biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 65:184-192, 2021 | DOI: 10.32615/bp.2021.008

Spermine alleviates heat-induced senescence in creeping bentgrass by regulating water and oxidative balance, photosynthesis, and heat shock proteins

L.L. LIANG, Y.Q. CAO, D. WANG, Y. PENG, Y. ZHANG, Z. LI*
Department of Grassland Science, College of Animal Science and Technology, Sichuan Agricultural University,
Chengdu 611130, China

Spermine (SPM) is involved in response to abiotic stress in plants, but the potential role of SPM in regulating senescence has not been well documented. Objectives of this study were to examine the effect of changes in endogenous polyamines (PAs) by SPM application on improving heat tolerance of creeping bentgrass (Agrostis stolonifera) and explore the SPM-regulated senescence associated with alterations of water and oxidative balance, photosynthesis, and heat shock proteins under heat stress. The results showed that persistent high temperature caused severe oxidative damage and significant decreases in chlorophyll (Chl) content, photosynthetic efficiency, and leaf water content leading to premature senescence in creeping bentgrass, as reflected by a significant upregulation of transcriptions of senescence-associated genes (AsSAG39, Ash36, and Asl20). The improvement of endogenous spermidine (SPD) and SPM content induced by SPM application could significantly alleviate heat stress damage to creeping bentgrass through maintaining higher Chl content, net photosynthetic rate, photochemical efficiency, and performance index on absorption basis, promoting osmotic adjustment ability and antioxidant enzyme (superoxid dismutase, catalase, peroxidase, and ascorbate peroxidase) activities to enhance the scavenging capacity of reactive oxygen species, and upregulating transcriptions of heat shock protein (HSP) genes (HSP90-5, HSP90.1-b1, HSP82, HSP70, HSP26.7, HSP17.8, and HSP12) helping to maintain normal synthesis and functions of proteins under high temperature stress, thereby delaying heat-induced leaf senescence. These findings reveal an important role of PAs in regulating senescence in perennial plants exposed to a high temperature environment.

Keywords: Agrostis stolonifera, antioxidants, osmotic adjustment, polyamines, reactive oxygen species, photochemical efficiency, thermotolerance.

Received: September 14, 2020; Revised: February 4, 2021; Accepted: February 9, 2021; Published online: July 13, 2021  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
LIANG, L.L., CAO, Y.Q., WANG, D., PENG, Y., ZHANG, Y., & LI, Z. (2021). Spermine alleviates heat-induced senescence in creeping bentgrass by regulating water and oxidative balance, photosynthesis, and heat shock proteins. Biologia plantarum65, Article 184-192. https://doi.org/10.32615/bp.2021.008
Download citation

Supplementary files

Download file6606_Liang_Suppl.pdf

File size: 254.32 kB

References

  1. Arnon, D.I.: Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. - Plant Physiol. 24: 1-15, 1949. Go to original source...
  2. Barrs, H.D., Weatherley, P.E.: A re-examination of the relative turgidity technique for estimating water deficits in leaves. - Aust. J. biol. Sci. 15: 413-428, 1962. Go to original source...
  3. Bian, H.W., Wang, J.H., Lin, W.Q., Ning, H., Zhu, M.Y.: Accumulation of soluble sugars, heat-stable proteins and dehydrins in cryopreservation of protocorm-like bodies of Dendrobium candidum by the air-drying method. - J. Plant Physiol. 159: 1139-1145, 2002. Go to original source...
  4. Blum, A., Ebercon, A.: Cell membrane stability as a measure of drought and heat tolerance in wheat. - Crop Sci. 21: 43-47, 1981. Go to original source...
  5. Camejo, D., Rodríguez, P., Ma, A.M., Dell'Amico, J.M., Torrecillas, A., Alarcón, J.J.: High temperature effects on photosynthetic activity of two tomato cultivars with different heat susceptibility. - J. Plant Physiol. 162: 281-289, 2005. Go to original source...
  6. Chance, B., Maehly, A.C.: Assay of catalases and peroxidases. - Methods Enzymol. 2: 764-775, 1955. Go to original source...
  7. Dhindsa, R.: Leaf senescence: correlation with increased levels of membrane permeability and lipid peroxidation and increased levels of superoxide dismutase and catalase. - J. exp. Bot. 32: 93-101, 1981. Go to original source...
  8. Elstner, E.F., Heupel, A.: Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase. - Anal. Biochem. 70: 616-620, 1976. Go to original source...
  9. Fu, X.Z., Xing, F., Wang, N.Q., Peng, L.Z., Chun C.P., Cao L., Ling L.L., Jiang C.L.: Exogenous spermine pretreatment confers tolerance to combined high-temperature and drought stress in vitro in trifoliate orange seedlings via modulation of antioxidative capacity and expression of stress-related genes. - Biotechnol. Biotechnol. Equipment. 28: 192-198, 2014. Go to original source...
  10. Giannopolitis, C.N., Ries, S.K.: Superoxide dismutases: I. Occurrence in higher plants. - Plant Physiol. 59: 309-314, 1977. Go to original source...
  11. Giles, K.L., Cohen, D., Beardsell, M.F.: Effects of water stress on the ultrastructure of leaf cells of sorghum bicolor. - Plant Physiol. 57: 11-14, 1976. Go to original source...
  12. Gill, S.S., Tuteja, N.: Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. - Plant Physiol. Biochem. 48: 909-930, 2010. Go to original source...
  13. Graham, I.A., Smith, L.S.M.: Induction of malate synthase gene expression in senescent and detached organs of cucumber. - Plant Cell 4: 349-357, 1992. Go to original source...
  14. Haba, P.D.L., Mata, L.D.L., Molina, E., Agueera, E.: High temperature promotes early senescence in primary leaves of sunflower (Helianthus annuus L.) plants. - Can. J. Plant. Sci. 94: 659-669, 2014. Go to original source...
  15. Hamdani, S., Gauthier, A., Msilini, N., Carpentier, R.: Positive charges of polyamines protect PSII in isolated thylakoid membranes during photoinhibitory conditions. - Plant Cell Physiol. 52: 866-873, 2011. Go to original source...
  16. Haslbeck, M.: sHsps and their role in the chaperone network. - Cell. Mol. Life Sci. 59: 1649-1657, 2002. Go to original source...
  17. Hoagland, D.R., Arnon, D.I.: The water culture method for growing plants without soil. - Calif. Agr. Exp. Sta. Circular 347: 357-359, 1950.
  18. Huang, B.R., Xu, C.P: Identification and characterization of proteins associated with plant tolerance to heat stress. - J. integr. Plant Biol. 50: 1230-1237, 2008. Go to original source...
  19. Jespersen, D., Zhang, J., Huang, B.R.: Chlorophyll loss associated with heat-induced senescence in bentgrass. - Plant Sci. 249: 1-12, 2016. Go to original source...
  20. Jiang, C.H., Xu, J.Y., Zhang, H., Zhang, X., Ming, F.: A cytosolic class I small heat shock protein, RcHSP17.8, of Rosa chinensis confers resistance to a variety of stresses to Escherichia coli, yeast and Arabidopsis thaliana. - Plant Cell Environ. 32: 1046-1059, 2009. Go to original source...
  21. Jibran, R., Hunter, D., Dijkwel, P.: Hormonal regulation of leaf senescence through integration of developmental and stress signals. - Plant mol. Biol. 82: 547-561, 2013. Go to original source...
  22. Kim, K.H., Alam, I., Kim, Y.G., Sharmin, S.A., Lee, K.W., Lee, S.H., Lee, B.H.: Overexpression of a chloroplast-localized small heat shock protein OsHSP26 confers enhanced tolerance against oxidative and heat stresses in tall fescue. - Biotechnol. Lett. 34: 371-377, 2012. Go to original source...
  23. Kubik, C., Honig, J., Bonos, S.A.: Characterization of 215 simple sequence repeat markers in creeping bentgrass (Agrostis stolonifera L.). - Mol. Ecol. Resour. 11: 872-876, 2011. Go to original source...
  24. Kumar, S., Gupta, D., Nayyar, H.: Comparative response of maize and rice genotypes to heat stress: status of oxidative stress and antioxidants. - Acta Physiol. Plant. 34: 75-86, 2012. Go to original source...
  25. Kusano, T., Yamaguchi, K., Berberich, T., Takahashi, Y.: The polyamine spermine rescues Arabidopsis from salinity and drought stresses. - Plant Signal. Behav. 2: 251-252, 2007. Go to original source...
  26. Li, S., Cui, L., Zhang, Y., Wang, Y., Mao, P.: The variation tendency of polyamines forms and components of polyamine metabolism in Zoysiagrass (Zoysia japonica Steud.) to salt stress with exogenous spermidine application. - Front. Physiol. 8: 208, 2017. Go to original source...
  27. Li, Z., Jing, W., Peng, Y., Quan, X., Xiao, Z.: Spermine alleviates drought stress in white clover with different resistance by influencing carbohydrate metabolism and dehydrins synthesis. - PLoS ONE 10: e0120708, 2015b. Go to original source...
  28. Li, Z., Zhang, Y., Zhang, X., Peng, Y., Merewitz, E., Ma, X., Huang, L., Yan, Y.: The alterations of endogenous polyamines and phytohormones induced by exogenous application of spermidine regulate antioxidant metabolism, metallothionein and relevant genes conferring drought tolerance in white clover. - Environ. exp. Bot. 124: 22-38, 2016. Go to original source...
  29. Li, Z., Zhou, H., Peng, Y., Zhang, X., Ma, X., Huang, L., Yan, Y.: Exogenously applied spermidine improves drought tolerance in creeping bentgrass associated with changes in antioxidant defense, endogenous polyamines and phytohormones. - Plant Growth Regul. 76: 71-82, 2015a. Go to original source...
  30. Liu, T., Liu, Z., Li, Z., Peng, Y., He, L.: Regulation of heat shock factor pathways by γ-aminobutyric acid (GABA) associated with thermotolerance of creeping bentgrass. - Int. J. mol. Sci. 20: 4713-4730, 2019. Go to original source...
  31. Livak, K.J., Schmittgen, T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. - Methods 25: 402-408, 2001. Go to original source...
  32. Moskova, I., Todorova, D., Alexieva, V., Segiev, I.: Protective effect of hydrogen peroxide against paraquat toxicity in young pea plants: possible role of endogenous polyamines. - Amer. J. Plant Sci. 5: 3408-3416, 2014. Go to original source...
  33. Mostofa, M.G., Yoshida, N., Fujita, M.: Spermidine pretreatment enhances heat tolerance in rice seedlings through modulating antioxidative and glyoxalase systems. - Plant Growth Regul. 73: 31-44, 2014. Go to original source...
  34. Murkowski, A.: Heat stress and spermidine: effect on chlorophyll fluorescence in tomato plants. - Biol. Plant. 44: 53-57, 2001. Go to original source...
  35. Nahar, K., Hasanuzzaman, M., Alam, M.M., Rahman, A., Mahmud, J.A., Suzuki, T., Fujita, M.: Insights into spermine-induced combined high temperature and drought tolerance in mung bean: osmoregulation and roles of antioxidant and glyoxalase system. - Protoplasma 254: 445-460, 2017. Go to original source...
  36. Nakano, Y., Asada, K.: Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. - Plant Cell Physiol. 22: 867-880, 1980. Go to original source...
  37. Perez-Amador, M.A., Leon, J., Green, P.J., Carbonell, J.: Induction of the arginine decarboxylase ADC2 gene provides evidence for the involvement of polyamines in the wound response in Arabidopsis. - Plant Physiol. 130: 1454-1463, 2002. Go to original source...
  38. Puyang, X.H., An, M.Y., Xu, L.X., Han, L.B., Zhang, X.Z.: Protective effect of exogenous spermidine on ion and polyamine metabolism in Kentucky bluegrass under salinity stress. - Hort. environ. Biotech. 57: 11-19, 2016. Go to original source...
  39. Ramos, R.M., Valente, I.M., Rodrigues, J.A.: Analysis of biogenic amines in wines by salting-out assisted liquid-liquid extraction and high-performance liquid chromatography with fluorimetric detection. - Talanta 124: 146-151, 2014. Go to original source...
  40. Sagor, G.H.M., Berberich, T., Takahashi, Y., Niitsu, M.: The polyamine spermine protects Arabidopsis from heat stress-induced damage by increasing expression of heat shock-related genes. - Transgenic Res. 22: 595-605, 2013. Go to original source...
  41. Sanchez-Rodriguez, E., Romero, L., Ruiz, J.M.: Accumulation of free polyamines enhances the antioxidant response in fruits of grafted tomato plants under water stress. - J. Plant Physiol. 190: 72-78, 2016. Go to original source...
  42. Schramm, F., Ganguli, A., Kiehlmann, E., Englich, G., Walch, D., Koskull-Döring, P.V.: The heat stress transcription factor HsfA2 serves as a regulatory amplifier of a subset of genes in the heat stress response in Arabidopsis. - Plant mol. Biol. 60: 759-772, 2006. Go to original source...
  43. Shukla, V., Ma, Y., Merewitz, E.B: Creeping bentgrass responses to drought stress and polyamine application. - J. amer. Soc. hort. Sci. 140: 102-107, 2015. Go to original source...
  44. Sun, L., Liu, Y., Kong, X., Zhang, D., Pan, J., Zhou, Y., Wang, L., Li, D., Yang, X.: ZmHSP16.9, a cytosolic class I small heat shock protein in maize (Zea mays), confers heat tolerance in transgenic tobacco. - Plant Cell Rep. 31: 1473-1484, 2012. Go to original source...
  45. Timperio, A.M., Egidi, M.G., Zolla, L.: Proteomics applied on plant abiotic stresses: role of heat shock proteins (HSP). - J. Proteomics 71: 391-411, 2008. Go to original source...
  46. Todorova, D., Katerova, Z., Shopova, E., Jodinskiene, M., Sergiev, I.: Responses of pea plants to heat stress and spermine treatment. - Zemdirbyste 103: 99-106, 2016. Go to original source...
  47. Tsukaguchi, T., Fukamachi, H., Ozawa, K., Takeda, H., Suzuki, K., Egawa, Y.: Diurnal change in water balance of heat-tolerant snap bean (Phaseolus vulgaris) cultivar and its association with growth under high temperature. - Plant Prod. Sci. 8: 375-382, 2005. Go to original source...
  48. Velikova, V., Yordanov, I., Edreva, A.: Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. - Plant Sci. 151: 59-66, 2000. Go to original source...
  49. Yamaguchi, K., Takahashi, Y., Berberich, T., Imai, A., Miyazaki, A., Takahashi, T., Michael, A., Kusano, T.: The polyamine spermine protects against high salt stress in Arabidopsis thaliana. - FEBS Lett. 580: 6783-6788, 2006. Go to original source...
  50. Yamaguchi, K., Takahashi, Y., Berberich, T., Imai, A., Takahashi, T., Michael, A.J., Kusano, T.: A protective role for the polyamine spermine against drought stress in Arabidopsis. - Biochem. biophys. Res. Commun. 352: 486-490, 2007. Go to original source...
  51. Zhang, J., Shi, Y., Zhang, X.Z., Du, H.M., Xu, B., Huang, B.R.: Melatonin suppression of heat-induced leaf senescence involves changes in abscisic acid and cytokinin biosynthesis and signaling pathways in perennial ryegrass (Lolium perenne L.). - Environ. exp. Bot. 138: 36-45, 2017. Go to original source...
  52. Zhang, J., Xing, J., Lu, Q.Y., Yu, G.H., Xu, B., Huang, B.R.: Transcriptional regulation of chlorophyll-catabolic genes associated with exogenous chemical effects and genotypic variations in heat-induced leaf senescence for perennial ryegrass. - Environ. exp. Bot. 167: 103858, 2019. Go to original source...
  53. Zhu, X., Shen, H.L.: Effect of high temperature stress on cell membrane in celery seedlings. - North. Hort. 7: 16-20, 2014.