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Physiology and Molecular Biology of Plants

, Volume 24, Issue 6, pp 993–1004 | Cite as

Exogenous nitric oxide donor and arginine provide protection against short-term drought stress in wheat seedlings

  • Mirza Hasanuzzaman
  • Kamrun Nahar
  • Anisur Rahman
  • Masashi Inafuku
  • Hirosuke Oku
  • Masayuki FujitaEmail author
Research Article

Abstract

Nitric oxide (NO) is an important plant signaling molecule that has a vital role in abiotic stress tolerance. In the present study, we assessed drought-induced (15 and 30% PEG, polyethylene glycol) damage in wheat (Triticum aestivum L. cv. Prodip) seedlings and mitigation by the synergistic effect of exogenous Arg (0.5 mM l-Arginine) and an NO donor (0.5 mM sodium nitroprusside, SNP). Drought stress sharply decreased the leaf relative water content (RWC) but markedly increased the proline (Pro) content in wheat seedlings. Drought stress caused overproduction of reactive oxygen species (ROS) and methylglyoxal (MG) due to the inefficiency of antioxidant enzymes, the glyoxalase system, and the ascorbate-glutathione pool. However, supplementation with the NO donor and Arg enhanced the antioxidant defense system (both non-enzymatic and enzymatic components) in drought-stressed seedlings. Application of the NO donor and Arg also enhanced the glyoxalase system and reduced the MG content by increasing the activities of the glyoxalase system enzymes (Gly I and Gly II), which restored the leaf RWC and further increased the Pro content under drought stress conditions. Exogenous NO donor and Arg application enhanced the endogenous NO content, which positively regulated the antioxidant system and reduced ROS production. Thus, the present study reveals the crucial roles of Arg and NO in enhancing drought stress tolerance in wheat seedlings by upgrading their water status and reducing oxidative stress and MG toxicity.

Keywords

Amino acid AsA–GSH pathway Glutathione Osmotic stress Oxidative stress Phytohormone 

Notes

Acknowledgements

The first author is grateful to the Japan Society for the Promotion of Science (JSPS), Japan for financial support. We acknowledge Taufika Islam Anee, Mazhar Ul Alam and Farah Tasmin, Laboratory of Plant Stress Responses, Faculty of Agriculture, Kagawa University, Japan for the critical reading and formatting of this manuscript.

Author contributions

M.H., M.F. and H.O. conceived and designed the experiments; M.H., K.N. and A.R. performed the experiments; M.H. and M.I. analyzed the data; M.F., M.I. and H.O. contributed reagents/materials/analysis tools; K.N. and M.H. wrote the manuscript. All authors have read and approved the final manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

References

  1. Addinsoft (2016) XLSTAT V. 2016.04.32525: data analysis and statistics software for Microsoft Excel. Addinsoft, ParisGoogle Scholar
  2. Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249CrossRefGoogle Scholar
  3. Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Kubiś J (2009) Interaction between polyamine and nitric oxide signaling in adaptive responses to drought in cucumber. J Plant Growth Regul 28:177–186CrossRefGoogle Scholar
  4. Arnon DT (1949) Copper enzymes in isolated chloroplasts polyphenaloxidase in Beta vulgaris. Plant Physiol 24:1–15CrossRefGoogle Scholar
  5. Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Aust J Biol Sci 15:413–428CrossRefGoogle Scholar
  6. Bates LS, Waldren RP, Teari D (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207CrossRefGoogle Scholar
  7. Beligni MV, Lamattina L (1999) Nitric oxide counteracts cytotoxic processes mediated by reactive oxygen species in plant tissues. Planta 208:337–344CrossRefGoogle Scholar
  8. Belkheiri O, Mulas M (2013) Effect of water stress on growth, water use efficiency and gas exchange as related to osmotic adjustment of two halophytes Atriplex spp. Funct Plant Biol 40:466–474CrossRefGoogle Scholar
  9. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  10. Chen F, Wang F, Wu F, Mao W, Zhang G, Zhou M (2010) Modulation of exogenous glutathione in antioxidant defense system against Cd stress in the two barley genotypes differing in Cd tolerance. Plant Physiol Biochem 48:663–672CrossRefGoogle Scholar
  11. Corpas FJ, Barroso JB, Carreras A, Valderrama R, Palma JM, León AM, Sandalio LM, del Río LA (2006) Constitutive arginine-dependent nitric oxide synthase activity in different organs of pea seedlings during plant development. Planta 224:246–254CrossRefGoogle Scholar
  12. Freedland RA, Crozier GL, Hicks BL, Meijer AJ (1984) Arginine uptake by isolated rat liver mitochondria. Biochim Biophys Acta 802:407–412CrossRefGoogle Scholar
  13. Freschi L (2013) Nitric oxide and phytohormone interactions: current status and perspectives. Front Plant Sci 4:398CrossRefGoogle Scholar
  14. Gan L, Wu X, Zhong Y (2015) Exogenously applied nitric oxide enhances the drought tolerance in hulless barley. Plant Prod Sci 18:52–56CrossRefGoogle Scholar
  15. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930CrossRefGoogle Scholar
  16. Gonzalez L, Gonzalez-Vilar M (2001) Determination of relative water content. In: Roger MJR (ed) Handbook of plant ecophysiology techniques. Springer, Amsterdam, pp 207–212Google Scholar
  17. Groppa MD, Rosales EP, Iannone MF, Benavides MP (2008) Nitric oxide, polyamines and Cd-induced phytotoxicity in wheat roots. Phytochem 69:2609–2615CrossRefGoogle Scholar
  18. Hao GP, Zhang JH (2010) The role of nitric oxide as a bioactive signaling molecule in plants under abiotic stress. In: Hayat S, Mori M, Pichtel J, Ahmad A (eds) Nitric oxide in plant physiology. Wiley, Weinheim, pp 115–138Google Scholar
  19. Hasanuzzaman M, Hossain MA, Fujita M (2010) Physiological and biochemical mechanisms of nitric oxide induced abiotic stress tolerance in plants. Am J Plant Physiol 5:295–324CrossRefGoogle Scholar
  20. Hasanuzzaman M, Hossain MA, Fujita M (2011) Nitric oxide modulates antioxidant defense and the methylglyoxal detoxification system and reduces salinity-induced damage of wheat seedlings. Plant Biotechnol Rep 5:353–365CrossRefGoogle Scholar
  21. Hasanuzzaman M, Hossain MA, Teixeria da Silva JA, Fujita M (2012) Plant responses and tolerance to abiotic oxidative stress: antioxidant defense is a key factor. In: Bandi V, Shanker AK, Shanker C, Mandapaka M (eds) Crop stress and its management: perspectives and strategies. Springer, Berlin, pp 261–316CrossRefGoogle Scholar
  22. Hasanuzzaman M, Nahar K, Gill SS, Fujita M (2014) Drought stress responses in plants, oxidative stress and antioxidant defense. In: Tuteja N, Gill SS (eds) Climate change and plant abiotic stress tolerance. Wiley, Weinheim, pp 209–250Google Scholar
  23. Hasanuzzaman M, Nahar K, Alam MM, Bhuyan MHMB, Oku H, Fujita M (2018a) Exogenous nitric oxide pretreatment protects Brassica napus L. seedlings from paraquat toxicity through the modulation of antioxidant defense and glyoxalase systems. Plant Physiol Biochem 126:173–186CrossRefGoogle Scholar
  24. Hasanuzzaman M, Oku H, Nahar K, Bhuyan MHMB, Mahmud JA, Baluska F, Fujita M (2018b) Nitric oxide-induced salt stress tolerance in plants: ROS metabolism, signaling, and molecular interactions. Plant Biotechnol Repo.  https://doi.org/10.1007/s11816-018-0480-0 CrossRefGoogle Scholar
  25. Hatamzadeh A, Molaahmad Nalousi A, Ghasemnezhad M, Biglouei MH (2015) The potential of nitric oxide for reducing oxidative damage induced by drought stress in two turfgrass species, creeping bentgrass and tall fescue. Grass Forage Sci 70:538–548CrossRefGoogle Scholar
  26. Hoekstra FA, Golovina EA, Buitink J (2001) Mechanisms of plant desiccation tolerance. Trends Plant Sci 6:431–438CrossRefGoogle Scholar
  27. Hu Y, Ge Y, Zhang C, Ju T, Cheng W (2009) Cadmium toxicity and translocation in rice seedlings are reduced by hydrogen peroxide pretreatment. Plant Growth Regul 59:51–61CrossRefGoogle Scholar
  28. Jiang J, Su M, Chen Y, Gao N, Jiao C, Sun Z, Li F, Wang C (2013) Correlation of drought resistance in grass pea (Lathyrus sativus) with reactive oxygen species scavenging and osmotic adjustment. Biologia 68:231–240CrossRefGoogle Scholar
  29. Kirkham MB (2005) Principles of soil and plant water relations. Elsevier, AmsterdamGoogle Scholar
  30. Kocheva KV, Kartseva T, Landjeva S, Georgiev GI (2009) Physiological response of wheat seedlings to mild and severe osmotic stress. Cereal Res Commun 37:199–208CrossRefGoogle Scholar
  31. Laspina NV, Groppa MD, Tomaro ML, Benavides MP (2005) Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci 169:323–330CrossRefGoogle Scholar
  32. Li X, Gong B, Xu K (2014) Interaction of nitric oxide and polyamines involves antioxidants and physiological strategies against chilling-induced oxidative damage in Zingiber officinale Roscoe. Sci Hortic 170:237–248CrossRefGoogle Scholar
  33. Monakhova OF, Chernyadev II (2002) Protective role of kartolin-4 in wheat plants exposed to soil drought. Appl Environ Microbiol 38:373–380Google Scholar
  34. Nahar K, Hasanuzzaman M, Alam MM, Fujita M (2015) Glutathione-induced drought stress tolerance in mung bean: coordinated roles of the antioxidant defense and methylglyoxal detoxification systems. AoB Plants 7:1–18CrossRefGoogle Scholar
  35. Nahar K, Hasanuzzaman M, Alam MM, Rahman A, Mahmud JA, Suzuki T, Fujita M (2016a) Polyamines confer salt tolerance in mung bean by reducing sodium uptake, improving nutrient homeostasis, antioxidant defense and methylgyoxal detoxification systems. Front Plant Sci.  https://doi.org/10.3389/fpls.2016.01104 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Nahar K, Hasanuzzaman M, Alam MM, Rahman A, Suzuki T, Fujita M (2016b) Polyamine and nitric oxide crosstalk: antagonistic effects on cadmium toxicity in mung bean plants through upregulating the metal detoxification, antioxidant defense and methylglyoxal detoxification systems. Ecotoxicol Environ Saf 126:245–255CrossRefGoogle Scholar
  37. Nasibi F, Heidari T, Asrar Z, Mansoori H (2013) Effect of arginine pre-treatment on nickel accumulation and alleviation of the oxidative stress in Hyoscyamus niger. J Soil Sci Plant Nutr 13:680–689Google Scholar
  38. Neill SJ, Desikan R, Clarke A, Hurat RD, Hancock JT (2002a) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot 53:1237–1247CrossRefGoogle Scholar
  39. Neill S, Desikan R, Hancock J (2002b) Hydrogen peroxide signalling. Curr Opin Plant Biol 5:388–395CrossRefGoogle Scholar
  40. Oz MT, Eyidogan F, Yucel M, Öktem HA (2015) Functional role of nitric oxide under abiotic stress conditions. In: Khan MN, Mobin M, Mohammad F, Corpasn FJ (eds) Nitric oxide action in abiotic stress responses in plants. Springer, New York, pp 21–41Google Scholar
  41. Petrov P, Petrova A, Dimitrov I, Tashev T, Olsovska K, Brestic M, Misheva S (2017) Relationships between leaf morpho-anatomy, water status and cell membrane stability in leaves of wheat seedlings subjected to severe soil drought. J Agro Crop Sci.  https://doi.org/10.1111/jac.12255 CrossRefGoogle Scholar
  42. Polverari A, Molesini B, Pezzotti M, Buonaurio R, Marte M, Delledonne M (2003) Nitric oxide-mediated transcriptional changes in Arabidopsis thaliana. Mol Plant Microbe Interact 16:1084–1105CrossRefGoogle Scholar
  43. Rahman A, Nahar K, Hasanuzzaman M, Fujita M (2016a) Calcium supplementation improves Na+/K+ ratio, antioxidant defense and glyoxalase systems in salt-stressed rice seedlings. Front Plant Sci.  https://doi.org/10.3389/fpls.2016.00609 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Rahman A, Hossain MS, Mahmud JA, Nahar K, Hasanuzzaman M, Fujita M (2016b) Manganese-induced salt stress tolerance in rice seedlings: regulation of ion homeostasis, antioxidant defense and glyoxalase systems. Physiol Mol Biol Plants 22:291–306CrossRefGoogle Scholar
  45. Sheokand S, Kumari A, Sawhney V (2008) Effect of nitric oxide and putrescine on antioxidative responses under NaCl stress in chickpea plants. Physiol Mol Biol Plant 14:355–362CrossRefGoogle Scholar
  46. Shi Q, Ding F, Wang X, Wei M (2007) Exogenous nitric oxide protect cucumber roots against oxidative stress induced by salt stress. Plant Physiol Biochem 45:542–550CrossRefGoogle Scholar
  47. Singh HP, Kaur S, Batish DR, Sharma VP, Sharma N, Kohli RK (2009) Nitric oxide alleviates arsenic toxicity by reducing oxidative damage in the roots of Oryza sativa (rice). Nitric Oxide 20:289–297CrossRefGoogle Scholar
  48. Sotiropoulos TE, Dimassi KN, Therios IN (2005) Effects of l-arginine and l-cysteine on growth, and chlorophyll and mineral contents of shoots of the apple rootstock EM 26 cultured in vitro. Biol Plant 49:443–445CrossRefGoogle Scholar
  49. Sung CH, Hong JK (2010) Sodium nitroprusside mediates seedling development and attenuation of oxidative stresses in Chinese cabbage. Plant Biotechnol Rep 4:243–251CrossRefGoogle Scholar
  50. Tapiero H, Mathé G, Couvreur P, Tew KD (2002) I. Arginine. Biomed Pharmacother 56:439–445CrossRefGoogle Scholar
  51. Todd CD, Cooke JEK, Mullen RT, Gifford DJ (2001) Regulation of loblolly pine (Pinus taeda L.) arginase in developing seedling tissue during germination and post-germinative growth. Plant Mol Biol 45:555–565CrossRefGoogle Scholar
  52. Wang YS, Yang ZM (2005) Nitric oxide reduces aluminum toxicity by preventing oxidative stressing the roots of Cassia tora L. Plant Cell Physiol 46:1915–1923CrossRefGoogle Scholar
  53. Wang F, Wang Q, Kwon S, Kwak S, Su W (2005) Enhanced drought tolerance of transgenic rice plants expressing a pea manganese superoxide dismutase. J Plant Physiol 162:465–472CrossRefGoogle Scholar
  54. Wendehenne D, Gould K, Lamotte O, Durner J, Vandelle E, Lecourieux D, Courtois C, Barnavon L, Bentéjac M, Pugin A (2005) NO signaling functions in the biotic and abiotic stress responses. BMC Plant Biol 5:S3CrossRefGoogle Scholar
  55. Wild R, Ooi L, Srikanth V, Münch G (2012) A quick, convenient and economical method for the reliable determination of methylglyoxal in millimolar concentrations: the N-acetyl-l-cysteine assay. Anal Bioanal Chem 403:2577–2581CrossRefGoogle Scholar
  56. Winter G, Todd CD, Trovato M, Forlani G, Funck D (2015) Physiological implications of arginine metabolism in plants. Front Plant Sci 6:534CrossRefGoogle Scholar
  57. Xu Y, Sun X, Jin J, Zhou H (2010) Protective effect of nitric oxide on light-induced oxidative damage in leaves of tall fescue. J Plant Physiol 167:512–518CrossRefGoogle Scholar
  58. Yadav SK, Singla-Pareek SL, Reddy MK, Sopory SK (2005) Methylglyoxal detoxification by glyoxalase system: a survival strategy during environmental stresses. Physiol Mol Biol Plants 11:1–11Google Scholar
  59. Yadav SK, Singla-Pareek SL, Sopory SK (2008) An overview on the role of methylglyoxal and glyoxalases in plants. Drug Metabol Drug Interact 23:51–68CrossRefGoogle Scholar
  60. Yu YG, Weiss RL (1992) Arginine transport in mitochondria of Neurospora crassa. J Biol Chem 267:15491–15495PubMedGoogle Scholar
  61. Yu CW, Murphy TM, Lin CH (2003) Hydrogen peroxide-induces chilling tolerance in mung beans mediated through ABA-independent glutathione accumulation. Funct Plant Biol 30:955–963CrossRefGoogle Scholar
  62. Zeid IM (2009) Effect of arginine and urea on polyamines content and growth of bean under salinity stress. Acta Physiol Plant 31:65–70CrossRefGoogle Scholar
  63. Zhang XL, Jia XF, Yu B, Gao Y, Bai JG (2011) Exogenous hydrogen peroxide influences antioxidant enzyme activity and lipid peroxidation in cucumber leaves at low light. Sci Hortic 129:656–662CrossRefGoogle Scholar
  64. Zheng C, Jiang D, Liu F, Dai T, Liu W, Jing Q, Cao W (2009) Exogenous nitric oxide improves seed germination in wheat against mitochondrial oxidative damage induced by high salinity. Environ Exp Bot 67:222–227CrossRefGoogle Scholar
  65. Zivcak M, Repková J, Olšovská K, Brestič M (2009) Osmotic adjustment in winter wheat varieties and its importance as a mechanism of drought tolerance. Cereal Res Commun 37:569–572Google Scholar
  66. Zivcak M, Brestic M, Sytar O (2016) Osmotic adjustment and plant adaptation to drought stress. In: Hossain MA, Wani S, Bhattacharjee S, Burritt D, Tran LS (eds) Drought stress tolerance in plants, vol 1. Springer, Cham, pp 105–143CrossRefGoogle Scholar

Copyright information

© Prof. H.S. Srivastava Foundation for Science and Society 2018

Authors and Affiliations

  • Mirza Hasanuzzaman
    • 1
    • 2
  • Kamrun Nahar
    • 3
  • Anisur Rahman
    • 1
  • Masashi Inafuku
    • 1
  • Hirosuke Oku
    • 1
  • Masayuki Fujita
    • 4
    Email author
  1. 1.Molecular Biotechnology Group, Center of Molecular Biosciences (COMB), Tropical Biosphere Research CenterUniversity of the RyukyusNishiharaJapan
  2. 2.Department of Agronomy, Faculty of AgricultureSher-e-Bangla Agricultural UniversityDhakaBangladesh
  3. 3.Department of Agricultural Botany, Faculty of AgricultureSher-e-Bangla Agricultural UniversityDhakaBangladesh
  4. 4.Laboratory of Plant Stress Responses, Faculty of AgricultureKagawa UniversityMiki-cho, Kita-gunJapan

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