Svoboda | Graniru | BBC Russia | Golosameriki | Facebook

Photosynthetica 2019, 57(2):367-376 | DOI: 10.32615/ps.2019.040

Effects of salicylic acid on photosynthetic activity and chloroplast morphology under light and prolonged darkness

P. POÓR1, P. BORBÉLY1, N. BÓDI2, M. BAGYÁNSZKI2, I. TARI1
1 Department of Plant Biology, University of Szeged, H-6726 Szeged, Közép fasor 52, Hungary
2 Department of Physiology, Anatomy and Neuroscience, University of Szeged, H-6726 Szeged, Közép fasor 52, Hungary

Salicylic acid (SA) is a key component of plant defence, which exerts a concentration-dependent effect on photosynthesis under multi-faceted influence of light. Photosynthetic activities and chloroplast morphology were studied in tomato plants after treatment with a sublethal, 0.1 mM, and a cell death-inducing, 1 mM concentrations of SA under normal photoperiod during light phase and after a prolonged dark phase. SA (1 mM) decreased the maximal (Fv/Fm) and effective quantum yields of PSII [Y(II)] and PSI [Y(I)] under both environmental conditions, however, the photoprotective processes were not significantly different between light and dark samples. Decrease in grana height, thylakoid dilation and deformation of lumen were also observed in the light. In contrast to illuminated samples, 0.1 mM SA decreased Y(II) and Y(I) after dark incubation, but nonphotochemical energy dissipation and cyclic electron flow increased, suggesting that the photoprotective mechanisms could be activated in plants exposed to prolonged darkness.

Additional key words: carotenoid; nonphotochemical quenching; photosystem II and I; soluble sugar; starch.

Received: March 13, 2018; Accepted: October 22, 2018; Prepublished online: February 4, 2019; Published: May 16, 2019  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
POÓR, P., BORBÉLY, P., BÓDI, N., BAGYÁNSZKI, M., & TARI, I. (2019). Effects of salicylic acid on photosynthetic activity and chloroplast morphology under light and prolonged darkness. Photosynthetica57(2), 367-376. doi: 10.32615/ps.2019.040
Download citation

References

  1. Ballaré C.L.: Light regulation of plant defense. - Annu. Rev. Plant Biol. 65: 335-363, 2014. Go to original source...
  2. Belkadhi A., De Haro A., Obregon S. et al.: Exogenous salicylic acid protects phospholipids against cadmium stress in flax (Linum usitatissimum L.). - Ecotox. Environ. Safe. 120: 102-109, 2015. Go to original source...
  3. Cerrudo I., Keller M.M., Cargnel M.D. et al.: Low red/far-red ratios reduce Arabidopsis resistance to Botrytis cinerea and jasmonate responses via a COI1-JAZ10-dependent, salicylic acid-independent mechanism. - Plant Physiol. 158: 2042-2052, 2012. Go to original source...
  4. Chandra-Shekara A.C., Gupte M., Navarre D. et al.: Light-dependent hypersensitive response and resistance signaling against Turnip Crinkle Virus in Arabidopsis. - Plant J. 45: 320-334, 2006. Go to original source...
  5. Chen Y.E., Cui J.M., Li G.X. et al.: Effect of salicylic acid on the antioxidant system and photosystem II in wheat seedlings. - Biol. Plantarum 60: 139-147, 2016. Go to original source...
  6. Cheng D.D., Liu M.J., Sun X.B. et al.: Light suppresses bacterial population through the accumulation of hydrogen peroxide in tobacco leaves infected with Pseudomonas syringae pv. tabaci. - Front Plant Sci. 7: 512, 2016. Go to original source...
  7. de Wit M., Spoel S.H., Sanchez-Perez G.F. et al.: Perception of low red:far-red ratio compromises both salicylic acid- and jasmonic acid-dependent pathogen defences in Arabidopsis. - Plant J. 75: 90-103, 2013. Go to original source...
  8. Fariduddin Q., Hayat S., Ahmad A.: Salicylic acid influences net photosynthetic rate, carboxylation efficiency, nitrate reductase activity, and seed yield in Brassica juncea. - Photosynthetica 41: 281-284, 2003. Go to original source...
  9. Gao Y., Liu W., Wang X. et al.: Comparative phytotoxicity of usnic acid, salicylic acid, cinnamic acid and benzoic acid on photosynthetic apparatus of Chlamydomonas reinhardtii. - Plant Physiol Bioch. 128: 1-12, 2018. Go to original source...
  10. Gebauer P., Korn M., Engelsdorf T. et al.: Sugar accumulation in leaves of Arabidopsis sweet11/sweet12 double mutants enhances priming of the salicylic acid-mediated defense response. - Front. Plant Sci. 8: 1378, 2017. Go to original source...
  11. Genty B., Briantais J.M., Baker N.R.: The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. - ‎Biochim. Biophys. Acta 990: 87-92, 1989. Go to original source...
  12. Goodspeed D., Chehab E.W., Min-Venditti A. et al.: Arabidopsis synchronizes jasmonate-mediated defense with insect circa-dian behavior. - P. Natl. Acad. Sci. USA 109: 4674-4677, 2012. Go to original source...
  13. Griebel T., Zeier J.: Light regulation and daytime dependency of inducible plant defenses in Arabidopsis: phytochrome signaling controls systemic acquired resistance rather than local defense. - Plant Physiol. 147: 790-801, 2008. Go to original source...
  14. Habibi G.: Exogenous salicylic acid alleviates oxidative damage of barley plants under drought stress. - Acta Biol. Szeged 56: 57-63, 2012.
  15. Hansen J., Møller I.: Percolation of starch and soluble carbo-hydrates from plant tissue for quantitative determination with anthrone. - Anal. Biochem. 68: 87-94, 1975. Go to original source...
  16. Hayat S., Masood A., Yusuf M. et al.: Growth of Indian mustard (Brassica juncea L.) in response to salicylic acid under high-temperature stress. - Braz. J. Plant Physiol. 21: 187-195, 2009. Go to original source...
  17. Hayat Q., Hayat S., Irfan M., Ahmad A.: Effect of exogenous salicylic acid under changing environment: A review. - Environ. Exp. Bot. 68: 14-25, 2010. Go to original source...
  18. Herbstová M., Tietz S., Kinzel C. et al.: Architectural switch in plant photosynthetic membranes induced by light stress. - P. Natl. Acad. Sci. USA 109: 20130-20135, 2012. Go to original source...
  19. Horváth E., Szalai G., Janda T.: Induction of abiotic stress tolerance by salicylic acid signaling. - J. Plant Growth Regul. 26: 290-300, 2007. Go to original source...
  20. Iwai M., Yokono M., Nakano A.: Visualizing structural dynamics of thylakoid membranes. - Sci. Rep.-UK 4: 3768, 2014. Go to original source...
  21. Jahns P., Holzwarth A.R.: The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. - ‎Biochim. Biophys. Acta 1817: 182-193, 2012. Go to original source...
  22. Janda K., Hideg É., Szalai G. et al.: Salicylic acid may indirectly influence the photosynthetic electron transport. - J. Plant Physiol. 169: 971-978, 2012. Go to original source...
  23. Janda T., Gondor O.K., Yordanova R. et al.: Salicylic acid and photosynthesis: signalling and effects. - Acta Physiol. Plant. 36: 2537-2546, 2014. Go to original source...
  24. Janda T., Szalai G., Leskó K. et al.: Factors contributing to enhanced freezing tolerance in wheat during frost hardening in the light. - Phytochemistry 68: 1674-1682, 2007. Go to original source...
  25. Kangasjärvi S., Neukermans J., Li S. et al.: Photosynthesis, photorespiration, and light signalling in defence responses. - J. Exp. Bot. 63: 1619-1636, 2012. Go to original source...
  26. Karpiński S., Szechyńska-Hebda M., Wituszyńska W., Burdiak P.: Light acclimation, retrograde signalling, cell death and immune defences in plants. - Plant Cell Environ. 36: 736-744, 2013. Go to original source...
  27. Kazan K., Manners J.M.: The interplay between light and jasmo-nate signalling during defence and development. - J. Exp. Bot. 62: 4087-4100, 2011. Go to original source...
  28. Kegge W., Weldegergis B.T., Soler R. et al.: Canopy light cues affect emission of constitutive and methyl jasmonate-induced volatile organic compounds in Arabidopsis thaliana. - New Phytol. 200: 861-874, 2013. Go to original source...
  29. Khan M.I.R., Fatma M., Per T.S. et al.: Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. - Front. Plant Sci. 6: 462, 2015. Go to original source...
  30. Kim E H., Li X.P., Razeghifard R. et al.: The multiple roles of light-harvesting chlorophyll a/b-protein complexes define structure and optimize function of Arabidopsis chloroplasts: a study using two chlorophyll b-less mutants. - Biochim. Biophys. Acta 1787: 973-984, 2009. Go to original source...
  31. Kirchhoff H.: Structural changes of the thylakoid membrane network induced by high light stress in plant chloroplasts. - Philos. T. Roy. Soc. B 369: 20130225, 2014. Go to original source...
  32. Kirchhoff H., Hall C., Wood M. et al.: Dynamic control of protein diffusion within the granal thylakoid lumen. - P. Natl. Acad. Sci. USA 108: 20248-20253, 2011. Go to original source...
  33. Klughammer C., Schreiber U.: Saturation pulse method for assessment of energy conversion in PS I. - Planta 192: 261-268, 1994. Go to original source...
  34. Kramer D.M., Johnson G., Kiirats O., Edwards G.E.: New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. - Photosynth. Res. 79: 209-218, 2004. Go to original source...
  35. Krantev A., Yordanova R., Janda T. et al.: Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. - J. Plant Physiol. 165: 920-931, 2008. Go to original source...
  36. Lei Y.B., Zheng Y.L., Dai K.J. et al.: Different responses of photosystem I and photosystem II in three tropical oilseed crops exposed to chilling stress and subsequent recovery. - Trees 28: 923-933, 2014. Go to original source...
  37. Lichtenthaler H.K., Wellburn A.R.: Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. - Biochem. Soc. T. 11: 591-592, 1983. Go to original source...
  38. Loake G., Grant M.: Salicylic acid in plant defence - the players and protagonists. - Curr. Opin. Plant Biol. 10: 466-472, 2007. Go to original source...
  39. López-Goldar X., Sampedro L., Zas R.: Carbon starvation by light deprivation does not constrain the ability of young pines to produce induced chemical defences in response to a bark-chewing herbivore. - Environ. Exp. Bot. 130: 141-150, 2016. Go to original source...
  40. Mateo A., Funck D., Mühlenbock P. et al.: Controlled levels of salicylic acid are required for optimal photosynthesis and redox homeostasis. - J. Exp. Bot. 57: 1795-1807, 2006. Go to original source...
  41. Mishev K., Ananiev E.D., Humbeck K.: Organ-specific effects of dark treatment on photosynthesis and the expression of photosynthesis-related genes. - Biol. Plantarum 55: 269-278, 2011. Go to original source...
  42. Miyake C.: Alternative electron flows (water-water cycle and cyclic electron flow around PSI) in photosynthesis: molecular mechanisms and physiological functions. - Plant Cell Physiol. 51: 1951-1963, 2010. Go to original source...
  43. Moharekar S.T., Lokhande S.D., Hara T. et al.: Effect of salicylic acid on chlorophyll and carotenoid contents of wheat and moong seedlings. - Photosynthetica 41: 315-317, 2003. Go to original source...
  44. Muthamilarasan M., Prasad M.: Plant innate immunity: an updated insight into defense mechanism. - J. Bioscience 38: 433-449, 2013. Go to original source...
  45. Müller P., Li X.P., Niyogi K.K.: Non-photochemical quenching. A response to excess light energy. - Plant Physiol. 125: 1558-1566, 2001. Go to original source...
  46. O'Leary B.M., Lee C.P., Atkin O.K. et al.: Variation in leaf respiration rates at night correlates with carbohydrate and amino acid supply. - Plant Physiol. 174: 2261-2273, 2017. Go to original source...
  47. Ort D.R., Baker N.R.: A photoprotective role for O2 as an alternative electron sink in photosynthesis? - Curr. Opin. Plant Biol. 5: 193-198, 2002. Go to original source...
  48. Panchal S., Melotto M.: Stomate-based defense and environmental cues. - Plant Signal. Behav. 12: 2021-2032, 2017. Go to original source...
  49. Pancheva T.V., Popova L.P.: Effect of salicylic acid on the synthesis of ribulose-1,5-bisphosphate carboxylase/oxyge-nase in barley leaves. - J. Plant Physiol. 152: 381-386, 1998. Go to original source...
  50. Pancheva T.V., Popova L.P., Uzunova A.N.: Effects of salicylic acid on growth and photosynthesis in barley plants. - J. Plant Physiol. 149: 57-63, 1996. Go to original source...
  51. Poór P., Gémes K., Horváth F. et al.: Salicylic acid treatment via the rooting medium interferes with stomatal response, CO2 fixation rate and carbohydrate metabolism in tomato, and decreases harmful effects of subsequent salt stress. - Plant Biol. 13: 105-114, 2011. Go to original source...
  52. Poór P., Takács Z., Bela K. et al.: Prolonged dark period modulates the oxidative burst and enzymatic antioxidant systems in the leaves of salicylic acid-treated tomato. - J. Plant Physiol. 213: 216-226, 2017. Go to original source...
  53. Poór P., Tari I.: Regulation of stomatal movement and photosynthetic activity in guard cells of tomato abaxial epidermal peels by salicylic acid. - Funct. Plant Biol. 39: 1028-1037, 2012. Go to original source...
  54. Rivas-San Vicente M., Plasencia J.: Salicylic acid beyond defence: its role in plant growth and development. - J. Exp. Bot. 62: 3321-3338, 2011. Go to original source...
  55. Roberts M.R., Paul N.D.: Seduced by the dark side: integrating molecular and ecological perspectives on the influence of light on plant defence against pests and pathogens. - New Phytol. 170: 677-699, 2006. Go to original source...
  56. Rocha J., Nitenberg M., Girard-Egrot A. et al.: Do galactolipid synthases play a key role in the biogenesis of chloroplast membranes of higher plants? - Front. Plant Sci. 9: 126, 2018. Go to original source...
  57. Roháček K., Barták M.: Technique of the modulated chlorophyll fluorescence: basic concepts, useful parameters, and some applications. - Photosynthetica 37: 339-363, 1999. Go to original source...
  58. Schreiber U., Klughammer C.: Non-photochemical fluorescence quenching and quantum yields in PS I and PS II: analysis of heat-induced limitations using Maxi-Imaging-PAM and Dual-PAM-100. - PAM Application Notes 1: 15-18, 2008.
  59. Suárez-Vidal E., López-Goldar X., Sampedro L., Zas R.: Effect of light availability on the interaction between maritime pine and the pine weevil: Light drives insect feeding behavior but also the defensive capabilities of the host. - Front. Plant Sci. 8: 1452, 2017. Go to original source...
  60. Takács Z., Poór P., Tari I.: Comparison of polyamine metabolism in tomato plants exposed to different concentrations of salicylic acid under light or dark conditions. - Plant Physiol. Bioch. 108: 266-278, 2016. Go to original source...
  61. Takahashi S., Milward S.E., Fan D.Y. et al.: How does cyclic electron flow alleviate photoinhibition in Arabidopsis? - Plant Physiol. 149: 1560-1567, 2009. Go to original source...
  62. Talapka P., Berkó A., Nagy L.I. et al.: Structural and molecular features of intestinal strictures in rats with Crohn's-like disease. - World J. Gastroentero. 22: 5154-5164, 2016. Go to original source...
  63. Uzunova A.N., Popova L.P.: Effect of salicylic acid on leaf anatomy and chloroplast ultrastructure of barley plants. - Photosynthetica 38: 243-250, 2000. Go to original source...
  64. van Doorn W.G.: Is the onset of senescence in leaf cells of intact plants due to low or high sugar levels? - J. Exp. Bot. 59: 1963-1972, 2008. Go to original source...
  65. Vos I.A., Pieterse C.M.J., Wees S.C.M.: Costs and benefits of hormone-regulated plant defences. - Plant Pathol. 62: 43-55, 2013. Go to original source...
  66. Zhang G., Liu Y., Ni Y. et al.: Exogenous calcium alleviates low night temperature stress on the photosynthetic apparatus of tomato leaves. - PloS ONE 9: doi:org/10.1371/journal.pone.0097322, 2014. Go to original source...
  67. Zhao H.J., Zhao X.J., Ma P.F. et al.: 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. Sin. 31: 259-263, 2011. Go to original source...