Photosynthetica 2021, 59(4):683-692 | DOI: 10.32615/ps.2021.061

The melatonin receptor CAND2 is involved in the regulation of photosynthesis and chloroplast gene expression in Arabidopsis thaliana under photooxidative stress

I.A. BYCHKOV, N.V. KUDRYAKOVA, E.S. POJIDAEVA, V.V. KUSNETSOV
K.A. Timiryazev Institute of Plant Physiology RAS, 35 Botanicheskaya St., 127276 Moscow, Russia

Melatonin is a well-known bioactive molecule able to mitigate photooxidative damage caused by excess light. Here we have shown that mutant Arabidopsis lines with disrupted genes for melatonin putative receptor CAND2/PMTR1 and GPA1 encoding the α-subunit of heterotrimeric G-protein were partially insensitive to melatonin treatment under high light stress. They exhibited a higher degree of photodamage due to a significantly decreased photosynthetic activity and diminished expression of chloroplast and nuclear-encoded genes and the corresponding proteins. A possible mechanism for melatonin-dependent regulation of chloroplast genes is associated with a change in the activity of the genes for chloroplast RNA polymerases. We conclude that under high light stress, melatonin may act as a hormone-like signaling molecule via the CAND2/PMTR1-mediated signaling pathway.

Additional key words: chloroplast genome expression; light stress; photosynthetic activity; phytomelatonin receptor.

Received: September 21, 2021; Revised: November 8, 2021; Accepted: November 29, 2021; Prepublished online: December 14, 2021; Published: December 17, 2021  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
BYCHKOV, I.A., KUDRYAKOVA, N.V., POJIDAEVA, E.S., & KUSNETSOV, V.V. (2021). The melatonin receptor CAND2 is involved in the regulation of photosynthesis and chloroplast gene expression in Arabidopsis thaliana under photooxidative stress. Photosynthetica59(4), 683-692. doi: 10.32615/ps.2021.061
Download citation

Supplementary files

Download fileBychkov_2808_supplement.docx

File size: 66.54 kB

References

  1. Arnao M.B., Hernández-Ruiz J.: Functions of melatonin in plants: a review. - J. Pineal Res. 59: 133-150, 2015. Go to original source...
  2. Back K.: Melatonin metabolism, signaling and possible roles in plants. - Plant J. 105: 376-391, 2021. Go to original source...
  3. Back K., Tan D.X., Reiter R.J.: Melatonin biosynthesis in plants: multiple pathways catalyze tryptophan to melatonin in the cytoplasm or chloroplasts. - J. Pineal Res. 61: 426-437, 2016. Go to original source...
  4. Bychkov I., Kudryakova N., Andreeva A. et al.: Melatonin modifies the expression of the genes for nuclear- and plastid-encoded chloroplast proteins in detached Arabidopsis leaves exposed to photooxidative stress. - Plant Physiol. Bioch. 144: 404-412, 2019. Go to original source...
  5. Cipolla-Neto J., Amaral F.G.: Melatonin as a hormone: New physiological and clinical insights. - Endocr. Rev. 39: 990-1028, 2018. Go to original source...
  6. Danilova M.N., Kudryakova N.V., Andreeva A.A. et al.: Differential impact of heat stress on the expression of chloroplast-encoded genes. - Plant Physiol. Bioch. 129: 90-100, 2018. Go to original source...
  7. Gruszecki W.I.: Light-driven regulatory mechanisms in the photosynthetic antenna complex LHCII. - Biochem. Soc. T. 38: 702-704, 2010. Go to original source...
  8. Heddad M., Noren H., Reiser V. et al.: Differential expression and localization of early light-induced proteins in Arabidopsis. - Plant Physiol. 142: 75-87, 2006. Go to original source...
  9. Kozuleva M.A., Lysenko E.A., Klaus A.A., Kuznetsov V.V.: Long-term hyperthermia impairs activity of both photosystems. - Dokl. Biochem. Biophys. 472: 71-73, 2017. Go to original source...
  10. Krantz M., Legen J., Gao Y. et al.: Modeling indicates degradation of mRNA and protein as a potential regulation mechanisms during cold acclimation. - J. Plant Res. 134: 873-883, 2021. Go to original source...
  11. Kühn K., Richter U., Meyer E.H. et al.: Phage-type RNA polymerase RPOTmp performs gene-specific transcription in mitochondria of Arabidopsis thaliana. - Plant Cell 21: 2762-2779, 2009. Go to original source...
  12. Kusnetsov V.V.: Chloroplasts: Structure and expression of the plastid genome. - Russ. J. Plant Physiol. 65: 465-476, 2018. Go to original source...
  13. Lee H.Y., Back K.: Melatonin induction and its role in high light stress tolerance in Arabidopsis thaliana. - J. Pineal. Res. 65: e12504, 2018. Go to original source...
  14. Lee H.Y., Back K.: The phytomelatonin receptor (PMRT1) Arabidopsis Cand2 is not a bona fide G protein-coupled melatonin receptor. - Melatonin Res. 3: 177-186, 2020. Go to original source...
  15. Lee H.Y., Back K.: Melatonin regulates chloroplast protein quality control via a mitogen-activated protein kinase signaling pathway. - Antioxidants 10: 511, 2021. Go to original source...
  16. Li D., Wei J., Peng Z. et al.: Daily rhythms of phytomelatonin signaling modulate diurnal stomatal closure via regulating reactive oxygen species dynamics in Arabidopsis. - J. Pineal Res. 68: e12640, 2020. Go to original source...
  17. Lichtenthaler H.K.: Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. - Method. Enzymol. 148: 350-382, 1987. Go to original source...
  18. Pfannschmidt T., Blanvillain R., Merendino L. et al.: Plastid RNA polymerases: orchestration of enzymes with different evolutionary origins controls chloroplast biogenesis during the plant life cycle. - J. Exp. Bot. 66: 6957-6973, 2015. Go to original source...
  19. Reiter R.J., Tan D.X., Zhou Z. et al.: Phytomelatonin: assisting plants to survive and thrive. - Molecules 20: 7396-7437, 2015. Go to original source...
  20. Sharif R., Xie C., Zhang H. et al.: Melatonin and its effects on plant systems. - Molecules 23: 2352, 2018. Go to original source...
  21. Sun C., Liu L., Wang L. et al.: Melatonin: A master regulator of plant development and stress responses. - J. Integr. Plant Biol. 63: 126-145, 2021. Go to original source...
  22. Tan D.X., Manchester L.C., Liu X. et al.: Mitochondria and chloroplasts as the original sites of melatonin synthesis: a hypothesis related to melatonin's primary function and evolution in eukaryotes. - J. Pineal Res. 54: 127-138, 2013. Go to original source...
  23. Tarasenko V.I., Katyshev A.I., Yakovleva T.V. et al.: RPOTmp, an Arabidopsis RNA polymerase with dual targeting, plays an important role in mitochondria, but not in chloroplasts. - J. Exp. Bot. 67: 5657-5669, 2016. Go to original source...
  24. Wan J., Zhang P., Wang R. et al.: Comparative physiological responses and transcriptome analysis reveal the roles of melatonin and serotonin in regulating growth and metabolism in Arabidopsis. - BMC Plant Biol. 18: 362, 2018. Go to original source...
  25. Wang D.Y, Wang J., Shi S.H. et al.: Exogenous melatonin ameliorates salinity-induced oxidative stress and improves photosynthetic capacity in sweet corn seedlings. - Photosynthetica 59: 327-336, 2021a. Go to original source...
  26. Wang L., Feng C., Zheng X. et al.: Plant mitochondria synthesize melatonin and enhance the tolerance of plants to drought stress. - J. Pineal Res. 63: e12429, 2017. Go to original source...
  27. Wang L.F., Li T.T., Zhang Y. et al.: CAND2/PMTR1 is required for melatonin-conferred osmotic stress tolerance in Arabidopsis. - Int. J. Mol. Sci. 22: 4014, 2021b. Go to original source...
  28. Weeda S., Zhang N., Zhao X. et al.: Arabidopsis transcriptome analysis reveals key roles of melatonin in plant defense systems. - PLoS ONE 9: e93462, 2014. Go to original source...
  29. Wei J., Li D.X., Zhang J.R. et al.: Phytomelatonin receptor PMTR1-mediated signaling regulates stomatal closure in Arabidopsis thaliana. - J. Pineal Res. 65: e12500, 2018. Go to original source...
  30. Zhang M., He S., Zhan Y. et al.: Exogenous melatonin reduces the inhibitory effect of osmotic stress on photosynthesis in soybean. - PLoS ONE 14: e0226542, 2019. Go to original source...
  31. Zhao D., Yu Y., Shen Y. et al.: Melatonin synthesis and function: evolutionary history in animals and plants. - Front. Endocrinol. 10: 249, 2019. Go to original source...
  32. Zhou X., Zhao H., Cao K. et al.: Beneficial roles of melatonin on redox regulation of photosynthetic electron transport and synthesis of D1 protein in tomato seedlings under salt stress. - Front. Plant Sci. 7: 1823, 2016. Go to original source...