Proteomic and physiological responses of the halophyte Cakile maritima to moderate salinity at the germinative and vegetative stages

Journal of Proteomics

Volumn 75, Issue 18, 2012, Pages 5667-5694

  Debez, Ahmed ^a,b   Braun, Hans Peter ^b   Pich, Andreas ^c   Taamalli, Wael ^a   Koyro, Hans Werner ^d   Abdelly, Chedly ^a   Huchzermeyer, Bernhard ^b  

^a CENTRE DE BIOTECHNOLOGIE DE BORJ CÉDRIA   (Tunisia)

^b LEIBNIZ UNIVERSITY HANNOVER   (Germany)

^c HANNOVER MEDICAL SCHOOL   (Germany)

^d JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Germination; Halophytes; Leaves; Proteome; Salt tolerance

Indexed keywords

SEED STORAGE PROTEIN;

AMINO ACID METABOLISM; ARTICLE; CAKILE MARITIMA; ENERGY METABOLISM; GERMINATION; GLYCOLYSIS; HALOPHYTE; MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTOSYNTHESIS; PLANT GROWTH; PLANT LEAF; PLANT LIFE CYCLE STAGE; PLANT SEED; PLANT WATER RELATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEOMICS; SALINITY; VEGETATIVE STAGE; WATER CONTENT;

BRASSICACEAE; GERMINATION; PHOTOSYNTHESIS; PLANT LEAVES; PLANT PROTEINS; PROTEOMICS; SALINITY; SALT-TOLERANT PLANTS; SEEDS; SODIUM CHLORIDE;

CAKILE MARITIMA;

EID: 84866184257     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2012.08.012     Document Type: Article

References (88)

1. Flowers T.J., Colmer T.D. Salinity tolerance in halophytes. New Phytol 2008, 179:945-963.
2. Debez A., Huchzermeyer B., Abdelly C., Koyro H.-W. Current challenges and future opportunities for a sustainable utilization of halophytes. Sabkha ecosystems, Tasks for vegetation science 46. 2011, 59-77. Springer. M. Ozturk, B. Böer, H.-J. Barth, M. Clüsener-Godt, A.M. Khan, S.W. Breckle (Eds.).
3. Manousaki E., Kalogerakis N. Halophytes-an emerging trend in phytoremediation. Int J Phytoremediation 2011, 13:959-969.
4. Ksouri R, Megdiche W, Jallali I., Debez A, Magné C., Abdelly C. Medicinal halophytes: potent source of health promoting biomolecules with medical, nutraceutical and food applications. Critical Reviews in Biotechnology 2012; (in press) doi: doi:10.3109/07388551.2011.630647.
5. Zarrouk M., El Almi H., Ben Youssef N., Sleimi N., Smaoui A., Ben Miled D., et al. Lipid composition of local halophytes seeds: Cakile maritima, Zygophyllum album and Crithmum maritimum. 10 years after the Al Ain meeting. 2003, 121-126. Kluwer Academic Publishers. H. Lieth, M. Moschenko (Eds.).
6. Ghars M.A., Debez A., Smaoui A., Zarrouk M., Grignon C., Abdelly C. Variability of fruit and seed-oil characteristics in Tunisian accessions of the halophyte Cakile maritima (Brassicaceae). Series: tasks for vegetation science. 2006, 40:55-67. Springer. M. Ajmal Khan, D.J. Weber (Eds.).
7. Debez A., Ben Hamed K., Grignon C., Abdelly C. Salinity effects on germination, growth, and seed production of the halophyte Cakile maritima. Plant Soil 2004, 262:179-189.
8. Debez A., Taamalli W., Saadaoui D., Ouerghi Z., Zarrouk M., Huchzermeyer B., et al. Salt effect on growth, photosynthesis, seed yield and oil composition of the potential crop halophyte Cakile maritima. Biosaline agriculture and salinity tolerance in plants 2006, 55-63. Birkhäuser, Verlag/Switzerland. M. Öztürk, Y. Waisel, M. Ajmal Khan, G. Görk (Eds.).
9. Megdiche W., Ben Amor N., Debez A., Hessini K., Ksouri R., Zuily-Fodil Y., et al. Salt tolerance of the annual halophyte Cakile maritima as affected by the provenance and the developmental stage. Acta Physiol Plant 2007, 29:375-384.
10. Ghars M.A., Debez A., Abdelly C. Interaction between salinity and original habitat during germination of the annual seashore halophyte Cakile maritima. Commun Soil Sci Plant Anal 2009, 40:3170-3180.
11. Chitteti B.R., Peng Z. Proteome and phosphoproteome differential expression under salinity stress in rice (Oryza sativa) roots. J Proteome Res 2007, 6:1718-1727.
12. Witzel K., Weidner A., Surabhi G.-K., Varshney R.K., Kunze G., Buck-Sorlin G.H., et al. Comparative analysis of the grain proteome fraction in barley genotypes with contrasting salinity tolerance during germination. Plant Cell Environ 2010, 33:211-222.
13. Sobhanian H., Aghaei K., Komatsu S. Changes in the plant proteome resulting from salt stress: toward the creation of salt-tolerant crops?. J Proteomics 2011, 74:1323-1337.
14. Zhang H., Han B., Wang T., Chen S., Li H., Zhang Y., et al. Mechanisms of plant salt response: insights from proteomics. J Proteome Res 2012, 11:49-67.
15. 4 plant. J Proteome Res 2010, 9:2882-2897.
16. 2 concentration enhances salinity tolerance in Aster tripolium L. Planta 2010, 231:583-594.
17. Tada Y., Kashimura T. Proteomic analysis of salt-responsive proteins in the mangrove plant, Bruguiera gymnorhiza. Plant Cell Physiol 2009, 50:439-446.
18. Sengupta S., Majumder A.L. Insight into the salt tolerance factors of a wild halophytic rice, Porteresia coarctata: a physiological and proteomic approach. Planta 2009, 229:911-929.
19. Yu J., Chen S., Zhao Q., Wang T., Yang C., Diaz C., et al. Physiological and proteomic analysis of salinity tolerance in Puccinellia tenuiflora. J Proteome Res 2011, 10:3852-3870.
20. Wang X., Fan P., Song H., Chen X., Li X., Li Yinxin Comparative proteomic analysis of differentially expressed proteins in shoots of Salicornia europaea under different salinity. J Proteome Res 2009, 8:3331-3345.
21. Askari H., Edqvist J., Hajheidari M., Kafi M., Salekdeh G.H. Effects of salinity levels on proteome of Suaeda aegyptiaca leaves. Proteomics 2006, 6:2542-2554.
22. Pang Q., Chen S., Dai S., Chen Y., Wang Y., Yan X. Comparative proteomics of salt tolerance in Arabidopsis thaliana and Thellungiella halophila. J Proteome Res 2010, 9:2584-2599.
23. Debez A., Koyro H.-W., Grignon C., Abdelly C., Huchzermeyer B. Relationship between the photosynthetic activity and the performance of Cakile maritima after long-term salt treatment. Physiol Plant 2008, 133:373-385.
24. Hunt R. Basic growth analysis 1990, Unwin Hyman, London.
25. Lichtenthaler H.K. Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology 1987, 148:350-382. Academic Press Inc., San Diego. R. Douce, L. Packer (Eds.).
26. Gould K.S., Markham K.R., Smith R.H., Goris J.J. Functional role of anthocyanins in the leaves of Quintinia serrata A.Cunn. J Exp Bot 2000, 51:1107-1115.
27. Maxwell K., Johnson G.N. Chlorophyll fluorescence-a practical guide. J Exp Bot 2000, 51:659-668.
28. Schägger H., Von Jagow G. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100kDa. Anal Biochem 1987, 166:368-379.
29. Führs H., Behrens C., Gallien S., Heintz D., Van Dorsselaer A., Braun H.-P., et al. Physiological and proteomic characterization of manganese sensitivity and tolerance in rice (Oryza sativa) in comparison with barley (Hordeum vulgare). Ann Bot 2010, 105:1129-1140.
30. Zeiser J.J., Klodmann J., Braun H.-P., Gerhard R., Justa I., Pich A. Effects of Clostridium difficile Toxin A on the proteome of colonocytes studied by differential 2D electrophoresis. J Proteomics 2011, 75:469-479.
31. Shi J., Zhen Y., Zheng R.-H. Proteome profiling of early seed development in Cunninghamia lanceolata (Lamb.) Hook. J Exp Bot 2010, 61:2367-2381.
32. Ben Amor N., Jimenez A., Megdiche W., Lundqvist M., Sevilla F., Abdelly C. Response of antioxidant systems to NaCl stress in the halophyte Cakile maritima. Physiol Plant 2006, 126:446-456.
33. Redondo-Gómez S., Naranjo E.M., Garzón O., Castillo J.M., Luque T., Figueroa M.E. Effects of salinity on germination and seedling establishment of endangered Limonium emarginatum (Willd.) O. Kuntze. J Coast Res 2008, 1:201-205.
34. 3, and nitrate may control seed germination of Crithmum maritimum (Apiaceae) under saline conditions. C R Biol 2009, 332:704-710.
35. Atia A., Smaoui A., Barhoumi Z., Abdelly C., Debez A. Differential response to salinity and water deficit stress in Polypogon monspeliensis (L.) Desf. provenances during germination. Plant Biol 2011, 13:541-545.
36. Yang M.F., Liu Y.J., Liu Y., Chen H., Chen F., Shen S.-H. Proteomic analysis of oil mobilization in seed germination and postgermination development of Jatropha curcas. J Proteome Res 2009, 8:1441-1451.
37. Gallardo K., Job C., Groot S.P.C., Puype M., Demol H., Vandekerckhove J., et al. Proteomic analysis of Arabidopsis seed germination and priming. Plant Physiol 2001, 126:835-848.
38. Yang P., Li X., Wang X., Chen H., Chen F., Shen S. Proteomic analysis of rice (Oryza sativa) seeds during germination. Proteomics 2007, 7:3358-3368.
39. Sahnoun-Abid I., Recorbet G., Zuber H., Sommerer N., Centeno D., Dumas-Gaudot E., et al. Proteomic characterisation of subclover seed storage proteins during germination. J Sci Food Agric 2009, 89:1787-1801.
40. Yacoubi R., Job C., Belghazi M., Chaibi W., Job D. Toward characterizing seed vigor in alfalfa through proteomic analysis of germination and priming. J Proteome Res 2011, 10:3891-3903.
41. Job C., Kersulec A., Ravasio L., Chareyre S., Pepin R., Job D. The solubilization of the basic subunit of sugarbeet seed 11-S globulin during priming and early germination. Seed Sci Res 1997, 7:225-244.
42. Soltani A., Gholipoor M., Zeinali E. Seed reserve utilization and seedling growth of wheat as affected by drought and salinity. Environ Exp Bot 2006, 55:195-200.
43. Sebei K., Debez A., Herchi W., Boukhchina S., Kallel H. Germination kinetics and seed reserve mobilization in two flax (Linum usitatissimum L.) cultivars under moderate salt stress. J Plant Biol 2007, 50:447-454.
44. Voigt E.L., Almeida T.D., Chagas R.M., Ponte L.F.A., Viégas R.A., Silveira J.A.G. Source-sink regulation of cotyledonary reserve mobilization during cashew (Anacardium occidentale) seedling establishment under NaCl salinity. J Plant Physiol 2009, 169:80-89.
45. Kranner I., Colville L. Metals and seeds: biochemical and molecular implications and their significance for seed germination. Environ Exp Bot 2011, 72:93-105.
46. Kuriakose S.V., Prasad M.N.V. Cadmium stress affects seed germination and seedling growth in Sorghum bicolor (L.) Moench by changing the activities of hydrolyzing enzymes. Plant Growth Regul 2008, 54:143-156.
47. Vitale A., Boston R.S. Endoplasmic reticulum quality control and the unfolded protein response: insights from plants. Traffic 2008, 9:1581-1588.
48. Matsuura H., Ishibashi Y., Shinmyo A., Kanaya S., Kato K. Genome-wide analyses of early translational responses to elevated temperature and high salinity in Arabidopsis thaliana. Plant Cell Physiol 2010, 51:448-462.
49. Graham I.A. Seed storage oil mobilization. Annu Rev Plant Biol 2008, 59:115-142.
50. Nonogaki H. Seed germination and reserve mobilization. Encyclopedia of Life Sciences (ELS) 2008, John Wiley & Sons, Ltd, Chichester. 10.1002/9780470015902.a0002047.pub2.
51. Penfield S., Li Y., Gilday A.D., Graham S., Graham I.A. Arabidopsis ABA INSENSITIVE4 regulates lipid mobilization in the embryo and reveals repression of seed germination by the endosperm. Plant Cell 2006, 18:1887-1899.
52. Catusse J., Strub J.-M., Job C., Van Dorsselaer A., Job D. Proteome-wide characterization of sugarbeet seed vigor and its tissue specific expression. Proc Natl Acad Sci 2008, 105:10262-10267.
53. Zhao J., Zuo K., Tang K. cDNA cloning and characterization of Enolase from chinese cabbage, Brassica campestris ssp. Pekinensis. Mitochondrial DNA 2004, 15:51-57.
54. Ahsan N., Lee D.-G., Lee S.-H., Kang K.Y., Lee J.J., Kim P.J., et al. Excess copper induced physiological and proteomic changes in germinating rice seeds. Chemosphere 2007, 67:1182-1193.
55. Demirevska K., Simova-Stoilova L., Vassileva V., Feller U. Rubisco and some chaperone protein responses to water stress and rewatering at early seedling growth of drought sensitive and tolerant wheat varieties. Plant Growth Regul 2008, 56:97-106.
56. Laino P., Shelton D., Finnie C., De Leonardis A.M., Mastrangelo A.M., Svensson B., et al. Comparative proteome analysis of metabolic proteins from seeds of durum wheat (cv. Svevo) subjected to heat stress. Proteomics 2010, 10:2359-2368.
57. Bourgeois M., Jacquin F., Savois V., Sommerer N., Labas V., Henry C., et al. Dissecting the proteome of pea mature seeds reveals the phenotypic plasticity of seed protein composition. Proteomics 2009, 9:254-271.
58. Müller K., Job C., Belghazi M., Job D., Leubner-Metzger G. Proteomics reveal tissue-specific features of the cress (Lepidium sativum L.) endosperm cap proteome and its hormone-induced changes during seed germination. Proteomics 2010, 10:406-416.
59. Gallardo K., Job C., Groot S.P.C., Puype M., Demol H., Vandekerckhove J., et al. Importance of methionine biosynthesis for Arabidopsis seed germination and seedling growth. Physiol Plant 2002, 116:238-247.
60. Pawlowski T.A. Proteomic approach to analyze dormancy breaking of tree seeds. Plant Mol Biol 2010, 73:15-25.
61. Guo G., Gea P., Ma C., Li X., Lv D., Wang S., et al. Comparative proteomic analysis of salt response proteins in seedling roots of two wheat varieties. J Proteomics 2012, 75:1867-1885.
62. Veeranagamallaiah G., Jyothsnakumari G., Thippeswamy M., Reddy P.C.O., Surabhi G.-K., Sriranganayakulu G., et al. Proteomic analysis of salt stress responses in foxtail millet (Setaria italica L. cv. Prasad) seedlings. Plant Sci 2008, 175:631-641.
63. Rajjou L., Duval M., Gallardo K., Catusse J., Bally J., Job C., et al. Seed germination and vigor. Annu Rev Plant Biol 2012, 6:507-533.
64. Ceriotti A. Waste disposal in the endoplasmic reticulum, ROS production and plant salt stress response. Cell Res 2011, 21:555-557.
65. Liu Y., Chang A. Heat shock response relieves ER stress. EMBO J 2008, 27:1049-1059.
66. Debez A., Saadaoui D., Slama I., Huchzermeyer B., Abdelly C. Responses of Batis maritima plants challenged with up to two-fold seawater NaCl salinity. J Plant Nutr Soil Sci 2010, 173:291-299.
67. +-ATPase activity and photosynthetic capacity of Cakile maritima under increasing salinity. Environ Exp Bot 2006, 57:285-295.
68. Ashraf M., Foolad M.R. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 2007, 59:206-216.
69. Storey R., Ahmad N., Wyn Jones R.G. Taxonomic and ecological aspects of the distribution of glycinebetaine and related compounds in plants. Oecologia 1977, 27:319-332.
70. Ksouri R., Megdiche W., Debez A., Falleh H., Grignon C., Abdelly C. Salinity effects on polyphenol content and antioxidant activities in leaves of the halophyte Cakile maritima. Plant Physiol Biochem 2007, 45:244-249.
71. Ellouzi H., Ben Hamed K., Cela J., Munné-Bosch S., Abdelly C. Early effects of salt stress on the physiological and oxidative status of Cakile maritima (halophyte) and Arabidopsis thaliana (glycophyte). Physiol Plant 2011, 142:128-143.
72. van den Berg A., Perkins T.D. Contribution of anthocyanins to the antioxidant capacity of juvenile and senescing sugar maple (Acer saccharum) leaves. Funct Plant Biol 2007, 34:714-719.
73. Hughes N.M., Morley C.B., Smith W.K. Coordination of anthocyanin decline and photosynthetic maturation in juvenile leaves of three deciduous tree species. New Phytol 2007, 175:675-685.
74. Redondo-Gómez S., Wharmby C., Castillo J.M., Mateos-Naranjo E., Luque C.J., De Cires A., et al. Growth and photosynthetic responses to salinity in an extreme halophyte, Sarcocornia fruticosa. Physiol Plant 2006, 128:116-124.
75. Redondo-Gómez S., Mateos-Naranjo E., Figueroa M.E., Davy A.J. Salt stimulation of growth and photosynthesis in an extreme halophyte, Arthrocnemum macrostachyum. Plant Biol 2010, 12:79-87.
76. 2 on crop photosynthesis and productivity: a review of field studies. Plant Cell Environ 1991, 14:807-818.
77. Mehler A.H. Studies on reactions of illuminated chloroplasts. I. Mechanism of the reduction of oxygen and other Hill reagents. Arch Biochem Biophys 1951, 33:65-77.
78. Brown A.H., Good N.E. Photochemical reduction of oxygen in chloroplast preparations and in green plant cells: I. Study of oxygen exchanges in vitro and in vivo. Arch Biochem Biophys 1955, 57:340-354.
79. Allen J.F. Induction of a Mehler reaction in chloroplast preparations by flavin mononucleotide: effects on photosynthesis by intact chloroplasts. Plant Sci Lett 1978, 12:151-159.
80. Avron M., Krogmann D.W., Jagendorf A.T. The relation of photosynthetic phosphorylation to the Hill reaction. Biochim Biophys Acta 1958, 30:144-153.
81. Koyro H.-W., Geissler N., Seenivasan R., Huchzermeyer B. Plant stress physiology: physiological and biochemical strategies allowing plants/crops to thrive under ionic stress. Handbook of plant and crop stress 2011, 1051-1093. CRC Press, Boca Raton. 3rd edition. M. Pessarakli (Ed.).
82. Wang X., Li X., Deng X., Han H., Shi W., Li Y. A protein extraction method compatible with proteomic analysis for the euhalophyte Salicornia europaea. Electrophoresis 2007, 28:3976-3987.
83. Bandehagh A., Salekdeh G.H., Toorchi M., Mohammadi A., Komatsu S. Comparative proteomic analysis of canola leaves under salinity stress. Proteomics 2011, 11:1965-1975.
84. Ma H., Song L., Shu Y., Wang S., Niu J., Wang Z., et al. Comparative proteomic analysis of seedling leaves of different salt tolerant soybean genotypes. J Proteomics 2012, 75:1529-1546.
85. Rokka A., Zhang L., Aro E.-M. Rubisco activase: an enzyme with a temperature-dependent dual function?. Plant J 2001, 25:463-471.
86. Stitt M., Lilley R McC., Heldt H.W. Adenine nucleotide levels in the cytosol, chloroplasts, and mitochondria of wheat leaf protoplasts. Plant Physiol 1982, 70:971-977.
87. Hampp R., Goller M., Ziegler H. Adenylate levels, energy charge, and phosphorylation potential during dark-light and light-dark transition in chloroplasts, mitochondria, and cytosol of mesophyll protoplasts from Avena sativa L. Plant Physiol 1982, 69:448-455.
88. Parker R., Flowers T.J., Moore A.L., Harpham N.V.J. An accurate and reproducible method for proteome profiling of the effects of salt stress in the rice leaf lamina. J Exp Bot 2006, 57:1109-1118.