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Overexpression of a peroxidase gene (AtPrx64) of Arabidopsis thaliana in tobacco improves plant’s tolerance to aluminum stress

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AtPrx64 is one of the peroxidases gene up-regulated in Al stress and has some functions in the formation of plant second cell wall. Its overexpression may improve plant tolerance to Al by some ways. Studies on its function under Al stress may help us to understand the mechanism of plant tolerance to Al stress.

Abstract

In Arabidopsis thaliana, the expressions of some genes (AtPrxs) encoding class III plant peroxidases have been found to be either up-regulated or down-regulated under aluminum (Al) stress. Among 73 genes that encode AtPrxs in Arabidopsis, AtPrx64 is always up-regulated by Al stress, suggesting this gene plays protective roles in response to such stress. In this study, transgenic tobacco plants were generated to examine the effects of overexpressing of AtPrx64 gene on the tolerance to Al stress. The results showed that overexpression of AtPrx64 gene increased the root growth and reduced the accumulation of Al and ROS in the roots. Compared with wild type controls, transgenic tobaccos had much less soluble proteins and malondialdehyde in roots and much more root citrate exudation. The activity of plasma membrane (PM) H+-ATPase, the phosphorylation of PM H+-ATPase and its interaction with 14-3-3 proteins increased in transgenic tobaccos; moreover, the content of lignin in root tips also increased. Taken together, these results showed that overexpression of AtPrx64 gene might enhance the tolerance of tobacco to Al stress.

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References

  • Arenhart RA, Schunemann M, Neto LB, Margis R, Wang ZY, Margis-Pinheiro M (2016) Rice ASR1 and ASR5 are complementary transcription factors regulating aluminium responsive genes. Plant Cell Environ 39:645–651

    Article  CAS  PubMed  Google Scholar 

  • Bayer EM, Bottrill AR, Walshaw J, Vigouroux M, Naldrett MJ, Thomas CL, Maule AJ (2006) Arabidopsis cell wall proteome defined using multidimensional protein identification technology. Proteomics 6:301–311

    Article  CAS  PubMed  Google Scholar 

  • Bennet RJ, Breen CM (1991) The aluminum signal: new dimensions to mechanisms of aluminum tolerance. Plant Soil 45:703–716

    Google Scholar 

  • Bindschedler LV, Dewdney J, Blee KA, Stone JM, Asai T, Plotnikov J, Denoux C, Hayes T, Gerrish C, Davies DR, Ausubel FM, Bolwell GP (2006) Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance. Plant J 47:851–863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonawitz ND, Im Kim J, Tobimatsu Y, Ciesielski PN, Anderson NA, Ximenes E, Maeda J, Ralph J, Donohoe BS, Ladisch M, Chapple C (2014) Disruption of mediator rescues the stunted growth of a lignin-deficient Arabidopsis mutant. Nature 509:376–380

    Article  CAS  PubMed  Google Scholar 

  • Camoni L, Visconti S, Marra M, Aducci P (2001) Adenosine 5′-monophosphate inhibits the association of 14-3-3 proteins with the plant plasma membrane H+-ATPase. J Biol Chem 276:31709–31712

    Article  CAS  PubMed  Google Scholar 

  • Chance B, Maehly AC (1955) Assay of catalase and peroxidase. Method Enzymol 59:764–775

    Article  Google Scholar 

  • Chandran D, Sharopova N, VandenBosch KA, Garvin DF, Samac DA (2008) Physiological and molecular characterization of aluminum resistance in Medicago truncatula. BMC Plant Biol 8:89

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen Q, Zhang XD, Wang SS, Wang QF, Wang GQ, Nian HJ, Li KZ, Yu YX, Chen LM (2011) Transcriptional and physiological changes of alfalfa in response to aluminium stress. J Agric Sci 149:737–751

    Article  CAS  Google Scholar 

  • Chen Q, Wu KH, Zhang YN, Phan XH, Li KZ, Yu YX, Chen LM (2012) Physiological and molecular responses of broad bean (Vicia faba L.) to aluminum stress. Acta Physiol Plant 34:2251–2263

    Article  CAS  Google Scholar 

  • Chen Q, Wu KH, Wang P, Yi J, Li KZ, Yu YX, Chen LM (2013) Overexpression of MsALMT1, from the aluminum-sensitive Medicago sativa, enhances malate exudation and aluminum resistance in tobacco. Plant Mol Biol Rep 31(3):769–774

    Article  Google Scholar 

  • Cosio C, Dunand C (2009) Specific functions of individual class III peroxidase genes. J Exp Bot 60:391–408

    Article  CAS  PubMed  Google Scholar 

  • Darko E, Ambrus H, Stefanovits-Banyai E, Fodor J, Bakos F, Barnaba B (2004) Aluminium toxicity, Al tolerance and oxidative stress in an Al-sensitive wheat genotype and in Al-tolerant lines developed by in vitro microspore selection. Plant Sci 166:583–591

    Article  CAS  Google Scholar 

  • Delhaize E, Ryan PR (1995) Aluminum toxicity and tolerance in plants. Plant Physiol 107:315–321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delhaize E, Hebb DM, Ryan PR (2001) Expression of a Pseudomonas aeruginosa citrate synthase gene in tobacco is not associated with either enhanced citrate accumulation or efflux. Plant Physiol 125:2059–2067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duroux L, Welinder KG (2003) The peroxidase gene family in plants: a phylogenetic overview. J Mol Evol 57:397–407

    Article  CAS  PubMed  Google Scholar 

  • Ezaki B, Gardner RC, Ezaki Y, Matsumoto H (2000) Expression of aluminum-induced genes in transgenic arabidopsis plants can ameliorate aluminum stress and/or oxidative stress. Plant Physiol 122:657–665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ezaki B, Katsuhara M, Kawamura M, Matsumoto H (2001) Different mechanisms of four aluminum (Al)-resistant transgenes for Al toxicity in arabidopsis. Plant  Physiol 127(3):918–927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gay CA, Gebicki JM (2003) Measurement of protein and lipid hydroperoxides in biological systems by the ferric-xylenol orange method. Anal Biochem 315:29–35

    Article  CAS  PubMed  Google Scholar 

  • Guo CL, Chen Q, Zhao XL, Chen XQ, Zhao Y, Wang L, Li KZ, Yu XY, Chen LM (2013) Al-enhanced expression and interaction of 14-3-3 protein and plasma membrane H+-ATPase is related to Al-induced citrate secretion in an Al-resistant black soybean. Plant Mol Biol Rep 31:1012–1024

    Article  CAS  Google Scholar 

  • Hiraga S, Sasaki K, Ito H, Ohashi Y, Matsui H (2001) A large family of clase III plant peroxidases. Plant cell Physiol 42:462–468

    Article  CAS  PubMed  Google Scholar 

  • Horsch RB, Rogers SG, Fraley RT (1985) Transgenic plants. Cold Spring Harbor Symp Quant Biol 50:433–437

    Article  CAS  PubMed  Google Scholar 

  • Hu Y, Wang NS, Hu XJ, Lin XY, Feng Y, Jin CW (2013) Nitrate nutrition enhances nickel accumulation and toxicity in Arabidopsis plants. Plant Soil 371:105–115

    Article  CAS  Google Scholar 

  • Huang CF, Yamaji N, Mitani N, Yano M, Nagamura Y, Ma JF (2009) A bacterial-type ABC transporter is involved in aluminum tolerance in rice. Plant Cell 21:655–667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Janicka-Russak M, Kabala K (2012) Abscisic acid and hydrogen peroxide induce modification of plasma membrane H+-ATPase from Cucumis sativus L. roots under heat shock. J Plant Physiol 169:1607–1614

    Article  CAS  PubMed  Google Scholar 

  • Kerkeb L, Venema K, Donaire JP, Rodriguez-Rosales MP (2002) Enhanced H+/ATP coupling ratio of H+-ATPase and increased 14-3-3 protein content in plasma membrane of tomato cells upon osmotic shock. Physiol Plant 116:37–41

    Article  PubMed  Google Scholar 

  • Kim YS, Park W, Nian H, Sasaki T, Ezaki B, Jang YS, Chung GC, Bae HJ, Ahn SJ (2010a) Aluminum tolerance associated with enhancement of plasma membrane H+-ATPase in the root apex of soybean. Soil Sci Plant Nutr 56:140–149

    Article  CAS  Google Scholar 

  • Kim MJ, Ciani S, Schachtman DP (2010b) A peroxidase contributes to ROS production during Arabidopsis root response to potassium deficiency. Mol Plant 3:420–427

    Article  CAS  PubMed  Google Scholar 

  • Kinraide TB (1990) Assessing the rhizotoxicity of the aluminate ion, Al(OH)4–. Plant Physiol 93:1620–1625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kochian LV, Hoekenga OA, Pineros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Biol 55:459–493

    Article  CAS  PubMed  Google Scholar 

  • Kopittke PM, Moore KL, Lombi E, Gianoncelli A, Ferguson BJ, Blamey FP, Menzies NW, Nicholson TM, McKenna BA, Wang P, Gresshoff PM, Kourousias G, Webb RI, Green K, Tollenaere A (2015) Identification of the primary lesion of toxic aluminum in plant roots. Plant Physiol 167(4):1402–1411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koua D, Cerutti L, Falquet L, Sigrist CJ, Theiler G, Hulo N, Dunand C (2009) PeroxiBase: a database with new tools for peroxidase family classification. Nucleic Acids Res 37:D261–D266

    Article  CAS  PubMed  Google Scholar 

  • Kumari M, Taylor GJ, Deyholos MK (2008) Transcriptomic responses to aluminum stress in roots of Arabidopsis thaliana. Mol Genet Genom 279:339–357

    Article  CAS  Google Scholar 

  • Lee Y, Rubio MC, Alassimone J, Geldner N (2013) A mechanism for localized lignin deposition in the endodermis. Cell 153:402–412

    Article  CAS  PubMed  Google Scholar 

  • Llorente F, Lopez-Cobollo RM, Catala R, Martinez-Zapater JM, Salinas J (2002) A novel cold-inducible gene from Arabidopsis, RCI3, encodes a peroxidase that constitutes a component for stress tolerance. Plant J 32:13–24

    Article  CAS  PubMed  Google Scholar 

  • Ma JF (2000) Role of organic acids in detoxification of aluminum in higher plants. Plant Cell Physiol 41:383–390

    Article  CAS  PubMed  Google Scholar 

  • Ma JF, Furukawa J (2003) Recent progress in the research of external Al detoxification in higher plants: a minireview. J Inorg Biochem 97:46–51

    Article  CAS  PubMed  Google Scholar 

  • Ma JF, Taketa S, Yang ZM (2000) Aluminum tolerance genes on the short arm of chromosome 3R are linked to organic acid release in triticale. Plant Physiol 122:687–694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278

    Article  CAS  PubMed  Google Scholar 

  • Maron LG, Guimaraes CT, Kirst M, Albert PS, Birchler JA, Bradbury PJ, Buckler ES, Coluccio AE, Danilova TV, Kudrna D, Magalhaes JV, Pineros MA, Schatz MC, Wing RA, Kochian LV (2013) Aluminum tolerance in maize is associated with higher MATE1 gene copy number. Proc Natl Acad Sci USA 110:5241–5246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsumoto H (2000) Cell biology of aluminum toxicity and tolerance in higher plants. Int Rev Cytol 200:1–46

    Article  CAS  PubMed  Google Scholar 

  • McKenna BA, Wehr JB, Mikkelsen D, Blamey FP, Menzies NW (2016) Aluminium effects on mechanical properties of cell wall analogues. Physiol Plant 158:382–388

    Article  CAS  PubMed  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Ohno T, Koyama H, Hara T (2003) Characterization of citrate transport through the plasma membrane in a carrot mutant cell line with enhanced citrate excretion. Plant Cell Physiol 44:156–162

    Article  CAS  PubMed  Google Scholar 

  • Passardi F, Longet D, Penel C, Dunand C (2004a) The class III peroxidase multigenic family in rice and its evolution in land plants. Phytochemistry 65:1879–1893

    Article  CAS  PubMed  Google Scholar 

  • Passardi F, Penel C, Dunand C (2004b) Performing the paradoxical: how plant peroxidases modify the cell wall. Trends Plant Sci 9:534–540

    Article  CAS  PubMed  Google Scholar 

  • Richards KD, Schott EJ, Sharma YK, Davis KR, Gardner RC (1998) Aluminum induces oxidative stress genes in Arabidopsis thaliana. Plant Physiol 116:409–418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roppolo D, De Rybel B, Tendon VD, Pfister A, Alassimone J, Vermeer JE, Yamazaki M, Stierhof YD, Beeckman T, Geldner N (2011) A novel protein family mediates Casparian strip formation in the endodermis. Nature 473:380–383

    Article  CAS  PubMed  Google Scholar 

  • Ryan PR, Tyerman SD, Sasaki T, Furuichi T, Yamamoto Y, Zhang WH, Delhaize E (2011) The identification of aluminium-resistance genes provides opportunities for enhancing crop production on acid soils. J Exp Bot 62:9–20

    Article  CAS  PubMed  Google Scholar 

  • Sasaki K, Hiraga S, Ito H, Seo S, Matsui H, Ohashi Y (2002) A wound-inducible tobacco peroxidase gene expresses preferentially in the vascular system. Plant Cell Physiol 43:108–117

    Article  CAS  PubMed  Google Scholar 

  • Shen R, Ma JF, Kyo M, Iwashita T (2002) Compartmentation of aluminium in leaves of an Al-accumulator, Fagopyrum esculentum Moench. Planta 215:394–398

    Article  CAS  PubMed  Google Scholar 

  • Shen H, He LF, Sasaki T, Yamamoto Y, Zheng SJ, Ligaba A, Yan XL, Ahn SJ, Yamaguchi M, Hideo S, Matsumoto H (2005) Citrate secretion coupled with the modulation of soybean root tip under aluminum stress. Up-regulation of transcription, translation, and threonine-oriented phosphorylation of plasma membrane H+-ATPase. Plant Physiol 138:287–296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shigeto J, Nagano M, Fujita K, Tsutsumi Y (2014) Catalytic profile of Arabidopsis peroxidases, AtPrx-2, 25 and 71, contributing to stem lignification. PLoS ONE 9:e105332

    Article  PubMed  PubMed Central  Google Scholar 

  • Snowden KC, Gardner RC (1993) Five genes induced by aluminum in wheat (Triticum aestivum L.) roots. Plant Physiol 103:855–861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Snowden KC, Richards KD, Gardner RC (1995) Aluminum-induced genes (induction by toxic metals, low calcium, and wounding and pattern of expression in root tips). Plant Physiol 107:341–348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor GJ, McDonald-Stephens JL, Hunter DB, Bertsch PM, Elmore D, Rengel Z, Reid RJ (2000) Direct measurement of aluminum uptake and distribution in single cells of Chara corallina. Plant Physiol 123:987–996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tognolli M, Penel C, Greppin H, Simon P (2002) Analysis and expression of the class III peroxidase large gene family in Arabidopsis thaliana. Gene 288:129–138

    Article  CAS  PubMed  Google Scholar 

  • Tokunaga N, Kaneta T, Sato S, Sato Y (2009) Analysis of expression profiles of three peroxidase genes associated with lignification in Arabidopsis thaliana. Physiol Plant 136:237–249

    Article  CAS  PubMed  Google Scholar 

  • Warinowski T, Koutaniemi S, Karkonen A, Sundberg I, Toikka M, Simola LK, Kilpelainen I, Teeri TH (2016) Peroxidases bound to the growing lignin polymer produce natural like extracellular lignin in a cell culture of Norway spruce. Front Plant Sci 7:1523

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang QF, Yi Q, Hu QQ, Zhao Y, Nian HJ, Li KZ, Yu YX, Izui K, Chen LM (2012) Simultaneous overexpression of citrate synthase and phosphoenolpyruvate carboxylase in leaves augments citrate exclusion and Al resistance in transgenic tobacco. Plant Mol Biol Rep 30:992–1005

    Article  CAS  Google Scholar 

  • Welinder KG, Justesen AF, Kjaersgard IV, Jensen RB, Rasmussen SK, Jespersen HM, Duroux L (2002) Structural diversity and transcription of class III peroxidases from Arabidopsis thaliana. Eur J Biochem 269:6063–6081

    Article  CAS  PubMed  Google Scholar 

  • Wu KH, Xiao SQ, Chen Q, Wang QF, Zhang YN, Li KZ, Yu YX, Chen LM (2013) Changes in the activity and transcription of antioxidant enzymes in response to Al stress in black soybeans. Plant Mol Biol Rep 31:141–150

    Article  CAS  Google Scholar 

  • Yokoyama R, Nishitani K (2006) Identification and characterization of Arabidopsis thaliana genes involved in xylem secondary cell walls. J Plant Res 119:189–194

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Wang H, Takemiya A, Song CP, Kinoshita T, Shimazaki K (2004) Inhibition of blue light-dependent H+ pumping by abscisic acid through hydrogen peroxide-induced dephosphorylation of the plasma membrane H+-ATPase in guard cell protoplasts. Plant Physiol 136:4150–4158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou G, Pereira JF, Delhaize E, Zhou M, Magalhaes JV, Ryan PR (2014) Enhancing the aluminium tolerance of barley by expressing the citrate transporter genes SbMATE and FRD3. J Exp Bot 65:2381–2390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported in part by the National Natural Science Foundation of China (No. 31260297, 31560351), the analysis and testing foundation of Kunming University of Science and Technology (20150736).

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KL and LC designed the research, YW and ZY performed most of the research, JH and HX performed part of the preparations of plant material, ZY and YW analyzed the data, YW and KL contributed to the discussion and wrote the article.

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Correspondence to Kunzhi Li.

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Yuanshuang Wu and Zhili Yang have contributed equally to this work.

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Wu, Y., Yang, Z., How, J. et al. Overexpression of a peroxidase gene (AtPrx64) of Arabidopsis thaliana in tobacco improves plant’s tolerance to aluminum stress. Plant Mol Biol 95, 157–168 (2017). https://doi.org/10.1007/s11103-017-0644-2

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