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BioMetals

, Volume 32, Issue 1, pp 1–9 | Cite as

Role of nitric oxide and hydrogen sulfide in plant aluminum tolerance

  • Huyi He
  • Yingqiu Li
  • Long-Fei HeEmail author
Article
  • 138 Downloads

Abstract

As gasotransmitter, nitric oxide (NO) and hydrogen sulfide (H2S) are involved in the regulation of plant tolerance to abiotic stresses. Aluminum (Al) toxicity triggers synthesis of NO and H2S and seriously affects plant growth and productivity. Exogenous NO and H2S alleviate Al toxicity in plants. However, the physiological and molecular mechanisms of NO and H2S in alleviating Al toxicity are very scattered. In this review, the advances in the effects of Al on the content of endogenous NO and H2S and the mechanisms of exogenous NO and H2S in alleviating Al toxicity in plants are summarized and discussed. The signaling pathway for the roles of NO and H2S in alleviating Al toxicity is also proposed.

Keywords

Aluminum Nitric oxide Hydrogen sulfide Oxidative stress Reactive oxygen species Tolerance gene 

Notes

Acknowledgements

This study was supported by grants from the National Natural Science Foundation of China (No. 31660352) and the Science and Technology Development Fund of Guangxi Academy of Agricultural Sciences (Guinongke2017JZ11 and Guinongke2017JZ21). We thank the reviewers for their helpful comments on this manuscript.

References

  1. Aroca A, Serna A, Gotor C, Romero LC (2015) S-sulfhydration: a cysteine posttranslational modification in plant systems. Plant Physiol 168:334–342CrossRefGoogle Scholar
  2. Astier J, Jeandroz S, Wendehenne D (2018) Nitric oxide synthase in plants: the surprise from algae. Plant Sci.  https://doi.org/10.1016/j.plantsci.2017.12.008 Google Scholar
  3. Bethke PC, Libourel IG, Reinohl V, Jones RL (2006) Sodium nitroprusside, cyanide, nitrite, and nitrate break Arabidopsis seed dormancy in a nitric oxide-dependent manner. Planta 223(4):805–812CrossRefGoogle Scholar
  4. Cai MZ, Zhang SN, Wang FM, Wang N, Xu SY (2011) Protective effect of exogenously applied nitric oxide on aluminum-induced oxidative stress in soybean plants. Russ J Plant Physiol 58:791–798CrossRefGoogle Scholar
  5. Chen J, Wang WH, Wu FH, You CY, Liu TW, Dong XJ, He JX, Zheng HL (2013) Hydrogen sulfide alleviates aluminum toxicity in barley seedlings. Plant Soil 362:301–318CrossRefGoogle Scholar
  6. Chen M, Cui W, Zhu K, Xie Y, Zhang C, Shen W (2014) Hydrogen-rich water alleviates aluminum-induced inhibition of root elongation in alfalfa via decreasing nitric oxide production. J Hazard Mater 267:40–47CrossRefGoogle Scholar
  7. Chen J, Wang WH, Wu FH, He EM, Liu X, Shangguan ZP, Zheng HL (2015) Hydrogen sulfide enhances salt tolerance through nitric oxide-mediated mantenance of ion homeostasis in barley seedling roots. Sci Rep 5:12516CrossRefGoogle Scholar
  8. da Rocha Oliveiros Marciano DP, Ramos FT, Alvim MN, Magalhaes JR, Franca MGC (2010) Nitric oxide reduces the stress effects of aluminum on the process of germination and early root growth of rice. J Plant Nutr Soil Sci 173:885–891CrossRefGoogle Scholar
  9. Dawood M, Cao F, Jiahanqir MM, Zhang G, Wu F (2012) Alleviation of aluminum toxicity by hydrogen sulfide is related to elevated ATPase, and suppressed aluminum uptake and oxidative stress in barley. J Hazard Mater 209–210:121–128CrossRefGoogle Scholar
  10. Faro MLL, Fox B, Whatmore JL, Winyard PG, Whiteman M (2014) Hydrogen sulfide and nitric oxide interactions in inflammation. Nitric Oxide 41(11):38CrossRefGoogle Scholar
  11. Gupta K, Hebelstrup KH, Mur LAJ, Igamberdiev AU (2011) Plant hemoglobins: important playsers at the crossroads between oxygen and nitric oxide. FEBS Lett 585(24):3843–3849CrossRefGoogle Scholar
  12. He HY, He LF, Li XF, Gu MH (2006) Effects of sodium nitroprusside on mitochondrial function of rye and wheat root tip under aluminum stress. J Plant Physiol Mol Biol 32(2):239–244Google Scholar
  13. He H, He L, Li X, Gu M (2007) Effect of SNP on Al adsorption of root tip cell wall from rye and wheat under aluminum stress. J Guangxi Agric Biol Sci 26(3):235–239 (in Chinese) Google Scholar
  14. He H, Zhan J, He L, Gu M (2012a) Nitric oxide signaling in aluminum stress in plants. Protoplasma 249:483–492CrossRefGoogle Scholar
  15. He HY, He LF, Gu MH, Li XF (2012b) Nitric oxide improves aluminum tolerance by regulating hormonal equilibrium in the root apices of rye and wheat. Plant Sci 183:123–130CrossRefGoogle Scholar
  16. He H, He L, Gu M (2012c) Interactions between nitric oxide and plant hormones in aluminum tolerance. Plant Signal Behav 7(4):469–471CrossRefGoogle Scholar
  17. He H, He L, Gu M (2014) The diversity of nitric oxide function in plant responses to metal stress. Biometals 27(2):219–228CrossRefGoogle Scholar
  18. He H, Huang W, Oo TL, Gu M, He LF (2017) Nitric oxide inhibits aluminum-induced programmed cell death in peanut (Arachis hypoganea L.) root tips. J Hazard Mater 333:285–292CrossRefGoogle Scholar
  19. He H, Huang W, Oo TL, Gu M, Zhan J, Wang A, He LF (2018) Nitric oxide suppresses aluminum-induced programmed cell death in peanut (Arachis hypoganea L.) root tips by improving mitochondrial physiological properties. Nitric Oxide 74:47–55CrossRefGoogle Scholar
  20. Hou NN, You JF, Pang JD, Xu MY, Chen G, Yang ZM (2010) The accumulation and transport of abscisic acid in soybean (Glycine max L.) under aluminum stress. Plant Soil 330:127–137CrossRefGoogle Scholar
  21. Illéš P, Schlicht M, Pavlovkin J, Lichtscheidl I, Baluška F, Ovecˇka M (2006) Aluminum toxicity in plants: internalization of aluminum into cells of the transition zone in Arabidopsis root apices relates to changes in plasma membrane potential, endosomal behaviour and nitric oxide production. J Exp Bot 57:4201–4213CrossRefGoogle Scholar
  22. Innocenti G, Pucciariello C, Gleuher ML, Hopkins J, de Stefano M, Delledonne M, Puppo A, Baudouin E, Frendo P (2007) Glutathione synthesis is regulated by nitric oxide in Medicago truncatula roots. Planta 225:1597–1602CrossRefGoogle Scholar
  23. Kolluru GK, Shen X, Kevil CG (2013) A tale of two gases: NO and H2S, foes or friends for life? Redox Biol 1:313–318CrossRefGoogle Scholar
  24. Li Z, Xing D (2011) Mechanistic study of mitochondria-dependent programmed cell death induced by aluminum phytotoxicity using fluorescence techniques. J Exp Bot 62(1):331–343CrossRefGoogle Scholar
  25. Li L, Wang Y, Shen W (2012) Roles of hydrogen sulfide and nitric oxide in the alleviation of cadmium-induced oxidative damage in alfalfa seedling roots. Biometals 25(3):617–631CrossRefGoogle Scholar
  26. Li ZG, Yang SZ, Long WB, And GXY, Shen ZZ (2013) Hydrogen sulfide may be a novel downstream signal molecule in nitric oxide-induced heat tolerance of maize (Zea mays L.) seedlings. Plant Cell Environ 36(8):1564–1572CrossRefGoogle Scholar
  27. Lindermayr C, Saalbach G, Durner J (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis thaliana. Plant Physiol 137:921–930CrossRefGoogle Scholar
  28. Liu J, Hou L, Liu G, Liu X, Wang X (2011) Hydrogen sulfide induced nitric oxide mediates ethylene-induced stomatal closure of Arabidopsis thaliana. Chin Sci Bull 56(33):3547–3553CrossRefGoogle Scholar
  29. Liu J, Hou ZH, Liu GH, Hou LX, Liu X (2012) Hydrogen sulfide may function downstream of nitric oxide in ethylene-induced stomatal closure in Vicia faba L. J Integr Agric 11(10):1644–1653CrossRefGoogle Scholar
  30. Massot N, Nicander B, Barcelo J, Poschenrieder C, Tillberg E (2002) A rapid increase in cytokinin levels and enhanced ethylene evolution precede Al3 + -induced inhibition of root growth in bean seedlings (Phaseolus vulgaris L.). Plant Growth Regul 37:105–112CrossRefGoogle Scholar
  31. Nagpure BV, Bian JS (2016) Interaction of hydrogen sulfide with nitric oxide in the cardiovascular system. Oxid Med Cell Longev 2016:6904327CrossRefGoogle Scholar
  32. Qian P, Sun R, Ali B, Gill RA, Xu L, Zhou W (2014) Effects of hydrogen sulfide on growth, antioxidative capacity, and ultrastructural changes in oilseed rape seedlings under aluminum toxicity. J Plant Growth Regul 33(3):526–538CrossRefGoogle Scholar
  33. Rausch T, Wachter A (2005) Sulfur metabolism: a versatile platform for launching defence operations. Trends Plant Sci 10:503–509CrossRefGoogle Scholar
  34. Scuffi D, Alvarez C, Laspina N, Gotor C, Lamattina L, Garcia-Mata C (2014) Hydrogen sulfide generated by l-cysteine desulfhydrase acts upstream of nitric oxide to modulate abscisic acid-dependent stomatal closure. Plant Physiol 166(4):2065–6076CrossRefGoogle Scholar
  35. Shi H, Ye T, Chan Z (2014) Nitric oxide-activated hydrogen sulfide is essential for cadmium stress response in bermudagrass (Cynodon dactylon (L). Pers.). Plant Physiol Biochem 74:99–107CrossRefGoogle Scholar
  36. Shjkowska-Rybkowska M, Czarnocka W, Sanko-Sawczenko I, Witon D (2018) Effect of short-term aluminum stress and mycorrhizal inoculation on nitric oxide metabolism in Medicago truncatula roots. J Plant Physiol 220:145–154CrossRefGoogle Scholar
  37. Sun P, Tian QY, Zhao MG, Dai XY, Huang JH, Li LH et al (2007) Aluminum-induced ethylene production is associated with inhibition of root elongation in Lotus japonicus L. Plant Cell Physiol 48:1229–1235CrossRefGoogle Scholar
  38. Sun P, Tian QY, Chen J, Zhang WH (2010) Aluminium induced inhibition of root elongation in Arabidopsis is mediated by ethylene and auxin. J Exp Bot 61:347–356CrossRefGoogle Scholar
  39. Sun C, Lu L, Liu L, Liu W, Yu Y, Liu X, Hu Y, Jin C, Lin X (2015a) Nitrate reductase-mediated early nitric oxide burst alleviates oxidative damage induced by aluminum through enhancement of antioxidant defenses in roots of wheat (Triticum aestivum). New Phytol 201:1240–1250CrossRefGoogle Scholar
  40. Sun C, Liu L, Yu Y, Liu W, Lu L, Jin C, Lin X (2015b) Nitric oxide alleviates aluminum-induced oxidative damage through regulating the ascorbate-glutathione cycle in roots of wheat. J Integ Plant Biol 57(6):550–561CrossRefGoogle Scholar
  41. Sun C, Lu L, Yu Y, Liu L, Hu Y, Ye Y, Jin C, Lin X (2016) Decreasing methylation of pectin caused by nitric oxide leads to higher aluminum binding in cell walls and greater aluminum sensitivity of wheat roots. J Exp Bot 67(3):979–989CrossRefGoogle Scholar
  42. Tian QY, Sun DH, Zhao MG, Zhang WH (2007) Inhibition of nitric oxide synthase (NOS) underlies aluminum-induced inhibition of root elongation in Hibiscus moscheutos. New Phytol 174:322–331CrossRefGoogle Scholar
  43. Wang R (2012) Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiol Rev 92(2):791–896CrossRefGoogle Scholar
  44. Wang YS, Yang ZM (2005) Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L. Plant Cell Physiol 46:1915–1923CrossRefGoogle Scholar
  45. Wang HH, Huang JJ, Bi YR (2010) Nitrate reductase-dependent nitric oxide production is involved in aluminum tolerance in red kidney bean roots. Plant Sci 179(3):281–288CrossRefGoogle Scholar
  46. Wang Y, Li L, Cui W, Xu S, Shen W, Wang R (2012) Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway. Plant Soil 351(1–2):107–119CrossRefGoogle Scholar
  47. Wang H, Huang J, Liang W, Liang X, Bi Y (2013) Involvement of putrescine and nitric oxide in aluminum tolerance by modulating citrate secretion from roots of red kidney bean. Plant Soil 366:479–490CrossRefGoogle Scholar
  48. Wang H, Li Y, Hou J, Huang J, Liang W (2016) Nitrate reductase-mediated nitric oxide production alleviates Al-induced inhibition of root elongation by regualting the ascorbate-glutathione cycle in soybean roots. Plant Soil.  https://doi.org/10.1007/s11104-016-3045-4 Google Scholar
  49. Wang H, Hou J, Li Y, Zhang Y, Huang J, Liang W (2017) Nitric oxide-mediated cytosolic glucose-6-phosphate dehydrogenase is involved in aluminum toxicity of soybean under high aluminum concentration. Plant Soil 416:39–52CrossRefGoogle Scholar
  50. Weiss D, Ori N (2007) Mechanisms of cross talk between gibberellin and other hormones. Plant Physiol 144:1240–1246CrossRefGoogle Scholar
  51. Whiteman M, Moore PK (2009) Hydrogen sulfide and the vasculature: a novel vasculoprotective entity and regulator of nitric oxide bioavailability? J Cell Mol Med 13(3):488–507CrossRefGoogle Scholar
  52. Whiteman M, Li L, Kostetski I, Chu SH, Siau JL, Bhatia M, Moore PK (2006) Evidence for the formation of a novel nitrosothiol from the gaseous mediators nitric oxide and hydrogen sulphide. Biochem Biophys Res Commun 343:303–310CrossRefGoogle Scholar
  53. Xue YJ, Tao L, Yang ZM (2008) Aluminum-induced cell wall peroxidase activity and lignin synthesis are differentially regulated by jasmonate and nitric oxide. J Agric Food Chem 56:9676–9684CrossRefGoogle Scholar
  54. Yamasaki H, Sakihama Y (2000) Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NR-dependent formation of active nitrogen species. FEBS Lett 468:89–92CrossRefGoogle Scholar
  55. Yang JL, Li YY, Zhang YJ, Zhang SS, Wu YR, Wu P, Zheng SJ (2008) Cell wall polysaccharides are specifically involved in the exclusion of aluminum from the rice root apex. Plant Physiol 146(2):602–611CrossRefGoogle Scholar
  56. Yang Y, Wang QL, Geng MJ, Guo ZH, Zhao ZQ (2011) Effect of indole-3-acetic acid on aluminum-induced efflux of malic acid from wheat (Triticum aestivum L.). Plant Soil 346:215–230CrossRefGoogle Scholar
  57. Yang LT, Chen LS, Peng HY, Guo P, Wang P, Ma CL (2012a) Organic acid metabolism in Citrus grandis leaves and roots is differently affected by nitric oxide and aluminum interactions. Sci Hortic 133:40–46CrossRefGoogle Scholar
  58. Yang LT, Qi YP, Chen LS, Sang W, Lin XJ, Wu YL, Yang CJ (2012b) Nitric oxide protects sour pummelo (Citrus grandis) seedlings against aluminum-induced-inhibition in growth and photosynthesis. Environ Exp Bot 82:1–13CrossRefGoogle Scholar
  59. Yang L, Tian D, Todd CD, Luo Y, Hu X (2013) Comparative proteome analyses reveal that nitric oxide is an important signal molecule in the response of rice to aluminum toxicity. J Proteome Res 12:1316–1330CrossRefGoogle Scholar
  60. Yin L, Wang S, Eltayeb AE, Uddin MI, Yamamoto Y, Tsuji W, Takeuchi Y, Tanaka K (2010) Overexpression of dehydroascorbate reductase, but not monodehydroascorbate reductase, confers tolerance to aluminum stress in transgenic tobacco. Planta 231(3):609–621CrossRefGoogle Scholar
  61. Yuan S, Patel RP, Kevil CG (2015) Working with nitric oxide and hydrogen sulfide in biological systems. Amer J Physiol-Lung Cell Mol Physiol 308(5):L403–L415CrossRefGoogle Scholar
  62. Zhan J, Wang TJ, He HY, Li CZ, He LF (2011) Effects of SNP on AhSAG and AhBI-1 genes expression and amelioration of aluminum stress to peanut (Arachis hypoganea L.). Acta Agron Sinica 37:459–468 (in Chinese) CrossRefGoogle Scholar
  63. Zhang H, Li YH, Hu LY, Wang SH, Zhang FQ, Hu KD (2008) Effects of exogenous nitric oxide donor on antioxidant metabolism in wheat leaves under aluminum stress. Russ J Plant Physiol 55:469–474CrossRefGoogle Scholar
  64. Zhang H, Tan ZQ, Hu LY, Wang SH, Luo JP, Jones RL (2010) Hydrogen sulfide alleviates aluminum toxicity in germinating wheat seedlings. J Integr Plant Biol 52:556–567CrossRefGoogle Scholar
  65. Zhang ZY, Wang HH, Wang XM, Bi YR (2011) Nitric oxide enhances aluminum tolerance by affecting cell wall polysaccharides in rice roots. Plant Cell Rep 30(9):1701–1711CrossRefGoogle Scholar
  66. Zhou Y, Xu XY, Chen LQ, Yang JL, Zheng SJ (2012) Nitric oxide exacerbated Al-induced inhibition of root elongation in rice bean by affecting cell wall and plasma membrane properties. Phytochemistry 76:46–51CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.College of AgronomyGuangxi UniversityNanningChina
  2. 2.Cash Crops Research Institute, Guangxi Academy of Agricultural SciencesNanningChina

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