Skip to main content
Log in

Regulation of nitrogen and phosphorus absorption by plasma membrane H+-ATPase in rice roots under simulated acid rain

  • Original Paper
  • Published:
International Journal of Environmental Science and Technology Aims and scope Submit manuscript

Abstract

The recognition of adverse environmental impact of acid rain is a prerequisite for finding feasible approaches to alleviate such damage to plants. We studied the regulation of nitrogen and phosphorus absorption by plasma membrane H+-ATPase and its expression at transcriptional levels in rice roots exposed to acid rain under hydroponic conditions. At pH 5.0 and 3.5, acid rain increased activity of plasma membrane H+-ATPase by increasing transcriptional levels of OSA1, 4, 5, 6, 7, 8, 9, and 10 and promoted ammonium absorption. However, nitrates and phosphorus contents in roots were decreased by acid rain (pH 3.5) due to a decrease in the H+ gradient. At pH 2.5, acid rain decreased nitrogen and phosphorus content in roots by decreasing plasma membrane H+-ATPase activity and its expression at transcriptional levels (OSA1OSA10) as well as synthesis of ATP and inhibited the growth. After a 5-day recovery (without acid rain), all the parameters in roots treated with acid rain (pH 5.0 or 3.5) were greater than the data measured during the exposure period. However, all the parameters in roots treated with acid rain (pH 2.5) could not be recovered because heavy acid rain caused irreversible inhibition on plasma membrane H+-ATPase activity. Hence, we concluded that plasma membrane H+-ATPase plays a role in adaptation of rice seedlings to acid rain by regulating the absorption of nitrogen and phosphorus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Alvarez-Pizarro JC, Gomes-Filho E, Prisco JT, Grossi-de-Sa MF, Neto OBO (2011) NH4 +-stimulated low-K+ uptake is associated with the induction of H+ extrusion by the plasma membrane H+-ATPase in sorghum roots under K+ deficiency. J Plant Physiol 168:1617–1626

    Article  CAS  Google Scholar 

  • Amtmann A, Blatt MR (2009) Regulation of macronutrient transport. New Phytol 181:35–52

    Article  CAS  Google Scholar 

  • Andonova LB (2007) Acid rain in a wider Europe: the post-communist transition and the future European acid rain policies. In: Visgillio G (ed) Acid in the environment: lessons learned and future prospects. Springer, US, pp 151–173

    Chapter  Google Scholar 

  • Arango M, Gevaudant F, Oufattole M, Boutry M (2003) The plasma membrane proton pump ATPase: the significance of gene subfamilies. Planta 216:355–365

    CAS  Google Scholar 

  • Baginski E, Foa P, Zak B (1967) Determination of phosphate: study of labile organic phosphate interference. Clin Chim Acta 15:155–158

    Article  CAS  Google Scholar 

  • 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 72:248–254

    Article  CAS  Google Scholar 

  • Britto DT, Siddiqi MY, Glass ADM, Kronzucker HJ (2001) Futile transmembrane NH4 + cycling: a cellular hypothesis to explain ammonium toxicity in plants. Proc Natl Acad Sci USA 98:4255–4258

    Article  CAS  Google Scholar 

  • Chang C, Hu Y, Sun S, Zhu Y, Ma G, Xu G (2009) Proton pump OSA8 is linked to phosphorus uptake and translocation in rice. J Exp Bot 60:557–565

    Article  CAS  Google Scholar 

  • Crawford NM, Glass ADM (1998) Molecular and physiological aspects of nitrate uptake in plants. Trends Plant Sci 3:389–395

    Article  Google Scholar 

  • DeHayes DH, Schaberg PG, Hawley GJ, Strimbeck GR (1999) Acid rain impacts on calcium nutrition and forest health alteration of membrane-associated calcium leads to membrane destabilization and foliar injury in red spruce. Bioscience 49:789–800

    Article  Google Scholar 

  • Du Y, Wei M, Reddy KR, Liu Z, Jin F (2014) Effect of acid rain pH on leaching behavior of cement stabilized lead-contaminated soil. J Hazard Mater 271:131–140

    Article  CAS  Google Scholar 

  • Farid M, Ali S, Ishaque W, Shakoor MB, Niazi NK, Bibi I, Dawood M, Gill RA, Abbas F (2015) Exogenous application of ethylenediamminetetraacetic acid enhanced phytoremediation of cadmium by brassica napus l. Int J Environ Sci Technol 12(12):3981–3992

    Article  CAS  Google Scholar 

  • Forde BG, Clarkson DT (1999) Nitrate and ammonium nutrition of plants: physiological and molecular perspectives. Adv. Bot. Res. 30:1–90

    Article  CAS  Google Scholar 

  • Glass AD, Britto DT, Kaiser BN, Kinghorn JR, Kronzucker HJ, Kumar A, Okamoto M, Rawat S, Siddiqi M, Unkles SE (2002) The regulation of nitrate and ammonium transport systems in plants. J Exp Bot 53:855–864

    Article  CAS  Google Scholar 

  • Guo S, Brück H, Sattelmacher B (2002) Effects of supplied nitrogen form on growth and water uptake of French bean(Phaseolus vulgaris L.) plants. Plant Soil 239:267–275

    Article  CAS  Google Scholar 

  • Guo R, Shi L, Yang Y (2009) Germination, growth, osmotic adjustment and ionic balance of wheat in response to saline and alkaline stresses. Soil Sci Plant Nutr 55:667–679

    Article  CAS  Google Scholar 

  • Hodge A, Berta G, Doussan C, Merchan F, Crespi M (2009) Plant root growth, architecture and function. Plant Soil 321:153–187

    Article  CAS  Google Scholar 

  • Holyoak C, Stratford M, McMullin Z, Cole M, Crimmins K, Brown A, Coote P (1996) Activity of the plasma membrane H+-ATPase and optimal glycolytic flux are required for rapid adaptation and growth of Saccharomyces cerevisiae in the presence of the weak-acid preservative sorbic acid. Appl Environ Microbiol 62:3158–3164

    CAS  Google Scholar 

  • Klobus G, Buczek J (1995) The role of plasma membrane oxidoreductase activity in proton transport. J Plant Physiol 146:103–107

    Article  CAS  Google Scholar 

  • Larsson C, Widell S, Kjellbom P (1987) Preparation of high-purity plasma membranes. Methods Enzymol 148:558–568

    Article  CAS  Google Scholar 

  • Liang CJ, Wang W (2013) Antioxidant response of soybean seedlings to joint stress of lanthanum and acid rain. Environ Sci Pollut Res 20:8182–8191

    Article  CAS  Google Scholar 

  • Liang CJ, van Dijk JP, Scholtens IM, Staats M, Prins TW, Voorhuijzen MM, da Silva AM, Arisi ACM, den Dunnen JT, Kok EJ (2014) Detecting authorized and unauthorized genetically modified organisms containing vip3A by real-time PCR and next-generation sequencing. Anal Bioanal Chem 406:2603–2611

    Article  CAS  Google Scholar 

  • Liang CJ, Ge YQ, Su L, Bu JJ (2015) Response of plasma membrane H+-ATPase in rice (Oryza sativa) seedlings to simulated acid rain. Environ Sci Pollut Res 22:535–545

    Article  CAS  Google Scholar 

  • Ling DJ, Huang QC, Ouyang Y (2010) Impacts of simulated acid rain on soil enzyme activities in a latosol. Ecotox. Environ. Safe. 73:1914–1918

    Article  CAS  Google Scholar 

  • Liu H, Jiang Y, Luo Y, Jiang W (2006) A simple and rapid determination of ATP, ADP and AMP concentrations in pericarp tissue of litchi fruit by high performance liquid chromatography. Food Technol. Biotechnol. 44:531–534

    CAS  Google Scholar 

  • Menz FC, Seip HM (2004) Acid rain in Europe and the United States: an update. Environ Sci Policy 7:253–265

    Article  CAS  Google Scholar 

  • Miller AJ, Smith SJ (1996) Nitrate transport and compartmentation in cereal root cells. J Exp Bot 47:843–854

    Article  CAS  Google Scholar 

  • Miranda KM, Espey MG, Wink DA (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide-Biol. Chem. 5:62–71

    Article  CAS  Google Scholar 

  • Nicot N, Hausman JF, Hoffmann L, Evers D (2005) Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress.J. Exp. Bot. 56:2907–2914

    Article  CAS  Google Scholar 

  • Palmgren MG (2001) Plant plasma membrane H+-ATPases: powerhouses for nutrient uptake. Annu. Rev. Plant Physiol. Plant 52:817–845

    Article  CAS  Google Scholar 

  • Pereira SIA, Barbosa L, Castro PML (2015) Rhizobacteria isolated from a metal-polluted area enhance plant growth in zinc and cadmium-contaminated soil. Int J Environ Sci Technol 12(7):2127–2142

    Article  CAS  Google Scholar 

  • Ramos S, Schuldiner S, Kaback HR (1976) The electrochemical gradient of protons and its relationship to active transport in Escherichia coli membrane vesicles. Proc Natl Acad Sci 73:1892–1896

    Article  CAS  Google Scholar 

  • Reid R, Hayes J (2003) Mechanisms and control of nutrient uptake in plants. In: Jeon KW (ed) International review of cytology—a survey of cell biology. Elsevier Academic Press Inc, San Diego, pp 73–114

    Google Scholar 

  • Sanchez DG, Rios GFL, Garcia MAH (2010) Acid rain and forest ecosystems. Rev Chapingo Ser Cienc For Am 16:187–206

    Google Scholar 

  • Santi S, Locci G, Monte R, Pinton R, Varanini Z (2003) Induction of nitrate uptake in maize roots: expression of a putative high-affinity nitrate transporter and plasma membrane H+-ATPase isoforms. J Exp Bot 54:1851–1864

    Article  CAS  Google Scholar 

  • Scheiner D (1976) Determination of ammonia and Kjeldahl nitrogen by indophenol method. Water Res 10:31–36

    Article  CAS  Google Scholar 

  • Sperandio MVL, Santos LA, Bucher CA, Fernandes MS, de Souza SR (2011) Isoforms of plasma membrane H+-ATPase in rice root and shoot are differentially induced by starvation and resupply of NO3 or NH4 +. Plant Sci 180:251–258

    Article  CAS  Google Scholar 

  • Sun Z, Wang L, Zhou Q, Huang X (2013) Effects and mechanisms of the combined pollution of lanthanum and acid rain on the root phenotype of soybean seedlings. Chemosphere 93:344–352

    Article  CAS  Google Scholar 

  • Sun Z, Wang L, Wang Q, Zhou Q, Huang X (2014) Interactive effects of cadmium and acid rain on photosynthetic light reaction in soybean seedlings. Environ Toxicol Chem 33:2013–2019

    Article  CAS  Google Scholar 

  • Tarhanen S, Metsarinne S, Holopainen T, Oksanen J (1999) Membrane permeability response of lichen Bryoria fuscescens to wet deposited heavy metals and acid rain. Environ Pollut 104:121–129

    Article  CAS  Google Scholar 

  • Tischer A, Werisch M, Dobbelin F, Camenzind T, Rillig MC, Potthast K, Hamer U (2015) Above- and belowground linkages of a nitrogen and phosphorus co-limited tropical mountain pasture system-responses to nutrient enrichment. Plant Soil 391:333–352

    Article  CAS  Google Scholar 

  • Undem C, Rios EJ, Maylor J, Shimoda LA (2012) Endothelin-1 augments Na+/H+ exchange activity in murine pulmonary arterial smooth muscle cells via rho kinase. Plos One 7:e463032012

  • Vansuyt G, Souche G, Straczek A, Briat JF, Jaillard B (2003) Flux of protons released by wild type and ferritin over-expressor tobacco plants: effect of phosphorus and iron nutrition. Plant Physiol Biochem 41:27–33

    Article  CAS  Google Scholar 

  • Wakeel A, Hanstein S, Pitann B, Schubert S (2010) Hydrolytic and pumping activity of H+-ATPase from leaves of sugar beet (Betavulgaris L.) as affected by salt stress. J Plant Physiol 167:725–731

    Article  CAS  Google Scholar 

  • Wang Z, Li S (2003) Effects of N forms and rates on vegetable growth and nitrate accumulation. Pedosphere 13:309–316

  • Wen K, Liang C, Wang L, Hu G, Zhou Q (2011) Combined effects of lanthanumion and acid rain on growth, photosynthesis and chloroplast ultrastructure in soybean seedlings. Chemosphere 84:601–608

    Article  CAS  Google Scholar 

  • Yang NC, Ho WM, Chen YH, Hu ML (2002) A convenient one-step extraction of cellular ATP using boiling water for the luciferin-luciferase assay of ATP. Anal Biochem 306:323–327

    Article  CAS  Google Scholar 

  • Zeng H, Liu G, Kinoshita T, Zhang R, Zhu Y, Shen Q, Xu G (2012) Stimulation of phosphorus uptake by ammonium nutrition involves plasma membrane H+-ATPase in rice roots. Plant Soil 357:205–214

    Article  CAS  Google Scholar 

  • Zhang Y, Wu L, Wang X (1996) Effects of acid rain on leaf injury and physiological characteristics of crops. Agro-Environ Prot. 15:197–208

    Google Scholar 

  • Zhang JE, Yu J, Ouyang Y, Xu H (2014) Impact of simulated acid rain on trace metals and aluminum leaching in Latosol from Guangdong province. China. Soil. Sediment. Contam. 23:725–735

    Article  Google Scholar 

  • Zhu Y, Di T, Xu G, Chen X, Zeng H, Yan F, Shen Q (2009) Adaptation of plasma membrane H+-ATPase of rice roots to low pH as related to ammonium nutrition. Plant, Cell Environ 32:1428–1440

    Article  CAS  Google Scholar 

  • Zhu Y, Zeng H, Shen Q, Ishikawa T, Subbarao GV (2012) Interplay among NH4 + uptake, rhizosphere pH and plasma membrane H+-ATPase determine the release of BNIs in sorghum roots—possible mechanisms and underlying hypothesis. Plant Soil 358:125–135

    Article  Google Scholar 

Download references

Acknowledgments

The authors are grateful for the financial support from the Natural Science Foundation of Jiangsu Province (No.BK20161131) and the National Natural Science Foundation of China (31000245, 31370517).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chanjuan Liang.

Additional information

Editorial responsibility: M. Abbaspour

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 27 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, B., Bu, J. & Liang, C. Regulation of nitrogen and phosphorus absorption by plasma membrane H+-ATPase in rice roots under simulated acid rain. Int. J. Environ. Sci. Technol. 14, 101–112 (2017). https://doi.org/10.1007/s13762-016-1125-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13762-016-1125-x

Keywords

Navigation