Photosynthetica 2022, 60(2):219-229 | DOI: 10.32615/ps.2022.006

Transgenerational effect of UV-B priming on photochemistry and associated metabolism in rice seedlings subjected to PEG-induced osmotic stress

A. SEN1, J.T. PUTHUR1, D. CHALLABATHULA2, M. BRESTIČ3, 4
1 Plant Physiology and Biochemistry Division, Department of Botany, University of Calicut, C.U. Campus P.O., 673635 Kerala, India
2 Department of Life Sciences, School of Life Sciences, Central University of Tamil Nadu, Thiruvarur, 610004 Tamil Nadu, India
3 Department of Plant Physiology, Slovak University of Agriculture, Nitra, Slovak Republic
4 Department of Botany and Plant Physiology, Faculty of Agrobiology, Food, and Natural Resources, Czech University of Life Sciences, 16500 Prague, Czech Republic

Rice being the major food crop for more than half of the world population is severely affected by drought stress starting from the establishment of the seedling. We focused on the UV-B priming mediated transgenerational drought tolerance of a drought-tolerant rice variety (Vaisakh) towards polyethylene glycol (PEG) 6,000 (20%)-induced drought. Results showed that priming in F0 generation and re-priming in F1 generation with UV-B enhanced the PEG stress tolerance potential of rice seedlings with increased expression of genes encoding antioxidant enzymes and stress-related proteins offering better protection to primed plants. UV-B priming maintained oxidative homeostasis of the plant cell thus ensuring uninterrupted mitochondrial and photosynthetic activities. Cumulatively, our results suggest that the transgenerational priming memory retained in the seeds is transferred to offspring without any loss. Moreover, re-priming in F1 generation further boosted the innate tolerance potential of a tolerant variety resulting in stable cellular redox homeostasis.

Additional key words: mitochondria activity; Oryza sativa; photosynthetic machinery; priming memory; stress proteins.

Received: September 16, 2021; Revised: January 19, 2022; Accepted: February 8, 2022; Prepublished online: March 4, 2022; Published: May 2, 2022  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
SEN, A., PUTHUR, J.T., CHALLABATHULA, D., & BRESTIČ, M. (2022). Transgenerational effect of UV-B priming on photochemistry and associated metabolism in rice seedlings subjected to PEG-induced osmotic stress. Photosynthetica, 60(2), 219-229. doi: 10.32615/ps.2022.006
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    Supplementary files

    Download fileSen_2807_supplement.docx

    File size: 1.22 MB

    References

    1. Ahmad M.A., Javed R., Adeel M. et al.: PEG 6000-stimulated drought stress improves the attributes of in vitro growth, steviol glycosides production, and antioxidant activities in Stevia rebaudiana Bertoni. - Plants 9: 1552, 2020. Go to original source...
    2. Aslam M., Maqbool M.A., Cengiz R.: Mechanisms of drought resistance. - In: Drought Stress in Maize (Zea mays L.). Pp. 19-36, Springer, Cham 2015. Go to original source...
    3. Asthir B.: Protective mechanisms of heat tolerance in crop plants. - J. Plant Interact. 10: 202-210, 2015. Go to original source...
    4. Badawi G.H., Kawano N., Yamauchi Y. et al.: Over-expression of ascorbate peroxidase in tobacco chloroplasts enhances the tolerance to salt stress and water deficit. - Physiol. Plantarum 121: 231-238, 2004a. Go to original source...
    5. Badawi G.H., Yamauchi Y., Shimada E. et al.: Enhanced tolerance to salt stress and water deficit by overexpressing superoxide dismutase in tobacco (Nicotiana tabacum) chloroplasts. - Plant Sci. 166: 919-928, 2004b. Go to original source...
    6. Bates L.S., Waldren R.P., Teare I.K.: Rapid determination of free proline for water studies. - Plant Soil 39: 205-207, 1973. Go to original source...
    7. Begcy K., Mariano E.D., Lembke C.G. et al.: Overexpression of an evolutionarily conserved drought-responsive sugarcane gene enhances salinity and drought resilience. - Ann. Bot.-London 124: 691-700, 2019. Go to original source...
    8. Boguszewska-Mańkowska B., Pieczyński M., Wyrzykowska A. et al.: Divergent strategies displayed by potato (Solanum tuberosum L.) cultivars to cope with soil drought. - J. Agron. Crop Sci. 204: 13-30, 2018. Go to original source...
    9. Bradford M.M.: A rapid and sensitive method for the quantification of microgram quantities of proteins utilizing the principle of protein-dye binding. - Anal. Biochem. 72: 248-254, 1976. Go to original source...
    10. Calabrese E.J.: Hormesis: changing view of the dose-response, a personal account of the history and current status. - Mutat. Res. 511: 181-189, 2002. Go to original source...
    11. Caldwell M.M.: Solar UV irradiation and the growth and development of higher plants. - In: Giese A.C. (ed.): Photophysiology: Current Topics in Photobiology and Photochemistry. Pp. 131-177. Academic Press, New York 1971. Go to original source...
    12. Chen J.X., Wang X.F.: Guide to Plant Physiological Experiments. Pp. 123-127. South China University of Technology Press, Guangzhou 2002.
    13. Chen K., Arora R.: Priming memory invokes seed stress-tolerance. - Environ. Exp. Bot. 94: 33-45, 2013. Go to original source...
    14. Crisp P.A., Ganguly D., Eichten S.R. et al.: Reconsidering plant memory: Intersections between stress recovery, RNA turnover, and epigenetics. - Sci. Adv. 2: e1501340, 2016. Go to original source...
    15. D±browski P., Kalaji M.H., Baczewska A.H. et al.: Delayed chlorophyll a fluorescence, MR 820, and gas exchange changes in perennial ryegrass under salt stress. - J. Lumin. 183: 322-333, 2017. Go to original source...
    16. D±browski P., Pawlu¶kiewicz B., Baczewska A.H. et al.: Chlorophyll a fluorescence of perennial ryegrass (Lolium perenne L.) varieties under long term exposure to shade. - Zemdirbyste 102: 305-312, 2015. Go to original source...
    17. Doke N.: Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophtora infestans and the hyphal wall components. - Physiol. Plant Pathol. 23: 345-357, 1983. Go to original source...
    18. Fatima A., Kataria S., Agrawal A.K. et al.: Use of synchrotron phase-sensitive imaging for the investigation of magnetopriming and solar UV-exclusion impact on soybean (Glycine max) leaves. - Cells 10: 1725, 2021. Go to original source...
    19. Giannopolitis C.N., Ries S.K.: Superoxide dismutases: I. Occurrence in higher plants. - Plant Physiol. 59: 309-314, 1977. Go to original source...
    20. Gill S.S., Tuteja N.: Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. - Plant Physiol. Bioch. 48: 909-930, 2010. Go to original source...
    21. Halliwell B., Gutteridge J.M.C.: Free Radicals in Biology and Medicine. Pp. 905. Oxford University Press, USA 2015. Go to original source...
    22. Hasanuzzaman M., Bhuyan M.H.M.B., Parvin K. et al.: Regulation of ROS metabolism in plants under environmental stress: A review of recent experimental evidence. - Int. J. Mol. Sci. 21: 8695, 2020. Go to original source...
    23. Heath R.L., Packer L.: Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. - Arch. Biochem. Biophys. 125: 189-198, 1968. Go to original source...
    24. Heyneke E., Luschin-Ebengreuth N., Krajcer I. et al.: Dynamic compartment specific changes in glutathione and ascorbate levels in Arabidopsis plants exposed to different light intensities. - BMC Plant Biol. 13: 104, 2013. Go to original source...
    25. Hussain S., Rao M.J., Anjum M.A. et al.: Oxidative stress and antioxidant defense in plants under drought conditions. - In: Hasanuzzaman M., Hakeem K., Nahar K., Alharby H. (ed.): Plant Abiotic Stress Tolerance. Pp. 207-219. Springer, Cham 2019. Go to original source...
    26. Junglee S., Urban L., Sallanon H., Lopez-Lauri F.: Optimized assay for hydrogen peroxide determination in plant tissue using potassium iodide. - Am. J. Anal. Chem. 5: 730-736, 2014. Go to original source...
    27. Kalaji H., Nalborczyk E.: Gas exchange of barley seedlings growing under salinity stress. - Photosynthetica 25: 197-202, 1991.
    28. Kar M., Mishra D.: Catalase, peroxidase, and polyphenol oxidase activities during rice leaf senescence. - Plant Physiol. 57: 315-319, 1976. Go to original source...
    29. Kaur G., Asthir B.: Molecular responses to drought stress in plants. - Biol. Plantarum 61: 201-209, 2017. Go to original source...
    30. Kollöffel C.: Respiration rate and mitochondrial activity in the cotyledons of Pisum sativum during germination. - Acta Bot. Neerl. 16: 111-122, 1967. Go to original source...
    31. KuĽnicki D., Meller B., Arasimowicz-Jelonek M. et al.: BABA-induced DNA methylome adjustment to intergenerational defense priming in potato to Phytophthora infestans. - Front. Plant Sci. 10: 650, 2019. Go to original source...
    32. Macovei A., Garg B., Raikwar S. et al.: Synergistic exposure of rice seeds to different doses of γ-ray and salinity stress resulted in increased antioxidant enzyme activities and gene-specific modulation of TC-NER pathway. - BioMed Res. Int. 2014: 676934, 2014. Go to original source...
    33. Mancinelli A.L., Yang C.P.H., Lindquist P. et al.: Photocontrol of anthocyanin synthesis: III. The action of streptomycin on the synthesis of chlorophyll and anthocyanin. - Plant Physiol. 55: 251-257, 1975. Go to original source...
    34. Mirecki R.M., Teramura A.H.: Effects of ultraviolet-B irradiance on soybean: V. The dependence of plant sensitivity on the photosynthetic photon flux density during and after leaf expansion. - Plant Physiol. 74: 475-480, 1984. Go to original source...
    35. Nakano Y., Asada K.: Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. - Plant Cell Physiol. 22: 867-880, 1981.
    36. Nayyar H., Gupta D.: Differential sensitivity of C3 and C4 plants to water deficit stress: association with oxidative stress and antioxidants. - Environ. Exp. Bot. 58: 106-113, 2006. Go to original source...
    37. Pandey A.K., Gautam A.: Stress responsive gene regulation in relation to hydrogen sulfide in plants under abiotic stress. - Physiol. Plantarum 168: 511-525, 2020. Go to original source...
    38. Pandey V., Shukla A.: Acclimation and tolerance strategies of rice under drought stress. - Rice Sci. 22: 147-161, 2015. Go to original source...
    39. Pogrzeba M., Rusinowski S., Sitko K. et al.: Relationships between soil parameters and physiological status of Miscanthus × giganteus cultivated on soil contaminated with trace elements under NPK fertilisation vs. microbial inoculation. - Environ. Pollut. 225: 163-174, 2017. Go to original source...
    40. Pradhan B., Baral S., Patra S. et al.: Delineation of gamma irradiation (60Co) induced oxidative stress by decrypting antioxidants and biochemical responses of microalga, Chlorella sp. - Biocatal. Agric. Biotechnol. 25: 101595, 2020. Go to original source...
    41. Rapacz M., Sasal M., Kalaji H.M., Ko¶cielniak J.: Is the OJIP test a reliable indicator of winter hardiness and freezing tolerance of common wheat and triticale under variable winter environments? - PLoS ONE 10: e0134820, 2015. Go to original source...
    42. Rawat N., Singla-Pareek S.L., Pareek A.: Membrane dynamics during individual and combined abiotic stresses in plants and tools to study the same. - Physiol. Plantarum 171: 653-676, 2021. Go to original source...
    43. Reddy A.R., Chaitanya K.V., Vivekanandan M.: Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. - J. Plant Physiol. 161: 1189-1202, 2004. Go to original source...
    44. Rossatto T., Amaral M.N., Benitez L.C. et al.: Gene expression and activity of antioxidative enzymes in rice plants, cv. BRS AG, under saline stress. - Physiol. Mol. Biol. Pla. 23: 865-875, 2017. Go to original source...
    45. Schmitt N., Dizengremel P.: Effect of osmotic stress on mitochondria isolated from etiolated mung bean and sorghum seedlings. - Plant Physiol. Bioch. 27: 17-26, 1989.
    46. Seleiman M.F., Al-Suhaibani N., Ali N. et al.: Drought stress impacts on plants and different approaches to alleviate its adverse effects. - Plants 10: 259, 2021. Go to original source...
    47. Semwal V.K., Khanna-Chopra R.: Reproductive sink enhanced drought induced senescence in wheat fertile line is associated with loss of antioxidant competence compared to its CMS line. - Physiol. Mol. Biol. Pla. 24: 591-604, 2018. Go to original source...
    48. Sen A., Challabathula D., Puthur J.T.: UV-B priming of Oryza sativa seeds augments the innate tolerance potential in a tolerant variety more effectively toward NaCl and PEG stressors. - J. Plant Growth Regul. 40: 1166-1180, 2021. Go to original source...
    49. Sen A., Puthur J.T.: Seed priming-induced physiochemical and molecular events in plants coupled to abiotic stress tolerance: an overview. - In: Hossain M.A., Liu F., Burritt D.J. et al. (ed.): Priming-Mediated Stress and Cross-Stress Tolerance in Crop Plants. Pp. 303-316. Academic Press, London 2020. Go to original source...
    50. Sen A., Puthur J.T.: Halo- and UV-B priming-mediated drought tolerance and recovery in rice seedlings. - Plant Stress 2: 100011, 2021. Go to original source...
    51. Sheteiwy M.S., Gong D., Gao Y. et al.: Priming with methyl jasmonate alleviates polyethylene glycol-induced osmotic stress in rice seeds by regulating the seed metabolic profile. - Environ. Exp. Bot. 153: 236-248, 2018. Go to original source...
    52. Sohag A.A.M., Tahjib-Ul-Arif M., Brestič M. et al.: Exogenous salicylic acid and hydrogen peroxide attenuate drought stress in rice. - Plant Soil Environ. 66: 7-13, 2020. Go to original source...
    53. Srivastava A., Strasser R.J., Govindjee: Differential effects of dimethylbenzoquinone and dichlorobenzoquinone on chlorophyll fluorescence transient in spinach thylakoids. - J. Photoch. Photobio. B 31: 163-169, 1995. Go to original source...
    54. 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...
    55. Sytar O., Zivcak M., Bruckova K. et al.: Shift in accumulation of flavonoids and phenolic acids in lettuce attributable to changes in ultraviolet radiation and temperature. - Sci. Hortic.-Amsterdam 239: 193-204, 2018. Go to original source...
    56. Tóth S.Z., Nagy V., Puthur J.T. et al.: The physiological role of ascorbate as photosystem II electron donor: protection against photoinactivation in heat-stressed leaves. - Plant Physiol. 156: 382-392, 2011. Go to original source...
    57. Tuba Z., Saxena D.K., Srivastava K. et al.: Chlorophyll a fluorescence measurements for validating the tolerant bryophytes for heavy metal (Pb) bio mapping. - Curr. Sci. 98: 1505-1508, 2010.
    58. Valenzuela-Avendaño J.P., Mota I.A.E., Uc G.L. et al.: Use of a simple method to isolate intact RNA from partially hydrated Selaginella lepidophylla plants. - Plant Mol. Biol. Rep. 23: 199-200, 2005. Go to original source...
    59. Vozhehova R., Kokovikhin S., Lykhovyd P.V. et al.: Statistical yielding models of some irrigated vegetable crops in dependence on water use and heat supply. - J. Water Land Dev. 45: 190-197, 2020. Go to original source...
    60. Wang X., Wang L., Shangguan Z.: Leaf gas exchange and fluorescence of two winter wheat varieties in response to drought stress and nitrogen supply. - PLoS ONE 11: e0165733, 2016. Go to original source...
    61. Wei Y., Liu W., Hu W. et al.: The chaperone MeHsp90 recruits MeWRKY20 and MeCatalase1 to regulate drought stress resistance in cassava. - New Phytol. 226: 476-491, 2020. Go to original source...
    62. Yamane K., Kawasaki M., Taniguchi M., Miyake H.: Correlation between chloroplast ultrastructure and chlorophyll fluorescence characteristics in the leaves of rice (Oryza sativa L.) grown under salinity. - Plant Prod. Sci. 11: 139-145, 2008. Go to original source...
    63. Yin D., Chen S., Chen F. et al.: Morphological and physiological responses of two chrysanthemum cultivars differing in their tolerance to waterlogging. - Environ. Exp. Bot. 67: 87-93, 2009. Go to original source...
    64. Zhang H., Xu N., Li X., Gu S.: Overexpression of 2-Cys Prx increased salt tolerance of photosystem Ⅱ (PSⅡ) in tobacco. - Peer J. Preprints: e2500v1, 2016. Go to original source...
    65. Zheng X.T., Yu Z.C., Tang J.W. et al.: The major photoprotective role of anthocyanins in leaves of Arabidopsis thaliana under long-term high light treatment: antioxidant or light attenuator? -Photosynth. Res. 149: 25-40, 2021. Go to original source...

    Return to the content