu Y, Schroeder JI (2010) Differential sodium and potassium transport selectivities of the rice OsHKT2; 1 and OsHKT2; 2 transporters in plant cells. Plant Physiol 152:341–355CrossRefGoogle Scholar
  63. Yemm EW, Cocking EC, Ricketts RE (1955) The determination of amino-acids with ninhydrin. Analyst 80:209–214CrossRefGoogle Scholar

Copyright information

© Prof. H.S. Srivastava Foundation for Science and Society 2018

Authors and Affiliations

  1. 1.Laboratoire des Plantes ExtrêmophilesCentre de Biotechnologie, Technopole de Borj CédriaHammam-LifTunisia
  2. 2.Institute of Pure and Applied BiologyBahauddin Zakariya UniversityMultanPakistan
  3. 3.Pakistan Science FoundationIslamabadPakistan

Personalised recommendations