Photosynthetica 2020, 58(4):961-973 | DOI: 10.32615/ps.2020.050

Effect of exogenously applied 20-hydroxyecdysone on the efficiency of primary photosynthetic processes substantially differs across plant species

D. HOLÁ, K. FRIMLOVÁ, M. KOČOVÁ, H. MARKOVÁ, O. ROTHOVÁ, L. TŮMOVÁ
Department of Genetics and Microbiology, Faculty of Science, Charles University, Viničná 5, 128 43 Prague, Czech Republic

The effects of 20-hydroxyecdysone on the primary photosynthetic processes (PPP) were examined across twelve plant species using the OJIP chlorophyll fluorescence analysis. Our experiments brought evidence that the ecdysteroids can function not only as protective compounds in plants but participate also in the regulation of photosynthesis. Exogenously applied 20-hydroxyecdysone positively affected the PPP particularly in French bean and canola. Contrary to this, the PPP were negatively influenced by 20-hydroxyecdysone in pea, sunflower, and wheat. The performace of the oxygen-evolving complex, the excitonic connectivity among PSII units, the electron transport between PSII and PSI, the size of the pool of the end electron acceptors, and the absorption and trapping of the excitation energy in the light-harvesting antennae were differently affected in individual plant species. Additionally, the older and younger leaves did not respond to 20-hydroxyecdysone in the same way and this was also a species-specific phenomenon.

Additional key words: electron transport chain; interspecific variability; OJIP analysis.

Received: February 28, 2020; Revised: June 7, 2020; Accepted: June 9, 2020; Prepublished online: June 30, 2020; Published: September 4, 2020  Show citation

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HOLÁ, D., FRIMLOVÁ, K., KOČOVÁ, M., MARKOVÁ, H., ROTHOVÁ, O., & TŮMOVÁ, L. (2020). Effect of exogenously applied 20-hydroxyecdysone on the efficiency of primary photosynthetic processes substantially differs across plant species. Photosynthetica58(4), 961-973. doi: 10.32615/ps.2020.050
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References

  1. Bajguz A.: Brassinosteroids - occurence and chemical structures in plants. - In: Hayat S., Ahmad A. (ed.): Brassinosteroids: A Class of Plant Hormone. Pp. 1-27. Springer, Dordrecht 2011. Go to original source...
  2. Bajguz A., Dinan L.: Effects of ecdysteroids on Chlorella vulgaris. - Physiol. Plantarum 121: 349-357, 2004. Go to original source...
  3. Bajguz A., Godlewska-Zylkiewicz B.: Protective role of 20-hydroxyecdysone against lead stress in Chlorella vulgaris cultures. - Phytochemistry 65: 711-720, 2004. Go to original source...
  4. Bajguz A., Koronka A.: Effect of ecdysone application on the growth and biochemical changes in Chlorella vulgaris cells. - Plant Physiol. Bioch. 39: 707-715, 2001. Go to original source...
  5. Bakrim A., Lamhamdi M., Sayah F., Chib F.: Effects of plant hormones and 20-hydroxyecdysone on tomato (Lycopersicum esculentum) seed germination and seedlings growth. - Afr. J. Biotechnol. 6: 2792-2802, 2007. Go to original source...
  6. Bakrim A., Maria A., Sayah F. et al.: Ecdysteroids in spinach (Spinacia oleracea L.): biosynthesis, transport and regulation of levels. - Plant Physiol. Bioch. 46: 844-854, 2008. Go to original source...
  7. Cheng F., Zhou Y.H., Xia X.J. et al.: Chloroplastic thioredoxin-f and thioredoxin-m1/4 play important roles in brassinosteroids-induced changes in CO2 assimilation and cellular redox homeostasis in tomato. - J. Exp. Bot. 65: 4335-4347, 2014. Go to original source...
  8. Dinan L., Savchenko T., Whiting P.: On the distribution of phytoecdysteroids in plants. - Cell Mol. Life Sci. 58: 1121-1132, 2001. Go to original source...
  9. Dobrikova A.G., Vladkova R.S., Rashkov G.D. et al.: Effects of exogenous 24-epibrassinolide on the photosynthetic membranes under non-stress conditions. - Plant Physiol. Bioch. 80: 75-82, 2014. Go to original source...
  10. Dobrikova A.G., Vladkova R.S., Stanoeva D. et al.: Effects of 24-epibrassinolide pre-treatment on UV-B-induced changes in the pigment content of pea leaves. - C. R. Acad. Bulg. Sci. 66: 543-550, 2013. Go to original source...
  11. Efimova M.V., Kusnetsov V.V., Kravtsov A.K. et al.: Expression of plastid genome and development of Arabidopsis thaliana with disturbed synthesis of brassinosteroids. - Russ. J. Plant Physl+ 59: 28-34, 2012a. Go to original source...
  12. Efimova M.V., Kusnetsov V.V., Kravtsov A.K. et al.: Regulation of the transcription of plastid genes in plants by brassino-steroids. - Dokl. Biol. Sci. 445: 272-275, 2012b. Go to original source...
  13. Efimova M.V., Vaňková R., Kusnetsov V.V. et al.: Effects of 24-epibrassinolide and green light on plastid gene transcription and cytokinin content of barley leaves. - Steroids 120: 32-40, 2017. Go to original source...
  14. Golovatskaya I.F.: Effect of ecdysterone on morphological and physiological processes in plants. - Russ. J. Plant. Physl+ 51: 452-458, 2004. Go to original source...
  15. Haitov B., Mamadalieva N., Egamberdieva D.: Plant-derived 20-hydroxyecdysone alleviates salt stress in cotton (Gossy-pium hirsutum L.) seedlings. - Asian Australasian J. Plant. Sci. Biotechnol. 7: 39-42, 2013.
  16. Holá D.: Brassinosteroids and photosynthesis. - In: Hayat S., Ahmad A. (ed.): Brassinosteroids: A Class of Plant Hormone. Pp. 143-192. Springer, Dordrecht 2011. Go to original source...
  17. Holá D., Kočová M., Rothová O. et al.: Exogenously applied 20-hydroxyecdysone increases the net photosynthetic rate but does not affect the photosynthetic electron transport or the content of photosynthetic pigments in Tetragonia tetragonioides L. - Acta Physiol. Plant. 35: 3489-3495, 2013. Go to original source...
  18. Janeczko A., Ko¶cielniak J., Pilipowicz M. et al.: Protection of winter rape photosystem 2 by 24-epibrassinolide under cadmium stress. - Photosynthetica 43: 293-298, 2005. Go to original source...
  19. Janeczko A., Swaczynová J.: Endogenous brassinosteroids in wheat treated with 24-epibrassinolide. - Biol. Plantarum 54: 477-482, 2010. Go to original source...
  20. Jiang Y.P., Cheng F., Zhou Y.H. et al.: Brassinosteroid-induced CO2 assimilation is associated with increased stability of redox-sensitive photosynthetic enzymes in the chloroplasts in cucumber plants. - Biochem. Bioph. Res. Co. 426: 390-394, 2012a. Go to original source...
  21. Jiang Y.P., Cheng F., Zhou Y.H. et al.: Cellular glutathione redox homeostasis plays an important role in the brassinosteroid induced increase in CO2 assimilation in Cucumis sativus. - New Phytol. 194: 932-943, 2012b. Go to original source...
  22. Jiang Y.P., Huang L.F., Cheng F. et al.: Brassinosteroids accelerate recovery of photosynthetic apparatus from cold stress by balancing the electron partitioning, carboxylation and redox homeostasis in cucumber. - Physiol. Plantarum 148: 133-145, 2013. Go to original source...
  23. Kamlar M., Rothová O., Salajková ©. et al.: The effect of exogenous 24-epibrassinolide on the ecdysteroid content in the leaves of Spinacia oleracea L. - Steroids 97: 107-112, 2015. Go to original source...
  24. Khamsuk O., Sonjaroon W., Suwanwong S. et al.: Effects of 24-epibrassinolide and the synthetic brassinosteroid mimic on chili pepper under drought. - Acta Physiol. Plant. 40: 106, 2018. Go to original source...
  25. Komatsu T., Kawaide H., Saito C. et al.: The chloroplast protein BPG2 functions in brassinosteroid mediated post-transcriptional accumulation of chloroplast rRNA. - Plant J. 61: 409-422, 2010. Go to original source...
  26. Krampolová E.: [Brassinosteroids and phytoecdysteroids cross-talk in planta.] B. Sc. Thesis, Palacký University in Olomouc, Faculty of Science, Olomouc, Czech Republic 2017. [In Czech] https://theses.cz/id/ct9iov
  27. Krumova S., Zhiponova M., Dankov K. et al.: Brassinosteroids regulate the thylakoid membrane architecture and the photo-system II function. - J. Photoch. Photobio. B 126: 97-104, 2013. Go to original source...
  28. Krumova S., Zhiponova M., Dankov K. et al.: Effects of enhanced brassinosteroid perception on photosynthetis in Arabidopsis thaliana line BRIOE. - C. R. Acad. Bulg. Sci. 64: 967-972, 2011.
  29. Lamhamdi M., Lafont R., Rharrabe K. et al.: 20-Hydroxyecdysone protects wheat seedlings (Triticum aestivum L.) against lead stress. - Plant Physiol. Bioch. 98: 64-71, 2016. Go to original source...
  30. Li J.T., Han X.P., Tang L. et al.: 20-Hydroxyecdysone protects wheat seedlings from salt stress. - Arch. Biol. Sci. 70: 379-386, 2018. Go to original source...
  31. Liu X., Feng Z.M., Zhou C.L. et al.: Brassinosteroid (BR) biosynthetic gene lhdd10 controls late heading and plant height in rice (Oryza sativa L.). - Plant Cell Rep. 35: 357-368, 2016. Go to original source...
  32. McDonald J.H.: Handbook of Biological Statistics. 3rd Edition. Pp. 126-130. Sparky House Publishing, Baltimore 2014.
  33. Moreau R.A., Nyström L., Whitaker B.D. et al.: Phytosterols and their derivatives: Structural diversity, distribution, metabolism, analysis, and health-promoting uses. - Prog. Lipid Res. 70: 35-61, 2018. Go to original source...
  34. Moreau R.A., Whitaker B.D., Hicks K.B.: Phytosterols, phytostanols, and their conjugates in foods: structural diversity, quantitative analysis, and health-promoting uses. - Prog. Lipid Res. 41: 457-500, 2002. Go to original source...
  35. Pociecha E., Dziurka M., Okleą»ková J., Janeczko A.: Brassino-steroids increase winter survival of winter rye (Secale cereale L.) by affecting photosynthetic capacity and carbohydrate metabolism during the cold acclimation process. - Plant Growth Regul. 80: 127-135, 2016. Go to original source...
  36. Rothová O., Holá D., Kočová M. et al.: 24-epibrassinolide and 20-hydroxyecdysone affect photosynthesis differently in maize and spinach. - Steroids 85: 44-57, 2014. Go to original source...
  37. Schröder F., Lisso J., Obata T. et al.: Consequences of induced brassinosteroid deficiency in Arabidopsis leaves. - BMC Plant Biol. 14: 309, 2014. Go to original source...
  38. Skoczowski A., Janeczko A., Gullner G. et al.: Response of brassinosteroid-treated oilseed rape cotyledons to infection with the wild type and HR-mutant of Pseudomonas syringae or with P. fluorescence. - J. Therm. Anal. Calorim. 104: 131-139, 2011. Go to original source...
  39. Sonjaroon W., Jutamanee K., Khamsuk O. et al.: Impact of brassinosteroid mimic on photosynthesis, carbohydrate content and rice seed set at reproductive stage under heat stress. - Agric. Nat. Resour. 52: 234-240, 2018. Go to original source...
  40. Sonjaroon W., Kaveeta L., Chai-arree W. et al.: Exogenous 7,8-dihydro-8α-20-hydroxyecdysone application improves antioxidative enzyme system, photosynthesis, and yield in rice under high-temperature condition. - Acta Physiol. Plant. 38: 202, 2016. Go to original source...
  41. Stirbet A., Govindjee: On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: Basics and applications of the OJIP fluorescence transient. - J. Photoch. Photobio. B 104: 236-257, 2011. Go to original source...
  42. Strasser R.J., Tsimilli-Michael M., Srivastava A.: Analysis of the chlorophyll a fluorescence transient. - In: Papageorgiou G.C., Govindjee (ed.): Chlorophyll a Fluorescence: A Signature of Photosynthesis. Advances in Photosynthesis and Respiration. Pp. 321-362. Springer, Dordrecht 2004. Go to original source...
  43. Sun Y., Fan X.Y., Cao D.M. et al.: Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. - Dev. Cell 19: 765-777, 2010. Go to original source...
  44. Tanaka K., Asami T., Yoshida S. et al.: Brassinosteroid homeo-stasis in Arabidopsis is ensured by feedback expressions of multiple genes involved in its metabolism. - Plant Physiol. 138: 1117-1125, 2005. Go to original source...
  45. Tarkowská D., Strnad M.: Plant ecdysteroids: plant sterols with intriguing distributions, biological effects and relations to plant hormones. - Planta 244: 545-555, 2016. Go to original source...
  46. Tarkowská D., Strnad M.: Isoprenoid‑derived plant signaling molecules: biosynthesis and biological importance. - Planta 247: 1051-1066, 2018. Go to original source...
  47. Thiem B., Kikowska M., Maliński M.P. et al.: Ecdysteroids: production in plant in vitro cultures. - Phytochem. Rev. 16: 603-622, 2017. Go to original source...
  48. Thussagunpanit J., Jutamanee K., Homvisasevongsa S. et al.: Characterization of synthetic ecdysteroid analogues as functional mimics of brassinosteroids in plant growth. - J. Steroid Biochem. Mol. Biol. 172: 1-8, 2018. Go to original source...
  49. Thussagunpanit J., Jutamanee K., Kaveeta L. et al.: Comparative effects of brassinosteroid and brassinosteroid mimic on improving photosynthesis, lipid peroxidation, and rice seed set under heat stress. - J. Plant Growth Regul. 34: 320-331, 2015a. Go to original source...
  50. Thussagunpanit J., Jutamanee K., Sonjaroon W. et al.: Effects of brassinosteroid and brassinosteroid mimic on photosynthetic efficiency and rice yield under heat stress. - Photosynthetica 53: 312-320, 2015b. Go to original source...
  51. Uhlík O., Kamlar M., Kohout L. et al.: Affinity chromatography reveals RuBisCO as an ecdysteroid-binding protein. - Steroids 73: 1433-1440, 2008. Go to original source...
  52. Valitova J.N., Sulkarnayeva A.G., Minibayeva F.V.: Plant sterols: diversity, biosynthesis and physiological functions. - Biochemistry-Moscow+ 81: 819-834, 2016. Go to original source...
  53. Yusuf M.A., Kumar D., Rajwanshi R. et al.: Overexpression of γ-tocopherol methyl transferase gene in transgenic Brassica juncea plants alleviates abiotic stress: Physiological and chlorophyll a fluorescence measurements. - BBA-Bioenergetics 1797: 1428-1438, 2010. Go to original source...