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Alleviation of phosphorus deficiency stress by moderate salinity in the halophyte Hordeum maritimum L.

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Abstract

Hordeum maritimum (Poacea) is a facultative halophyte potentially useful for forage production in saline zones. Here, we assessed whether moderate NaCl-salinity can modify the plant response to phosphorus (P) shortage. Plants were cultivated for 55 days under low or sufficient P supply (5 or 60 μmol plant−1 week−1 KH2PO4, respectively), with or without 100 mM NaCl. When individually applied, salinity and P deficiency significantly restricted whole-plant growth, with a more marked effect of the latter stress. Plants subjected to P deficiency showed a significant increase in root growth (as length and dry weight) and root/shoot DW ratio. Enhanced root growth and elongation presumably correspond to the well-known root adaptive response to mineral deficiency. However, leaf relative water content, leaf P concentration, and leaf gas exchange parameters were significantly restricted. The interactive effects of salinity and P deficiency were not added one to another neither on whole plant biomass nor on plant nutrient uptake. Indeed, 100 mM NaCl-addition to P-deficient plants significantly restored the plant growth and improved CO2 assimilation rate, root growth, K+/Na+ ratio and leaf proline and soluble sugar concentrations. It also significantly enhanced leaf total antioxidant capacity and leaf anthocyanin concentration. This was associated with significantly lower leaf osmotic potential, leaf Na+ and malondialdehyde (MDA) concentration. Taken together, these results suggest that mild salinity may mitigate the adverse effects of phosphorus deficiency on H. maritimum by notably improving the plant photosynthetic activity, the osmotic adjustment capacity, the selective absorption of K+ over Na+ and antioxidant defence.

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References

  • Abdelly C, Lachaâl M, Grignon C, Soltani A, Hajji M (1995) Association épisodique d’halophytes strictes et de glycophytes dans un écosystème hydromorphe salé en zone semi-aride. Agronomie 15:557–568

    Article  Google Scholar 

  • Arnon DI, Hoagland DR (1940) Crop production in artificial solutions and in soil with special reference to factors affecting yields and absorption of inorganic nutrients. Soil Sci 50:463–484

    CAS  Google Scholar 

  • Attipali RR, Kolluru VC, Munusamy V (2004) Drought induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 161:1189–1202

    Article  Google Scholar 

  • Ayala-Silva T, Beyl CA (2005) Changes in spectral reflectance of wheat leaves in response to specific macronutrient deficiency. Adv Space Res 35:305–317

    Article  PubMed  CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Beer S, Shomer-ilan A, Waisel Y (1975) Salt-stimulated Phosphoenolpyruvate Carboxylase in Cakile maritime. Physiologia Plantarum 293–295

  • Blumwald E (2000) Sodium transport and salt tolerance in plants. Curr Opin Cell Biol 12:431–434

    Article  PubMed  CAS  Google Scholar 

  • Cha-Um S, Kirdmanee C (2009) Effect of salt stress on proline accumulation, photosynthetic ability and growth characters in two maize cultivars. Pak J Bot 41:87–98

    CAS  Google Scholar 

  • Chen Z, Zhou M, Newman I, Mendham N, Zhang G, Shabala S (2007) Potassium and sodium relations in salinized barley tissues as a basis of differential salt tolerance. Funct Plant Biol 34:150–162

    Article  CAS  Google Scholar 

  • Cuénod A, Pottier-Alapetite G, Labbe A (1954) Flore analytique et synoptique de la Tunisie. Cryptogames vasculaires, gymnospermes et monocotylédones, 159, S.E.F.A.N. (Société Editions Françaises en Afrique du Nord), Tunis, Tunisie

  • Cuin TA, Shabala S (2007) Compatible solutes reduce ROS-induced potassium efflux in Arabidopsis roots. Plant Cell Env 30:875–885

    Article  CAS  Google Scholar 

  • Debez A, Koyro HW, Grignon C, Abdelly C, Huchzermeyer B (2008) Relationship between the photosynthetic activity and the performance of Cakile maritima after long-term salt treatment. Physiol Plant 133:373–385

    Article  PubMed  CAS  Google Scholar 

  • Degl’Innocenti E, Hafsi C, Guidi L, Navari-Izzo F (2009) The effect of salinity on photosynthetic activity in potassium-deficient barley species. J Plant Physiol 166:1968–1981

    Google Scholar 

  • Eshel A, Waisel Y, Ramati A (1974) The role of sodium in stomatal movements of a halophyte: a study by X-ray microanalysis. In: Wherman J (ed) Proceedings of the 7th international colloquium on plant analysis and fertiliser problems. German Society of Plant Nutrition, Hannover, Germany

  • Fang Z, Boukamp JC, Solomos T (1998) Chlorophyllase activities and chlorophyll degradation during leaf senescence in non-yellowing mutant and wild type of Phaseolus vulgaris L. J Exp Bot 49:503–510

    Article  CAS  Google Scholar 

  • Fleury P, Leclerc M (1943) La méthode nitrovanadomolybdique de Mission pour le dosage colorimétrique du phosphore, Son intérêt en biochimie. Bull Soc Ch Biol 25:201–205

    CAS  Google Scholar 

  • Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963

    Article  PubMed  CAS  Google Scholar 

  • Gosset DR, Banks SW, Millhollon EP, Lucas M (1996) Antioxidant response to NaCl stress in a control and an NaCl-tolerant cotton cell line grown in the presence of paraquat, buthionine sulfoximine, and exogenous glutathione. Plant Physiol 112:803–809

    CAS  Google Scholar 

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

    Google Scholar 

  • Grattan SR, Grieve CM (1999) Salinity-mineral nutrient relations in horticultural crops. Sci Hortic 78:127–157

    Article  CAS  Google Scholar 

  • Grattan SR, Maas EV (1988) Effect of salinity on leaf P accumulation and injury in soybean. I. Influence of varying CaCl2/NaCl. Plant Soil 109:65–71

    Article  CAS  Google Scholar 

  • Hafsi C, Lakhdhar A, Rabhi M, Debez A, Abdelly C, Ouerghi Z (2007) Interactive effects of salinity and potassium availability on growth, water status, and ionic composition of Hordeum maritimum. J Plant Nutr Soil Sci 170:469–473

    Article  CAS  Google Scholar 

  • Hafsi C, Romero-Puertas MC, del Río LA, Sandalio LM, Abdelly C (2010) Differential antioxidative response in barley leaves subjected to the interactive effects of salinity and potassium deprivation. Plant Soil 334:449–460

    Article  CAS  Google Scholar 

  • Hewitt EJ (1966) Sand and water culture methods used in the study of plant nutrition. Commonw Bur Hort Tech Commun 22:431–446

    Google Scholar 

  • Jacobson L (1951) Maintenance of iron supply in nutrient solutions by a single addition of ferric-potassium-ethylene-diamine-tetraa-cetate. Plant Physiol 26:411–413

    Article  PubMed  CAS  Google Scholar 

  • Jiang C, Gao X, Liao L, Harberd N, Fu X (2007) Phosphate Starvation, root architecture and anthocyanin accumulation response are modulated by the gibberelin-DELLA signaling pathway in Arabidopsis. Plant Physiol 145:1460–1470

    Article  PubMed  CAS  Google Scholar 

  • Kaya C, Kirnak H, Higgs D (2001) The effects of high salinity (NaCl) and supplementary phosphorus and potassium on physiology and nutrition development of Spinach. Bulg J Plant Physiol 27(3–4):47–59

    CAS  Google Scholar 

  • Khosravinejad F, Heydari R, Farboodnia T (2008) Effects of salinity on photosynthetic pigments, respiration, and water content in two barley varieties. Pak J Biol Sci 11:2438–2442

    Google Scholar 

  • Lambers HY, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot 98:693–713

    Article  PubMed  Google Scholar 

  • Li YS, Mao XT, Tian QY, Li LH, Zhang WH (2009) Phosphorus deficiency-induced reduction in root hydraulic conductivity in Medicago falcata is associated with ethylene production. Environ Exp Bot 67:172–177

    Google Scholar 

  • Li Y-S, Gao Y, Tian Q-Y, Shi F-L, Li L, Zhang WH (2011) Stimulation of root acid phosphatase by phosphorus deficiency is regulated by ethylene in Medicago falcata. Environ Exp Bot 71:114–120

    Google Scholar 

  • Lichtenthaler HK, Welburn AR (1983) Determination of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592

    CAS  Google Scholar 

  • Martinez JP, Kinet JM, Bajji M, Lutts S (2005) NaCl alleviates polyethylene glycol-induced water stress in the halophyte species Atriplex halimus L. J Exp Bot 56(419):2421–2431

    Article  PubMed  CAS  Google Scholar 

  • Matar A, Torrent J, Ryan J (1992) Soil and fertilizer phosphorus and crop responses in the dry land mediterranean zone. Adv Soil Sci 18:81–146

    Article  CAS  Google Scholar 

  • Mittler R, Blumwald E (2010) Genetic engineering for modern agriculture: challenges and perspectives. Annu Rev Plant Biol 61:443–462

    Article  PubMed  CAS  Google Scholar 

  • Mtimet A (2001) Soils of Tunisia. In: Zdruli P, Steduto P, Lacirignola C, Montanarella L (eds) Soil resources of Southern and Eastern Mediterranean Countries. Bari, Italy, pp 243–262

    Google Scholar 

  • Navarro JM, Botella MA, Cerdá A, Martinez V (2001) Phosphorus uptake and translocation in salt-stressed melon plants. J Plant Physiol 158:375–381

    Article  CAS  Google Scholar 

  • Phang TH, Shao G, Liao H, Yan X, Lam HM (2009) High external phosphate (Pi) increases sodium ion uptake and reduces salt tolerance of ‘Pi-tolerant’ soybean. Physiol Plant 135:412–425

    Article  PubMed  CAS  Google Scholar 

  • Prieto P, Pineda M, Aguilar M (1999) Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenumcomplex: specific application to the determination of vitamin E. Anal Biochem 269:337–341

    Article  PubMed  CAS  Google Scholar 

  • Qiu N, Lu Q, Lu C (2003) Photosynthesis, photosystem II efficiency and the xanthophyll cycle in the salt-adapted halophyte Atriples centalasiatica. New Phytol 159:479–486

    Article  CAS  Google Scholar 

  • Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134:1683–1696

    Google Scholar 

  • Rubio L, Linares-Rueda A, García-Sánchez MJ, Fernández JA (2005) Physiological evidence for a sodium-dependent high affinity phosphate and nitrate transport at the plasma membrane of leaf and root cells of Zostera marina L. J Exp Bot 56:613–622

    Article  PubMed  CAS  Google Scholar 

  • Schonfeld MA, Johnson RC, Carver BF, Mornhinweg DW (1988) Water relations in winter wheat as drought resistance indicators. Crop Sci 28:526–531

    Article  Google Scholar 

  • Shabala S, Cuin TA (2006) Osmoregulation versus osmoprotection: reevaluating the role of compatible solutes. In: Teixeira da Silva J (ed) Floriculture, ornamental and plant biotechnology advances and topical issues. Global Science, Tokyo

    Google Scholar 

  • Shabala SN, Cuin TA (2007) Potassium transport and plant salt tolerance. Physiol Plant 133:651–669

    Google Scholar 

  • Silberbush M, Ben-Asher J (1989) The effect of NaCl concentration on NO3 –, K+ and orthophosphate-P influx to peanut roots. Sci Hort 39:279–287

    Article  CAS  Google Scholar 

  • Subbarao GV, Wheeler RM, Levine LH, Stutte GW (2001) Glycine betaine accumulation, ionic and water relations of red-beet at contrasting levels of sodium supply. J Plant Physiol 158:767–776

    Article  PubMed  CAS  Google Scholar 

  • Sultana N, Ikeda T, Itoh R (1999) Effect of NaCl salinity on photosynthesis and dry matter accumulation in developing rice grains. Environ Exp Bot 42(3):211–220

    Article  CAS  Google Scholar 

  • Szabados L, Savouré (2009) A proline: a multifunctional amino acid 2009. Trends Plant Sci 15:89–97

  • Talbi Zribi O, Abdelly C, Debez A (2011) Interactive effects of salinity and phosphorus availability on growth, water relations, nutritional status and photosynthetic activity of barley (Hordeum vulgare L.). Plant Biol 13:872–880

    Google Scholar 

  • Tewari RK, Kumar P, Tewari N, Srivastava S, Sharma PN (2004) Macronutrient deficiencies and differential antioxidant responses-influence on the activity and expression of superoxide dismutase in maize. Plant Sci 166:687–694

    Article  CAS  Google Scholar 

  • Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a non-renewable resource. New Phytol 157:423–447

    Article  CAS  Google Scholar 

  • Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plants extracts by anthrone. Biochem J 90:508–514

    Google Scholar 

  • Yousfi S, Rabhi M, Hessini K, Abdelly C, Gharsalli M (2010) Differences in efficient metabolite management and nutrient metabolic regulation between wild and cultivated barley grown at high salinity. Plant Biol 12(4):650–658

    PubMed  CAS  Google Scholar 

  • Yuan H, Liu D (2008) Signaling components involved in plant responses to phosphate starvation. J Integr Plant Biol 50:849–859

    Article  PubMed  CAS  Google Scholar 

  • Yuncai Hu Y, Schmidhalter Urs (2005) Drought and salinity: a comparison of their effects on mineral nutrition of plants. J Plant Nutr Soil Sci 168:541–549

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the Tunisian Ministry of Higher Education and Scientific Research (LR02CB02) and the Tunisian-French “Comité Mixte de Coopération Universitaire” (CMCU) network # 08G0917.

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  1. Laboratoire des Plantes Extrêmophiles, Centre de Biotechnologie, Technopole de Borj Cédria, BP 901, 2050, Hammam-Lif, Tunisia

    Ons Talbi Zribi, Nehla Labidi, Inès Slama, Ahmed Debez, Riadh Ksouri, Mokded Rabhi, Abderrazak Smaoui & Chedly Abdelly

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  1. Ons Talbi Zribi
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Correspondence to Ons Talbi Zribi.

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Zribi, O.T., Labidi, N., Slama, I. et al. Alleviation of phosphorus deficiency stress by moderate salinity in the halophyte Hordeum maritimum L.. Plant Growth Regul 66, 75–85 (2012). https://doi.org/10.1007/s10725-011-9631-9

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