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Involvement of nitric oxide in 5-aminolevulinic acid-induced antioxidant defense in roots of Elymus nutans exposed to cold stress

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Biologia Plantarum

Abstract

Nitric oxide (NO) and 5-aminolevulinic acid (5ALA) play fundamental roles in plant responses to environmental stresses, but their cross-talk in antioxidant defense in cold-stressed Elymus nutans Griseb. have not been investigated. We herein report that 5ALA and NO donor, sodium nitroprusside (SNP), alleviated cold stress-induced plant growth inhibition and lipid peroxidation in roots of two E. nutans ecotypes (Damxung, DX and Zhengdao, ZD). However, application of an NO scavenger 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide potassium salt (PTIO) differentially blocked these protective effects indicating that an inhibition of NO accumulation reduced 5ALA-enhanced cold resistance. Application of exogenous 5ALA or NO markedly up-regulated activities of superoxide dismutase, catalase, ascorbate peroxidase, and glutathione reductase, enhanced reduced glutathione accumulation and reduced glutathione to oxidized glutathione ratio, activated plasma membrane (PM) H+-ATPase, and reduced Na+/K+ ratio in roots of the two E. nutans ecotypes. Moreover, in the presence of 5ALA, nitric oxide synthase (NOS) activity and NO release in cold-resistant DX were higher than those in cold-sensitive ZD. Conversely, both NO treatment and inhibition of endogenous NO accumulation by PTIO or NOS inhibitor Nω-nitro-L-arginine did not induce 5ALA production. These results suggest that NO might be acting as a downstream signal to mediate 5ALA-induced cold resistance by activating antioxidant defense and PM H+-ATPase and maintaining Na+ and K+ homeostasis.

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Abbreviations

5ALA:

5-aminolevulinic acid

APX:

ascorbate peroxidase

AsA:

reduced ascorbate

CAT:

catalase

CK:

control

DHA:

dehydroascorbate

GR:

glutathione reductase

GSH:

reduced glutathione

GSSG:

oxidized glutathione

H2O2 :

hydrogen peroxide

L-NNA:

Nω-nitro-L-arginine

MDA:

malondialdehyde

MDHAR:

monodehydroascorbate reductase

NADPH:

nicotinamide adenine dinucleotide phosphate

NO:

nitric oxide

NR:

nitrate reductase

NOS:

nitric oxide synthase

PGR:

plant growth regulator

PM:

plasma membrane

PTIO:

2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide potassium salt

ROS:

reactive oxygen species

RNS:

reactive nitrogen species

SNP:

sodium nitroprusside

SOD:

superoxide dismutase

TCA:

trichloroacetic acid

Tu:

tungstate

References

  • Ahn, S.J., Im, Y.J., Chung, G.C., Cho, B.H.: Inducible expression of plasma membrane H+-ATPase in the roots of fig leaf gourd plants under chilling root temperature. — Physiol. Plant. 106: 35–40, 1999.

    Article  CAS  Google Scholar 

  • Akram, N.A., Ashraf, M.: Regulation in plant stress tolerance by a potential plant growth regulator, 5-aminolevulinic acid. — J. Plant Growth Regul. 32: 663–679, 2013.

    Article  CAS  Google Scholar 

  • Ali, B., Tao, Q.J., Zhou, Y.F., Gill, R.A., Ali, S., Rafiq, M.T., Xu, L., Zhou, W.J.: 5-Aminolevolinic acid mitigates the cadmium-induced changes in Brassica napus as revealed by the biochemical and ultra-structural evaluation of roots. - Ecotox. environ. Safe. 92: 271–280, 2013.

    Article  CAS  Google Scholar 

  • Ali, B., Xu, X., Gill, R.A., Yang, S., Ali, S., Tahir, M., Zhou, W.J.: Promotive role of 5-aminolevulinic acid on mineral nutrients and antioxidative defense system under lead toxicity in Brassica napus. — Ind. Crop. Prod. 52: 617–626, 2014.

    Article  CAS  Google Scholar 

  • Arasimowicz-Jelonek, M., Floryszak-Wieczore, K.J., Kubis, J.: Involvement of nitric oxide in water stress-induced responses of cucumber roots. — Plant Sci. 177: 682–690, 2009.

    Article  CAS  Google Scholar 

  • Aroca, R., Irigoyen, J.J., Sánchez-Dı́az, M.: Photosynthetic characteristics and protective mechanisms against oxidative stress during chilling and subsequent recovery in two maize varieties differing in chilling sensitivity. — Plant Sci. 161: 719–726, 2001.

    Article  CAS  Google Scholar 

  • Bai, X.G., Chen, J.H., Kong, X.X., Todd, C.D., Yang, Y.P., Hu, X.Y., Li, D.Z.: Carbon monoxide enhances the chilling tolerance of recalcitrant Baccaurea ramiflora seeds via nitric oxide-mediated glutathione homeostasis. — Free Radical Biol. Med. 53: 710–720, 2012.

    Article  CAS  Google Scholar 

  • Balestrasse, K.B., Tomaro, M.L., Batlle, A., Noriega, G.O.: The role of 5-aminolevulinic acid in the response to cold stress in soybean plants. — Phytochemistry 71: 2038–2045, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Beauchamp, C., Fridovich, I.: Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels. — Anal. Biochem. 44: 276–287, 1971.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Cakmak, I., Marschner, H.: Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves. — Plant Physiol. 98: 1222–1227, 1992.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corpas, F.J., Chaki, M., Fernández-Ocaña, A., Valderrama, R., Palma, J.M., Carreras, A., Begara-Morales, J.C., Airaki, M., Del Barroso, L.A., Barroso, J.B.: Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions. — Plant Cell Physiol. 49: 1711–1722, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Crawford, N.M.: Mechanisms for nitric oxide synthesis in plants. — J. exp. Bot. 57: 471–478, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Dhindsa, R.S., Plumb-dhindsa, P., Thorpe, T.A.: Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation and decreased levels of superoxide dismutase and catalase. — J. exp. Bot. 32: 93–101, 1981.

    Article  CAS  Google Scholar 

  • Erdal, S., Dumlupinar, R.: Exogenously treated mammalian sex hormones affects in organic constituents of plants. — Biol. Trace Element Res. 143: 500–506, 2011.

    Article  CAS  Google Scholar 

  • Fu, J.J., Sun, Y.F., Chu, X.T., Xu, Y.F., Hu, T.M.: Exogenous 5-aminolevulenic acid promotes seed germination in Elymus nutans against oxidative damage induced by cold stress. — PLoS ONE 9: e107152, 2014.

    Article  Google Scholar 

  • Gill, S.S., Hasanuzzaman, M., Nahar, K., Macovei, A., Tuteja, N.: Importance of nitric oxide in cadmium stress tolerance in crop plants. — Plant Physiol. Biochem. 63: 254–261, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Harel, E., Klein, S.: Light dependent formation of 5-aminolevulinic acid in etiolated leaves of higher plants. — Biochem. biophys. Res. Commun. 49: 364–370, 1972.

    Article  CAS  PubMed  Google Scholar 

  • He, Y., Tang, R.H., Hao, Y., Stevens, R.D., Cook, C.W., Ahn, S.M., Jing, L., Yang, Z., Chen, L., Guo, F.: Nitric oxide represses the Arabidopsis floral transition. — Science 305: 1671–1968, 2004.

    Article  Google Scholar 

  • Hotta, Y., Tanaka, T., Luo, B.S., Takeuchi, Y., Konnai, M.: Improvement of cold resistance in rice seedlings by 5-aminolevulinic acid. — J. Pest Sci. 23: 29–33, 1998.

    Article  CAS  Google Scholar 

  • Kampfenkel, K., Van Montagu, M., Inzé, D.: Extraction and determination of ascorbate and dehydroascorbate from plant tissue. — Anal. Biochem. 225: 165–167, 1995.

    Article  CAS  PubMed  Google Scholar 

  • Kang, H.M., Saltveit, M.E.: Chilling tolerance of maize, cucumber and rice seedling leaves and roots are differentially affected by salicylic acid. — Physiol. Plant. 115: 571–576, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Khan, M.N., Siddiqui, M.H., Mohammad, F., Naeem, M.: Interactive role of nitric oxide and calcium chloride in enhancing tolerance to salt stress. — Nitric Oxide 27: 210–218, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Kong, W.W., Huang, C.Y., Chen, Q., Zou, Y.J., Zhang, J.X.: Nitric oxide alleviates heat stress-induced oxidative damage in Pleurotus eryngii var. tuoliensis. — Fungal. Genet. Biol. 49: 15–20, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Korkmaz, A., Korkmaz, Y., Demirkıran, A.R.: Enhancing chilling stress tolerance of pepper seedlings by exogenous application of 5-aminolevulinic acid. — Environ. exp. Bot. 67: 495–501, 2010.

    Article  CAS  Google Scholar 

  • Law, M.Y., Charles, S.A., Halliwell, B.: Glutathione and ascorbic-acid in spinach (Spinacia oleracea) chloroplasts — the effect of hydrogen-peroxide and of paraquat. — Biochem. J. 210: 899–903, 1983.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma, L., Zhang, H., Sun, L., Jiao, Y., Zhang, G., Miao, C., Hao, F.: NADPH oxidase AtrbohD and AtrbohF function in ROS-dependent regulation of Na+/K+ homeostasis in Arabidopsis under salt stress. — J. exp. Bot. 63: 305–317, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Mishra, P.K., Bisht, S.C., Ruwari, P., Selvakumar, G., Joshi, G.K., Bisht, J.K., Bhatt, J.C., Gupta, H.S.: Alleviation of cold stress in inoculated wheat (Triticum aestivum L.) seedlings with psychrotolerant pseudomonads from NW Himalayas. — Arch. Microbiol. 193: 497–513, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Mittler, R.: Oxidative stress, antioxidants and stress tolerance. — Trends Plant Sci. 7: 405–410, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Murphy, M.E., Noack E.: Nitric oxide assay using hemoglobin method. — Methods Enzymol. 233: 240–250, 1994.

    Article  CAS  PubMed  Google Scholar 

  • Naeem, M.S., Jin, Z.L., Wan, G.L., Liu, D., Liu, H.B., Yoneyama, K., Zhou, W.J.: 5-Aminolevulinic acid improves photosynthetic gas exchange capacity and ion uptake under salinity stress in oilseed rape (Brassica napus L.). - Plant Soil 332: 405–415, 2010.

    Article  CAS  Google Scholar 

  • Naeem, M.S., Rasheed, M., Liu, D., Jin, Z.L., Ming, D.F., Yoneyama, K., Takeuchi, Y., Zhou, W.J.: 5-Aminolevulinic acid ameliorates salinity-induced metabolic, water-related and biochemical changes in Brassica napus L. - Acta Physiol. Plant. 33: 517–528, 2011.

    Article  CAS  Google Scholar 

  • Naeem, M.S., Warusawitharana, H., Liu, H.B., Liu, D., Ahmad, R., Waraich, E.A., Xu, L., Zhou, W.J.: 5-Aminolevulinic acid alleviates the salinity-induced changes in Brassica napus as revealed by the ultrastructural study of chloroplast. - Plant Physiol. Biochem. 57: 84–92, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Nakano, Y., Asada, K.: Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplast. — Plant Cell Physiol. 22: 867–880, 1981.

    CAS  Google Scholar 

  • Palmgren, M.G., Askerlund, P., Fredrikson, K., Widell, S., Sommarin, M., Larsson, C.: Sealed inside-out and right-side-out plasma membrane vesicles: optimal conditions for formation and separation. — Plant Physiol. 92: 871–880, 1990.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryter, S.W., Otterbein, L.E., Morse, D., Choi, A.M.K.: Heme oxygenase/carbon monoxide signaling pathways: regulation and functional significance. — Mol. Cell Biochem. 234: 249–263, 2002.

    Article  PubMed  Google Scholar 

  • Santa-Cruz, D.M., Pacienza, N.A., Polizio, A.H., Balestrasse, K.B., Tomaro, M.L., Yannarelli, G.G.: Nitric oxide synthase-like dependent NO production enhances heme oxygenase up-regulation in ultraviolet-B-irradiated soybean plants. — Phytochemistry 71: 1700–1707, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Shaedle, M., Bassham, J.A.: Chloroplast glutathione reductase. — Plant Physiol. 59: 1011–1012, 1977.

    Article  Google Scholar 

  • Shi, H., Li, R., Cai, W. Liu, W., Wang, C., Lu, Y.: Increasing nitric oxide content in Arabidopsis thaliana by expressing rat neuronal nitric oxide synthase resulted in enhanced stress tolerance. — Plant Cell Physiol. 53: 344–357, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Shi, H., Ye, T., Chen, F., Cheng, Z., Wang, Y., Yang, P., Zhang, Y., Chan, Z.: Manipulation of arginase expression modulate abiotic stress tolerance in Arabidopsis: effect on arginine metabolism and ROS accumulation. — J. exp. Bot. 64: 1367–1379, 2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song, L., Ding, W., Zhao, M., Sun, B., Zhang, L.: Nitric oxide protects against oxidative stress under heat stress in the calluses from two ecotypes of reed. — Plant Sci. 171: 449–458, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Song, L.L., Ding, W., Shen, J., Zhang, Z.G., Bi, Y.R., Zhang, L.X.: Nitric oxide mediates abscisic acid induced thermotolerance in the calluses from two ecotypes of reed under heat stress. — Plant Sci. 175: 826–832, 2008.

    Article  CAS  Google Scholar 

  • Sun, Y.P., Zhang, Z.P., Wang, L.J.: Promotion of 5-amino-levulinic acid treatment on leaf photosynthesis is related with increase of antioxidant enzyme activity in watermelon seedlings grown under shade condition. — Photosynthetica 47: 347–354, 2009.

    Article  CAS  Google Scholar 

  • Tartoura, K.A.H., Youssef, S.A.: Stimulation of ROS-scavenging systems in squash (Cucurbita pepo L.) plants by compost supplementation under normal and low temperature conditions. — Sci. Hort. 130: 862–868, 2011.

    Article  CAS  Google Scholar 

  • Vital, S.A., Fowler, R.W., Virgen, A., Gossett, D.R., Banks, S.W., Rodriguez, J.: Opposing roles for superoxide and nitric oxide in the NaCl stress-induced upregulation of antioxidant enzyme activity in cotton callus tissue. — Environ. exp. Bot. 62: 60–68, 2008.

    Article  CAS  Google Scholar 

  • Wang, J.J., Jiang, W.B., Huang, B.J.: Promotion of 5-aminolevulinic acid on photosynthesis of melon (Cucumis melo) seedlings under low light and chilling stress conditions. — Physiol. Plant. 121: 258–264, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Wendehenne, D., Pugin, A., Klessig, D.F., Durner, J.: Nitric oxide: comparative synthesis and signaling in animal and plant cells. — Trends Plant Sci. 6: 177–183, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Xu, M.J., Dong, J.F., Zhang, M., Xu, X.B., Sun, L.N.: Cold-induced endogenous nitric oxide generation plays a role in chilling tolerance of loquat fruit during postharvest storage. — Postharvest Biol. Technol. 65: 5–12, 2012.

    Article  CAS  Google Scholar 

  • Xu, Y.F., Chu, X.T., Fu, J.J., Yang, L.Y., Hu, T.M.: Crosstalk of nitric oxide with calcium induced tolerance of tall fescue leaves to high irradiance. — Biol. Plant. 60: 376–384, 2016.

    Article  Google Scholar 

  • Xu, Y.F., Sun, X.L., Jin, J.W., Zhou, H.: Protective effect of nitric oxide on light-induced oxidative damage in leaves of tall fescue. — J. Plant Physiol. 167: 512–518, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Yu, C.W., Murphy, T.M., Lin, C.H.: Hydrogen peroxide-induced chilling tolerance in mung beans mediated through ABA-independent glutathione accumulation. — Funct. Plant Biol. 30: 955–963, 2003.

    Article  CAS  Google Scholar 

  • Zhang, A., Zhang, J., Zhang, J., Ye, N., Zhang, H., Tan, M., Jiang, M.: Nitric oxide mediates brassinosteroid-induced ABA biosynthesis involved in oxidative stress tolerance in maize leaves. — Plant Cell Physiol. 52: 181–192, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, A.Y., Jiang, M.Y., Zhang, J.H, Ding, H.D., Xu, S.C., Hu, X.L., Tan, M.P.: Nitric oxide induced by hydrogen peroxide mediates abscisic acid-induced activation of the mitogen-activated protein kinase cascade involved in antioxidant defense in maize leaves. — New Phytol. 175: 36–50, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, J., Li, D.M., Gao, Y., Yu, B., Xia, C.X., Bai, J.G.: Pretreatment with 5-aminolevulinic acid mitigates heat stress of cucumber leaves. — Biol. Plant. 56: 780–784, 2012.

    Article  CAS  Google Scholar 

  • Zhang, L.G., Zhou, S., Xuan, Y., Sun, M., Zhao, L.Q.: Protective effect of nitric oxide against oxidative damage in Arabidopsis leaves under ultraviolet-B irradiation. — J. Plant Biol. 52: 135–140, 2009a.

    Article  Google Scholar 

  • Zhang, W.F., Zhang, F., Raziuddin, R., Gong, H.J., Yang, Z.M., Lu, L., Ye, Q.F., Zhou, W.J.: Effects of 5-aminolevulinic acid on oilseed rape seedling growth under herbicide toxicity stress. — J. Plant Growth Regul. 27: 159–169, 2008.

    Article  Google Scholar 

  • Zhang, Y.K., Han, X.J., Chen, X.L., Jin, H., Cui, X.M.: Exogenous nitric oxide on antioxidative system and ATPase activities from tomato seedlings under copper stress. — Sci. Hort. 123: 217–223, 2009b.

    Article  CAS  Google Scholar 

  • Zhang, Y.Y., Wang, L.L., Liu, Y.L., Zhang, Q., Wei, Q.P., Zhang, W.H.: Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast. — Planta 224: 545–555, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Zhao, L., He, J.X., Wang, X.M., Zhang, L.X.: Nitric oxide protects against polyethylene glycol-induced oxidative damage in two ecotypes of reed suspension cultures. — J. Plant Physiol. 165: 182–191, 2008.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Grassland Science, College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi, 712100, P.R. China

    J. J. Fu, X. T. Chu, Y. F. Sun, Y. F. Xu & T. M. Hu

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  1. J. J. Fu
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  2. X. T. Chu
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  3. Y. F. Sun
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  4. Y. F. Xu
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  5. T. M. Hu
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Correspondence to Y. F. Xu or T. M. Hu.

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Acknowledgement

This work was supported by the Natural Science Foundation Research Project of Shaanxi Province of China (No. 2016JM3025), the National Natural Science Foundation of China (No. 31402129), the Northwest A&F University Fundamental Research Special Fund (No. QN2011100) and the Key Projects in the National Science & Technology Pillar Program in the Twelfth Five-Year Plan Period (No. 2011BAD17B05).

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Fu, J.J., Chu, X.T., Sun, Y.F. et al. Involvement of nitric oxide in 5-aminolevulinic acid-induced antioxidant defense in roots of Elymus nutans exposed to cold stress. Biol Plant 60, 585–594 (2016). https://doi.org/10.1007/s10535-016-0635-1

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