Visn. Hark. nac. agrar. univ., Ser. Biol., 2020, Issue 2 (50), p. 35-53


Yu. E. Kolupaev1, 2, S. P. Beschasnyi3, M. A. Shkliarevskyi1, Yu. V. Karpets1

1Dokuchaev Kharkiv National Agrarian University
(Kharkiv, Ukraine)
2Karazin Kharkiv National University
(Kharkiv, Ukraine)
3Kherson State University
(Kherson, Ukraine)

The review is devoted to the role of carbon monoxide (CO) in stress signaling and plant adaptation to unfavorable abiotic factors. Main pathways of CO synthesis in plant cells are described, hemoxygenase-1 is briefly characterized as the main enzymatic source of carbon monoxide, and data on its subcellular localization are presented. Individual aspects of the CO action in plant and animal cells are compared. Information about induction of carbon monoxide synthesis under influence of various stressors: dehydration, salinization, heavy metal ions, UV-B, extreme temperatures are summarized. Data about influence of exogenous CO and its donors on resistance of plants to stress factors of various natures are analyzed. Attention is accented on the influence of carbon monoxide on state of antioxidant and osmoprotective systems of plants, its participation in the regulation of stomatal apparatus functioning. Role of other signaling mediators in physiological (stress-protective) action of CO in plant cells, in particular, cGMP, nitric oxide, Ca2+ ions, reactive oxygen species (ROS), and hydrogen sulfide, is discussed. Information is given about the role of carbon monoxide in transduction of ROS signals, new gasotransmitters methane and hydrogen, phytohormones (auxin, cytokinins, and abscisic acid). It is noted that the mechanisms of CO participation in functioning of signal network of plant cells have not yet been disclosed. Possibilities of using CO for activating of stress-protective reactions of plants and for improving preservation of harvested fruits are discussed.

Key words: carbon monoxide, gasotransmitters, signaling, guanylate cyclase, nitric oxide, calcium, reactive oxygen species, antioxidant system, stress reactions, resistance



1. Kolupaev Yu.E., Karpets Yu.V. 2014. Reactive oxygen species and stress signaling in plants. Ukr. Biochem. J. 86 (4) : 18-35. (In Russian).
2. Kukoba T.V., Moibenko A.A. Heme oxygenase and carbon monoxide: the protection or the injury of the cells?. Fiziol. Zhurn. 2002. 48 (5) : 79-92. (In Ukrainian).
3. Tashireva L.A., Starikova E.G., Novitskii V.V., Ryazantseva N.V. 2012. Intracellular targets of proapoptotic influence of gaseous transmitters. Vestnik Ross. Akad. Med. Nauk. 67 (10) : 77-81. (In Russian).
4. Bai X., Chen J., Kong X., Todd C.D., Yang Y., Hu X. Li D.Z. 2012. Carbon monoxide enhances the chilling tolerance of recalcitrant Baccaurea ramiflora seeds via nitric oxide-mediated glutathione homeostasis. Free Radical Biol. Med. 53 : 710-720.
5. Balestrasse K.B., Yannarelli G.G., Noriega G.O., Batlle A., Tomaro M.L. 2008. Heme oxygenase and catalase gene expression in nodules and roots of soybean plants subjected to cadmium stress. Biometals. 21 : 433-441.
6. Baudouin E. 2011. The language of nitric oxide signaling. Plant Biol (Stuttg.). 13 (2) : 233-242.
7. Cao Z., Huang B., Wang Q., Xuan W., Ling T., Zhang B., Chen X., Nie L., Shen W. 2007. Involvement of carbon monoxide produced by heme oxy-genase in ABA-induced stomatal closure in Vicia faba and its proposed signal transduction pathway. Chin. Sci. Bull. 52 (17) : 2365-2373.
8. Chen X.Y., Ding X., Xu S., Wang R., Xuan W., Cao Z.Y., Chen J., Wu H.H., Ye M.B., Shen W.B. 2009. Endogenous hydrogen peroxide plays a positive role in the upregulation of heme oxygenase and acclimation to oxidative stress in wheat seedling leaves. J. Integr. Plant Biol. 51 (10) : 951-960.
9. Chen Y.H., Chao Y.Y., Hsu Y.Y., Hong C.Y., Kao C.H. 2012. Heme oxygenase is involved in nitric oxide- and auxin-induced lateral root formation in rice. Plant Cell Rep. 31 (6) :1085-1091.
10. Chen Y.H., Chao Y.Y., Hsu Y.Y., Kao C.H. 2013. Heme oxygenase is involved in H2O2-induced lateral root formation in apocynin-treated rice. Plant Cell Rep. 32 (2) : 219-226.
11. Chen Y., Wang M., Hu L., Liao W., Dawuda M.M., Li C. 2017. Carbon monoxide is involved in hydrogen gas-induced adventitious root development in cucumber under simulated drought stress. Front Plant Sci. 8 : 128.
12. Chen Q., Gong C., Ju X., Zhu Z., Shen W., Shen Z., Cui J. 2018. Hemin through the heme oxygenase 1/ferrous iron, carbon monoxide system involved in zinc tolerance in Oryza Sativa L. J. Plant Growth Regul. 37 : 947-957.
13. Cheng T., Hu L., Wang P., Yang X., Peng Y., Lu Y., Chen J., Shi J. 2018. Carbon monoxide potentiates high temperature-induced nicotine biosynthesis in Tobacco. Int. J. Mol. Sci. 19 : 188.
14. Cui W.T., Qi,F., Zhang, Y.H., Cao, H., Zhang, J., Wang, R., Shen W. 2015. Methane-rich water induces cucumber adventitious rooting through heme oxygenase1/carbon monoxide and Ca2+ pathways. Plant Cell Rep. 34 : 435-445.
15. Davis S., Bhoo S.H., Durski A.M., Walker J.M., Viersta R.D. 2001. The heme oxygenase family required for phytochrome chromophore biosynthesis is necessary for proper photomorphogenesis in higher plants. Plant Physiol. 126 : 656-669.
16. Dekker J., Hargrove M. 2002. Weedy adaptation in Setaria spp. V. Effects of gaseous environment on giant foxtail (Setaria faberii) (Poaceae) seed germination. Amer. J. Bot. 89, : 410-416.
17. Demidchik V., Shabala S., Isayenkov S., Cuin T.A., Pottosin I. 2018. Calcium transport across plant membranes: mechanisms and functions. New Phytol. 220 (1) : 49-69.
18. Durante W., Johnson F.K., Robert A., Johnson R.A. 2006. Role of carbon monoxide in cardiovascular function. J. Cell. Mol. Med. 10 : 672-686.
19. Emborg T.J., Walker J.M., Noh B., Vierstra R.D. 2006. Multiple heme oxygenase family members contrib-ute to the biosynthesis of the phytochrome chromophore in Arabidopsis. Plant Physiolo. 140 : 856-868.
20. Foyer C.H., Noctor G. 2009. Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid. Redox Signal. 11 : 861-906.
21. Gniazdowska A., Krasuska U., Debska K., Andryka P., Bogatek R. 2010. The beneficial effect of small toxic molecules on dormancy alleviation and germination of apple embryos is due to NO formation. Planta. 232 : 999-1005.
22. Hancock J.T. 2019. Hydrogen sulfide and environmental stresses. Environ. Exp. Bot. 161 : 50-56.
23. Huang J., Han B., Xu S., Zhou M., Shen W. 2011. Heme oxygenase-1 is involved in the cytokinin-induced alleviation of senescence in detached wheat leaves during dark incubation. J. Plant Physiol. 168 (8) : 768-775.
24. He H., He L.F. 2018. Regulation of gaseous signaling molecules on proline metabolism in plants. Plant Cell Reports. 37 : 387-392
25. He H., He L. 2014a. Heme oxygenase 1 and abiotic stresses in plants. Acta Physiol Plant. 36 : 581-588.
26. He H., He L. 2014b. The role of carbon monoxide signaling in the responses of plants to abiotic stresses. Nitric Oxide. V. 42 : P. 40-43.
27. Hsu Y.Y., Chao Y.Y., Kao C.H. 2013. Cobalt chloride-induced lateral root formation in rice: the role of heme oxygenase. J. Plant Physiol. 170 (12) : 1075-1081.
28. Jeandroz S., Wipf D., Stuehr D.J, Lamattina L., Melkonian M., Tian Z., Zhu Y., Carpenter E.J., Wong G.K., Wendehenne D. 2016. Occurrence, structure, and evolution of nitric oxide synthase-like proteins in the plant kingdom. Sci. Signal. 9:re2.
29. Jin Q., Zhu K., Xie Y., Shen W. 2013. Heme oxygenase-1 is involved in ascorbic acid-induced alleviation of cadmium toxicity in root tissues of Medicago sativa. Plant Soil. 366 : 605-616.
30. Jin Q., Cui W., Xie Y., Shen W. 2016. Carbon monoxide: A ubiquitous gaseous signaling molecule in plants. In: Gasotransmitters in Plants, Signaling and Communication in Plants. Eds. Lamattina L., Garcia-Mata C. Switzerland: Springer International Publishing, pp. 3-19.
31. Khan M.N., Mobin M., Abbas Z.K. 2015. Nitric oxide and high temperature stress: A physiological per-spective. In: Nitric Oxide Action in Abiotic Stress Responses in Plants. Eds. Khan M.N. et al. Switzer-land: Springer International Publishing, pp. 77-93.
32. Kolupaev Yu.E., Karpets Yu.V., Beschasniy S.P., Dmitriev A.P. 2019. Gasotransmitters and their role in adaptive reactions of plant cells. Cytol. Genet. 53 (5) : 392-406.
33. Lamattina L., Garcia-Mata C. 2016. Preface. In: Gasotransmitters in Plants, Signaling and Communica-tion in Plants. Eds. Lamattina L., Garcia-Mata C. Switzerland: Springer International Publishing, pp. v-ix. doi: 10.1007/978-3-319-40713-5.
34. Lamotte O., Guold K., Lecourieux D., Sequeira-Legrand A., Lebrun-Garcia A., Durner J., Pugin A., Wendehenne D. 2004. Analysis of nitric oxide signaling functions in tobacco cells challenged by the elicitor cryptogein. Plant Physiol. 135 : 516-529.
35. Li L., Wei S., Shen W. 2020. The role of methane in plant physiology: a review. Plant Cell Rep. 39 : 171-179.
36. Li Z.-G.,Gu S.-P. 2016. Hydrogen sulfide as a signal molecule in hematin-induced heat tolerance of to-bacco cell suspension. Biol. Plant. 60 : 595-600.
37. Lin J.S., Lin H.H., Li Y.C., King Y.C., Sung R.J., Kuo Y.W., Lin C.C., Shen Y.H., Jeng S.T. 2014. Carbon monoxide regulates the expression of the wound-inducible gene ipomoelin through antioxidation and MAPK phosphorylation in sweet potato. J. Exp. Bot. 65 (18) : 5279-5290.
38. Lin Y.T., Zhang W., Qi F., Cui W.T., Xie Y.J., Shen W.B. 2014. Hydrogen-rich water regulates cucumber adventitious root development in a heme oxygenase-1/carbon monoxide-dependent manner. J. Plant Physiol. 171 : 1-8.
39. Ling T., Zhang B., Cui W., Wu M., Lin J., Zhou W., Huang J., Shen W. 2009. Carbon monoxide mitigates salt-induced inhibition of root growth and sup-presses programmed cell death in wheat primary roots by inhibiting superoxide anion overproduction. Plant Sci. 177 : 331-340.
40. Liu K., Xu S., Xuan W., Ling T., Cao Z., Huang B., Sun Y., Fang L., Liu Z., Zhao N., Shen W. 2007. Carbon monoxide counteracts the inhibition of seed germination and alleviates oxidative damage caused by salt stress in Oryza sativa. Plant Sci. 172 : 544-555.
41. Liu Y., Xu S., Ling T., Xu L., Shen W. 2010. Heme oxygenase/carbon monoxide system participates in regulating wheat seed germination under osmotic stress involving the nitric oxide pathway. J. Plant Physiol. 167 : 1371-1379.
42. Matsumoto F., Obayashi T., Sasaki-Sekimoto Y., Ohta H., Takamiya K.-I., Masuda T. 2004. Gene expression profiling of the tetrapyrrole metabolic pathway in Arabidopsis with a miniarray system. Plant Physiol. 135 : 2379-2391.
43. Meng D.K., Chen J., Yang Z.M. 2011. Enhancement of tolerance of Indian mustard (Brassica juncea) to mercury by carbon monoxide. J. Hazardous Materials. 186 : 1823-1829.
44. Motterlini R, Foresti R. 2017. Biological signaling by carbon monoxide and carbon monoxide-releasing molecules. Amer. J. Physiol. Cell Physiol. 312 (3) : 302-313.
45. Muramoto T., Kohchi T., Yokota A., Hwang I., Good-man H.M. 1999. The Arabidopsis photomorphogenic mutant hy1 is deficient in phytochrome chromophore biosynthesis as a result of a mutation in a plastid heme oxygenase. Plant Cell. 11 : 335-348.
46. Neill S., Barros R., Bright J., Desikan R., Hancock J., Harrison J., Morris P., Ribeiro D., Wilson I. 2008. Nitric oxide, stomatal closure and abiotic stress. J. Exp. Bot. 59 : 165-176.
47. Rentel M.C., Knight M.R. 2004. Oxidative stress-induced calcium signaling in Arabidopsis. Plant Physiol. 135 : 1471-1479.
48. Sa Z.S., Huang L.Q., Wu G.L., Ding J.P., Chen\ X.Y., Yu T., Ci S., Shen W.B. 2007. Carbon monoxide: a novel antioxidant against oxidative stress in wheat seedling leaves. J. Integr. Plant Biol. 49 : 638-645.
49. Santa-Cruz D.M., Pacienza N.A., Polizio A.H., Balestrasse K.B., Tomaro M.L., Yannarelli G.G. 2010. Nitric oxide synthase-like dependent NO production enhances heme oxygenase up-regulation in ultravio-let-B-irradiated soybean plants. Phytochem. 71 :1700-1707.
50. She X.-P., Song X.-G. 2008. Carbon monoxide-induced stomatal closure involves generation of hydrogen peroxide in Vicia faba guard cells. J. Integr. Plant Biol. 50 : 1539-1548.
51. Shekhawat G.S., Verma K. 2010. Haem oxygenase (HO): an overlooked enzyme of plant metabolism and defence. J. Exp. Bot. 61 : 2255-2270.
52. Shen Q., Jiang M., Li H., Che L.L., Yang Z.M. 2011. Expression of a Brassica napus heme oxygenase confers plant tolerance to mercury toxicity. Plant Cell Environ. 34 (5) : 752-763.
53. Siegel S.M., Siegel B.Z. 1987. Biogenesis of carbon monoxide: production by fungi and seed plants in the dark, Phytochem. 26 : 3117-3119.
54. Song X.G., She X.P., Zhang B. 2008. Carbon monoxide-induced stomatal closure in Vicia faba is dependent on nitric oxide synthesis. Physiol. Plant. 132 (4) : 514-525.
55. Tenhunen R., MarverH.S., Schmid R. 1968. The enzymatic conversion of haem to bilirubin by microso-mal haemoxygenase. Proc. Natl. Acad Sci USA. 61 : 748-755.
56. Terry M.J., Linley P.J., Kohchi T. 2002. Making light of it: the role of plant heme oxygenases in phyto-chrome chromophore synthesis. Biochemical Soc. Transactions. 30 : 604-609.
57. Trchounian A., Petrosyan M., Sahakyan N. 2016. Plant cell redox homeostasis and reactive oxygen species. In: Redox State as a Central Regulator of Plant-Cell Stress Responses. Eds. D.K. Gupta et al. Switzer-land: Springer International Publishing, pp. 25-50.
58. Verma K., Dixit S., Shekhawat G.S., Alam A. 2015. Antioxidant activity of heme oxygenase 1 in Brassica juncea (L.) Czern. (Indian mustard) under salt stress. Turk. J. Biol. 39 : 540-549.
59. Wang R. 2014. Gasotransmitters: growing pains and joys. Trends Biochem. Sci. 39 (5) : 227-232.
60. Wang M., Liao W. 2016. Carbon monoxide as a signal-ing molecule in plants. Front. Plant Sci. 7 : 572.
61. Wei Y.Y., Zheng Q., Liu Z.P., Yang Z.M. 2011. Regu-lation of tolerance of Chlamydomonas reinhardtii to heavy metal toxicity by heme oxygenase-1 and carbon monoxide. Plant Cell Physiol. 52 :1665-1675.
62. Wei M.-Y., Chao Y.-Y., Kao C.H. 2013. NaCl-induced heme oxygenase in roots of rice seedlings is mediat-ed through hydrogen peroxide. Plant Growth Regul. 69 : 209-214.
63. Wilkinson W.J., Kemp P.J. 2011. Carbon monoxide: an emerging regulator of ion channels. J. Physiol. 589 (13) : 3055-3062.
64. Wilks S.S. 1959. Carbon monoxide in green plants. Science. 129 : 964-966.
65. 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. 2008. 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. 31 : 1864-1881.
66. Xie Y.J., Zhang C., Lai D.W., Sun Y., Samma M.K., Zhang J., Shen W. 2014. Hydrogen sulfide delays GA-triggered programmed cell death in wheat aleurone layers by the modulation of glutathione homeostasis and heme oxygenase-1 expression. J. Plant Physiol. 171 : 53-62.
67. Xu S., Sa Z.‐S., Cao Z.‐Y., Xuan W., Huang B.‐K., Ling T.‐F., Hu Q.‐Y., Shen W.‐B. 2006. Carbon monoxide alleviates wheat seed germination inhibition and counteracts lipid peroxidation mediated by salinity. J. Integr. Plant Biol. 48 : 1168-1176.
68. Xuan W., Huang L., Li M., Huang B., Xu S., Liu H., Gao Y., Shen W. 2007. Induction of growth elongation in wheat root segments by heme molecules: a regulatory role of carbon monoxide in plants?. Plant Growth Regul. 52 : 41-51.
69. Yang L., Ji J., Wang H., Harris-Shultz K.R., Abd Allah E.F., Luo Y., Guan Y., Hu X. 2016. Carbon monoxide interacts with auxin and nitric oxide to cope with iron deficiency in Arabidopsis. Front Plant Sci. 7 : 112.
70. Yao Y., Yang Y., Li C., Huang D., Zhang J., Wang C., Li W., Wang N., Deng Y., Liao W. 2019. Research progress on the functions of gasotransmitters in plant responses to abiotic stresses. Plants (Basel). 8 (12). pii: E605.
71. Yuan X.X., Wang J., Xie Y.J., Shen W.B. 2009. Effects of carbon monoxide on salt tolerance and proline content of roots in wheat seedling. Plant Physiol. Commun. 45 (6) : 567-570.
72. Zhang C., Li Y., Yuan F., Hu S., He P. 2012. Effects of hematin and carbon monoxide on the salinity stress responses of Cassia obtusifolia L. seeds and seed-lings. Plant Soil. 359 : 85-105.
73. Zhang S., Li Y., Pei F. 2014a. Carbon monoxide fumigation improved the quality, nutrients, and antioxi-dant activities of postharvest peach. Int. J. Food Sci. Article ID 834150.
74. Zhang S., Li Q., Mao Yu. 2014b. Effect of carbon monoxide on active oxygen metabolism of postharvest Jujube. J. Food Technol. Res. 1 (2) : 146-155.
75. Zheng Q., Meng Q., Wei Y.Y. Yang Z.M. 2011. Allevi-ation of Copper-Induced Oxidative Damage in Chlamydomonas reinhardtii by Carbon Monoxide. Arch Environ. Contam. Toxicol. 61 : 220-227.
76. Zhu K., Zhang J., Cui W., Jin Q., Samma M.K., ShenW. 2014. Role of heme oxygenase-1 in spermidine-induced alleviation of salt toxicity during alfalfa seed germination. Plant Soil. 375 : 275-287.
77. Zilli C.G. Santa-Cruz D.M., Balestrasse K.B. 2014. Heme oxygenase-independent endogenous production of carbon monoxide by soybean plants subjected to salt stress. Environ. Exp. Bot. 102 : 11-16.