Skip to main content
SpringerLink
Log in

Effect of exogenous abscisic acid on morphology, growth and nutrient uptake of rice (Oryza sativa) roots under simulated acid rain stress

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Application of proper ABA can improve acid tolerance of rice roots by balancing endogenous hormones and promoting nutrient uptake.

Abstract

Abscisic acid (ABA) has an important signaling role in enhancing plant tolerance to environmental stress. To alleviate the inhibition on plant growth and productivity caused by acid rain, it is crucial to clarify the regulating mechanism of ABA on adaptation of plants to acid rain. Here, we studied the effects of exogenously applied ABA on nutrients uptake of rice roots under simulated acid rain (SAR) stress from physiological, biochemical and molecular aspects. Compared to the single SAR treatment (pH 4.5 or 3.5), exogenous 10 μM ABA alleviated the SAR-induced inhibition of root growth by balancing endogenous hormones (abscisic acid, indole-3-acetic acid, gibberellic acid and zeatin), promoting nutrient uptake (nitrate, P, K and Mg) in rice roots, and increasing the activity of the plasma membrane H+-ATPase by up-regulating expression levels of genes (OSA2, OSA4, OSA9 and OSA10). However, exogenous 100 μM ABA exacerbated the SAR-caused inhibition of root growth by disrupting the balance of endogenous hormones, and inhibiting nutrient uptake (nitrate, P, K, Ca and Mg) through decreasing the activity of the plasma membrane H+-ATPase. These results indicate that proper concentration of exogenous ABA could enhance tolerance of rice roots to SAR stress by promoting nutrients uptake and balancing endogenous hormones.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

GA:

Gibberellic acid

IAA:

Indole-3-acetic acid

SAR:

Simulated acid rain

ZT:

Zeatin

References

  • Abbasi T, Poornima P, Kannadasan T, Abbasi SA (2013) Acid rain: past, present, and future. Int J Environ Eng 5(3):229–272

    Article  Google Scholar 

  • Achuo EA, Prinsen E, Hofte M (2006) Influence of drought, salt stress and abscisic acid on the resistance of tomato to Botrytis cinerea and Oidium neolycopersici. Plant Pathol 55(2):178–186

    Article  CAS  Google Scholar 

  • Alvarez-Pizarro JC, Gomes-Filho E, Prisco JT, Grossi-De-Sá MF, de Oliveira-Neto OB (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(14):1617–1626

    Article  CAS  Google Scholar 

  • Arango M, Gevaudant F, Oufattole M, Boutry M (2003) The plasma membrane proton pump ATPase: the significance of gene subfamilies. Planta 216(3):355–365

    CAS  PubMed  Google Scholar 

  • Bo KL, Hong SH, Dong SL (2000) Chemical composition of precipitation and wet deposition of major ions on the Korean peninsula. Atmos Environ 34(4):563–575

    Article  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, Kronzucker HJ (2002) NH4 + toxicity in higher plants: a critical review. J Plant Physiol 159(6):567–584

    Article  CAS  Google Scholar 

  • Busov VB, Brunner AM, Strauss SH (2008) Genes for control of plant stature and form. New Phytol 177(3):589–607

    Article  CAS  Google Scholar 

  • Cheng Z, Jin R, Cao M, Liu X, Chan Z (2016) Exogenous application of ABA mimic 1 (AM1) improves cold stress tolerance in bermudagrass (Cynodon dactylon). Plant Cell Tiss Org 125(2):231–240

    Article  CAS  Google Scholar 

  • Coskun D, Britto DT, Li M, Becker A, Kronzucker HJ (2013) Rapid ammonia gas transport accounts for futile transmembrane cycling under NH3/NH4 + toxicity in plant roots. Plant Physiol 163(4):1859–1867

    Article  CAS  Google Scholar 

  • Ericsson T (1995) Growth and shoot: root ratio of seedlings in relation to nutrient availability. Plant Soil 168–169(1):205–214

    Article  Google Scholar 

  • Fageria NK, Moreira A (2011) The role of mineral nutrition on root growth of crop plants. Adv Agronomy 110:251–331

    Article  CAS  Google Scholar 

  • Forino LMC, Castiglione MR, Bartoli G, Balestri M, Andreucci A, Tagliasacchi AM (2012) Arsenic-induced morphogenic response in roots of arsenic hyperaccumulator fern Pteris vittata. J Hazard Mater 235:271–278

    Article  Google Scholar 

  • Fu J, Wu Y, Miao Y, Xu Y, Zhao E, Wang J, Sun H, Liu Q, Xue Y, Xu Y, Hu T (2017) Improved cold tolerance in Elymus nutans by exogenous application of melatonin may involve ABA-dependent and ABA-independent pathways. Sci Rep 7:39865. https://doi.org/10.1038/srep39865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gomez-Cadenas A, Verhey SD, Holappa LD, Shen QX, Ho THD, Walker-Simmons MK (1999) An abscisic acid-induced protein kinase, PKABA1, mediates abscisic acid-suppressed gene expression in barley aleurone layers. Proc Natl Acad Sci USA 96(4):1767–1772

    Article  CAS  Google Scholar 

  • Gong H, Chen K, Chen G, Zhu X, Wang S, Zhang C (2003) Effects of gradual drought on the fatty acid composition of polar lipids, H+-ATPase AND 5’-AMPase activities in the plasma membranes of two spring wheat leaves. Acta Phytoecol Sinica 27(4):459–465

    CAS  Google Scholar 

  • Guajardo E, Correa JA, Contreras-Porcia L (2016) Role of abscisic acid (ABA) in activating antioxidant tolerance responses to desiccation stress in intertidal seaweed species. Planta 243(3):767–781

    Article  CAS  Google Scholar 

  • Hermans C, Vuylsteke M, Coppens F, Craciun A, Inze D, Verbruggen N (2010) Early transcriptomic changes induced by magnesium deficiency in Arabidopsis thaliana reveal the alteration of circadian clock gene expression in roots and the triggering of abscisic acid-responsive genes. New Phytol 187(1):119–131

    Article  CAS  Google Scholar 

  • Hou S, Zhu J, Ding M, Lv G (2008) Simultaneous determination of gibberellic acid, indole-3-acetic acid and abscisic acid in wheat extracts by solid-phase extraction and liquid chromatography-electrospray tandem mass spectrometry. Talanta 76(4):798–802

    Article  CAS  Google Scholar 

  • Imada S, Yamanaka N, Tamai S (2010) Contribution of root growth responses to leaf traits and relative growth rate of Populus alba under different water-table conditions. Trees-Struct Funct 24(6):1163–1172

    Article  Google Scholar 

  • Imran MA, Hussain S, Hussain M, Ch MN, Meo AA (2014) Effect of simulated acid rain (SAR) on some morphochemical aspects of mash (Vigna mungo l.). Pak J Bot 46(1):245–250

  • Janicka-Russak M, Klobus G (2007) Modification of plasma membrane and vacuolar H+-ATPases in response to NaCl and ABA. J Plant Physiol 164(3):295–302

    Article  CAS  Google Scholar 

  • Janicka-Russak M, Kabala K, Wdowikowska A, Klobus G (2013) Modification of plasma membrane proton pumps in cucumber roots as an adaptation mechanism to salt stress. J Plant Physiol 170(10):915–922

    Article  CAS  Google Scholar 

  • Jansen MA, Re VDN, Tan MY, Prinsen E, Lagrimini LM, Thorneley RN (2001) Phenol-oxidizing peroxidases contribute to the protection of plants from ultraviolet radiation stress. Plant Physiol 126(3):1012–1023

    Article  CAS  Google Scholar 

  • Ju S, Yin N, Wang L, Zhang C, Wang Y (2017) Effects of silicon on Oryza sativa L. seedling roots under simulated acid rain stress. PLoS One 12(3):e0173378. https://doi.org/10.1371/journal.pone.0173378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ke L, Wong TWY, Wong AHY, Wong YS, Tam NFY (2003) Negative effects of humic acid addition on phytoremediation of pyrene-contaminated sediments by mangrove seedlings. Chemosphere 52(9):1581–1591

    Article  CAS  Google Scholar 

  • Khoshgoftarmanesh AH, Schulin R, Chaney RL, Daneshbakhsh B, Afyuni M (2010) Micronutrient-efficient genotypes for crop yield and nutritional quality in sustainable agriculture. A review. Agron Sustain Dev 30(1):83–107

    Article  CAS  Google Scholar 

  • Klobus G, Buczek J (1995) The role of plasma-membrane oxidoreductase activity in proton transport. J Plant Physiol 146(1–2):103–107

    Article  CAS  Google Scholar 

  • Koricheva J, Roy S, Vranjic JA, Haukioja E, Hughes PR, Hanninen O (1997) Antioxidant responses to simulated acid rain and heavy metal deposition in birch seedlings. Environ Pollut 95(2):249–258

    Article  CAS  Google Scholar 

  • Kumaravelu G, Ramanujam MP (1998) Effect of simulated acid rain on nodulation and nitrogen metabolism in Vigna radiata cultivars. Biol Plant 41(3):445–450

    Article  CAS  Google Scholar 

  • Li C, Junttila O, Heino P, Palva ET (2003) Different responses of northern and southern ecotypes of Betula pendula to exogenous ABA application. Tree Physiol 23(7):481–487

    Article  CAS  Google Scholar 

  • Liang C, Ge Y, Su L, Bu J (2015) Response of plasma membrane H+-ATPase in rice (Oryza sativa) seedlings to simulated acid rain. Environ Sci Pollut R 22(1):535–545

    Article  CAS  Google Scholar 

  • Likens GE, Driscoll CT, Buso DC (1996) Long-term effects of acid rain: response and recovery of a forest ecosystem. Science 272(5259):244–246

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25(4):402–408

    Article  CAS  Google Scholar 

  • López MA, Bannenberg G, Castresana C (2008) Controlling hormone signaling is a plant and pathogen challenge for growth and survival. Curr Opin Plant Biol 11(4):420–427

    Article  Google Scholar 

  • Luo L, Xu F, Weng H, Hong S, Duan L, Li Z (2011) Inducing effects and its biological mechanisms of ABA on the chilling resistance of sweet pepper seedlings. Acta Bot Boreali-Occident Sin 31(1):94–100

    CAS  Google Scholar 

  • Maathuis FJM, Salt DE, Williams L (2009) Physiological functions of mineral macronutrients. Curr Opin Plant Biol 12(3):250–258

    Article  CAS  Google Scholar 

  • Machado J, Azevedo J, Freitas M, Pinto E, Almeida A, Vasconcelos V, Campos A (2017) Analysis of the use of microcystin-contaminated water in the growth and nutritional quality of the root-vegetable, Daucus carota. Environ Sci Pollut R 24(1):752–764

    Article  CAS  Google Scholar 

  • Marcinska I, Czyczylo-Mysza I, Skrzypek E, Grzesiak MT, Janowiak F, Filek M, Dziurka M, Dziurka K, Waligorski P, Juzon K, Cyganek K, Grzesiak S (2013) Alleviation of osmotic stress effects by exogenous application of salicylic or abscisic acid on wheat seedlings. Int J Mol Sci 14(7):13171–13193

    Article  Google Scholar 

  • Matilla AJ, Carrillo-Barral N, del Carmen Rodriguez-Gacio M (2015) An update on the role of NCED and CYP707A ABA metabolism genes in seed dormancy induction and the response to after-ripening and nitrate. J Plant Growth Regul 34(2):274–293

    Article  CAS  Google Scholar 

  • Michelet B, Boutry M (1995) The plasma-membrane H+-ATPase (a highly regulated enzyme with multiple physiological functions). Plant Physiol 108(1):1–6

    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 Ch 5(1):62–71

    Article  CAS  Google Scholar 

  • Mohan M, Kumar S (1998) Review of acid rain potential in India: future threats and remedial measures. Curr Sci India 75(6):579–593

    CAS  Google Scholar 

  • Oh E, Yamaguchi S, Hu J, Yusuke J, Jung B, Paik I, Lee H, Sun T, Kamiya Y, Choi G (2007) PIL5, a phytochrome-interacting bHLH protein, regulates gibberellin responsiveness by binding directly to the GAI and RGA promoters in Arabidopsis seeds. Plant Cell 19(4):1192–1208

    Article  CAS  Google Scholar 

  • Oufattole M, Arango M, Boutry M (2000) Identification and expression of three new Nicotiana plumbaginifolia genes which encode isoforms of a plasma-membrane H+-ATPase, and one of which is induced by mechanical stress. Planta 210(5):715–722

    Article  CAS  Google Scholar 

  • Palma F, Lopez-Gomez M, Tejera NA, Lluch C (2014) Involvement of abscisic acid in the response of Medicago sativa plants in symbiosis with Sinorhizobium meliloti to salinity. Plant Sci 223:16–24

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ramlall C, Varghese B, Ramdhani S, Pammenter NW, Bhatt A, Berjak P, Sershen (2015) Effects of simulated acid rain on germination, seedling growth and oxidative metabolism of recalcitrant-seeded Trichilia dregeana grown in its natural seed bank. Physiol Plant 153(1):149–160

    Article  CAS  Google Scholar 

  • Reis S, Grennfelt P, Klimont Z, Amann M, ApSimon H, Hettelingh JP, Holland M, LeGall AC, Maas R, Posch M, Spranger T, Sutton MA, Williams M (2012) From acid rain to climate change. Science 338(6111):1153–1154

    Article  CAS  Google Scholar 

  • Ruiz-Lozano JM, Del MAM, Bárzana G, Vernieri P, Aroca R (2009) Exogenous ABA accentuates the differences in root hydraulic properties between mycorrhizal and non mycorrhizal maize plants through regulation of PIP aquaporins. Plant Mol Biol 70(5):565–579

    Article  CAS  Google Scholar 

  • Russell RS (1979) Plant root systems: their function and interaction with the soil. Field Crop Res 2(4):177–179

    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(389):1851–1864

    Article  CAS  Google Scholar 

  • Scheiner D (1976) Determination of ammonia and Kjeldahl nitrogen by indophenol method. Water Res 10(1):31–36

    Article  CAS  Google Scholar 

  • Sedmak JJ, Grossberg SE (1977) A rapid, sensitive, and versatile assay for protein using Coomassie brilliant blue G250. Anal Biochem 79(1–2):544–552

    Article  CAS  Google Scholar 

  • Seo M, Hanada A, Kuwahara A, Endo A, Okamoto M, Yamauchi Y, North H, Marion-Poll A, Sun T, Koshiba T, Kamiya Y, Yamaguchi S, Nambara E (2006) Regulation of hormone metabolism in Arabidopsis seeds: phytochrome regulation of abscisic acid metabolism and abscisic acid regulation of gibberellin metabolism. Plant J 48(3):354–366

    Article  CAS  Google Scholar 

  • Shen H, Chen J, Wang Z, Yang C, Sasaki T, Yamamoto Y, Matsumoto H, Yan X (2006) Root plasma membrane H+-ATPase is involved in the adaptation of soybean to phosphorus starvation. J Exp Bot 57(6):1353–1362

    Article  CAS  Google Scholar 

  • Sripinyowanich S, Klomsakul P, Boonburapong B, Bangyeekhun T, Asami T, Gu H, Buaboocha T, Chadchawan S (2013) Exogenous ABA induces salt tolerance in indica rice (Oryza sativa L.): the role of OsP5CS1 and OsP5CR gene expression during salt stress. Environ Exp Bot 86(2):94–105

    Article  CAS  Google Scholar 

  • Sumner JB (1944) A method for the colorimetric determination of phosphorus. Science 100(2601):413–414

    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 (Beta vulgaris L.) as affected by salt stress. J Plant Physiol 167(9):725–731

    Article  CAS  Google Scholar 

  • Walch-Liu P, Neumann G, Bangerth F, Engels C (2000) Rapid effects of nitrogen form on leaf morphogenesis in tobacco. J Exp Bot 51(343):227–237

    Article  CAS  Google Scholar 

  • Wang T, Zhang X, Li C (2007) Growth, abscisic acid content, and carbon isotope composition in wheat cultivars grown under different soil moisture. Biol Plant 51(1):181–184

    Article  CAS  Google Scholar 

  • Wang Y, Ma F, Li M, Liang D, Zou J (2011) Physiological responses of kiwifruit plants to exogenous ABA under drought conditions. Plant Growth Regul 64(1):63–74

    Article  CAS  Google Scholar 

  • Wei L, Lv B, Wang M, Ma H, Yang H, Liu X, Jiang C, Liang Z (2015) Priming effect of abscisic acid on alkaline stress tolerance in rice (Oryza sativa L.) seedlings. Plant Physiol Bioch 90:50–57

    Article  CAS  Google Scholar 

  • Wen K, Liang C, Wang L, Hu G, Zhou Q (2011) Combined effects of lanthanum ion and acid rain on growth, photosynthesis and chloroplast ultrastructure in soybean seedlings. Chemosphere 84(5):601–608

    Article  CAS  Google Scholar 

  • Wu X, Liang C (2017) Enhancing tolerance of rice (Oryza sativa) to simulated acid rain by exogenous abscisic acid. Environ Sci Pollut R 24(5):4860–4870

    Article  CAS  Google Scholar 

  • Yan A, Chen Z (2017) The pivotal role of abscisic acid signaling during transition from seed maturation to germination. Plant Cell Rep 36(5):689–703

    Article  CAS  Google Scholar 

  • Zentella R, Zhang ZL, Park M, Thomas SG, Endo A, Murase K, Fleet CM, Jikumaru Y, Nambara E, Kamiya Y, Sun T-P (2007) Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19(10):3037–3057

    Article  CAS  Google Scholar 

  • Zhang B, Bu J, Liang C (2016) Root morphology and growth regulated by mineral nutrient absorption in rice roots exposed to simulated acid rain. Water Air Soil Poll. https://doi.org/10.1007/s11270-016-3151-1

  • Zhang B, Bu J, Liang C (2017a) Regulation of nitrogen and phosphorus absorption by plasma membrane H+-ATPase in rice roots under simulated acid rain. Int J Environ Sci Te 14(1):101–112

    Article  CAS  Google Scholar 

  • Zhang Y, Li Q, Zhang F, Xie G (2017b) Estimates of economic loss of materials caused by acid deposition in China. Sustainability 9(4):488. https://doi.org/10.3390/su9040488

    Article  CAS  Google Scholar 

  • Zhao M, Han Y, Feng Y, Li F, Wang W (2012) Expansins are involved in cell growth mediated by abscisic acid and indole-3-acetic acid under drought stress in wheat. Plant Cell Rep 31(4):671–685

    Article  CAS  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(10):1428–1440

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful for the financial support from the Natural Science Foundation of Jiangsu Province (No. BK20161131), the National Natural Science Foundation of China (31000245, 31370517) and Postgraduate Research and Practice Innovation Program of Jiangsu Province (KYCX17_1485).

Author information

Authors and Affiliations

  1. State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, 214122, China

    Hongyue Liu & Chanjuan Liang

  2. Jiangsu Key Laboratory of Anaerobic Biotechnology, School of Environmental and Civil Engineering, Jiangnan University, Wuxi, 214122, China

    Hongyue Liu, Xiaoqian Ren, Jiuzheng Zhu, Xi Wu & Chanjuan Liang

  3. Jiangsu Cooperative Innovation Center of Technology and Material of Water Treatment, Jiangnan University, Wuxi, 214122, China

    Chanjuan Liang

Authors
  1. Hongyue Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaoqian Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jiuzheng Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xi Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chanjuan Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chanjuan Liang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interests.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 17 kb)

Supplementary material 2 (TIFF 537 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, H., Ren, X., Zhu, J. et al. Effect of exogenous abscisic acid on morphology, growth and nutrient uptake of rice (Oryza sativa) roots under simulated acid rain stress. Planta 248, 647–659 (2018). https://doi.org/10.1007/s00425-018-2922-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-018-2922-x

Keywords

Search

Navigation