Ammonium enhances resistance to salinity stress in citrus plants

Journal of Plant Physiology

Volumn 169, Issue 12, 2012, Pages 1183-1191

  Fernández Crespo, Emma ^a   Camañes, Gemma ^a   García Agustín, Pilar ^a  

^a UNIVERSITAT JAUME I   (Spain)

Author keywords

Ammonium nutrition; Citrus; Salinity; SIMR

Indexed keywords

ABSCISIC ACID; HYDROGEN PEROXIDE; POLYAMINE; PROLINE; QUATERNARY AMMONIUM DERIVATIVE; SODIUM CHLORIDE;

ADAPTATION; ARTICLE; CITRUS; DRUG EFFECT; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGICAL STRESS; PLANT ROOT; SALINITY;

ABSCISIC ACID; ADAPTATION, PHYSIOLOGICAL; CITRUS; HYDROGEN PEROXIDE; PLANT ROOTS; POLYAMINES; PROLINE; QUATERNARY AMMONIUM COMPOUNDS; SALINITY; SODIUM CHLORIDE; STRESS, PHYSIOLOGICAL;

CARRIZO; CITRONCIRUS WEBBERI; CITRUS;

EID: 84863864477     PISSN: 01761617     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jplph.2012.04.011     Document Type: Article

References (76)

1. Al-Yassin A. Review: adverse effects of salinity on citrus. Int J Agric Biol 2005, 7:668-680.
2. Bagh K., Hiraoki T., Thorpe T.A., Vogel H.J. Nitrogen-15 NMR studies of nitrogen metabolism in Picea glauca buds. Plant Physiol Biochem 2004, 42:803-809.
3. Bañuls J., Primo-Millo E. Effects of chloride and sodium on gas exchange parameters and water relations of Citrus plants. Physiol Plant 1992, 86:115-123.
4. Bartels D., Sunkar R. Drought and salt tolerance in plants. Crit Rev Plant Sci 2005, 24:23-58.
5. Bates L.S., Waldren R.P., Teare I.D. Rapid determination of free proline in eater stress studies. Plant Soil 1973, 39:205-208.
6. + cycling: a cellular hypothesis to explain ammonium toxicity in plants. Proc Natl Acad Sci U S A 2001, 98:4255-4258.
7. + toxicity in higher plants: a critical review. J Plant Physiol 2002, 159:567-584.
8. Bruce J.A., Matthes M.C., Napier J.A., Pickett J.A. Stressful 'memories' of plants: evidence and possible mechanisms. Plant Sci 2007, 173:603-608.
9. Brumós J., Colmenero-Flores J.M., Conesa A., Izquierdo P., Sánchez G., Iglesias D.J., et al. Membrane transporters and carbon metabolism implicated in chloride homeostasis differentiate salt stress responses in tolerant and sensitive Citrus rootstocks. Funct Integr Genomics 2009, 9(3):293-309.
10. Camañes G., Cerezo M., Primo-Millo E., Alan G., García-Agustín P. Ammonium transport and CitAMT1 expression are regulated by N in Citrus plants. Planta 2009, 229:331-342.
11. Chattopadhayay M.K., Tiwari B.S., Chattopadhayay G., Bose A., Sengupta D.N., Ghosh B. Protective role of exogenous polyamines on salinity-stressed rice (Oryza sativa) plants. Physiol Plant 2002, 116:192-199.
12. Chen C., Dickman M.B. Proline suppresses apoptosis in the fungal pathogen Colletotrichum trifolii. Proc Natl Acad Sci U S A 2005, 102:3459-3464.
13. Chen S., Vaghchhipawala Z., Li W., Asard H., Dickman M.B. Tomato phospholipid hydroperoxide glutathione peroxidase inhibits cell death induced by Bax and oxidative stresses in yeast and plants. Plant Physiol 2004, 135:1630-1641.
14. Chen Z., Silva H., Klessig R.F. Active oxygen species in the induction of plant systemic acquired resistance by SA. Science 1993, 262:1883-1886.
15. Chun-Juan D., Xiao-Dong Y., Jin-Yuan L. Enzymatic properties of a recombinant phospholipid hydroperoxide glutathione peroxidase from Momordica charantia and its complementation function in yeast. Biochemistry 2009, 74:502-508.
16. Clark R.B. Nutrient solution growth of sorghum and corn in mineral nutrition studies. J Plant Nutr 1982, 5:1039-1057.
17. Claussen W., Lenz F. Effect of ammonium or nitrate nutrition on net photosynthesis, growth, and activity of the enzymes nitrate reductase and glutamine synthetase in blueberry, raspberry and strawberry. Plant Soil 1999, 208:95-102.
18. Conrath U., Pieterse C.M.J., Mauch-Mani B. Priming in plant-pathogen interactions. Trends Plant Sci 2002, 7:210-216.
19. Conrath U., Beckers G.J.M., Flors V., Garcia-Agustin P., Jakab G., Mauch F., et al. Priming: getting ready for battle. Mol Plant Microbe Interact 2006, 19:1062-1071.
20. Coruzzi G., Bush D.R. Nitrogen and carbon nutrient and metabolite signalling in plants. Plant Physiol 2001, 125:61-64.
21. Criqui M.C., Jamet E., Parmentier Y., Marbach J., Durr A., Fleck J. Isolation and characterization of a plant cDNA showing homology to animal glutathione peroxidases. Plant Mol Biol 1992, 18:623-627.
22. Dat J., Vandenabeele S., Vranova E., Van Montagu M., Inzé D., Van Breusegem F. Dual action of active oxygen species during plant stress responses. Cell Mol Life Sci 2000, 57:779-795.
23. Ellouzi H., Hamed K.B., Cela J., Munné-Bosch S., Abdelly C. Early effects of salt stress on the physiological and oxidative status of Cakile maritime (halophyte) and Arabidopsis thaliana (glycophyte). Physiol Plant 2011, 142:128-143.
24. Flors V., Leyva M.D., Vicedo B., Finiti I., Real M.D., García-Agustín P. Absence of the endo-beta-1,4-glucanases Cel1 and Cel2 reduces susceptibility to Botrytis cinerea in tomato. Plant J 2007, 52:1027-1040.
25. Flors V., Ton J., van Doorn R., Jakab G., García-Agustín P., Mauch-Mani B. Interplay between JA, SA and ABA signaling during basal and induced resistance against Pseudomonas syringae and Alternaria brassicicola. Plant J 2008, 54:81-92.
26. Foyer C.H., López-Delgado H., Dat J.F., Scott I.M. Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signaling. Physiol Plant 1997, 100:241-254.
27. Foyer C.H., Noctor G. Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 2005, 28:1056-1071.
28. Galis I., Gaquerel E., Pandey S.P., Baldwin I.T. Molecular mechanisms underlying plant memory in JA-mediated defence responses. Plant Cell Environ 2009, 38:617-627.
29. Gaspar T., Frank T., Bisbis B., Kevers C., Jouve L., Hausman J.F., et al. Concepts in plant stress physiology. Application to plant tissue cultures. Plant Growth Regul 2002, 37:263-285.
30. Gerendás J., Zhu Z., Bendixen R., Ratcliffe R.G., Sattelmacher B. Physiological and biochemical processes related to ammonium toxicity in higher plants. Z Pflanzernähr Bodenkd 1997, 160:239-251.
31. Gould K.S., Lister C. Flavonoid functions in plants. Flavonoids: chemistry, biochemistry, and applications 2006, 397-441. CRC Press, Boca Raton. M. Andersen Oslash, K.R. Markham (Eds.).
32. Groppa M.D., Tomaro M.L., Benavides M.P. Polyamines as protectors against cadmium or copper-induced oxidative damage in sunflower leaf discs. Plant Sci 2001, 161:481-488.
33. Groppa M.D., Benavides M.P. Polyamines and abiotic stress: recent advances. Amino Acids 2008, 34:35-45.
34. Halim V., Eschen-Lippold L., Altmann S., Birschwilks M., Scheel D., Rosahl S. Salicylic acid is important for basal defense of Solanum tuberosum against Phytophthora infestans. Mol Plant Microbe Interact 2007, 11:1346-1352.
35. Hernandez J.A., Almansa M.S. Short-term effects of salt stress on antioxidant systems and leaf water relations of pea leaves. Physiol Plant 2002, 115:251-257.
36. Hoagland D.R., Arnon D.J. The water culture method for growing plants without soil. Calif Agric Exp State Circ 1950, 347:1-32.
37. Horvath E., Janda T., Szalai G., Paldi E. In vitro salicylic acid inhibition of catalase activity in maize: differences between the isozymes and a possible role in the induction of chilling tolerance. Plant Sci 2002, 163:1129-1135.
38. Jakab G., Ton J., Flors V., Zimmerli L., Metraux P., Mauch-Mani B. Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses. Plant Physiol 2005, 139:267-274.
39. Jones D.L., Kochian L.V. Aluminum inhibition of the 1,4,5-trisphosphate signal transduction pathway in wheat roots: a role in aluminum toxicity?. Plant Cell 1995, 7:1913-1922.
40. Jubany-Marí T., Munné-Bosch S., López-Carbonell M., Alegre L. Hydrogen peroxide is involved in the acclimation of the Mediterranean shrub, Cistus albidus L., to summer drought. J Exp Bot 2009, 60:107-120.
41. Kakkar R.K., Sawhney V.K. Polyamine research in plants-a changing perspective. Physiol Plant 2003, 116:281-292.
42. Kishor P.B., Sangam S., Amrutha R.N., Sri Laxmi P., Naidu K.R., Rao K.R.S.S., et al. Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr Sci 2005, 88:424-438.
43. Kravchuk Z., Vicedo B., Flors V., Camañes G., González-Bosch C., García-Agustín P. Priming for JA-dependent defenses using hexanoic acid is an effective mechanism to protect Arabidopsis against B. cinerea. J Plant Physiol 2011, 168:359-366.
44. Lasa B., Frechilla S., Lamsfus C., Aparicio-Tejo P.M. The sensitivity to ammonium nutrition is related to nitrogen accumulation. Sci Hort 2001, 91:143-152.
45. + efflux and GMPase activity. Plant Cell Environ 2010, 34(6):933-946.
46. Li W., Liu J.Y., Zhao N. Cloning and characterization of phospholipid hydroperoxide glutathione peroxidase gene from Momordica charantia. Prog Biochem Biophys 2001, 28:908-911.
47. - in barley seedlings. Physiol Plant 2008, 134:134-150.
48. Lopez-Climent M., Arbona V., Perez-Clemente R.M., Gomez-Cadenas A. Relationship between salt tolerance and photosynthetic machinery performance in citrus. Environ Exp Bot 2008, 62:176-184.
49. Macarisin D., Wisniewski M.E., Bassett C., Thannhauser T. Proteomic analysis of b-aminobutyric acid priming and abscisic acid-induction of drought resistance in crabapple (Malus pumila): effect on general metabolism, the phenylpropanoid pathway and cell wall enzymes. Plant Cell Environ 2009, 32:1612-1631.
50. Marschner H. Mineral nutrition of higher plants 1995, Academic Press, London. 2nd ed.
51. Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 2002, 7:405-410.
52. Munns R., Tester M. Mechanism of salinity tolerance. Annu Rev Plant Biol 2008, 59:651-681.
53. Nylander M., Svensson J., Palva E.T., Welin B.V. Stress-induced accumulation and tissue-specific localization of dehydrins in Arabidopsis thaliana. Plant Mol Biol 2001, 45:263-279.
54. Oostendorp M., Kunz W., Dietrich B., Staub T. Induced disease resistance in plants by chemicals. Eur J Plant Pathol 2001, 107:19-28.
55. Overmyer K., Brosché M., Kangasjärvi J. Reactive oxygen species and hormonal control of cell death. Trends Plant Sci 2003, 8:335-342.
56. Pedranzani H., Racagni G., Alemano S., Miersch O., Ramírez I., Peña-Cortés H., et al. Salt tolerant tomato plants show increased levels of jasmonic acid. Plant Growth Regul 2003, 41:149-158.
57. Potters G., Pasternak T.P., Guisez Y., Palme K.J., Jansen M.A.K. Stress-induced morphogenic responses: growing out of trouble?. Trends Plant Sci 2007, 12:98-105.
58. Potters G., Pasternak T.P., Guisez Y., Jansen M.A. Different stresses, similar morphogenic responses: integrating a plethora of pathways. Plant Cell Environ 2009, 32:158-169.
59. Ravindran K.C., Venkatesa K., Balakrishan V., Chellappan K.P., Balasubramanian T. Restoration of saline land by halophytes for Indian soils. Soil Biol Biochem 2007, 39:2661-2664.
60. Romero-Aranda R., Moya J.L., Tadeo F.R., Legaz F., Primo-Millo E., Talon M. Physiological and anatomical disturbances induced by chloride salts in sensitive and tolerant citrus: beneficial and detrimental effects of cations. Plant Cell Environ 1998, 21:1243-1253.
61. Sakamoto M., Munemura I., Tomita R., Kobayashi K. Involvement of hydrogen peroxide in leaf abscission signaling, revealed by analysis with an in vitro abscission system in Capsicum plants. Plant J 2008, 56:13-27.
62. Sanchez-Casas P., Klessig D.F. A salicylic acid-binding activity and a salicylic acid-inhibitable catalase activity are present in a variety of plant species. Plant Physiol 1994, 106:1675-1679.
63. Sánchez-López J., Camañes G., Flors V., Cristian Barrera V., Vicedo B., Cerezo M., et al. Underivatized polyamine analysis in plant samples by ion-pair LC coupled with electrospray tandem mass spectrometry. Plant Physiol Biochem 2009, 47:592-598.
64. Shah J. The salicylic acid loop in plant defense. Curr Opin Plant Biol 2003, 6:365-371.
65. Svistoonoff S., Creff A., Reymond M., Sigoillot-Claude C., Ricaud L., Blanchet A., et al. Root tip contact with low-phosphate media reprograms plant root architecture. Nat Genet 2007, 39:792-796.
66. Szabados L., Savouré A. Proline: a multifunctional amino acid. Trends Plant Sci 2009, 15(2):89-97.
67. Tang W., Newton R.J. Polyamines reduce salt-induced oxidative damage by increasing the activities of antioxidant enzymes and decreasing lipid peroxidation in Virginia pine. Plant Growth Regul 2005, 46:31-43.
68. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 1997, 11:1187-1194.
69. Van der Ent S., Van Hulten M., Pozo M.J., Czechowski T., Udvardi M.K., Pieterse C.M., et al. Priming of plant innate immunity by rhizobacteria and beta-aminobutyric acid: differences and similarities in regulation. New Phytol 2009, 183:419-431.
70. Vicedo B., Flors V., Leyva M.D., Finiti I., Kravchuk Z., Real M.D., et al. Hexanoic acid-induced resistance against Botrytis cinerea in tomato plants. Mol Plant Microbe Interact 2009, 22:1455-1465.
71. Walch-Liu P., Neumann G., Bangerth F., Engels C. Rapid effects of nitrogen form on leaf morphogenesis in tobacco. J Exp Bot 2000, 51:227-237.
72. +. Plant Physiol 1993, 103:1249-1258.
73. Yang N., Zhu C., Gan L., Denny Ng, Xia K. Ammonium-stimulated root hair branching is enhanced by methyl jasmonate and suppressed by ethylene in Arabidopsis thaliana. J Plant Biol 2011, 54(2):92-100.
74. Zhu B., Chen T.H., Li P.H. Expression of three osmotin-like protein genes in response to osmotic stress and fungal infection in potato. Plant Mol Biol 1995, 28:17-26.
75. Zhu B., Su J., Chong M., Verma D.P.S., Fare Y., Wu R. Overexpression of d-pyrolline-5-carboxylate synthetase gene and analysis of tolerance to water- and salt stress in transgenic rice. Plant Sci 1998, 139:41-48.
76. Zhu J.K. Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 2002, 53:247-273.