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Boron toxicity is alleviated by hydrogen sulfide in cucumber (Cucumis sativus L.) seedlings

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Abstract

Boron (B) is an essential micronutrient for plants, which when occurs in excess in the growth medium, becomes toxic to plants. Rapid inhibition of root elongation is one of the most distinct symptoms of B toxicity. Hydrogen sulfide (H2S) is emerging as a potential messenger molecule involved in modulation of physiological processes in plants. In the present study, we investigated the role of H2S in B toxicity in cucumber (Cucumis sativus) seedlings. Root elongation was significantly inhibited by exposure of cucumber seedlings to solutions containing 5 mM B. The inhibitory effect of B on root elongation was substantially alleviated by treatment with H2S donor sodium hydrosulfide (NaHS). There was an increase in the activity of pectin methylesterase (PME) and up-regulated expression of genes encoding PME (CsPME) and expansin (CsExp) on exposure to high B concentration. The increase in PME activity and up-regulation of expression of CsPME and CsExp induced by high B concentration were markedly reduced in the presence of H2S donor. There was a rapid increase in soluble B concentrations in roots on exposure to high concentration B solutions. Treatment with H2S donor led to a transient reduction in soluble B concentration in roots such that no differences in soluble B concentrations in roots in the absence and presence of NaHS were found after 8 h exposure to the high concentration B solutions. These findings suggest that increases in activities of PME and expansin may underlie the inhibition of root elongation by toxic B, and that H2S plays an ameliorative role in protection of plants from B toxicity by counteracting B-induced up-regulation of cell wall-associated proteins of PME and expansins.

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Abbreviations

B:

Boron

MDA:

Malondialdehyde

PME:

Pectin methylesterases

RGII:

Rhamnogalacturonan II

References

  • Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24:1337–1344

    Article  CAS  Google Scholar 

  • Ardıc M, Sekmen AH, Turkan I, Tokur S, Ozdemir F (2009) The effects of boron toxicity on root antioxidant systems of two chickpea (Cicer arietinum L.) cultivars. Plant Soil 314:99–108

    Article  Google Scholar 

  • Bevins DG, Lukaszewski KM (1998) Boron in plant structure and function. Annu Rev Plant Biol 49:481–500

    Article  Google Scholar 

  • Blamey FPC (2001) The role of the cell wall in aluminum toxicity. In: Ae N, Arihara J, Okada K, Srinivasan A (eds) Plant nutrient acquisition: new perspectives. Springer, Tokyo, pp 201–226

    Google Scholar 

  • Camacho-Cristóbal JJ, Herrera-Rodríguez MB, Beato VM, Rexach J, Navarro-Gochicoa MT, Maldonado JM, González-Fontes A (2008) The expression of several cell wall-related genes in Arabidopsis roots is down-regulated under boron deficiency. Environ Exp Bot 63:351–358

    Article  Google Scholar 

  • Cervilla LM, Blasco B, Ríos JJ, Romero L, Ruiz JM (2007) Oxidative stress and antioxidants in tomato (Solanum lycopersicum) plants subjected to boron toxicity. Ann Bot 100:747–756

    Article  CAS  PubMed  Google Scholar 

  • Cervilla LM, Rosales MA, Rubio-Wilhelmi MM, Sánchez-Rodríguez E, Blasco B, Ríos JJ, Romero L, Rui JM (2009) Involvement of lignification and membrane permeability in the tomato root response to boron toxicity. Plant Sci 176:545–552

    Article  CAS  Google Scholar 

  • Chantachume Y, Smith D, Hollamby GJ, Paull JG, Rathjen AJ (1995) Screening for boron tolerance in wheat by solution culture in filter paper. Plant Soil 177:249–254

    Article  CAS  Google Scholar 

  • Choi EY, Kolesil P, Mcneill A, Collins H, Zhang QS, Huynh BL, Graham R, Stangoulis JCR (2007) The mechanism of boron tolerance for maintenance of root growth in barley (Hordeum vulgare L.). Plant Cell Environ 30:984–993

    Article  CAS  PubMed  Google Scholar 

  • Cosgrove DJ (2005) Growth of the plant cell wall. Nature Rev Mol Cell Biol 6:850–861

    Article  CAS  Google Scholar 

  • Dell B, Huang LB (1997) Physiological response of plants to low boron. Plant Soil 193:103–120

    Article  CAS  Google Scholar 

  • Gaines TP, Mitchell GA (1979) Boron determination in plant tissue by azomethine-H method. Soil Sci Plant Anal 10:1099–1108

    Article  CAS  Google Scholar 

  • Ghanati F, Morita A, Yokota H (2002) Induction of suberin and increase of lignin content by excess boron in tobacco cells. Soil Sci Plant Nutr 48:357–364

    CAS  Google Scholar 

  • Gunes A, Soylemezoglu G, Inal A, Bagci EG, Coban S, Sahin O (2006) Antioxidant and stomatal responses of grapevine (Vitis vinifera L.) to boron toxicity. Sci Hort 110:279–284

    Article  CAS  Google Scholar 

  • Hällgren JE, Fredriksson SÅ (1982) Emission of hydrogen sulfide from sulfate dioxide-fumigated pine trees. Plant Physiol 70:456–459

    Article  PubMed  Google Scholar 

  • Hayes JE, Reid RJ (2004) Boron tolerance in barley is mediated by boron efflux from the roots. Plant Physiol 136:3376–3382

    Article  CAS  PubMed  Google Scholar 

  • Holdaway-Clarke TL, Weddle NM, Kim S, Robi A, Parris C, Kunkell JG, Hepler PK (2003) Effect of extracellular calcium, pH and borate on growth oscillations in Lilium formosanum pollen tubes. J Exp Bot 54:65–72

    Article  CAS  PubMed  Google Scholar 

  • Holloway RE, Alston AM (1992) The effects of salt and boron on growth of wheat. Aust J Agric Res 43:987–1001

    Article  CAS  Google Scholar 

  • Ishii T, Matsunaga T, Hayashi N (2001) Formation of rhamnogalacturonan II-borate dimmer in pectin determines cell wall thickness of pumpkin tissue. Plant Physiol 126:1698–1705

    Article  CAS  PubMed  Google Scholar 

  • Karabal E, Yűcel M, Ökte HA (2003) Antioxidants responses of tolerant and sensitive barley cultivars to boron toxicity. Plant Sci 164:925–933

    Article  CAS  Google Scholar 

  • Kimura Y, Kimura H (2004) Hydrogen sulfide protects neurons from oxidative stress. FASEB J 18:1165–1167

    CAS  PubMed  Google Scholar 

  • Lefer DJ (2007) A new gaseous signaling molecule emerges: cardioprotective role of hydrogen sulfide. Proc Natl Acad Sci USA 104:17907–17908

    Article  CAS  PubMed  Google Scholar 

  • Matoh T (1997) Boron in plant cell walls. Plant Soil 193:59–70

    Article  CAS  Google Scholar 

  • Micheli F (2001) Pectinmethylesterases: cell wall enzymes with important roles in plant physiology. Trends Plant Sci 6:414–419

    Article  CAS  PubMed  Google Scholar 

  • Molassiotis A, Sotiropoulos T, Tanou G, Diamantidis G, Therios I (2006) Boron induced oxidative damage and antioxidant and nucleolytic responses in shoot tips culture of the apple rootstock EM9 (Malusdomestica Borkh). Environ Exp Bot 56:54–62

    Article  CAS  Google Scholar 

  • Nable RO (1988) Resistance to boron toxicity amongst several wheat cultivars: a preliminary examination of the resistance mechanism. Plant Soil 112:45–52

    Article  CAS  Google Scholar 

  • O’Neill MA, Eberhard S, Darvill AG, Albersheim P (2001) Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth. Science 294:846–849

    Article  PubMed  Google Scholar 

  • O’Neill MA, Ishii T, Albersheim P, Darvill AG (2004) Rhamnogalacturonan II: structure and function of a borate cross-linked cell wall pectic polysaccharide. Annu Rev Plant Biol 55:109–139

    Article  PubMed  Google Scholar 

  • Pelloux J, Rustérucci C, Mellerowicz EJ (2007) New insights into pectin methylesterase structure and function. Trends Plant Sci 12:267–277

    Article  CAS  PubMed  Google Scholar 

  • Reid RJ (2007) Identification of boron transporter genes likely to be responsible for tolerance to boron toxicity in wheat and barley. Plant Cell Physiol 48:1673–1678

    Article  CAS  PubMed  Google Scholar 

  • Reid RJ, Hayes JE, Post A, Stagoulis JCR, Graham RD (2004) A critical analysis of the causes of boron toxicity in plants. Plant Cell Environ 25:1405–1414

    Article  Google Scholar 

  • Richard L, Qin LX, Gadal P, Goldberg R (1994) Molecular cloning and characterization of a putative pectin methylesterase cDNA in Arabidopsis thaliana. FEBS Lett 355:135–139

    Article  CAS  PubMed  Google Scholar 

  • Roessner U, Patterson JH, Forbes MG, Fincher GB, Langridge P, Bacic A (2006) An investigation of boron toxicity in barley using metabolomics. Plant Physiol 142:1087–1101

    Article  CAS  PubMed  Google Scholar 

  • Ryan PR, DiTomaso JM, Kochian LV (1993) Aluminum toxicity in roots: an investigation of spatial sensitivity and the role of the root cap. J Exp Bot 44:437–446

    Article  CAS  Google Scholar 

  • Ryden P, Sugimoto-Shirasu K, Smith AC, Findlay K, Reiter WD, McCann MC (2003) Tensile properties of Arabidopsis cell walls depend on both a xyloglucan cross-linked microfibrillar network and rhamnogalacturonan II-borate complexes. Plant Physiol 132:1033–1040

    Article  CAS  PubMed  Google Scholar 

  • Schmohl N, Pilling J, Fisahn J, Horst WJ (2000) Pectin methylesterase modulates aluminum sensitivity in Zea mays and Solanum tuberosum. Physiol Plant 109:419–427

    Article  CAS  Google Scholar 

  • Sekiya J, Schmidt A, Wilson LG, Filner P (1982) Emission of hydrogen sulfide by leaf tissue in response to l-cysteine. Plant Physiol 70:430–436

    Article  CAS  PubMed  Google Scholar 

  • Stangoulis JCR, Reid RJ (2002) Boron toxicity in plants and animals. In: Goldbach HE et al (eds) Boron in plant and animal nutrition. Kluwer Academic Press, New York, pp 227–240

    Google Scholar 

  • Wang R (2002) Two’s company, three’s a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J 16:1792–1798

    Article  CAS  PubMed  Google Scholar 

  • 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 146:602–611

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Hu LY, Hu KD, He YD, Wang SH, Luo JP (2008) Hydrogen sulfide promotes wheat seed germination and alleviates the oxidative damage against copper stress. J Integr Plant Biol 50:1518–1529

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Ye YK, Wang SH, Luo JP, Tang J, Ma DF (2009) Hydrogen sulfide counteracts chlorophyll loss in sweet potato seedling leaves and alleviates oxidative damage against osmotic stress. Plant Growth Regul 58:243–250

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National High Technology and Research Development Program of P. R. China (Grant no. 2007AA091705) and National Science Foundation of China (30788003). We thank the two anonymous reviewers for their constructive suggestions.

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  1. State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, The Chinese Academy of Sciences, Beijing, 100093, People’s Republic of China

    Bao-Lan Wang, Lei Shi, Yin-Xing Li & Wen-Hao Zhang

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  1. Bao-Lan Wang
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  2. Lei Shi
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  4. Wen-Hao Zhang
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Correspondence to Wen-Hao Zhang.

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Wang, BL., Shi, L., Li, YX. et al. Boron toxicity is alleviated by hydrogen sulfide in cucumber (Cucumis sativus L.) seedlings. Planta 231, 1301–1309 (2010). https://doi.org/10.1007/s00425-010-1134-9

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