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Physiological and biochemical mechanisms of the ornamental Eugenia myrtifolia L. plants for coping with NaCl stress and recovery

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Abstract

Main Conclusion

We studied the response of Eugenia myrtifolia L. plants, an ornamental shrub native to tropical and subtropical areas, to salt stress in order to facilitate the use of these plants in Mediterranean areas for landscaping. E. myrtifolia plants implement a series of adaptations to acclimate to salinity, including morphological, physiological and biochemical changes. Furthermore, the post-recovery period seems to be detected by Eugenia plants as a new stress situation.

Different physiological and biochemical changes in Eugenia myrtifolia L. plants after being subjected to NaCl stress for up to 30 days (Phase I) and after recovery from salinity (Phase II) were studied. Eugenia plants proved to be tolerant to NaCl concentrations between 44 and 88 mM, displaying a series of adaptative mechanisms to cope with salt-stress, including the accumulation of toxic ions in roots. Plants increased their root/shoot ratio and decreased their leaf area, leaf water potential and stomatal conductance in order to limit water loss. In addition, they displayed different strategies to protect the photosynthetic machinery, including the limited accumulation of toxic ions in leaves, increase in chlorophyll content, changes in chlorophyll fluorescence parameters, leaf anatomy and antioxidant defence mechanisms. Anatomical modifications in leaves, including an increase in palisade parenchyma and intercellular spaces and decrease in spongy parenchyma, served to facilitate CO2 diffusion in a situation of reduced stomatal aperture. Salinity produced oxidative stress in Eugenia plants as evidenced by oxidative stress parameters values and a reduction in APX and ASC levels. Nevertheless, SOD and GSH contents increased. The post-recovery period is detected as a new stress situation, as observed through effects on plant growth and alterations in chlorophyll fluorescence and oxidative stress parameters.

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Abbreviations

APX:

Ascorbate peroxidase

ASC:

Ascorbate reduced form

DHAR:

Dehydroascorbate reductase

GR:

Glutathione reductase

GSH:

Glutathione reduced form

GSSG:

Glutathione oxidised form

MDHAR:

Monodehydroascorbate reductase

POX:

Peroxidase

SOD:

Superoxide dismutase

References

  • Acosta-Motos JR, Álvarez S, Hernández JA, Sánchez-Blanco MJ (2014a) Irrigation of Myrtus communis L. plants with reclaimed water: morphological and physiological responses to different levels of salinity. J Hortic Sci Biotechnol 89:487–494

    Google Scholar 

  • Acosta-Motos JR, Álvarez S, Barba-Espín G, Hernández JA, Sánchez-Blanco MJ (2014b) Salts and nutrients present in regenerated waters induce changes in water relations, antioxidative metabolism, ion accumulation and restricted ion uptake in Myrtus communis L. plants. Plant Physiol Biochem 85:41–50

    Article  CAS  PubMed  Google Scholar 

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  CAS  PubMed  Google Scholar 

  • Alarcón JJ, Morales MA, Torrecillas A, Sánchez-Blanco MJ (1999) Growth, water relations and accumulation of organic and inorganic solutes in the halophyte Limonium latifolium cv. Avignon and its interspecific hybrid Limonium caspia × Limonium latifolium cv. Beltlaard during salt stress. J Plant Physiol 154:795–801

    Article  Google Scholar 

  • Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341

    Article  CAS  PubMed  Google Scholar 

  • Álvarez S, Sánchez-Blanco MJ (2014) Long-term effect of salinity on plant quality, water relations, photosynthetic parameters and ion distribution in Callistemon citrinus. Plant Biol 16:757–764

    Article  PubMed  Google Scholar 

  • Álvarez S, Gómez-Bellot MJ, Castillo M, Bañón S, Sánchez-Blanco MJ (2012) Osmotic and saline effect on growth, water relations, and ion uptake and translocation in Phlomis purpurea plants. Environ Exp Bot 78:138–145

    Article  Google Scholar 

  • Arbona V, Flors V, Jacas J, García-Agustín P, Gómez-Cadenas A (2003) Enzymatic and non-enzymatic antioxidant responses of Carrizo citrange, a salt-sensitive citrus rootstock, to different levels of salinity. Plant Cell Physiol 44:388–394

    Article  CAS  PubMed  Google Scholar 

  • Arrigoni O, Dipierro S, Borraccino G (1981) Ascorbate free radical reductase: a key enzyme of the ascorbic acid system. FEBS Lett 125:242–244

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51:163–190

    Article  CAS  Google Scholar 

  • Bose J, Rodrigo-Moreno A, Shabala S (2014) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65:1241–1257

    Article  CAS  PubMed  Google Scholar 

  • Brisson LF, Zelitch I, Havir EA (1998) Manipulation of catalase levels produces altered photosynthesis in transgenic tobacco plants. Plant Physiol 116:259–269

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cassaniti C, Leonardi C, Flowers TJ (2009) The effects of sodium chloride on ornamental shrubs. Sci Hort 122:586–593

    Article  CAS  Google Scholar 

  • Cazalé AC, Rouet-Mayer MA, Barbier-Brygoo H, Mathieu Y, Lauriére C (1998) Oxidative burst and hypoosmotic stress in tobacco cell suspensions. Plant Physiol 116:659–669

    Article  PubMed Central  PubMed  Google Scholar 

  • 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  PubMed Central  CAS  PubMed  Google Scholar 

  • Chaves MM, Costa JM, Madeira Saibo NJ (2011) Recent advances in photosynthesis under drought and salinity. In: Turkan I (ed) Advances in botanical research. Plant responses to drought and salinity stress: development in a post-genomic era, vol 57. Elsevier Ltd, San Diego, pp 50–103

    Google Scholar 

  • Colmer TD, Muñiz R, Flowers TJ (2005) Improving salt tolerance of wheat and barley: future prospects. Aus J Exp Agric 45:1425–1443

    Article  CAS  Google Scholar 

  • Corpas FJ, Gómez M, Hernández JA, del Río LA (1993) Metabolism of activated oxygen in peroxisomes from two Pisum sativum L. cultivars with different sensitivity to sodium chloride. J Plant Physiol 141:160–165

    Article  CAS  Google Scholar 

  • Dalton DA, Baird LM, Langeberg L, Taugher CY, Anyan WR, Vance CV, Sarath G (1993) Subcellular localization of oxygen defense enzymes in soybean (Glycine max L. Merr.) root nodules. Plant Physiol 102:481–489

    PubMed Central  CAS  PubMed  Google Scholar 

  • Diaz-Vivancos P, Dong YP, Ziegler K, Markovic J, Pallardó FV, Pellny T, Verrier P, Foyer CH (2010) Recruitment of glutathione into the nucleus during cell proliferation adjusts whole cell redox homeostasis in Arabidopsis thaliana and lowers the oxidative defence shield. Plant J 64:825–838

    Article  Google Scholar 

  • Diaz-Vivancos P, Faize M, Barba-Espin G, Faize L, Petri C, Hernández JA, Burgos L (2013) Ectopic expression of cytosolic superoxide dismutase and ascorbate peroxidase leads to salt stress tolerance in transgenic plums. Plant Biotech J 11:976–985

    Article  CAS  Google Scholar 

  • Duarte B, Santos D, Marques JC, Caçador I (2013) Ecophysiological adaptations of two halophytes to salt stress: photosynthesis, PS II photochemistry and anti-oxidant feedback. Implications for resilience in climate change. Plant Physiol Biochem 67:178–188

    Article  CAS  PubMed  Google Scholar 

  • Edwards EA, Rawsthorne S, Mullineaux PM (1990) Subcellular distribution of multiple forms of glutathione reductase in leaves of pea (Pisum sativum L.). Planta 180:278–284

    Article  CAS  PubMed  Google Scholar 

  • Fernández-García N, Olmos E, Bardisi E, García-De la Garma J, López-Berenguer C, Rubio-Asensio JS (2014) Intrinsic water use efficiency controls the adaptation to high salinity in a semi-arid adapted plant, henna (Lawsonia inermis L.). J Plant Physiol 171:64–75

    Article  PubMed  Google Scholar 

  • Flowers TJ, Yeo AR (1981) Variability in the resistance of sodium chloride salinity within rice (Oryza sativa L.) varieties. New Phytol 88:363–373

    Article  CAS  Google Scholar 

  • Foyer CH, Harbison J (1994) Oxygen metabolism and the regulation of photosynthetic electron transport. In: Foyer CH, Mullineaux P (eds) Causes of photooxidative stresses and amelioration of defense systems in plants. CRC Press, Boca Raton, pp 1–42

    Google Scholar 

  • Gadallah MAA (1999) Effects of proline and glycinebetaine on Vicia faba responses to salt stress. Biol Plant 42:249–257

    Article  CAS  Google Scholar 

  • Gest N, Gautier H, Stevens R (2013) Ascorbate as seen through plant evolution: the rise of a successful molecule? J Exp Bot 64:33–53

    Article  CAS  PubMed  Google Scholar 

  • Gil R, Bautista I, Boscaiu M, Lidón A, Wanklade S, Sánchez H, Llinares J, Vicente O (2014) Responses of five mediterranean halophytes to seasonal changes in environmental conditions. AoB Plants. doi:10.1093/aobpla/plu049

    PubMed Central  PubMed  Google Scholar 

  • Gómez JM, Hernández JA, Jiménez A, del Río LA, Sevilla F (1999) Differential response of antioxidative enzymes of chloroplasts and mitochondria to long-term NaCl stress of pea plants. Free Rad Res 31:S11–S18

    Article  Google Scholar 

  • Greenway H, Munns R (1980) Mechanism of salt tolerance in non- halophytes. Annu Rev Plant Phys 31:149–190

    Article  CAS  Google Scholar 

  • Gueta-Dahan Y, Yaniv Z, Zilinskas BA, Ben-Hayyim G (1997) Salt and oxidative stress: similar and specific responses and their relation to salt tolerance in Citrus. Planta 203:460–469

    Article  CAS  PubMed  Google Scholar 

  • Halliwell B, Gutteridge JMC (2000) Free radicals in biology and medicine. Oxford University Press, London

    Google Scholar 

  • Hardikar SA, Pandey AN (2008) Growth, water status and nutrient accumulation of seedling of Acacia senegal (L.) Willd in response to soil salinity. An Biol 30:17–28

    Google Scholar 

  • Hernández JA, Almansa MS (2002) Short-term effects of salt stress on antioxidant systems and leaf water relations of pea plants. Physiol Plant 115:251–257

    Article  PubMed  Google Scholar 

  • Hernández JA, Olmos E, Corpas FJ, Sevilla F, del Río LA (1995) Salt-induced oxidative stress in chloroplast of pea plants. Plant Sci 105:151–167

    Article  Google Scholar 

  • Hernández JA, Campillo A, Jiménez A, Alarcón JJ, Sevilla F (1999) Response of antioxidant systems and leaf water relations to NaCl stress in pea plants. New Phytol 141:241–251

    Article  Google Scholar 

  • Hernández JA, Jiménez A, Mullineaux PM, Sevilla F (2000) Tolerance of pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defenses. Plant Cell Environ 23:853–862

    Article  Google Scholar 

  • Hernández JA, Ferrer MA, Jiménez A, Ros-Barceló A, Sevilla F (2001) Antioxidant systems and O .−2 /H2O2 production in the apoplast of Pisum sativum L. leaves: its relation with NaCl-induced necrotic lesions in minor veins. Plant Physiol 127:817–831

    Article  PubMed Central  PubMed  Google Scholar 

  • Hernández JA, Aguilar A, Portillo B, López-Gómez E, Mataix-Beneyto J, García-Legaz MF (2003) The effect of calcium on the antioxidant enzymes from salt-treated loquat and anger plants. Funct Plant Biol 30:1127–1137

    Article  Google Scholar 

  • Hossain MA, Asada A (1984) Inactivation of ascorbate peroxidase in spinach chloroplasts on dark addition of hydrogen peroxide: its protection by ascorbate. Plant Cell Physiol 25:1285–1295

    CAS  Google Scholar 

  • Ikbal FE, Hernández JA, Barba-Espín G, Koussa T, Aziz A, Faize M, Diaz-Vivancos P (2014) Enhanced salt-induced antioxidative responses involve a contribution of polyamine biosynthesis in grapevine plants. J Plant Physiol 171:779–788

    Article  CAS  PubMed  Google Scholar 

  • Jones HG (1983) Estimation of an effective soil water potential at the root surface of transpiring plants. Plant Cell Environ 6:671–674

    Google Scholar 

  • Koyro HW (2006) Effect of salinity on growth, photosynthesis, water relations and solute composition of the potential cash crop halophyte Plantago coronopus (L.). Environ Exp Bot 56:136–146

    Article  CAS  Google Scholar 

  • Lee MH, Cho EJ, Wi SG, Bae H, Kim JE, Cho JY, Lee S, Kim JH, Chung BY (2013) Divergences in morphological changes and antioxidant responses in salt-tolerant and salt-sensitive rice seedlings after salt stress. Plant Physiol Biochem 70:325–335

    Article  CAS  PubMed  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, London

    Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence: a practical guide. J Exp Bot 51:659–668

    Article  CAS  PubMed  Google Scholar 

  • McCord JM, Fridovich I (1969) Superoxide dismutase. An enzymic function for erytrocuprein (hemocuprein). J Biol Chem 244:6049–6055

    CAS  PubMed  Google Scholar 

  • Mehta P, Jajoo A, Mathur S, Bharti S (2010) Chlorophyll a fluorescence study revealing effects of high salt stress on photosystem II in wheat leaves. Plant Physiol Biochem 48:16–20

    Article  CAS  PubMed  Google Scholar 

  • Mittal S, Kumari N, Sharma V (2012) Differential response of salt stress on Brassica juncea: photosynthetic performance, pigment, proline, D1 and antioxidant enzymes. Plant Physiol Biochem 54:17–26

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Zilinskas BA (1994) Regulation of pea cytosolic ascorbate peroxidase and other antioxidant enzymes during the progression of drought stress and following recovery from drought. Plant J 5:397–405

    Article  CAS  PubMed  Google Scholar 

  • Mittova V, Tal M, Volokita M, Guy M (2003) Up-regulation of the leaf mitochondrial and peroxisomal antioxidative systems in response to salt-induced oxidative stress in the wild salt-tolerant tomato species Lycopersicon pennellii. Plant Cell Environ 26:845–856

    Article  CAS  PubMed  Google Scholar 

  • Moradi F, Ismail AM (2007) Responses of photosynthesis, chlorophyll fluorescence and ROS-scavenging systems to salt stress during seedling and reproductive stages in rice. Ann Bot 99:1161–1179

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Munns R, Weir R (1981) Contribution of sugars to osmotic adjustment in elongating and expanded zones of wheat leaves during moderate water deficits at two light levels. Aust J Plant Physiol 8:93–105

    Article  CAS  Google Scholar 

  • Naliwajski MR, Skłodowska M (2014) The oxidative stress and antioxidant systems in cucumber cells during acclimation to salinity. Biol Plant 58:47–54

    Article  CAS  Google Scholar 

  • Navarro A, Bañón S, Conejero W, Sánchez-Blanco MJ (2008) Ornamental characters, ion accumulation and water status in Arbutus unedo seedlings irrigated with saline water and subsequent relief and transplanting. Environ Exp Bot 62:364–370

    Article  CAS  Google Scholar 

  • Nobel PS (1983) Biophysical plant physiology and ecology. Freeman and Company, New York, pp 61–79

    Google Scholar 

  • Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484

    Article  CAS  PubMed  Google Scholar 

  • Olmos E, Sánchez-Blanco MJ, Ferrández T, Alarcón JJ (2007) Subcellular effects of drought stress in Rosmarinus officinalis. Plant Biol 9:77–84

    Article  CAS  PubMed  Google Scholar 

  • Osakabe Y, Yamaguchi-Shinozaki K, Shinozaki K, Phan Tran LS (2014) ABA control of plant macroelement membrane transport systems in response to water deficit and high salinity. New Phytol 202:35–49

    Article  PubMed  Google Scholar 

  • Ozgur R, Uzilday B, Sekmen AH, Turkan I (2013) Reactive oxygen species regulation and antioxidant defence in halophytes. Funct Plant Biol 40:832–847

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Pellny TK, Locato V, Vivancos PD, Markovic J, De Gara L, Pallardó FV, Foyer CH (2009) Pyridine nucleotide cycling and control of intracellular redox state in relation to poly (ADP-ribose) polymerase activity and nuclear localisation of glutathione during exponential growth of Arabidopsis cells in culture. Mol Plant 2:442–456

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Clemente RM, Montoliu A, Izquierdo-Zandalinas S, De Ollas C, Gómez-Cadenas A (2012) Carrizo citrange plants do not require the presence of roots to modulate the response to osmotic stress. Sci World J 2012:1–13. doi:10.1100/2012/795396

    Article  Google Scholar 

  • Pitman MG (1975) Ion transport in whole plants. In: Baker DA, Hall JL (eds) Ion transport in plant cells and tissues. North-Holland Publishing Co, Amsterdam, pp 267–308

    Google Scholar 

  • Planchet E, Verdu I, Delahaie J, Cukier C, Girard C, Morère-Le Paven MC, Limami AM (2014) Abscisic acid-induced nitric oxide and proline accumulation in independent pathways under water-deficit stress during seedling establishment in Medicago truncatula. J Exp Bot 65:2161–2170

    Article  CAS  PubMed  Google Scholar 

  • Romero-Trigueros C, Nortes PA, Pedrero F, Mounzer O, Alarcón JJ, Bayona JM, Nicolás E (2014) Assessment of the viability of using saline reclaimed water in grapefruit in medium to long term. Span J Agric Res 12:1137–1148

    Article  Google Scholar 

  • Ros-Barceló A (1998) The generation of H2O2 in the xylem of Zinnia elegans is mediated by an NADPH-oxidase-like enzyme. Planta 207:207–216

    Article  Google Scholar 

  • Roxas VP, Lodhi SA, Garrett DK, Mahan JR, Allen RD (2000) Stress tolerance in transgenic tobacco seedlings that overexpress glutathione S-transferase/glutathione peroxidase. Plant Cell Environ 41:1229–1234

    Article  CAS  Google Scholar 

  • Sánchez-Blanco MJ, Morales MA, Torrecillas A, Alarcón JJ (1998) Diurnal and seasonal osmotic potential changes in Lotus creticus plants grown under saline stress. Plant Sci 136:1–10

    Article  Google Scholar 

  • Shu S, Yuan LY, Guo SR, Sun J, Yuan YH (2013) Effects of exogenous spermine on chlorophyll fluorescence, antioxidant system and ultrastructure of chloroplasts in Cucumis sativus L. under salt stress. Plant Physiol Biochem 63:209–216

    Article  CAS  PubMed  Google Scholar 

  • 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 Physiol 149:1154–1165

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the Spanish Ministry of Economy and Competitiveness co-financed by FEDER funds (Project CICYT AGL 2011-30022-C02-01-02) and by The Fundación Séneca-Agencia de Ciencia y Tecnología de la Región de Murcia (11883/PI/09 and 15356/PI/10). Authors thank Mrs Ansley Evans for correction of the English.

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Correspondence to José Antonio Hernández.

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425_2015_2315_MOESM1_ESM.pdf

Suppl. Fig. S1 Contents of Cl (a), Na+ (b), K+ (c) and Ca2+ (d) in different organs of E. myrtifolia plants at the end of the salinity period (Phase I) and after the recovery period (Phase II). Data represent the mean ± SE from 6 plants. Different letters in the same experimental period indicate significant differences according to Duncan’s test (P ≤ 0.05). (PDF 537 kb)

425_2015_2315_MOESM2_ESM.pdf

Suppl. Fig. S2 Influence of the different irrigation treatments on accumulated evapotranspiration (ET) in E. myrtifolia plants during stress period (Phase I). (PDF 124 kb)

425_2015_2315_MOESM3_ESM.pdf

Suppl. Fig. S3 Chlorophyll fluorescence parameters in leaves of E. myrtifolia at 15 and 30 days of NaCl stress (Phase I) and after the recovery period (Phase II). Images of the coefficient of photochemical quenching (qP), the effective PSII quantum yield [Y(II)] and the maximal PSII quantum yield (F v/F m), the non-photochemical quenching coefficient (qN), non-photochemical quenching (NPQ) and the quantum yield of regulated energy dissipation [Y(NPQ)]. (PDF 508 kb)

425_2015_2315_MOESM4_ESM.pdf

Suppl. Fig. S4 Light microscopy images showing the effect of NaCl on the percentage of area occupied by palisade parenchyma (PP), spongy parenchyma (SP) and intercellular spaces (IS) in leaves from E. myrtifolia plants at the end of the salinity period. (Phase I: a, control; c, S4; e, S8; g, S12) and after the recovery period (Phase II: b, control; d, S4; f, S8; h, S12). (PDF 401 kb)

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Acosta-Motos, JR., Diaz-Vivancos, P., Álvarez, S. et al. Physiological and biochemical mechanisms of the ornamental Eugenia myrtifolia L. plants for coping with NaCl stress and recovery. Planta 242, 829–846 (2015). https://doi.org/10.1007/s00425-015-2315-3

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