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

Planta

Volumn 242, Issue 4, 2015, Pages 829-846

  Acosta Motos, José Ramón ^a   Diaz Vivancos, Pedro ^a   Álvarez, Sara ^a   Fernández García, Nieves ^a   Sanchez Blanco, María Jesús ^a   Hernández, José Antonio ^a  

^a RESEARCH GROUP ON QUALITY   (Spain)

Author keywords

ASC GSH cycle; Gas exchange; Leaf anatomy; Oxidative stress; Recovery capacity; Water relations

Indexed keywords

CHLOROPHYLL; SODIUM CHLORIDE; WATER;

EUGENIA; FLUORESCENCE; GROWTH, DEVELOPMENT AND AGING; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGY;

CHLOROPHYLL; EUGENIA; FLUORESCENCE; OXIDATIVE STRESS; SODIUM CHLORIDE; WATER;

EID: 84941188505     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-015-2315-3     Document Type: Article

References (74)

1. 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
2. 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
3. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126
4. 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
5. Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341
6. 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
7. 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
8. 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
9. Arrigoni O, Dipierro S, Borraccino G (1981) Ascorbate free radical reductase: a key enzyme of the ascorbic acid system. FEBS Lett 125:242–244
10. Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Einviron Exp Bot 59:206–216
11. Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51:163–190
12. 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
13. Brisson LF, Zelitch I, Havir EA (1998) Manipulation of catalase levels produces altered photosynthesis in transgenic tobacco plants. Plant Physiol 116:259–269
14. Cassaniti C, Leonardi C, Flowers TJ (2009) The effects of sodium chloride on ornamental shrubs. Sci Hort 122:586–593
15. 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
16. 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
17. 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
18. Colmer TD, Muñiz R, Flowers TJ (2005) Improving salt tolerance of wheat and barley: future prospects. Aus J Exp Agric 45:1425–1443
19. 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
20. 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
21. 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
22. 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
23. 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
24. 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
25. 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
26. Flowers TJ, Yeo AR (1981) Variability in the resistance of sodium chloride salinity within rice (Oryza sativa L.) varieties. New Phytol 88:363–373
27. 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
28. Gadallah MAA (1999) Effects of proline and glycinebetaine on Vicia faba responses to salt stress. Biol Plant 42:249–257
29. 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
30. 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
31. 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
32. Greenway H, Munns R (1980) Mechanism of salt tolerance in non- halophytes. Annu Rev Plant Phys 31:149–190
33. 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
34. Halliwell B, Gutteridge JMC (2000) Free radicals in biology and medicine. Oxford University Press, London
35. 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
36. 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
37. 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
38. 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
39. 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
40. 2 production in the apoplast of Pisum sativum L. leaves: its relation with NaCl-induced necrotic lesions in minor veins. Plant Physiol 127:817–831
41. 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
42. 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
43. 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
44. Jones HG (1983) Estimation of an effective soil water potential at the root surface of transpiring plants. Plant Cell Environ 6:671–674
45. 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
46. 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
47. Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, London
48. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence: a practical guide. J Exp Bot 51:659–668
49. McCord JM, Fridovich I (1969) Superoxide dismutase. An enzymic function for erytrocuprein (hemocuprein). J Biol Chem 244:6049–6055
50. 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
51. 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
52. 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
53. 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
54. 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
55. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Ann Rev Plant Biol 59:651–681
56. 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
57. Naliwajski MR, Skłodowska M (2014) The oxidative stress and antioxidant systems in cucumber cells during acclimation to salinity. Biol Plant 58:47–54
58. 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
59. Nobel PS (1983) Biophysical plant physiology and ecology. Freeman and Company, New York, pp 61–79
60. 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
61. Olmos E, Sánchez-Blanco MJ, Ferrández T, Alarcón JJ (2007) Subcellular effects of drought stress in Rosmarinus officinalis. Plant Biol 9:77–84
62. 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
63. Ozgur R, Uzilday B, Sekmen AH, Turkan I (2013) Reactive oxygen species regulation and antioxidant defence in halophytes. Funct Plant Biol 40:832–847
64. Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349
65. 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
66. 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
67. 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
68. 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
69. 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
70. 2 in the xylem of Zinnia elegans is mediated by an NADPH-oxidase-like enzyme. Planta 207:207–216
71. 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
72. 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
73. 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
74. 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