Salicylic acid and photosynthesis: signalling and effects

Acta Physiologiae Plantarum

Volumn 36, Issue 10, 2014, Pages 2537-2546

  Janda, Tibor ^a   Gondor, Orsolya Kinga ^a   Yordanova, Rusina ^b   Szalai, Gabriella ^a   Pál, Magda ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b INSTITUTE OF PHYSIOLOGY   (Bulgaria)

Author keywords

Fluorescence quenching; Net photosynthesis; Oxidative stress; Salicylic acid; Stomatal conductivity; Stress responses

Indexed keywords

EID: 84907883403     PISSN: 01375881     EISSN: 18611664     Source Type: Journal    
DOI: 10.1007/s11738-014-1620-y     Document Type: Review

References (83)

1. Alibert G, Boudet A, Ranjeva R (1972) Studies on the enzymes catalysts of biosynthesis of phenolic acids in Quercus pedunculata. III. Sequential formation of cinnamic, p-coumaric and caffeic acids from phenylalanine by isolated cell organelles. Physiol Plant 27:240–243
2. Ananieva EA, Alexieva VS, Popova LP (2002) Treatment with salicylic acid decreases the effects of paraquat on photosynthesis. J Plant Physiol 159:685–693
3. Arfan M, Athar HR, Ashraf M (2007) Does exogenous application of salicylic acid through the rooting medium modulate growth and photosynthetic capacity in two differently adapted spring wheat cultivars under salt stress? J Plant Physiol 164:685–694
4. Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51:163–190
5. Bilger W, Bjorkman O (1991) Temperature dependence of violaxanthin deepoxidation and non-photochemical fluorescence quenching in intact leaves of Gossypium hirsutum L. and Malva parviflora L. Planta 184:226–234
6. Çag S, Cevahir-Öz G, Sarsag M, Gören-Saglam N (2009) Effect of salicylic acid on pigment, protein content and peroxidase activity in excised sunflower cotyledons. Pak J Bot 41:2297–2303
7. Catinot J, Buchala A, Abou-Mansour E, Metraux JP (2008) Salicylic acid production in response to biotic and abiotic stress depends on isochorismate in Nicotiana benthamiana. FEBS Lett 582:473–478
8. Chandra A, Bhatt RK (1998) Biochemical physiological response to salicylic acid in relation to the systemic acquired resistance. Photosynthetica 35:255–258
9. Chen Z, Zheng Z, Huang J, Lai Z, Fan B (2009) Biosynthesis of salicylic acid in plants. Plant Sign Behav 4:493–496
10. Clough SJ, Fengler KA, Yu IC, Lippok B, Smith RK Jr, Bent AF (2000) The Arabidopsis dnd1 ‘defense, no death’ gene encodes a mutated cyclic nucleotide-gated ion channel. Proc Natl Acad Sci USA 97:9323–9328
11. Ducruet JM (2003) Chlorophyll thermoluminescence of leaf discs: simple instruments and progress in signal interpretation open the way to new ecophysiological indicators. J Exp Bot 54:2419–2430
12. El-Basyouni SZ, Chen D, Ibrahim RK, Neish AC, Towers GHN (1964) The biosynthesis of hydroxybenzoic acids in higher plants. Phytochemistry 3:485–492
13. Enyedi AJ (1999) Induction of salicylic acid biosynthesis and systemic acquired resistance using the active oxygen species generator rose Bengal. J Plant Physiol 154:106–112
14. Fariduddin Q, Hayat S, Ahmad A (2003) Salicylic acid influences net photosynthetic rate, carboxylation efficiency, nitrate reductase activity, and seed yield in Brassica juncea. Photosynthetica 41:281–284
15. Fraser CM, Chappel C (2011) The phenylpropanoid pathway in Arabidopsis. Arab Book 9:e0152
16. Gawroński P, Górecka M, Bederska M, Rusaczonek A, Ślesak I, Kruk J, Karpiński S (2013) Isochorismate synthase 1 is required for thylakoid organization, optimal plastoquinone redox status, and state transitions in Arabidopsis thaliana. J Exp Bot 64:3669–3679
17. Gémes K, Poór P, Sulyok Z, Szepesi Á, Szabó M, Tari I (2008) Role of salicylic acid pretreatment in the photosynthetic performance of tomato plants (Lycopersicon esculentum Mill. L. cvar. Rio Fuego) under salt stress. Acta Biol Szegediensis 52:161–162
18. Ghai N, Setia RC, Setia N (2002) Effects of paclobutrazol and salicylic acid on chlorophyll content, hill activity and yield components in Brassica napus L. (cv. GSL-1). Phytomorphology 52:83–87
19. Gutiérrez-Coronado MA, Trejo-López C, Larqué-Saavedra A (1998) Effect of salicylic acid on the growth of roots and shoots in soybean. Plant Physiol Biochem 36:563–565
20. Hayat S, Fariduddin Q, Ali B, Ahmad A (2005) Effect of salicylic acid on growth and enzyme activities of wheat seedlings. Acta Agron Hung 53:433–437
21. Hayat Q, Hayat S, Irfan M, Ahmad A (2010) Effect of exogenous salicylic acid under changing environment: a review. Environ Exp Bot 68:14–25
22. Herrman KM, Weaver LM (1999) The shikimate pathway. Annu Rev Plant Physiol Plant Mol Biol 50:473–503
23. Horváth E, Szalai G, Janda T (2007) Induction of abiotic stress tolerance by salicylic acid signaling. J Plant Growth Regul 26:290–300
24. Janda T, Szalai G, Tari I, Páldi E (1999) Hydroponic treatment with salicylic acid decreases the effects of chilling injury in maize (Zea mays L.) plants. Planta 208:175–180
25. Janda T, Szalai G, Antunovics Z, Horváth E, Páldi E (2000) Effect of benzoic acid and aspirin on chilling tolerance and photosynthesis in young maize plants. Maydica 45:29–33
26. Janda T, Szalai G, Leskó K, Yordanova R, Apostol S, Popova LP (2007) Factors contributing to enhanced freezing tolerance in wheat during frost hardening in the light. Phytochemistry 68:1674–1682
27. Janda K, Hideg É, Szalai G, Kovács L, Janda T (2012) Salicylic acid may indirectly influence the photosynthetic electron transport. J Plant Physiol 169:971–978
28. Khan W, Prithiviraj B, Smith DL (2003) Photosynthetic responses of corn and soybean to foliar application of salicylates. J Plant Physiol 160:485–492
29. Klambt HD (1962) Conversion in plants of benzoic acid to salicylic acid and its β-d-glucoside. Nature 196:491
30. Kosova K, Prasil IT, Vitamvas P, Dobrev P, Motyka V, Flokova K, Novak O, Turecková V, Rolcik J, Pesek B, Travnickova A, Gaudinova A, Galiba G, Janda T, Vlasakova E, Prasilova P, Vankova R (2012) Complex phytohormone responses during the cold acclimation of two wheat cultivars differing in cold tolerance, winter Samanta and spring Sandra. J Plant Physiol 169:567–576
31. Krantev A, Yordanova R, Janda T, Szalai G, Popova L (2008) Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. J Plant Physiol 165:920–931
32. Krik V, Bouyer D, Schöbinger U, Bechtold N, Herzog M, Bonneville JM, Hülskamp M (2001) CPR5 is involved in cell proliferation and cell death control and encodes a novel transmembrane protein. Curr Biol 11:1891–1895
33. Kusumi K, Yaeno T, Kojo K, Hirayama M, Hirokawa D, Yara A, Iba K (2006) The role of salicylic acid in the glutathione-mediated protection against photooxidative stress in rice. Physiol Plant 128:651–661
34. Li L, Dong CJ, Shang QM (2013) Role of endogenous salicylic acid in responding of cucumber leaf photosynthetic systems to low temperature stress. Acta Hortic Sinica 40:487–497
35. Liu W, Ai XZ, Liang WJ, Wang HT, Liu SX, Zheng N (2009) Effects of salicylic acid on the leaf photosynthesis and antioxidant enzyme activities of cucumber seedlings under low temperature and light intensity. Chin J Appl Ecol 20:441–445
36. Majláth I, Szalai G, Soós V, Sebestyén E, Balázs E, Vanková R, Dobrev PI, Tandori J, Janda T (2012) Effect of light on the gene expression and hormonal status of winter and spring wheat plants during cold hardening. Physiol Plant 145:296–314
37. Maslenkova L, Peeva V, Stojnova Z, Popova L (2009) Salicylic acid-induced changes in photosystem II reactions in barley plants. Biotechnol Biotechnol Equip (23/2009/se special edition/on-line)
38. Mateo A, Mühlenbock P, Rusterucci C, Chang CC, Miszalski Z, Karpinska B, Parker JE, Mullineaux PM, Karpinski S (2004) Lesion simulating disease 1 is required for acclimation to conditions that promote excess excitation energy. Plant Physiol 136:2818–2830
39. Mateo A, Funck D, Mühlenbock P, Kular B, Mullineaux PM, Karpinski S (2006) Controlled levels of salicylic acid are required for optimal photosynthesis and redox homeostasis. J Exp Bot 57:1795–1807
40. Metodiev MV, Kicheva MI, Stoinova ZG, Popova LP (2002) Two-dimensional electrophoretic analysis of salicylic acid-induced changes in polypeptide pattern of barley leaves. Biol Plant 45:585–588
41. Meuwly P, Métraux JP (1993) Ortho-anisic acid as internal standard for the simultaneous quantitation of salicylic acid and its putative biosynthetic precursors in cucumber leaves. Anal Biochem 214:500–505
42. Moradkhani S, Khavari Nejad RA, Dilmaghani K, Chaparzadeh N (2012) Effect of salicylic acid treatment on cadmium toxicity and leaf lipid composition in sunflower. J Stress Physiol Biochem 8:78–89
43. Munné-Bosch S, Penuelas J, Llusia J (2007) A deficiency in salicylic acid alters isoprenoid accumulation in water-stressed NahG transgenic Arabidopsis plants. Plant Sci 172:756–762
44. Noreen S, Ashraf M (2008) Alleviation of adverse effects of salt stress on sunflower (Helianthus annuus L.) by exogenous application of salicylic acid: growth and photosynthesis. Pak J Bot 40:1657–1663
45. Pál M, Horváth E, Janda T, Páldi E, Szalai G (2005) Cadmium stimulates the accumulation of salicylic acid and its putative precursors in maize (Zea mays L.) plants. Physiol Plant 125:356–364
46. Pál M, Kovács V, Vida G, Szalai G, Janda T (2013) Changes induced by powdery mildew in the salicylic acid and polyamine contents and the antioxidant enzyme activities of wheat lines. Eur J Plant Pathol 135:35–47
47. Pál M, Kovács V, Szalai G, Soós V, Ma X, Liu H, Mei H, Janda T (2014) Salicylic acid and abiotic stress responses in rice. J Agron Crop Sci 200:1–11
48. Pancheva TV, Popova LP (1998) Effect of salicylic acid on the synthesis of ribulose-1,5-bisphosphate carboxylase/oxygenase in barley leaves. J Plant Physiol 152:381–386
49. Pancheva TV, Popova LP, Uzunova AN (1996) Effects of salicylic acid on growth and photosynthesis in barley plants. J Plant Physiol 149:57–63
50. Penuelas J, Munné-Bosch S (2005) Isoprenoids: an evolutionary pool for photoprotection. Trends Plant Sci 10:166–169
51. Poór P, Tari I (2012) Regulation of stomatal movement and photosynthetic activity in guard cells of tomato abaxial epidermal peels by salicylic acid. Funct Plant Biol 39:1028–1037
52. 2 fixation rate and carbohydrate metabolism in tomato, and decreases harmful effects of subsequent salt stress. Plant Biol 13:105–114
53. Popova LP, Maslenkova LT, Yordanova RY, Ivanova AP, Krantev AP, Szalai G, Janda T (2009) Exogenous treatment with salicylic acid attenuates cadmium toxicity in pea seedlings. Plant Physiol Biochem 47:224–231
54. Qiu C, Ji W, Guo Y (2011) Effects of high temperature and strong light on chlorophyll fluorescence, the D1 protein, and Deg1 protease in Satsuma mandarin, and the protective role of salicylic acid. Acta Ecol Sinica 31:3802–3810
55. Radwan DEM, Soltan DM (2012) The negative effects of clethodim in photosynthesis and gas-exchange status of maize plants are ameliorated by salicylic acid pretreatment. Photosynthetica 50:171–179
56. Raskin I (1992a) Role of salicylic acid in plants. Annu Rev Plant Physiol Plant Mol Biol 43:439–463
57. Raskin I (1992b) Salicylate, a new plant hormone. Plant Physiol 99:799–803
58. Sahu GK, Kar M, Sabat SC (2002) Electron transport activities of isolated thylakoids from wheat plants grown in salicylic acid. Plant Biol 4:321–328
59. Saruhan N, Saglam A, Kadioglu A (2012) Salicylic acid pretreatment induces drought tolerance and delays leaf rolling by inducing antioxidant systems in maize genotypes. Acta Physiol Plant 34:97–106
60. Sasheva P, Yordanova R, Janda T, Szalai G, Maslenkova L (2013) Study of primary photosynthetic reactions in winter wheat cultivars after cold hardening and freezing. Effect of salicylic acid. Bulg J Agric Sci 19:45–48
61. Shakirova FM (2007) Role of hormonal system in the manisfestation of growth promoting and anti-stress action of salicylic acid. In: Hayat S, Ahmad A (eds) Salicylic acid, a plant hormone. Springer, Dordrecht, pp 69–89
62. Silverman P, Seskar M, Kanter D, Schweizer P, Métraux JP, Raskin I (1995) Salicylic acid in rice. Biosynthesis, conjugation, and possible role. Plant Physiol 108:633–639
63. Singh PK, Gautam S (2013) Role of salicylic acid on physiological and biochemical mechanism of salinity stress tolerance in plants. Acta Physiol Plant 35:2345–2353
64. Spetea C, Hundal T, Lundin B, Heddad M, Adamska I, Andersson B (2004) Multiple evidence for nucleotide metabolism in the chloroplast thylakoid lumen. Proc Natl Acad Sci USA 101:1409–1414
65. Szalai G, Janda T (2009) Effect of salt stress on the salicylic acid synthesis in young maize (Zea mays L.) plants. J Agron Crop Sci 195:165–171
66. Szalai G, Horgosi S, Soós V, Majláth I, Balázs E, Janda T (2011) Salicylic acid treatment of pea seeds induces its de novo synthesis. J Plant Physiol 168:213–219
67. Szalai G, Krantev A, Yordanova R, Popova LP, Janda T (2013) Influence of salicylic acid on phytochelatin synthesis in Zea mays during Cd stress. Turk J Bot 37:708–714
68. Tirani MM, Nasibi F, Kalantari KM (2013) Interaction of salicylic acid and ethylene and their effects on some physiological and biochemical parameters in canola plants (Brassica napus L.). Photosynthetica 51:411–418
69. Tóth SZ, Schansker G, Garab G (2013) The physiological roles and metabolism of ascorbate in chloroplasts. Physiol Plant 148:161–175
70. Uzunova AN, Popova LP (2000) Effect of salicylic acid on leaf anatomy and chloroplast ultrastructure of barley plants. Photosynthetica 38:243–250
71. Vicent MRS, Plasencia J (2011) Salicylic acid beyond defence: its role in plant growth and development. J Exp Bot 62:3321–3338
72. Vogt T (2010) Phenylpropanoid biosythesis. Mol Plant 3:2–20
73. Wang LJ, Fan L, Loescher W, Duan W, Liu GJ, Cheng JS, Luo HB, Li SH (2010) Salicylic acid alleviates decreases in photosynthesis under heat stress and accelerates recovery in grapevine leaves. BMC Plant Biol 10:34
74. War AR, Paulraj MG, War MY, Ignacimuthu S (2011) Role of salicylic acid in induction of plant defense system in chickpea (Cicer arietinum L.). Plant Signal Behav 6:1787–1792
75. Wildermuth MC (2006) Variations on a theme: synthesis and modification of plant benzoic acids. Curr Opin Plant Biol 9:288–296
76. Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase in required to synthesize salicylic acid for plant defence. Nature 414:562–565
77. Wu LJ, Zu XF, Wang XT, Sun AG, Zhang J, Wang SX, Chen YH (2013) Comparative proteomic analysis of the effects of salicylic acid and abscisic acid on maize (Zea mays L.) leaves. Plant Mol Biol Rep 31:507–516
78. Xue LJ, Guo W, Yuan Y, Anino EO, Nyamdari B, Wilson MC, Frost CJ, Chen HY, Babst BA, Harding SA, Tsai CJ (2013) Constitutively elevated salicylic acid levels alter photosynthesis and oxidative state but not growth in transgenic populous. Plant Cell 25:2714–2730
79. Yalpani N, Enyedi AJ, León J, Raskin I (1994) Ultraviolet light and ozone stimulate accumulation of salicylic acid, pathogenesis-related proteins and virus resistance in tobacco. Planta 193:372–376
80. Yang Y, Qi M, Mei C (2004) Endogenous salicylic acid protects rice plants from oxidative damage caused by aging as well as biotic and abiotic stress. Plant J 40:909–919
81. Yoshida S, Ito M, Nishida I, Watanabe A (2002) Identification of a novel gene HYS1/CPR5 that has a repressive role in the induction of leaf senescence and pathogen-defence responses in Arabidopsis thaliana. Plant J 29:427–437
82. Yu IC, Parker J, Bent AF (1998) Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant. Proc Natl Acad Sci USA 95:7819–7824
83. Zhao HJ, Zhao XJ, Ma PF, Wang YX, Hu WW, Li LH, Zhao YD (2011) Effects of salicylic acid on protein kinase activity and chloroplast D1 protein degradation in wheat leaves subjected to heat and high light stress. Acta Ecol Sinica 31:259–263