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Improved drought tolerance by early IAA- and ABA-dependent H2O2 accumulation induced by α-naphthaleneacetic acid in soybean plants

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Abstract

α-Naphthaleneacetic acid (NAA), a synthetic auxin, improves plant stress tolerance. A hydroponic experiment was carried out to investigate how NAA pretreatment could improve drought resistance in soybean seedlings. NAA pretreatment triggered an early increase in hydrogen peroxide (H2O2), indole-3-acetic acid (IAA) and abscisic acid (ABA), a late elevation of net photosynthetic rate (Pn), a late decrease in malondialdehyde (MDA) and electrolyte leakage and a rise in antioxidant enzyme activities during both early and late phases, under drought stress. However, the application of the ABA biosynthesis inhibitor tungstate and the IAA biosynthesis inhibitors l-Amino-oxyphenylpropionic acid and aminoethoxyvinylglycine resulted in an early decrease in H2O2 and an early and late decline in the activities of antioxidant enzymes in NAA-pretreated stressed plants. Moreover, the inhibitors also induced an increase in H2O2, MDA and electrolyte leakage and decrease in Pn in the late phase in stressed leaves pretreated with NAA. Similarly, the application of the NADPH oxidase inhibitor diphenyleneiodonium and H2O2 scavenger dimethylthiourea arrested the early accumulation of H2O2, but not of IAA and ABA in stressed plants pretreated with NAA, and blocked the early and late rise in antioxidant enzyme activities, the late increase in Pn and the late decrease in H2O2, MDA and electrolyte leakage induced by NAA in drought-stressed plants. Our data suggest that NAA application triggers early IAA- and ABA-dependent H2O2 accumulation, which, in turn, results in an enhancement of antioxidant capacity and drought stress tolerance in soybean seedlings.

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Abbreviations

AOPP:

l-Amino-oxyphenylpropionic acid

APX:

Ascorbate peroxidase

AVG:

Aminoethoxyvinylglycine

CAT:

Catalase

DMTU:

Dimethylthiourea

DPI:

Diphenyleneiodoniumchloride

GR:

Glutathione reductase

H2O2 :

Hydrogen peroxide

IAA:

Indole-3-acetic acid

MDA:

Malondialdehyde

NAA:

α-Naphthaleneacetic acid

NOX:

NADPH oxidase

O2 − :

Superoxide anion radical

Pn:

Net photosynthetic rate

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

References

  • Arshad M, Naazar A, Ghafoor A (2006) Character correlation and path coefficient in soybean Glycine max (L) Merrill. Pak J Bot 38:121–130

    Google Scholar 

  • Barakat N, Laudadio V, Cazzato E, Tufarelli V (2013) Antioxidant potential and oxidative stress markers in wheat (Triticum aestivum) treated with phytohormones under salt-stress condition. Int J Agric Biol 15:843–849

    CAS  Google Scholar 

  • Battal P, Erez ME, Turker M, Berber I (2008) Molecular and physiological changes in maize (Zea mays) induced by exogenous NAA, ABA and MeJA during cold stress. Ann Bot Fenn 45:173–185. doi:10.5735/085.045.0302

    Article  Google Scholar 

  • Böhmer M, Schroeder JI (2011) Quantitative transcriptomic analysis of abscisic acid-induced and reactive oxygen species-dependent expression changes and proteomic profiling in Arabidopsis suspension cells. Plant J 67:105–118. doi:10.1111/j.1365-313X.2011.04579.x

    Article  CAS  PubMed  PubMed Central  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. doi:10.1016/0003-2697(76)90527-3

    Article  CAS  PubMed  Google Scholar 

  • de Carvalho MHC (2008) Drought stress and reactive oxygen species: production, scavenging and signaling. Plant Signal Behav 3:156–165. doi:10.4161/psb.3.3.5536

    Article  Google Scholar 

  • Eccher G, Botton A, Dimauro M, Boschetti A, Ruperti B, Ramina A (2013) Early induction of apple fruitlet abscission is characterized by an increase of both isoprene emission and abscisic acid content. Plant Physiol 161:1952–1969. doi:10.1104/pp.112.208470

    Article  CAS  Google Scholar 

  • Fini A, Guidi L, Ferrini F, Brunetti C, Ferdinandoa MD, Biricoltia S, Pollastria S, Calamaia L, Tattini M (2012) Drought stress has contrasting effects on antioxidant enzymes activity and phenylpropanoid biosynthesis in Fraxinus ornus leaves: an excess light stress affair? J Plant Physiol 169:929–939. doi:10.1016/j.jplph.2012.02.014

    Article  CAS  PubMed  Google Scholar 

  • Gallagher SR, Leonard RT (1982) Effect of vanadate, molybdate, and azide on membrane-associated ATPase and soluble phosphatase activities of corn roots. Plant Physiol 70:1335–1340. doi:10.1104/pp.70.5.1335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gechev TS, Breusegem FV, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. Bio Essays 28:1091–1101. doi:10.1002/bies.20493

    CAS  Google Scholar 

  • Hsu YT, Kao CH (2007) Heat shock-mediated H2O2 accumulation and protection against Cd toxicity in rice seedlings. Plant Soil 300:137–147. doi:10.1007/s11104-007-9396-0

    Article  CAS  Google Scholar 

  • Janda T, Szalai G, Tari I, Páldi E (1999) Hydroponic treatment with salicylic acid decreases the effects of chilling injury in maize (Zea mays L.) plants. Planta 208:175–180. doi:10.1007/s004250050547

    Article  CAS  Google Scholar 

  • Jiang M, Zhang J (2002) Involvement of plasma-membrane NADPH oxidase in abscisic acid- and water stress-induced antioxidant defense in leaves of maize seedlings. Planta 215:1022–1030. doi:10.1007/s00425-002-0829-y

    Article  CAS  PubMed  Google Scholar 

  • Jiang M, Zhang J (2003) Cross-talk between calcium and reactive oxygen species originated from NADPH oxidase in abscisic acid-induced antioxidant defence in leaves of maize seedling. Plant Cell Environ 26:929–939. doi:10.1046/j.1365-3040.2003.01025.x

    Article  CAS  PubMed  Google Scholar 

  • Jiang M, Zhang J (2004) Abscisic acid and antioxidant defense in plant cells. Acta Bot Sin 46:1–9

    CAS  Google Scholar 

  • Jiang H, Xing X, Zhou Q, Jiang H (2015) Effects of exogenous α-naphthaleneacetic acid on the antioxidation system in soybean leaves subjected to long-term drought stress during flowering. Chin J Appl Ecol 26:1718–1726

    CAS  Google Scholar 

  • Jubany-Marí T, Munné-Bosch S, López-Carbonell M, Alegre L (2009) Hydrogen peroxide is involved in the acclimation of the Mediterranean shrub, Cistus albidus L., to summer drought. J Exp Bot 60:107–120. doi:10.1093/jxb/ern274

    Article  CAS  PubMed  Google Scholar 

  • Kang G, Wang C, Sun G, Wang Z (2003) Salicylic acid changes activities of H2O2-metabolizing enzymes and increases the chilling tolerance of banana seedlings. Environ Exp Bot 50:9–15. doi:10.1016/S0098-8472(02)00109-0

    Article  CAS  Google Scholar 

  • Karataş İ, Öztürk L, Erşahin Y, Okatan Y (2010) Effects of auxin on photosynthetic pigments and some enzyme activities during dark-induced senescence of Tropaeolum leaves. Pak J Bot 42:1881–1888

    Google Scholar 

  • Leonard RT, Hansen D, Hodges TK (1973) Membrane-bound adenosine triphosphatase activities of oat roots. Plant Physiol 51:749–754. doi:10.1104/pp.51.4.749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li W, Qian C, Mo Y, Hu Y, Xie J (2013) Tolerance of banana for fusarium wilt is associated with early H2O2 accumulation in the roots. Afr J Biotechnol 10:11378–11387. doi:10.5897/AJB11.994

    Google Scholar 

  • Liu Z, Guo Y, Bai J (2010) Exogenous hydrogen peroxide changes antioxidant enzyme activity and protects ultrastructure in leaves of two cucumber ecotypes under osmotic stress. J Plant Growth Regul 29:171–183. doi:10.1007/s00344-009-9121-8

    Article  CAS  Google Scholar 

  • Lopez-Carbonell M, Alegre L, van Onckelen H (1994) Effects of water stress on cellular ultrastructure and on concentrations of endogenous abscisic acid and indole-3-acetic acid in Fatsia japonica leaves. Plant Growth Regul 14:29–35. doi:10.1007/BF00024138

    Article  CAS  Google Scholar 

  • Najeeb U, Atwell BJ, Bange MP, Tan DKY (2015) Aminoethoxyvinylglycine (AVG) ameliorates waterlogging-induced damage in cotton by inhibiting ethylene synthesis and sustaining photosynthetic capacity. Plant Growth Regul 76:83–98. doi:10.1007/s10725-015-0037-y

    Article  CAS  Google Scholar 

  • Piotrowska-Niczyporuk A, Bajguz A (2014) The effect of natural and synthetic auxins on the growth, metabolite content and antioxidant response of green alga Chlorella vulgaris (Trebouxiophyceae). Plant Growth Regul 73:57–66. doi:10.1007/s10725-013-9867-7

    Article  CAS  Google Scholar 

  • Polidoros A, Scandalios J (1999) Role of hydrogen peroxide and different classes of antioxidants in the regulation of catalase and glutathione-S-transferase gene expression in maize (Zea mays L.). Physiol Plant 106:112–120. doi:10.1034/j.1399-3054.1999.106116.x

    Article  CAS  Google Scholar 

  • Rasmusson AG, Møller IM (1990) NADP-utilizing enzymes in the matrix of plant mitochondria. Plant Physiol 94:1012–1018. doi:10.1104/pp.94.3.1012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruan Z (2014) Effects of NAA on physiological indexes of Caryota obtusa seedlings under variable temperature stress. Acta Agric Zhejiangensis 26:609–614

    Google Scholar 

  • Sagi M, Fluhr R (2001) Superoxide production by plant homologues of the gp91phox NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol 126:1281–1290. doi:10.1104/pp.126.3.1281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shirasu K, Nakajima H, Rajasekhar VK, Dixon RA, Lamb C (1997) Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell 9:261–270. doi:10.1105/tpc.9.2.261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soeno K, Goda H, Ishii T, Ogura T, Tachikawa T, Sasaki E, Yoshida S, Fujioka S, Asami T, Shimada Y (2010) Auxin biosynthesis inhibitors, identified by a genomics-based approach, provide insights into auxin biosynthesis. Plant Cell Physiol 51:524–536. doi:10.1093/pcp/pcq032

    Article  CAS  PubMed  Google Scholar 

  • Tan W, Liu J, Dai T, Jing Q, Cao W, Jiang D (2008) Alterations in photosynthesis and antioxidant enzyme activity in winter wheat subjected to post-anthesis water-logging. Photosynthetica 46:21–27. doi:10.1007/s11099-008-0005-0

    Article  CAS  Google Scholar 

  • Tian X, He M, Wang Z, Zhang J, Song Y, He Z, Dong Y (2015) Application of nitric oxide and calcium nitrate enhances tolerance of wheat seedlings to salt stress. Plant Growth Regul 77:343–356. doi:10.1007/s10725-015-0069-3

    Article  CAS  Google Scholar 

  • Tyburski J, Dunajska K, Mazurek P, Piotrowska B, Tretyn A (2009) Exogenous auxin regulates H2O2 metabolism in roots of tomato (Lycopersicon esculentum Mill.) seedlings affecting the expression and activity of Cu Zn-superoxide dismutase, catalase, and peroxidase. Acta Physiol Plant 31:249–260. doi:10.1007/s11738-008-0225-8

    Article  CAS  Google Scholar 

  • van Breusegem F, Vranová E, Dat JF, Inzé D (2001) The role of active oxygen species in plant signal transduction. Plant Sci 161:405–414. doi:10.1016/S0168-9452(01)00452-6

    Article  Google Scholar 

  • Vanacker H, Carver TLW, Foyer CH (2000) Early H2O2 accumulation in mesophyll cells leads to induction of glutathione during the hyper-sensitive response in the barley-powdery mildew interaction. Plant Physiol 123:1289–1300. doi:10.1104/pp.123.4.1289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verslues PE, Ober ES, Sharp RE (1998) Root growth and oxygen relations at low water potentials. Impact of oxygen availability in polyethylene glycol solutions. Plant Physiol 116:1403–1412. doi:10.1104/pp.116.4.1403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang S, Sui X, Hu L, Sun J, Wei Y, Zhang Z (2010) Effects of exogenous abscisic acid pre-treatment of cucumber (Cucumis sativus) seedson seedling growth and water-stress tolerance. N Z J Crop Hortic 38:7–18. doi:10.1080/01140671003619274

    Article  CAS  Google Scholar 

  • Wang S, Liang D, Li C, Hao Y, Ma F, Shu H (2012) Influence of drought stress on the cellular ultrastructure and antioxidant system in leaves of drought-tolerant and drought-sensitive apple rootstocks. Plant Physiol Biochem 51:81–89. doi:10.1016/j.plaphy.2011.10.014

    Article  CAS  PubMed  Google Scholar 

  • Weiler EW, Jordan PS, Conrad W (1981) Levels of indole-3-acetic acid in intact and decapitated coleoptiles as determined by a specific and highly sensitive solid-phase enzyme immunoassay. Planta 153:561–571. doi:10.1007/BF00385542

    Article  CAS  PubMed  Google Scholar 

  • Wu Z, Zhang C, Yan J, Yue Q, Ge Y (2015) Effects of sulfur supply and hydrogen peroxide pretreatment on the responses by rice under cadmium stress. Plant Growth Regul 77:299–306. doi:10.1007/s10725-015-0064-8

    Article  CAS  Google Scholar 

  • Xiong J, Fu G, Yang Y, Zhu C, Tao L (2012) Tungstate: is it really a specific nitrate reductase inhibitor in plant nitric oxide research? J Exp Bot 63:33–41. doi:10.1093/jxb/err268

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Zhang J, Wang Z, Zhu Q, Wang W (2001) Hormonal changes in the grains of rice subjected to water stress during grain filling. Plant Physiol 127:315–323. doi:10.1104/pp.127.1.315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Zhang L, Dong F, Gao J, Galbraith DW, Song C (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 126:1438–1448. doi:10.1104/pp.126.4.1438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang M, Duan L, Tian X, He Z, Li J, Wang B, Li Z (2007) Uniconazole-induced tolerance of soybean to water deficit stress in relation to changes in photosynthesis, hormones and antioxidant system. J Plant Physiol 164:709–717. doi:10.1016/j.jplph.2006.04.008

    Article  CAS  PubMed  Google Scholar 

  • Zhao L, Zhang F, Guo J, Yang Y, Li B, Zhang L (2004) Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiol 134:849–857. doi:10.1104/pp.103.030023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This study was funded by a program supported by the National Eleventh-Five Year Key Project of Scientific and Technical Supporting Programs of China (2009BADA8B02) and Fundamental Research Funds for the Central Universities (KYZ201202-3).

Author contributions

X Xing and S Wang conceived and coordinated the study. X Xing, Q Zhou and H Xing participated in the design of the study. X Xing and HQ Jiang conducted the majority of the experiments. X Xing, HD Jiang, and Q Zhou drafted the manuscript. All authors have read and approved the final manuscript.

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Authors and Affiliations

  1. College of Agronomy, Nanjing Agricultural University, Nanjing, 210095, Jiangsu, People’s Republic of China

    Xinghua Xing, Hongqiang Jiang, Qin Zhou, Han Xing, Haidong Jiang & Shaohua Wang

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  1. Xinghua Xing
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  2. Hongqiang Jiang
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  3. Qin Zhou
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  4. Han Xing
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  5. Haidong Jiang
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  6. Shaohua Wang
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Correspondence to Haidong Jiang or Shaohua Wang.

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Xing, X., Jiang, H., Zhou, Q. et al. Improved drought tolerance by early IAA- and ABA-dependent H2O2 accumulation induced by α-naphthaleneacetic acid in soybean plants. Plant Growth Regul 80, 303–314 (2016). https://doi.org/10.1007/s10725-016-0167-x

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