Abstract
Alternative respiration pathway (AP) is an important pathway which can be induced by environment stresses in plants. In the present study, we show a new mechanism involving the AP in nitrogen deprivation-induced tolerance of Poa annua callus to salt stress. The AP capacity markedly increased under a 600 mM NaCl treatment or nitrogen deprivation pretreatment and reached a maximum under the nitrogen deprivation pretreatment combined with the NaCl treatment (–N+NaCl). Malondialdehyde (MDA) and H2O2 content and Na+/K+ ratio significantly increased under the 600 mM NaCl treatment but less under the–N+NaCl treatment. Moreover, both the nitrogen deprivation and the NaCl stress stimulated the plasma membrane (PM) H+-ATPase activity and increased pyruvate content. The maximal stimulating effect was found under the–N+NaCl treatment. When the AP capacity was reduced by salicylhydroxamic acid (SHAM, an inhibitor of AP), content of MDA and H2O2 and Na+/K+ ratio dramatically increased, whereas PM H+-ATPase activity decreased. Moreover, exogenous application of pyruvate produced a similar effect as the nitrogen deprivation pretreatment. The effects of SHAM on the Poa annua callus were counteracted by catalase (a H2O2 scavenger) and diphenylene iodonium (a plasma membrane NADPH oxidase inhibitor). Taken together, our results suggest that the nitrogen deprivation enhanced the capacity of AP by increasing pyruvate content, which in turn prevented the Poa annua callus from salt-induced oxidative damages and Na+ over-uptake.
Similar content being viewed by others
Abbreviations
- AOX:
-
alternative oxidase
- AP:
-
alternative respiration pathway
- APX:
-
ascorbate peroxidase
- CAT:
-
catalase
- CP:
-
cytochrome respiration pathway
- c-PTIO:
-
2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide potassium salt
- DPI:
-
diphenylene iodonium
- EL:
-
electrolyte leakage
- PM:
-
plasma membrane
- POD:
-
peroxidase
- ROS:
-
reactive oxygen species
- SHAM:
-
salicylhydroxamic acid
- SOD:
-
superoxide dismutase
- TBARS:
-
thiobarbituric acid reactive substances
- MDA:
-
malondialdehyde
- Valt :
-
capacity of alternative respiration pathway
- Vcyt :
-
capacity of cytochrome respiration pathway
- Vres :
-
capacity of residue respiration pathway
References
Adam, A.L., Bestwick, C.S., Barna, B., Mansfield, J.W.: Enzymes regulating the accumulation of active oxygen species during the hypersensitive reaction of bean to Pseudomonas syringae pv. phaseolicola. — Planta 197: 240–249, 1995.
Aebi, H.: Catalase in vitro. — Methods Enzymol. 105: 121–126, 1982.
Apel, K., Hirt, H.: Reactive oxygen species: metabolism, oxidative stress, and signal transduction. — Annu. Rev. Plant Biol. 55: 373–399, 2004.
Asada, K.: Production and scavenging of reactive oxygen species in chloroplasts and their functions. — Plant Physiol. 141: 391–396, 2006.
Ballesteros, E., Kerkeb, B., Donaire, J.P., Belver, A.: Effects of salt stress on H+-ATPase activity plasma membrane-enriched vesicles isolated from sunflower roots. — Plant Sci. 134: 181–190, 1998.
Bartoli, C.G., Gomez, F., Martinez, D.E., Guiamet, J.J.: Mitochondria are the main target for oxidative damage in leaves of wheat (Triticum aestivum L.). — J. exp. bot. 55: 1663–1669, 2004.
Borsani, O., Valpuesta, V., Botella, M.A.: Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. — Plant Physiol. 126: 1024–1030, 2001.
Bose, J., Rodrigo-Moreno, A., Shabala, S.: ROS homeostasis in halophytes in the context of salinity stress tolerance. — J. exp. Bot. 64: 1241–1257, 2014.
Boubakri, H., Wahab, M.A., Chong, J., Gertz, C., Gandoura, S., Mliki, A., Bertsch, C., Soustre-Gacougnolle I.: Methionine elicits H2O2 generation and defense gene expression in grapevine and reduces Plasmopara viticola infection. — J. Plant Physiol. 170: 1561–1568, 2013.
Boyer, J.S.: Plant productivity and environment. — Science 218: 443–448, 1982.
Bradford, M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. — Anal. Biochem. 72: 248–254, 1976.
Burke, J.J., Gamble, P.E., Hatfield, J.L., Quisenberry, J.E.: Plant morphological and biochemical responses to field water deficits. I. Responses of glutathione reductase activity and paraquat sensitivity. — Plant Physiol. 79: 415–419, 1985.
Chen, J., Wang, W.H., Wu, F.H., You, C.Y., Liu, T.W., Dong, X.J., He, J.X., Zheng, H.L.: Hydrogen sulfide alleviates aluminum toxicity in barley seedlings. — Plant Soil 362: 301–318, 2013.
Chen, S., McElroy, J.S., Flessner, M.L., Dane, F.: Utilizing next-generation sequencing to study homeologous poly-morphisms and herbicide-resistance-endowing mutations in Poa annua acetolactate synthase genes. — Pest Manage. Sci. 71: 1141–1148, 2014.
Chung, J.S., Zhu, J.K., Bressan, R.A., Hasegawa, P.M., Shi, H.: Reactive oxygen species mediate Na+-induced SOS1 mRNA stability in Arabidopsis. — Plant J. 53: 554–565, 2008.
Clifton, R., Lister, R., Parker, K.L., Sappl, P.G., Elhafez, D., Millar, A.H., Day, D.A., Whelan, J.: Stress-induced co-expression of alternative respiratory chain components in Arabidopsis thaliana. — Plant mol. Biol. 58: 193–212, 2005.
Ding, Y.Z., Feng, R.W., Wang, R.G., Guo, J.K., Zheng, X.Q.: A dual effect of Se on Cd toxicity: evidence from plant growth, root morphology and responses of the antioxidative systems of paddy rice. — Plant Soil 375: 289–301, 2014.
Duo, L.A., Gao, Y. B., Zhao, S. L.: Growth responses of Poa pratensis to the stress of four heavy metals. — Acta bot. boreal.-occident. sin. 26: 0183–0187, 2006.
Fiorani, F., Umbach, A.L., Siedow, J.N.: The alternative oxidase of plant mitochondria is involved in the acclimation of shoot growth at low temperature. A study of Arabidopsis AOX1a transgenic plants. — Plant Physiol. 139: 1795–1805, 2005.
Foyer, C.H., Noctor, G.: Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. — Plant Cell 17: 1866–1875, 2005.
Foyer, C.H., Noctor, G.: Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. — Antioxid. Redox Signal. 11: 861–905, 2009.
Gill, S.S., Tuteja, N.: Reactive oxygen species and antioxidant mechinery in abiotic stress tolerance in crop plants. — Plant Physiol. Biochem. 48: 909–930, 2010.
Giraud, E., Ho, LH., Clifton, R., Carroll, A., Estavillo, G., Tan, Y.F., Howell, K.A., Ivanova, A., Pogson, B.J., Millar, A.H., Whelan, J.: The absence of alternative oxidase1a in Arabidopsis results in acute sensitivity to combined light and drought stress. — Plant Physiol. 147: 595–610, 2008.
Han, R.M., Lefevre, I., Albacete, A., Perez-Alfocea, F., Barba-Espin, G., Diaz-Vivancos, P., Quinet, M., Ruan, C.J., Hernandez, J.A., Cantero-Navarro, E., Lutts, S.: Antioxidant enzyme activities and hormonal status in response to Cd stress in the wetland halophyte Kosteletzkya virginica under saline conditions. — Physiol. Plant. 147: 352–368, 2013.
Hasanuzzaman, M., Fujita, M.: Selenium pretreatment upregulates the antioxidant defense and methylglyoxal detoxification system and confers enhanced tolerance to drought stress in rapeseed seedlings. — Biol. trace Elements Res. 143: 1758–1776, 2011.
Hassidim, M., Braun, Y., Lener, H.R., Reihold, L.: Studies on H+ translocating ATPase in plants of varying resistance to salinity. — Plant Physiol. 81: 1057–1061, 1986.
Heide, O.M.: Flowering responses of contrasting ecotypes of Poa annua and their putative ancestors Poa infirma and Poa supina. — Ann. Bot. 87: 795–804, 2001.
Hemp, A.: Introduced plants on Kilimanjaro: tourism and its impact. — Plant Ecol. 197: 17–29, 2007.
Hu, W.H., Shi, K., Song, X.S., Xia, X.J., Zhou, Y.H., Yu, J.Q.: Different effects of chilling on respiration in leaves and roots of cucumber (Cucumis sativus). — Plant Physiol. Biochem. 44: 837–843, 2006.
Janda, T., Szalai, G., Tari, I., Paldi, E.: Hydroponic treatment with salicylic acid decreases the effects of chilling injury in maize (Zea mays L.) plants. — Planta 208: 175–180, 1999.
Jiang, Y.P., Cheng, F., Zhou, Y.H., Xia, X.J., Mao, W.H., Shi, K., Chen, Z.X., Yu, J.Q.: Cellular glutathione redox homeostasis plays an important role in the brassinosteroidinduced increase in CO2 assimilation in Cucumis sativus. — New Phytol. 194: 932–943, 2012.
Kumar, N., Vyas, D., Kumar, S.: Plants at high altitude exhibit higher component of alternative respiration. — J. Plant Physiol. 164: 31–38, 2007.
Li, J.S., Chen, G.L., Wang, X.M., Zhang, Y.L., Jia, H.L., Bi, Y.R.: Glucose-6-phosphate dehydrogenase-dependent hydrogen peroxide production is involved in the regulation of plasma membrane H+-ATPase and Na+/H+ antiporter protein in salt-stressed callus from Carex moorcroftii. — Physiol. Plant. 141: 239–250, 2011.
Li, J.S., Jia, H.L., Wang, J., Cao, Q.H., Wen, Z.C.: Hydrogen sulfide is involved in maintaining ion homeostasis via regulating plasma membrane Na+/H+ antiporter system in the hydrogen peroxide-dependent manner in salt-stress Arabidopsis thaliana root. — Protoplasma 251: 899–912, 2014.
Li, J.S., Wang, X.M., Bi, Y.R.: Tissure culture and rapid propagation of Carex moorcroftii. — Plant Physiol. Commun. 44: 516–517, 2008.
Lin, Y.L., Chao, Y.Y., Kao, C.H.: Exposure of rice seedlings to heat shock protects against subsequent Cd-induced decrease in glutamine synthetase activity and increase in specific protease activity in leaves. — J. Plant Physiol. 167: 1061–1065, 2010.
Liu, Y.G., Wu, R.R., Wan, Q., Xie, G.Q., Bi YR.: Glucose-6- phosphate dehydrogenase plays a pivotal role in nitric oxide-involved defense against oxidative stress under salt stress in red kidney bean roots. — Plant. Cell physiol. 48: 511–522, 2007.
Lv, Y. W., He, J. Y., Bai, X. M., Dong, Qin., Lei, Y. W.: Evaluation of physiological responses and resistances of nine wild Poa to low temperature. — Acta argestia sin. 22: 326–333, 2014.
Maxwell, D.P., Wang, Y., McIntosh, L.: The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. — Proc. nat. Acad. Sci. USA 96: 8271–8276, 1999.
Millar, A.H., Atkin, O.K., Menz, R.I., Henry, B., Farquhar, G., Day, D.A.: Analysis of respiratory chain regulation in roots of soybean seedlings. — Plant Physiol. 117: 1083–1093, 1998.
Molina-Montenegro, M.A., Carrasco-Urra, F., Rodrigo, C., Convey, P., Valladares, F., Gianoli, E.: Occurrence of the non-native annual bluegrass on the Antarctic mainland and its negative effects on native plants. — Conserv. Biol. 26: 717–723, 2012.
Morsomme, P., Boutry, M.: The plant plasma membrane H(+)- ATPase: structure, function and regulation. — Biochim. biophys. Acta 1465: 1–16, 2000.
Munné-Bosch, S., Alegre, L.: Cross-stress tolerance and stress "memory" in plants: an integrated view. — Environ. exp. Bot. 94: 1–2, 2013.
Munns, R., Tester, M.: Mechanisms of salinity tolerance. — Annu. Rev. Plant Biol. 59: 651–681, 2008.
Neill, S.J., Desikan, R., Clarke, A., Hurst, R.D., Hancock, J.T.: Hydrogen peroxide and nitric oxide as signalling molecules in plants. — J. exp. Bot. 53: 1237–1242, 2002.
Niu, X., Bressan, R.A., Hasegawa, P.M., Pardo, J.M.: Ion homeostasis in NaCl stress environments. — Plant Physiol. 109: 735–742, 1995.
Parsons, H.L., Yip, J.Y.H., Vanlerberghe, G.C.: Increased respiratory restriction during phosphate-limited growth in transgenic tobacco cells lacking alternative oxidase. — Plant Physiol. 121: 1309–1320, 1999.
Peng, Y., Huang, B. R., Xu, L.X., Ll, Z.: Heat stress effects on osmotic potential, membrane fatty acid composition and lipid peroxidation content of two Kentucky Bluegrass cultivars differing in drought tolerance. — Acta Horticult. sin. 40: 971–980, 2013.
Procházková, D., Sairam, R.K., Srivastava, G.C., Singh, D.V.: Oxidative stress and antioxidant activity as the basis of senescence in maize leaves. — Plant Sci. 161: 765–771, 2001.
Puyang, X. H., An, M. Y., Han, L. B., Zhang, X. B.: Protective effect of spermidine on salt stress induced oxidative damage in two Kentucky bluegrass (Poa pratensis L.) cultivars. — Ecotoxic. Environ. Safety 117: 96–106, 2015.
Qiu, Q.S., Su, X.F.: The influence of extracellular-side Ca2+ on the activity of the plasma membrane H+-ATPase from wheat roots. — Aust. J. Plant Physiol. 25: 923–928, 1998.
Rea, P.A., Poole, R.J., Vacuolar H+-translocating pyrophosphatase. — Annu. Rev. Plant Physiol. 44: 157–180, 1993.
Rea, P.A., Sander, D.: Tonoplast energization: two H+ pumps, one membrane. — Physiol. Plant. 71: 131–141, 1987.
Saidi, I., Chtourou, Y., Djebali, W.: Selenium alleviates cadmium toxicity by preventing oxidative stress in sunflower (Helianthus annuus) seedlings. — J. Plant Physiol. 171: 85–91, 2014.
Serrano, R., Mulet, J.M., Rios, G.: A glimpse of the mechanisms of ion homeostasis during salt stress. — Plant Sci. 162: 897–904, 1999.
Sairam, P.K, Srivastava, G.C.: Changes in antioxidant activity in subcellular fraction of tolerant and susceptible wheat genotypes in response to long term salt stress. — Plant Sci. 162: 897–904, 2002.
Sieger, S.M., Kristensen, B.K., Robson, C.A., Amirsadeghi, S., Eng, E.W., Abdel-Mesih, A., Moller, I.M., Vanlerberghe, G.C.: The role of alternative oxidase in modulating carbon use efficiency and growth during macronutrient stress in tobacco cells. — J. exp. Bot. 56: 1499–1515, 2005.
Smith, C.A., Melino, V.J., Sweetman, C., Soole, K.L.: Manipulation of alternative oxidase can influence salt tolerance in Arabidopsis thaliana. — Physiol. Plant. 137: 459–472, 2009.
Sun, J., Wang, M.J., Ding, M.Q., Deng, S.R., Liu, M.Q., Lu, C.F., Zhou, X.Y., Shen, X., Zheng, X.J., Zhang, Z.K., Song, J., Hu, Z.M., Xu, Y., Chen, S.L.: H2O2 and cytosolic Ca2+ signals triggered by the PM H-coupled transport system mediate K+/Na+ homeostasis in NaCl-stressed Populus euphratica cells. — Plant. Cell Environ. 33: 943–958, 2010.
Umbach, A.L., Fiorani, F., Siedow, J.N.: Characterization of transformed Arabidopsis with altered alternative oxidase levels and analysis of effects on reactive oxygen species in tissue. — Plant Physiol. 139: 1806–1820, 2005.
Vanlerberghe, G.C., McIntosh, L.: Alternative oxidase: from gene to function. — Annu. Rev. Plant Physiol.. 48: 703–734, 1997.
Veljovic-Jovanovic, S., Noctor, G., Foyer, C.H.: Are leaf hydrogen peroxide concentrations commonly overestimated? The potential influence of artefactual interference by tissue phenolics and ascorbate. — Plant Physiol. Biochem. 40: 501–507, 2002.
Walter, J., Jentschh, A., Beierkuhnlein, C., Kreyling, J.: Ecological stress memory and cross stress tolerance in plants in the face of climate extremes. — Environ. exp. Bot. 94: 3–8, 2012.
Wang, H.H., Huang, J.J., Liang, X.L., Bi, Y.R.: Involvement of hydrogen peroxide, calcium, and ethylene in the induction of the alternative pathway in chilling-stressed Arabidopsis callus. — Planta 235: 53–67, 2012.
Wang, H,H,, Liang, X,L., Huang, J.J., Zhang, D.K., Lu, H.X., Liu, Z.J., Bi, Y.R.: Involvement of ethylene and hydrogen peroxide in induction of alternative respiratory pathway in salt-treated Arabidopsis calluses. — Plant. Cell Physiol. 51: 1754–1765, 2010.
Wang, L., Guo, Y.J., Jia, L.X., Chu, H.Y., Zhou, S., Chen, K.M., Wu, D., Zhao, L.Q.: Hydrogen peroxide acts upstream of nitric oxide in the heat shock pathway in Arabidopsis seedlings. — Plant Physiol. 164: 2184–2196, 2014.
Wang, X.M., Hou, C., Liu, J., He, W.L., Nan, W.B., Gong, H.L., Bi, Y.R.: Hydrogen peroxide is involved in the regulation of rice (Oryza sativa L.) tolerance to salt stress. — Acta Physiol. Plant. 35: 891–900. 2013.
Wang, X.M., Ma, Y.Y., Huang, C.H., Wan, Q., Li, J.S., Bi, Y.R.: Glucose-6-phosphate dehydrogenase plays a central role in modulating reduced glutathione levels in reed callus under salt stress. — Planta 227: 611–623, 2008.
Watanabe, C.K., Hachiya, T., Takahara, K., Kawai-Yamada, M., Uchimiya, H., Uesono, Y., Terashima, I., Noguchi, K.: Effects of AOX1a deficiency on plant growth, gene expression of respiratory components and metabolic profile under low-nitrogen stress in Arabidopsis thaliana. — Plant Cell Physiol. 51: 810–822, 2010.
Wu, Y.X., Ding, N., Zhao, X., Zhao, M., Chang, Z.Q., Liu, J.Q., Zhang, L.X.: Molecular characterization of PeSOS1 the putative Na+/H+ antioporter of Populus euphratica. — Plant mol. Biol. 65: 1–11, 2007.
Yip, J.Y., Vanlerberghe, G,C.: Mitochondrial alternative oxidase acts to dampen the generation of active oxygen species during a period of rapid respiration induced to support a high rate of nutrient uptake. — Physiol. Plant. 112: 327–333, 2001.
Yu, L., Ma, H. L.: The endogenous hormone level and drought adaptability of four Kentucky bluegrass species in Gansu. — China J. Desert Res. 35: 0182–0188, 2015.
Zhao, L.Q., Zhang, F., Guo, J.K., Yang, Y.L., Li, B.B., Zhang, L.X.: Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. — Plant Physiol. 134: 849–857, 2004.
Zhu, J., Fu, X., Koo, Y.D., Zhu, J.K., Jenney, F.E., Jr., Adams, M.W., Zhu. Y., Shi, H., Yun, D.J., Hasegawa, P.M., Bressan, R.A.: An enhancer mutant of Arabidopsis salt overly sensitive 3 mediates both ion homeostasis and the oxidative stress response. — Mol. cell. Biol. 27: 5214–5224, 2007.
Zhu, J.K.: Regulation of ion homeostasis under salt stress. — Cur. Opin. Plant Biol. 6: 441–445, 2003.
Zhu, Y., Zuo, M.X., Liang, Y.L., Jiang, M.Y., Zhang, J.H., Scheller, H.V., Tan, M.P., Zhang, A.Y.: MAP65-1a positively regulates H2O2 amplification and enhances brassinosteroid-induced antioxidant defence in maize. — J. exp. Bot. 64: 3787–3802, 2013.
Author information
Authors and Affiliations
Corresponding author
Additional information
Acknowledgement
This work was supported by the Major State Basic Research Development Program of China (973 Program; 2012CB026105), the National High Technology Research and Development Program (2007AA021401), the Foundation of Science and Technology Program of Lanzhou City (2015-3-53), the Foundation of Science and Technology Program of Gansu Province (1506RJZA209), the Scientific research project of Qinghai-Tibetan DC Interconnection Project in State Grid Corporation of China, and the Foundation of Science and Technology Program of Gansu Province (1208RJZA224). The first two authors contributed equally to this work.
Rights and permissions
About this article
Cite this article
Zhao, C.Z., Li, P., Wang, X.M. et al. Nitrogen deprivation induces cross-tolerance of Poa annua callus to salt stress. Biol Plant 60, 543–554 (2016). https://doi.org/10.1007/s10535-016-0626-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10535-016-0626-2