Abstract
The effect of polyamine biosynthesis inhibitors on the salt stress response of rice seedlings was investigated. For this, DL-α-difluoromethylarginine (DFMA) and DL-α-difluoromethylornithine (DFMO), two competitive inhibitors of arginine decarboxylase (ADC) and ornithine decarboxylase (ODC), were used. The ADC and ODC are rate-limiting enzymes involved in synthesis of putrescine. The effective quantum yield of photosynthetic energy conversion (ΦPSII) decreased with the salt stress, and this decrease was highly significant in the treatments with DFMA and DFMO. Interestingly, addition of exogenous putrescine reduced the decline of ΦPSII. Putrescine content strongly decreased after one day of the inhibitor treatment. Although the content of spermidine (converted from putrescine) also showed an initial decrease in response to the inhibitors, it recovered to a similar level to that in the control after 3 d of treatment. Under the salt stress, the effect of the inhibitors on the different compounds was similar. Moreover, the addition of exogenous putrescine partially suppressed the decrease in spermidine and spermine content. A positive correlation between the spermidine and spermine content and the ΦPSII was observed. The results suggest that, under salt stress, a decrease in polyamine biosynthesis and/or polyamine content has a strong negative effect on leaves and increases salt stress sensitivity.
Abbreviations
- ADC:
-
arginine decarboxylase
- DFMA:
-
DL-α-difluoromethylarginine
- DFMO:
-
DL-α-difluoromethylornithine
- ODC:
-
ornithine decarboxylase
- ΦPSII :
-
effective quantum yield of photosynthetic energy conversion
References
Alcázar, R., Planas, J., Saxena, T., Zarza, X., Bortolotti, C., Cuevas, J., Bitrián, M., Tiburcio, A.F., Altabella, T.: Putrescine accumulation confers drought tolerance in transgenic Arabidopsis plants over-expressing the homologous Arginine decarboxylase 2 gene. — Plant Physiol. Biochem. 48: 547–552, 2010.
Bouchereau, A., Aziz, A., Larher, F., Martin-Tanguy, J.: Polyamines and environmental challenges: recent development. — Plant Sci. 140: 103–125, 1999.
Boyer, J.S.: Plant productivity and environment. — Science 218: 443–448, 1982.
Chattopadhayay, M.K., Tiwari, B.S., Chattopadhyay, G., Bose, A., Sengupta, D.N., Ghosh, B.: Protective role of exogenous polyamines on salinity-stressed rice (Oryza sativa) plants. — Physiol. Plant. 116: 192–199, 2002.
Cuevas, J.C., López-Cobollo, R., Alcázar, R., Zarza, X., Koncz, C., Altabella, T., Salinas, J., Tiburcio, A.F., Ferrando, A.: Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. — Plant Physiol. 148: 1094–1105, 2008.
Flores, H.E.: Changes in polyamine metabolism in response to abiotic stress. - In: Slocum, R.D., Flores, H.E. (ed.): Biochemistry and Physiology of Polyamines in Plants. Pp. 213–228. CRC Press, Boca Raton 1991.
Flores, H.E., Galston, A.W.: Analysis of polyamines in higher plants by high performance liquid chromatography. — Plant Physiol. 69: 701–706, 1982.
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 hightemperature and drought stress in vitro in trifoliate orange seedlings via modulation of antioxidative capacity and expression of stress-related genes. — Biotechnol. Biotech. Eq. 28: 192–198, 2015.
Kallio, A., McCann, P.P., Bey, P.: DL-difluoromethyl arginine: a potent enzyme-activated irreversible inhibitor of bacterial arginine decarboxylases. — Biochemistry 20: 3163–3166, 1981.
Kasugai, S.: Studies on the hydroponic cultures. — J. Sci. Soil Manure 13: 669–822, 1939.
Lee, T.M.: Polyamine regulation of growth and chilling tolerance of rice (Oryza sativa L.) roots cultured in vitro. — Plant Sci. 122: 111–117, 1997.
Li, J., Hu, L., Zhang, L., Pan, X., Hu, X.: Exogenous spermidine is enhancing tomato tolerance to salinityalkalinity stress by regulating chloroplast antioxidant system and chlorophyll metabolism. — BMC Plant Biol. 15: 303, 2015.
Marler, T.E., Mickelbart, M.V.: Growth and chlorophyll fluorescence of Spondias purpurea L. as influenced by salinity. — Trop. Agr. 70: 245–247, 1993.
Martin-Tanguy, J.: Metabolism and function of polyamines in plants: recent development (new approaches). — Plant Growth Regul. 34: 135–148, 2001.
Metcalf, B.W., Bey, P., Danzin, C., Jung, M.J., Casara, P., Vevert, J.P.: Catalytic irreversible inhibition of mammalian ornithine decarboxylase (E.C. 4.1.1.17) by substrate and product analogues. — J. amer. chem. Soc. 100: 2551–2553, 1978.
Mirdehghan, S.H., Rahimi, S.: Pre-harvest application of polyamines enhances antioxidants and table grape (Vitis vinifera L.) quality during postharvest period. — Food Chem. 196: 1040–1047, 2015.
Nahar, K., Hasanuzzaman, M., Alam, M.M., Fujita, M.: Exogenous spermidine alleviates low temperature injury in mung bean (Vigna radiata L.) seedlings by modulating ascorbate-glutathione and glyoxalase pathway. — Int. J. mol. Sci. 16: 30117–30132, 2015.
Roy, M., Wu, R.: Overexpression of S-adenosylmethionine decarboxylase gene in rice increases polyamine levels and enhances sodium chloride-stress. — Plant Sci. 163: 987–992, 2002.
Smith, M.A., Davies, P.J., Reid, J.B.: Role of polyamines in gibberellin-induced internode growth in peas. — Plant Physiol. 78: 92–99, 1985.
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.
Yamamoto, A., Shim, I.S., Fujihara, S., Yoneyama, T., Usui, K.: Effect of difference in nitrogen media on salt-stress response and contents of nitrogen compounds in rice seedlings. — Soil Sci. Plant Nutr. 50: 85–93, 2004.
Yamamoto, A., Sawada, H., Shim, I.S., Usui, K., Fujihara, S.: Effect of salt stress on physiological response and leaf polyamine content in NERICA rice seedlings. — Plant Soil Environ. 57: 571–576, 2011.
Yamamoto, A., Shim, I.S., Fujihara, S.: Chilling-stress responses by rice seedlings grown with different ammonium concentrations and its relationship to leaf spermidine. — J. Plant Biol. 55: 191–197, 2012.
Yancey, P.H., Clark, M.E., Hand, S.C., Bowlus, P.D., Somero, G.N.: Living with water stress: evolution of osmolyte systems. — Science 217: 1214–1217, 1982.
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Acknowledgements: The authors are grateful to Prof. Dr. Akira Shirahata of the Josai University for kindly providing inhibitors DFMA and DFMO. The authors are also grateful to Prof. Tadakatsu Yoneyama from the University of Tokyo and Prof. Kenji Usui from the University of Tsukuba for instructive comments on the manuscript.
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Yamamoto, A., Shim, IS. & Fujihara, S. Inhibition of putrescine biosynthesis enhanced salt stress sensitivity and decreased spermidine content in rice seedlings. Biol Plant 61, 385–388 (2017). https://doi.org/10.1007/s10535-016-0676-5
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DOI: https://doi.org/10.1007/s10535-016-0676-5