Skip to main content
SpringerLink
Log in

Autophagy and Programmed Cell Death Are Critical Pathways in Jasmonic Acid Mediated Saline Stress Tolerance in Oryza sativa

  • Original Article
  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Saline stress is the most limiting condition impacting the plant growth, development, and productivity. In this present study, jasmonic acid (JA) was used as a foliar spray on the rice seedlings grown under saline stress. Increase in photosynthetic pigments, anthocyanin, and total protein content was observed with JA treatment while NaCl showed reduction in biochemical constituents and enhanced antioxidant enzyme activity. The leaf cells of NaCl-treated seedlings accumulated more ROS and had more fragmented nuclei, whereas JA decreased the accumulation and fragmentation during saline stress. In NaCl treatment, gene expression analysis showed many fold upregulation in comparison with other treatments. The results suggest that JA acts as a promoter for growth, physiological, biochemical, and cellular contents, as well as ameliorate the effects of saline stress. The expression of genes demonstrated that saline stress may promote autophagy, which leads to autophagic cell death, and improve tolerance to saline stress in rice seedlings via the jasmonic acid signaling pathway. However, the mechanism by which jasmonate signaling induces autophagy and cell death is unknown and requires further exploration.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data Availability

Not applicable.

Code Availability

Not applicable.

References

  1. Wasternack, C., & Hause, B. (2013). Jasmonates: Biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Annals of Botany, 111(6), 1021–1058

  2. Santino, A., Taurino, M., De Domenico, S., Bonsegna, S., Poltronieri, P., Pastor, V., & Flors, V. (2013). Jasmonate signaling in plant development and defense response to multiple (a)biotic stresses. Plant Cell Reports. https://doi.org/10.1007/s00299-013-1441-2

    Article  PubMed  Google Scholar 

  3. El-Esawi, M. A. (2016). Jasmonic acid: Genetic pathway, signal transduction and action in plant development and defence. Biochemistry & Physiology: Open Access, 5(2), 1–2. https://doi.org/10.4172/2165-7890.1000E149

    Article  Google Scholar 

  4. Qiu, Z., Guo, J., Zhu, A., Zhang, L., & Zhang, M. (2014). Exogenous jasmonic acid can enhance tolerance of wheat seedlings to salt stress. Ecotoxicology and Environmental Safety. https://doi.org/10.1016/j.ecoenv.2014.03.014

    Article  PubMed  Google Scholar 

  5. Munns, R. (2002). Comparative physiology of salt and water stress. Plant, Cell and Environment, 25(2), 239–250. https://doi.org/10.1046/J.0016-8025.2001.00808.X

    Article  CAS  PubMed  Google Scholar 

  6. Qin, H., & Huang, R. (2020). The phytohormonal regulation of Na+/K+ and reactive oxygen species homeostasis in rice salt response. Molecular Breeding, 40(5), 1–13. https://doi.org/10.1007/S11032-020-1100-6

    Article  Google Scholar 

  7. Ma, X., Feng, F., Wei, H., Mei, H., Xu, K., Chen, S., & Luo, L. (2016). Genome-wide association study for plant height and grain yield in rice under contrasting moisture regimes. Frontiers in Plant Science, 7(NOVEMBER2016), 1801. https://doi.org/10.3389/FPLS.2016.01801/BIBTEX

    Article  PubMed  PubMed Central  Google Scholar 

  8. Muranaka, S., Shimizu, K., & Kato, M. (2002). Ionic and osmotic effects of salinity on single-leaf photosynthesis in two wheat cultivars with different drought tolerance. Photosynthetica, 40(2), 201–207. https://doi.org/10.1023/A:1021337522431

    Article  CAS  Google Scholar 

  9. Murphy, L. R., Kinsey, S. T., & Durako, M. J. (2003). Physiological effects of short-term salinity changes on Ruppia maritima. Aquatic Botany, 4(75), 293–309. https://doi.org/10.1016/S0304-3770(02)00206-1

    Article  Google Scholar 

  10. Zhu, J. K. (2016). Abiotic stress signaling and responses in plants. Cell, 167(2), 313–324. https://doi.org/10.1016/J.CELL.2016.08.029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Miller, G., Suzuki, N., Ciftci-Yilmaz, S., & Mittler, R. (2010). Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, Cell and Environment. https://doi.org/10.1111/j.1365-3040.2009.02041.x

    Article  PubMed  Google Scholar 

  12. He, C., & Klionsky, D. J. (2009). Regulation mechanisms and signaling pathways of autophagy. Annual review of genetics, 43, 67. https://doi.org/10.1146/Annurev-Genet-102808-114910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Mizushima, N., Yoshimori, T., & Ohsumi, Y. (2011). The role of Atg proteins in autophagosome formation. Annual review of cell and developmental biology, 27, 107–132. https://doi.org/10.1146/ANNUREV-CELLBIO-092910-154005

    Article  CAS  PubMed  Google Scholar 

  14. Gong, Q., Li, P., Ma, S., Indu Rupassara, S., & Bohnert, H. J. (2005). Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. The Plant journal : For cell and molecular biology, 44(5), 826–839. https://doi.org/10.1111/J.1365-313X.2005.02587.X

    Article  CAS  Google Scholar 

  15. Liu, Y., Xiong, Y., & Bassham, D. C. (2009). Autophagy is required for tolerance of drought and salt stress in plants. Autophagy. https://doi.org/10.4161/auto.5.7.9290

    Article  PubMed  PubMed Central  Google Scholar 

  16. Xia, K., Liu, T., Ouyang, J., Wang, R., Fan, T., & Zhang, M. (2011). Genome-wide identification, classification, and expression analysis of autophagy-associated gene homologues in rice (Oryza sativa L.). DNA research : an international journal for rapid publication of reports on genes and genomes, 18(5), 363–377. https://doi.org/10.1093/DNARES/DSR024

    Article  CAS  Google Scholar 

  17. Zhai, Y., Guo, M., Wang, H., Lu, J., Liu, J., Zhang, C., & Lu, M. (2016). Autophagy, a conserved mechanism for protein degradation, responds to heat, and other abiotic stresses in Capsicum annuum L. Frontiers in Plant Science. https://doi.org/10.3389/fpls.2016.00131

    Article  PubMed  PubMed Central  Google Scholar 

  18. Liao, C. Y., & Bassham, D. C. (2020). Combating stress: The interplay between hormone signaling and autophagy in plants. Journal of experimental botany, 71(5), 1723–1733. https://doi.org/10.1093/JXB/ERZ515

    Article  CAS  PubMed  Google Scholar 

  19. Gou, W., Li, X., Guo, S., Liu, Y., Li, F., & Xie, Q. (2019). Autophagy in plant: A new orchestrator in the regulation of the phytohormones homeostasis. International Journal of Molecular Sciences, 20(12), 2900.

  20. Yoshimoto, K., Jikumaru, Y., Kamiya, Y., Kusano, M., Consonni, C., Panstruga, R., & Shirasu, K. (2009). Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. The Plant Cell, 21(9), 2914–2927. https://doi.org/10.1105/TPC.109.068635

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Mackinney, G. (1941). Absorption of light by chlorophyll. Absorption of Light by Chlorophyll, 140, 315–323.

    CAS  Google Scholar 

  22. Laxmi, A., Paul, L. K., Raychaudhuri, A., Peters, J. L., & Khurana, J. P. (2006). Arabidopsis cytokinin-resistant mutant, cnr1, displays altered auxin responses and sugar sensitivity. Plant Molecular Biology, 62(3), 409–425. https://doi.org/10.1007/s11103-006-9032-z

    Article  CAS  PubMed  Google Scholar 

  23. Lowry, O. H., Rosebrough, N. J., Farr, A. L., & Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. The Journal of Biological Chemistry, 193(1), 265–75.

  24. Idrees, M., Naeem, M., Aftab, T., Khan, M. M. A.,& Moinuddin. (2011). Salicylic acid mitigates salinity stress by improving antioxidant defence system and enhances vincristine and vinblastine alkaloids production in periwinkle [Catharanthus roseus (L.) G. Don]. Acta Physiologiae Plantarum, 33(3), 987–999.https://doi.org/10.1007/s11738-010-0631-6

  25. Chandlee, J. M., & Scandalios, J. G. (1984). Analysis of variants affecting the catalase developmental program in maize scutellum. Theoretical and Applied Genetics. https://doi.org/10.1007/BF00262543

    Article  PubMed  Google Scholar 

  26. Beauchamp, C., & Fridovich, I. (1971). Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels. Analytical biochemistry, 44(1), 276–87. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/4943714. Accessed 01.12.2018

  27. Khan, M. S., Pandey, M. K., & Hemalatha, S. (2018). Comparative studies on the role of organic biostimulant in resistant and susceptible cultivars of rice grown under saline stress - organic biostimulant alleviate saline stress in tolerant and susceptible cultivars of rice. Journal of Crop Science and Biotechnology, 21(5), 459–467.

  28. Sudhir, P., & Murthy, S. D. S. (2004). Effects of salt stress on basic processes of photosynthesis. Photosynthetica. https://doi.org/10.1007/S11099-005-0001-6

    Article  Google Scholar 

  29. Qados, A. A. M. S. (2011). Effect of salt stress on plant growth and metabolism of bean plant Vicia faba (L.). Journal of the Saudi Society of Agricultural Sciences, 10(1), 7–15.

  30. Ayala-Astorga, G. I., & Alcaraz-Meléndez, L. (2010). Salinity effects on protein content, lipid peroxidation, pigments, and proline in Paulownia imperialis (Siebold & Zuccarini) and Paulownia fortunei (Seemann & Hemsley) grown in vitro. Electronic Journal of Biotechnology. https://doi.org/10.2225/vol13-issue5-fulltext-13

    Article  Google Scholar 

  31. Qiu, Z. B., Guo, J. L., Zhu, A. J., Zhang, L., & Zhang, M. M. (2014). Exogenous jasmonic acid can enhance tolerance of wheat seedlings to salt stress. Ecotoxicology and environmental safety, 104(1), 202–208. https://doi.org/10.1016/J.ECOENV.2014.03.014

    Article  CAS  PubMed  Google Scholar 

  32. Parida, A. K., Das, A. B., & Mohanty, P. (2004). Defense potentials to NaCl in a mangrove, Bruguiera parviflora: Differential changes of isoforms of some antioxidative enzymes. Journal of Plant Physiology, 161(5), 531–542.

  33. Jithesh, M. N., Prashanth, S. R., Sivaprakash, K. R., & Parida, A. K. (2006). Antioxidative response mechanisms in halophytes: Their role in stress defence. Journal of Genetics, 85(3), 237–254. https://doi.org/10.1007/BF02935340

    Article  CAS  PubMed  Google Scholar 

  34. Matamoros, M. A. (2003). Biochemistry and molecular biology of antioxidants in the rhizobia-legume symbiosis. PLANT PHYSIOLOGY. https://doi.org/10.1104/pp.103.025619

    Article  PubMed  PubMed Central  Google Scholar 

  35. Anjum, S. A., Xie, X., & Wang, L. (2011). Morphological, physiological and biochemical responses of plants to drought stress. African Journal of Agricultural Research. https://doi.org/10.5897/AJAR10.027

    Article  Google Scholar 

  36. Li, Q., Yang, A., & Zhang, W. H. (2017). Comparative studies on tolerance of rice genotypes differing in their tolerance to moderate salt stress. BMC Plant Biology. https://doi.org/10.1186/s12870-017-1089-0

    Article  PubMed  PubMed Central  Google Scholar 

  37. Yazdani, M., & Mahdieh, M. (2012). Salinity induced apoptosis in root meristematic cells of rice, 2(1), 2–5. https://doi.org/10.7763/IJBBB.2012.V2.66

    Article  Google Scholar 

  38. Browse, J. (2009). Jasmonate passes muster: A receptor and targets for the defense hormone. Annual Review of Plant Biology. https://doi.org/10.1146/annurev.arplant.043008.092007

    Article  PubMed  Google Scholar 

  39. Santino, A., Taurino, M., De Domenico, S., Bonsegna, S., Poltronieri, P., Pastor, V., & Flors, V. (2013). Jasmonate signaling in plant development and defense response to multiple (a)biotic stresses. Plant cell reports, 32(7), 1085–1098. https://doi.org/10.1007/S00299-013-1441-2

    Article  CAS  PubMed  Google Scholar 

  40. Svyatyna, K., & Riemann, M. (2012). Light-dependent regulation of the jasmonate pathway. Protoplasma. https://doi.org/10.1007/s00709-012-0409-3

    Article  PubMed  Google Scholar 

  41. Lu, Z., Liu, D., & Liu, S. (2007). Two rice cytosolic ascorbate peroxidases differentially improve salt tolerance in transgenic Arabidopsis. Plant Cell Reports. https://doi.org/10.1007/s00299-007-0395-7

    Article  PubMed  Google Scholar 

  42. Pérez-Clemente, R. M., Vives, V., Zandalinas, S. I., López-Climent, M. F., Muñoz, V., & Gómez-Cadenas, A. (2013). Biotechnological approaches to study plant responses to stress. BioMed Research International. https://doi.org/10.1155/2013/654120

    Article  PubMed  Google Scholar 

  43. Im, J. H., Lee, H., Kim, J., Kim, H. B., Seyoung, K., Kim, B. M., & An, C. S. (2012). A salt stress-activated mitogen-activated protein kinase in soybean is regulated by phosphatidic acid in early stages of the stress response. Journal of Plant Biology. https://doi.org/10.1007/s12374-011-0036-8

    Article  Google Scholar 

  44. Yousfi, F. E., Makhloufi, E., Marande, W., Ghorbel, A. W., Bouzayen, M., & Bergès, H. (2017). Comparative analysis of WRKY genes potentially involved in salt stress responses in Triticum turgidum L. ssp. durum. Frontiers in Plant Science, 7, 2034. https://doi.org/10.3389/fpls.2016.02034

  45. Lai, Z., Wang, F., Zheng, Z., Fan, B., & Chen, Z. (2011). A critical role of autophagy in plant resistance to necrotrophic fungal pathogens. Plant Journal. https://doi.org/10.1111/j.1365-313X.2011.04553.x

    Article  Google Scholar 

  46. Akimoto-Tomiyama, C., Sakata, K., Yazaki, J., Nakamura, K., Fujii, F., Shimbo, K., & Minami, E. (2003). Rice gene expression in response to N-acetylchitooligosaccharide elicitor: Comprehensive analysis by DNA microarray with randomly selected ESTs. Plant Molecular Biology. https://doi.org/10.1016/j.athoracsur.2017.01.116

    Article  PubMed  Google Scholar 

  47. Ramamoorthy, R., Jiang, S. Y., Kumar, N., Venkatesh, P. N., & Ramachandran, S. (2008). A comprehensive transcriptional profiling of the WRKY gene family in rice under various abiotic and phytohormone treatments. Plant and Cell Physiology. https://doi.org/10.1093/pcp/pcn061

    Article  PubMed  Google Scholar 

  48. Miao, Y., Laun, T. M., Smykowski, A., & Zentgraf, U. (2007). Arabidopsis MEKK1 can take a short cut: It can directly interact with senescence-related WRKY53 transcription factor on the protein level and can bind to its promoter. Plant Molecular Biology. https://doi.org/10.1007/s11103-007-9198-z

    Article  PubMed  Google Scholar 

  49. Besseau, S., Li, J., & Palva, E. T. (2012). WRKY54 and WRKY70 co-operate as negative regulators of leaf senescence in Arabidopsis thaliana. Journal of Experimental Botany. https://doi.org/10.1093/jxb/err450

    Article  PubMed  PubMed Central  Google Scholar 

  50. Tsugane, K., Kobayashi, K., Niwa, Y., Ohba, Y., Wada, K., & Kobayashi, H. (1999). A recessive Arabidopsis mutant that grows photoautotrophically under salt stress shows enhanced active oxygen detoxification. The Plant Cell, 11(7), 1195–1206. https://doi.org/10.1105/TPC.11.7.1195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Slavikova, S., Ufaz, S., Avin-Wittenberg, T., Levanony, H., & Galili, G. (2008). An autophagy-associated Atg8 protein is involved in the responses of Arabidopsis seedlings to hormonal controls and abiotic stresses. Journal of Experimental Botany. https://doi.org/10.1093/jxb/ern244

    Article  PubMed  PubMed Central  Google Scholar 

  52. Bassham, D. C., Laporte, M., Marty, F., Moriyasu, Y., Ohsumi, Y., Olsen, L. J., & Yoshimoto, K. (2006). Autophagy in development and stress responses of plants. Autophagy. https://doi.org/10.4161/auto.2092

    Article  PubMed  Google Scholar 

  53. Shibuya, K., Niki, T., & Ichimura, K. (2013). Pollination induces autophagy in petunia petals via ethylene. Journal of Experimental Botany, 64(4), 1111. https://doi.org/10.1093/JXB/ERS395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by B. S. Abdur Rahman Crescent Institute of Science and Technology, Chennai, TN, India.

Author information

Authors and Affiliations

  1. School of Life Sciences, B. S. Abdur Rahman Crescent Institute of Science and Technology, Chennai, TN, India

    Mohd Shahanbaj Khan & S. Hemalatha

Authors
  1. Mohd Shahanbaj Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Hemalatha
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. Hemalatha.

Ethics declarations

Ethics Approval

Not applicable.

Consent to Participate

Not applicable.

Consent for Publication

Not applicable.

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khan, M.S., Hemalatha, S. Autophagy and Programmed Cell Death Are Critical Pathways in Jasmonic Acid Mediated Saline Stress Tolerance in Oryza sativa. Appl Biochem Biotechnol 194, 5353–5366 (2022). https://doi.org/10.1007/s12010-022-04032-1

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-022-04032-1

Keywords

Search

Navigation