Skip to main content
SpringerLink
Log in

Role of salicylic acid in alleviating photochemical damage and autophagic cell death induction of cadmium stress in Arabidopsis thaliana

  • Paper
  • Published:
Photochemical & Photobiological Sciences Aims and scope Submit manuscript

Abstract

As a widespread pollutant in the environment, cadmium (Cd) would be accumulated in leaves and cause phytotoxic effect on plants. Salicylic acid (SA), a natural signal molecule, plays an important role in eliciting specific responses to biotic and abiotic stresses. In our case, the effect of SA on Cd-induced photochemical damage and cell death in Arabidopsis was studied. The results illustrated that Cd could cause a series of physiological events such as chloroplast structure change (e.g. irregular mesophyll cell as well as ultrastructure change), reactive oxygen species (ROS) production and cell death. Furthermore, chlorophyll fluorescence parameters (Fv/Fm, qN and ETR) showed a rapid decrease in wild-type (WT) Arabidopsis after treatment with 50 µM CdCl2, identical with the change in chlorophyll delayed fluorescence (DF) intensity. The changes of these parameters showed the damage of Cd toxicity to photosynthetic apparatus. We found that cell death might be autophagic cell death, which might be caused by Cd toxicity induced oxidative stress just like photosynthetic damage. The NahG plants with lower SA accumulation level showed more sensitivity to Cd toxicity, although they exhibited a decrease both in chlorophyll fluorescence parameters and DF intensity. Exogenously SA prevented the Cd-induced photochemical efficiency decrease and mitigated Cd toxicity. Additionally, SA pretreatment could alleviate Cd-induced ROS overproduction. In conclusion, our results suggested that SA could prevent Cd-induced photosynthetic damage and cell death, which might be due to the inhibition of ROS overproduction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. C. Alice, A. K. Elizabeth and I. S. Julian, An improved grafting technique for mature Arabidopsis plants demonstrates long-distance shoot-to-root transport of phytochelatins in Arabidopsis, Plant Physiol., 2006, 141, 108–120.

    Article  CAS  Google Scholar 

  2. M. K. Joshi and P. Mohanty, Chlorophyll a fluorescence as a probe of heavy metal ion toxicity in plants, in: G. C. Papageorgiou (ed.): Chlorophyll a Fluorescence: Signature of Photosynthesis. Springer, Dordrecht, 2004, pp. 637–637.

    Chapter  Google Scholar 

  3. E. Franco, S. Alessandrelli, J. Masojidek, A. Margonelli and M. T. Giardi, Modulation of D1 protein turnover under cadmium and heat stresses monitored by [35S] methionine incorporation, Plant Sci., 1999, 144, 53–61.

    Article  CAS  Google Scholar 

  4. C. M. Lu, N. W. Qiu, B. S. Wang and J. H. Zhang, Salinity treatment shows no effects on photosystem II photochemistry, but increases the resistance of photosystem II to heat stress in halophyte Suaeda salsa, J. Exp. Bot., 2003, 54, 851–860.

    Article  CAS  PubMed  Google Scholar 

  5. H. Küpper, F. Küpper and M. Spiller, Environmental relevance of heavy metal substituted chlorophylls using the example of water plants, J. Exp. Bot., 1996, 47, 259–266.

    Article  Google Scholar 

  6. T. Baszynski, L. Wajda, M. Krol, D. Wolinska, Z. Krupa and A. Tukendrof, Photosynthetic activities of cadmium treated tomato plants, Plant Physiol., 1980, 98, 365–370.

    Article  Google Scholar 

  7. M. C. Romero-Puertas, M. Rodriguez-Serrano, F. J. Corpas, M. Gómez, L. A. Delrío and L. M. Sandalio, Cadmium-induced subcel-lular accumulation of O2-and H2O2 in pea leaves, Plant, Cell Environ., 2004, 27, 1122–1134.

    Article  CAS  Google Scholar 

  8. R. Mittle, Oxidative stress, antioxidants and stress tolerance [J], Trends Plant Sci., 2002, 7, 405–410.

    Article  Google Scholar 

  9. A. Krantev, R. Yordanova, T. Janda, G. Szalaib and L. Popova, Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants, J. Plant Physiol., 2008, 165, 920–931.

    Article  CAS  PubMed  Google Scholar 

  10. O. Borsani, V. Valpuesta and M. A. Botella, Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings, Plant Physiol., 2001, 126, 1024–1030.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. J. F. Dat, C. H. Foyer and I. M. Scott, Changes in salicylic acid and antioxidants during induced thermotolerance in mustard seedlings, Plant Physiol., 1998, 118, 1455–1461.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. T. Senaratna, D. Touchell, E. Bunns and K. Dixon, Acetyl salicylic acid (aspirin) and salicylic acid induce multiple stress tolerance in bean and tomato plants, Plant Growth Regul., 2000, 30, 157–161.

    Article  CAS  Google Scholar 

  13. T. G. Janda, I. T. Szalai and E. Padi, Hydroponic treatment with salicylic acid decrease the effects of chilling injury in maize (Zea mays L.) plant, Planta, 1999, 208, 175–180.

    Article  CAS  Google Scholar 

  14. A. Mishra and M. A. Chudhuri, Effect of salicylic acid on heavy metal-induced membrane deterioration in rice, Biol. Plant., 1999, 42, 409–415.

    Article  CAS  Google Scholar 

  15. A. Metwally, I. Finkermeier, M. Georgi and K. J. Dietz, Salicylic acid alleviates the cadmium toxicity in barley seedlings, Plant Physiol., 2003, 132, 272–281.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. M. Pal, G. Szalai, E. Horvath, T. Janda and E. Paldi, Effect of salicylic acid during heavy metal stress, Proc. 7th Hungarian Congress Plant Physiol., 2002, 46, 119–120.

    Google Scholar 

  17. G. Drazic and N. Mihailovic, Modification of cadmium toxicity in soybean seedlings by salicylic acid, Plant Sci., 2005, 168, 511–517.

    Article  CAS  Google Scholar 

  18. K. Yoshimoto, Y. Takano and Y. Sakai, Autophagy in plants and phytopathogens, FEBS Lett., 2010, 584, 1350–1358.

    Article  CAS  PubMed  Google Scholar 

  19. H. E. Tao, H. J. Wang and Y. Z. Tan, The roles of autophagy in cell survival and cell death, Prog. Physiol. Sci., 2008, 39, 37–40.

    Google Scholar 

  20. B. Mauch-Mani and A. J. Slusarenko, Production of salicylic acid precursors is a major function of phenylalanine ammonialyase in the resistance of Arabidopsis to Peronospora parasitica, Plant Cell, 1996, 8, 203–212.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. L. R. Zhang, D. Xing and J. S. Wang, A non-invasive and real-time monitoring of the regulation of photosynthetic metabolism biosensor based on measurement of delayed fluorescence in vivo, Sensors, 2007, 7, 52–66.

    Article  CAS  PubMed Central  Google Scholar 

  22. K. B. Bonfig, U. Schreiber, A. Gabler, T. Roitsch and S. Berger, Infection with virulent and avirulent P.syringae strains differentially affects photosynthesis and sink metabolism in Arabidopsis leaves, Planta, 2006, 225, 1–12.

    Article  CAS  PubMed  Google Scholar 

  23. L. R. Zhang, Q. X. Xu, D. Xing, C. J. Gao and H. W. Xiong, Realtime detection of Caspase-3-like protease activation in vivo using fluorescence resonance energy transfer during plant programmed cell death induced by ultraviolet C overexposure, Plant Physiol., 2009, 150, 1773–1783.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Y. H. Bi, W. L. Chen, W. N. Zhang, Q. Zhou, L. J. Yun and D. Xing, Production of reactive oxygen species, impairment of photosynthetic function and dynamic changes in mitochondria are early events in cadmium induced cell death in Arabidopsis thaliana, Biol. Cell, 2009, 101, 629–643.

    Article  CAS  PubMed  Google Scholar 

  25. C. J. Gao, D. Xing, L. L. Li and L. R. Zhang, Implication of reactive oxygen species and mitochondrial dysfunction in the early stages of plant programmed cell death induced by ultraviolet-C overexposure, Planta, 2007, 227, 755–767.

    Article  CAS  PubMed  Google Scholar 

  26. Y. Moriyasu, M. Hattori, G. Y. Jauh and J. C. Rogers, Alpha tonoplast intrinsic protein is specifically associated with vacuole membrane involved in an autophagic process, Plant Cell Physiol., 2003, 44, 795–802.

    Article  CAS  PubMed  Google Scholar 

  27. L. P. Popova, L. T. Maslenkova, R. Y. Yordanova, A. P. Ivanova, A. P. Krantev, G. Szalai and T. Janda, Exogenous treatment with salicylic acid attenuates cadmium toxicity in pea seedlings, Plant Physiol. Biochem., 2009, 47, 224–231.

    Article  CAS  PubMed  Google Scholar 

  28. L. A. Belkhadi, H. Hediji, Z. Abbes, I. Nouairi, Z. Barhoumi, M. Zarrouk, W. ChaIbi and W. Djebali, Effects of exogenous salicylic acid pre-treatment on cadmium toxicity and leaf lipid content in Linum usitatissimum L, Ecotoxicol. Environ. Saf., 2010, 73, 1004–1011.

    Article  CAS  PubMed  Google Scholar 

  29. H. R. Moussa and S. M. El-Gamal, Effect of salicylic acid pretreatment on cadmium toxicity in wheat, Biol. Plant., 2010, 54, 315–320.

    Article  CAS  Google Scholar 

  30. K. Apel and H. Hirt, Reactive oxygen species: metabolism, oxidative stress, and signal transduction, Annu. Rev. Plant Biol., 2004, 55, 373–399.

    Article  CAS  PubMed  Google Scholar 

  31. W. Jakubowski and G. Bartosz, 2,7-Dichlorofluorescein oxidation and reactive oxygen species: what does it measure?, Cell Biol. Int., 2000, 24, 757–760.

    Article  CAS  PubMed  Google Scholar 

  32. L. S. di Toppi and R. Gabbrielli, Response to cadmium in higher plants, Environ. Exp. Bot., 1999, 41, 105–130.

    Article  Google Scholar 

  33. I. McCarthy, M. C. Romero-Puertas, J. M. Palma, L. M. Sandalio, F. J. Corpas, M. Gómez and L. A. Delrío, Cadmium induces senescence symptoms in leaf peroxisomes of pea plants, Plant, Cell Environ., 2001, 24, 1065–1073.

    Article  CAS  Google Scholar 

  34. B. Guo, Y. C. Liang and Y. G. Zhu, Does salicylic acid regulate antioxidant defense system, cell death, cadmium uptake and partitioning to acquire cadmium tolerance in rice?, J. Plant Physiol., 2009, 166, 20–31.

    Article  CAS  PubMed  Google Scholar 

  35. G. Ouzounidou, M. Moustakas and E. P. Eleftheriou, Physiological and ultrastructural effects of cadmium on wheat (Triticum aestivum L.) leaves, Arch. Environ. Contam. Toxicol., 1997, 32, 154–160.

    Article  CAS  PubMed  Google Scholar 

  36. D. H. Yang, The effects of heavy metals on the structure and function of photosynthetic membranes in higher plants, Chin. Bull. Bot., 1991, 8, 26–29.

    Google Scholar 

  37. L. M. Sandalio, H. C. Dalurzo, M. Gomez, M. C. Romero-Puertas and L. A. del Rio, Cadmiun-induced changes in the growth and oxidative metabolism of pea plants, J. Exp. Bot., 2001, 52, 2115–2126.

    Article  CAS  PubMed  Google Scholar 

  38. J. Soukupová, S. Smatanová, L. Nedbal and A. Jegorov, Plant response to destruxins visualized by imaging of chlorophyll fluorescence, Physiol. Plant., 2003, 118, 399–405.

    Article  Google Scholar 

  39. B. Gielen, H. J. De Boeck, C. M. H. M. Lemmens, R. Valcke, I. Nijs and R. Ceulemans, Grassland species will not necessarily benefit from future elevated air temperatures: a chlorophyll fluorescence approach to study autumn physiology, Physiol. Plant., 2005, 125, 52–63.

    Article  CAS  Google Scholar 

  40. B. Guo, Y. C. Liang, Y. G. Zhu and F. J. Zhao, Role of salicylic acid in alleviating oxidative damage in rice roots (Oryza sativa) subjected to cadmium stress, Environ. Pollut., 2007, 147, 743–749.

    Article  CAS  PubMed  Google Scholar 

  41. M. J. Lenardo, C. K. McPhee and L. Yu, Autophagic cell death, Methods Enzymol., 2009, 453, 71–31.

    Google Scholar 

  42. Q. H. Shi and Z. J. Zhu, Effects of exogenous salicylic acid on manganese toxicity, element contents and antioxidantive system in cucumber, Environ. Exp. Bot., 2008, 63, 317–326.

    Article  CAS  Google Scholar 

  43. T. P. Delaney, S. Uknes, B. Vernooij, L. Friedrich, K. Weymann, D. Negrotto, T. Gaffney, M. Gut-Rella, H. Kessmann, E. Ward and J. Ryals, A central role of salicylic acid in plant disease resistance, Science, 1994, 266, 1247–1246.

    Article  CAS  PubMed  Google Scholar 

  44. T. C. Dinis, V. M. Maderia and L. M. Almeida, Action of phenolic derivates (acetaminophen, salicylate, and 5-aminosalicylate) as inhibitors of membrane lipid peroxidation and as peroxyl radical scavengers, Arch. Biochem. Biophys., 1994, 315, 161–169.

    Article  CAS  PubMed  Google Scholar 

  45. L. P. Popova, L. T. Maslenkova, R. Y. Yordanova, A. P. Ivanova, A. P. Krantev, G. Szalai and T. Janda, Exogenous treatment with salicylic acid attenuates cadmium toxicity in pea seedlings, Plant Physiol. Biochem., 2009, 47, 224–231.

    Article  CAS  PubMed  Google Scholar 

  46. M. S. Zawoznik, M. D. Groppa, M. L. Tomaro and M. P. Benavides, Endogenous salicylic acid potentiates cadmium-induced oxidative stress in Arabidopsis thaliana, Plant Sci., 2007, 173, 190–197.

    Article  CAS  Google Scholar 

  47. D. Bassham, Plant autophagy—more than a starvation response, Curr. Opin. Plant Biol., 2007, 10, 587–593.

    Article  CAS  PubMed  Google Scholar 

  48. S. Shimizu, T. Kanaseki, N. Mizushima, T. Mizuta, S. Arakawa-Kobayashi, C. B. Thompson and Y. Tsujimoto, Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes, Nat. Cell Biol., 2004, 6, 1221–1228.

    Article  CAS  PubMed  Google Scholar 

  49. L. Yu, A. Alva, H. Su, P. Dutt, E. Freundt, S. Welsh, E. H. Baehrecke and M. J. Lenardo, Regulation of an ATG7-beclin1 program of autophagic cell death by caspase-8, Science, 2004, 304, 1500–1502.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. MOE Key Laboratory of Laser Life Science and Institute of Laser Life Science, South China Normal University, Guangzhou, 510631, China

    WeiNa Zhang & WenLi Chen

  2. College of Life Science, Guangdong Key Lab of Biotechnology for Plant Development, South China Normal University, Guangzhou, 510631, China

    WenLi Chen

Authors
  1. WeiNa Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. WenLi Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to WenLi Chen.

Additional information

Electronic supplementary information (ESI) available. See DOI: 10.1039/c0pp00305k

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, W., Chen, W. Role of salicylic acid in alleviating photochemical damage and autophagic cell death induction of cadmium stress in Arabidopsis thaliana. Photochem Photobiol Sci 10, 947–955 (2011). https://doi.org/10.1039/c0pp00305k

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/c0pp00305k

Search

Navigation