Ukr.Biochem.J. 2021; Volume 93, Issue 3, May-Jun, pp. 39-48


The effect of CO donor hemin on the antioxidant and osmoprotective systems state in Arabidopsis of a wild-type and mutants defective in jasmonate signaling under salt stress

M. A. Shkliarevskyi1, Yu. E. Kolupaev1,2*, T. O. Yastreb1,
Yu. V. Karpets1, A. P. Dmitriev3

1Dokuchaev Kharkiv National Agrarian University, Ukraine;
2Karazin Kharkiv National University, Ukraine;
3Institute of Cell Biology and Genetic Engineering, National Academy of Sciences of Ukraine, Kyiv;

Received: 6 December 2020; Accepted: 17 May 2021

The role of the gasotransmitter carbon monoxide (CO) in signaling and adaptive processes in plants has been studied insufficiently. There are indirect data indicating jasmonate signaling participation in realization of CO effects, but  the possible connection between carbon monoxide and jasmonate signaling during plant adaptation to salt stress remains unclear. We studied the carbon monoxide donor hemin effect on the Arabidopsis of a wild-type (Col-0) and defective in jasmonate signaling coi1 and jin1 mutants response to the salt stress.  Arabidopsis thaliana 4-week-old plants were grown on a modified Hoagland’s medium. Plants were incubated for 24 h in usual or 2 µM hemin containing culture medium, then transferred to 150 mM NaCl containing media and incubated for 24 h before the medium was replaced with the usual one. It was shown that salt stress caused water deficiency and superoxide dismutase and catalase activity decrease in the plants of all three genotypes. Treatment with 2 μM hemin stabilized the levels of catalase activity and  photosynthetic pigments and increased guaiacol peroxidase activity in a wild-type, but not in  coi1 and jin1 mutant plants after  stress induction. Treated with hemin wild-type Arabidopsis plants accumulated more proline and sugars in response to stress than treated coi1 and jin1 mutants. It was concluded that jasmonate signaling can be involved in adaptive processes induced by exogenous carbon monoxide.

Keywords: , , , , , , ,


  1. Sukmansky OI, Reutov VP. Gasotransmitters: Physiological Role and Involvement in the Pathogenesis of the Diseases. Usp Fiziol Nauk. 2016;47(3):30-58. (In Russian). PubMed
  2. Jin Q, Cui W, Xie Y, Shen W. Carbon monoxide: A ubiquitous gaseous signaling molecule in plants. In: Lamattina L, Garcia-Mata C (eds). Gasotransmitters in Plants, Signaling and Communication in Plants, Switzerland: Springer International Publishing, 2016: 3-19.  CrossRef
  3. Kolupaev YuE, Karpets YuV, Beschasniy SP, Dmitriev AP. Gasotransmitters and their role in adaptive reactions of plant cells. Cytol Genet. 2019; 53(5): 392-406.  CrossRef
  4. He H, He L. The role of carbon monoxide signaling in the responses of plants to abiotic stresses. Nitric Oxide. 2014;42:40-43. PubMed, CrossRef
  5. Wang R. Gasotransmitters: growing pains and joys. Trends Biochem Sci. 2014;39(5):227-232. PubMed, CrossRef
  6. Khan MN, Mobin M, Abbas ZK. Nitric oxide and high temperature stress: A physiological perspective. In: Khan MN. et al (ed). Nitric Oxide Action in Abiotic Stress Responses in Plants. Switzerland: Springer International Publishing, 2015: 77-93.  CrossRef
  7. Li L, Wei S, Shen W. The role of methane in plant physiology: a review. Plant Cell Rep. 2020;39(2):171-179. PubMed, CrossRef
  8. Chen Y, Wang M, Hu L, Liao W, Dawuda MM, Li C. Carbon Monoxide Is Involved in Hydrogen Gas-Induced Adventitious Root Development in Cucumber under Simulated Drought Stress. Front Plant Sci. 2017;8:128. PubMed, PubMedCentral, CrossRef
  9. Hancock JT. Hydrogen sulfide and environmental stresses. Environ Exp Bot. 2019; 161: 50-56. CrossRef
  10. Liu Y, Xu S, Ling T, Xu L, Shen W. Heme oxygenase/carbon monoxide system participates in regulating wheat seed germination under osmotic stress involving the nitric oxide pathway. J Plant Physiol. 2010;167(16):1371-1379. PubMed, CrossRef
  11. Wei MY, Chao YY, Kao CH. NaCl-induced heme oxygenase in roots of rice seedlings is mediated through hydrogen peroxide. Plant Growth Regul. 2013;69(3):209-214. CrossRef
  12. Verma K, Dixit S, Shekhawat GS, Alam A. Antioxidant activity of heme oxygenase 1 in Brassica juncea (L.) Czern. (Indian mustard) under salt stress. Turk J Biol. 2015; 39: 540-549.  CrossRef
  13. Zhang C, Li Y, Yuan F, Hu S, He P. Effects of hematin and carbon monoxide on the salinity stress responses of Cassia obtusifolia L. seeds and seedlings. Plant Soil. 2012;359(1-2):85-105. CrossRef
  14. Chen Q, Gong C, Ju X, Zhu Z, Shen W, Shen Z, Cui J. Hemin through the heme oxygenase 1/ferrous iron, carbon monoxide system involved in zinc tolerance in Oryza sativa L. J Plant Growth Regul. 2018;37(3):947-957.  CrossRef
  15. Shkliarevskyi MA, Karpets YuV, Kolupaev YuE, Lugovaya AA, Dmitriev AP. Calcium-dependent changes in cellular redox homeostasis and heat resistance of wheat plantlets under influence of hemin (carbon monoxide donor). Cytol Genet. 2020;54(6):522-530.  CrossRef
  16. Xu S, Sa ZS, Cao ZY, Xuan W, Huang BK, Ling TF, Hu QY, Shen WB. Carbon monoxide alleviates wheat seed germination inhibition and counteracts lipid peroxidation mediated by salinity. J Integr Plant Biol. 2006;48(10):1168-1176. CrossRef
  17. Ling T, Zhang B, Cui W, Wu M, Lin J, Zhou W, Huang J, Shen W. Carbon monoxide mitigates salt-induced inhibition of root growth and suppresses programmed cell death in wheat primary roots by inhibiting superoxide anion overproduction. Plant Sci. 2009;177(4):331-340. CrossRef
  18. Xie Y, Ling T, Han Y, Liu K, Zheng Q, Huang L, Yuan X, He Z, Hu B, Fang L, Shen Z, Yang Q, Shen W. Carbon monoxide enhances salt tolerance by nitric oxide-mediated maintenance of ion homeostasis and up-regulation of antioxidant defence in wheat seedling roots. Plant Cell Environ. 2008;31(12):1864-1881. PubMed, CrossRef
  19. Yuan XX, Wang J, Xie YJ, Shen WB. Effects of carbon monoxide on salt tolerance and proline content of roots in wheat seedling. Plant Physiol. Commun. 2009; 45(6): 567-570.
  20. Shan C, Wang T, Zhou Y, Wang W. Hydrogen sulfide is involved in the regulation of ascorbate and glutathione metabolism by jasmonic acid in Arabidopsis thaliana. Biol Plant. 2018;62(1):188-193. CrossRef
  21. Huang X, Stettmaier K, Michel C, Hutzler P, Mueller MJ, Durner J. Nitric oxide is induced by wounding and influences jasmonic acid signaling in Arabidopsis thaliana. Planta. 2004;218(6):938-946.
    PubMed, CrossRef
  22. Banerjee A, Tripathi DK, Roychoudhury A. Hydrogen sulphide trapeze: Environmental stress amelioration and phytohormone crosstalk. Plant Physiol Biochem. 2018;132:46-53.
    PubMed, CrossRef
  23. Cheng T, Hu L, Wang P, Yang X, Peng Y, Lu Y, Chen J, Shi J. Carbon Monoxide Potentiates High Temperature-Induced Nicotine Biosynthesis in Tobacco. Int J Mol Sci. 2018;19(1):188.
    PubMed, PubMedCentral, CrossRef
  24. Ton J, Flors V, Mauch-Mani B. The multifaceted role of ABA in disease resistance. Trends Plant Sci. 2009;14(6):310-317.
    PubMed, CrossRef
  25. Lackman P, González-Guzmán M, Tilleman S, Carqueijeiro I, Pérez AC, Moses T, Seo M, Kanno Y, Häkkinen ST, Van Montagu MC, Thevelein JM, Maaheimo H, Oksman-Caldentey KM, Rodriguez PL, Rischer H, Goossens A. Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco. Proc Natl Acad Sci USA. 2011;108(14):5891-5896.
    PubMed, PubMedCentral, CrossRef
  26. Palmieri MC, Sell S, Huang X, Scherf M, Werner T, Durner J, Lindermayr C. Nitric oxide-responsive genes and promoters in Arabidopsis thaliana: a bioinformatics approach. J Exp Bot. 2008;59(2):177-186.
    PubMed, CrossRef
  27. Yastreb TO, Kolupaev YuE, Shkliarevskyi MA, Dmitriev AP. Participation of jasmonate signaling components in the development of Arabidopsis thaliana’s salt resistance induced by H2S and NO donors. Russ J Plant Physiol. 2020;67(5):827-834.
  28. Babenko LM, Shcherbatiuk MM, Skaterna TD, Kosakivska IV. Lipoxygenases and their metabolites in formation of plant stress tolerance. Ukr Biochem J. 2017;89(1):5-21.
    PubMed, CrossRef
  29. Kolupaev YuE, Yastreb TO. Jasmonate signaling and plant adaptation to abiotic stressors (Review). Appl Biochem Microbiol. 2021;57(1):1-19.
  30. Yastreb ТО, Kolupaev YuE, Shvidenko NV, Dmitriev AP. Action of methyl jasmonate and salt stress on antioxidant system of Arabidopsis plants defective in jasmonate signaling genes. Ukr Biochem. J. 2018; 90(5): 50-59.
  31. Rozentsvet OA, Nesterov VN, Bogdanova ES. Structural, physiological, and biochemical aspects of salinity tolerance of halophytes. Russ J Plant Physiol. 2017; 64(4): 251-265.
  32.  Semchuk NM, Vasylyk YV, Lushchak OV, Lushchak VI. Effect of short-term salt stress on oxidative stress markers and antioxidant enzymes activity in tocopherol-deficient Arabidopsis thaliana plants. Ukr Biokhim Zhurn. 2012;84(4):41-48. PubMed
  33. Goncharova EA. The Water status of cultivated plants and its diagnostics. St. Petersburg: Vavilov Res. Inst. Plant Industry, 2005. 112 p. (In Russian).
  34. Bates LS, Walden RP, Tear GD. Rapid determination of free proline for water-stress studies. Plant Soil. 1973;39(1):205-207. CrossRef
  35. Zhao K, Fan H, Zhou S, Song J. Study on the salt and drought tolerance of Suaeda salsa and Kalanchцe claigremontiana under isoosmotic salt and water stress. Plant Sci. 2003;165(4):837-844. CrossRef
  36. Kolupaev YuE, Yastreb TO, Oboznyi AI, Ryabchun NI, Kirichenko VV. Constitutive and cold-induced resistance of rye and wheat seedlings to oxidative stress. Russ J Plant Physiol. 2016; 63(3): 326-337. CrossRef
  37.  Shlyk AA. Determination of chlorophylls and carotenoids in extracts of green leaves. In: Pavlinova OA. (ed) Biochemical Methods in Plant Physiology. Moscow: Nauka, 1971: 154-170. (In Russian).
  38. Munns R. Comparative physiology of salt and water stress. Plant Cell Environ. 2002;25(2):239-250. PubMed, CrossRef
  39. Santos CV. Regulation of chlorophyll biosynthesis and degradation by salt stress in sunflower leaves. Sci Horticult. 2004;103(1):93-99. CrossRef
  40. Zhu L, Yang Z, Zeng X, Gao J, Liu J, Yi B, Ma C, Shen J, Tu J, Fu T, Wen J. Heme oxygenase 1 defects lead to reduced chlorophyll in Brassica napus. Plant Mol Biol. 2017;93(6):579-592. PubMed, CrossRef
  41. Syvash OO, Zolotareva OK. Regulation of chlorophyll degradation in plant tissues. Biotechnologia Acta. 2017;10(3):20-30. CrossRef
  42. Kaya A, Doganlar ZB. Exogenous jasmonic acid induces stress tolerance in tobacco (Nicotiana tabacum) exposed to imazapic. Ecotoxicol Environ Saf. 2016;124:470-479. PubMed, CrossRef
  43. Radchenko MP, Sychuk АM, Morderer YY. Decrease of the herbicide fenoxaprop phytotoxicity in drought conditions: the role of the antioxidant enzymatic system. J Plant Protect Res. 2014; 54(4): 390-394. CrossRef
  44. Kolupaev YuE, Karpets YuV, Kabashnikova LF. Antioxidative system of plants: cellular compartmentalization, protective and signaling functions, mechanisms of regulation (Review). Appl Biochem Microbiol. 2019;55(5):441-459. CrossRef
  45. He H, He LF. Regulation of gaseous signaling molecules on proline metabolism in plants. Plant Cell Rep. 2018;37(3):387-392. PubMed, CrossRef
  46. Sin’kevich MS, Deryabin AN, Trunova TI. Characteristics of oxidative stress in potato plants with modified carbohydrate metabolism. Russ J Plant Physiol. 2009;56(2):168-174. CrossRef
  47. Radyukina NL, Shashukova AV, Makarova SS, Kuznetsov VV. Exogenous proline modifies differential expression of superoxide dismutase genes in UV-B-irradiated Salvia officinalis plants. Russ J Plant Physiol. 2011;58(1):36-44. CrossRef

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