Skip to main content
Log in

A pqr2 mutant encodes a defective polyamine transporter and is negatively affected by ABA for paraquat resistance in Arabidopsis thaliana

  • Regular Paper
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

Despite the paraquat-resistant mutants that have been reported in plants, this study identified a novel A. thaliana mutant (pqr2) from an XVE inducible activation library based on its resistance to 2 μM paraquat. The pqr2 mutant exhibited a termination mutation in the exon of AT1G31830/PAR1/PQR2, encoded a polyamine uptake transporter AtPUT2/PAR1/PQR2. The PQR2 mutation could largely reduce superoxide accumulation and cell death in the pqr2 plants under paraquat treatment. Moreover, compared with wild type, the pqr2 mutant exhibited much reduced tolerance to putrescine, a classic polyamine compound, which confirmed that PQR2 encoded a defective polyamine transporter. Notably, co-treated with ABA and paraquat, both pqr2 mutant and wild type exhibited a lethal phenotype from seed germination, but the wild type like pqr2 mutant, could remain paraquat-resistance while co-treated with high dosage of Na2WO4, an ABA synthesis inhibitor. Gene expression analysis suggested that ABA signaling should widely regulate paraquat-responsive genes distinctively in wild type and pqr2 mutant. Hence, this study has for the first time reported about ABA negative effect on paraquat-resistance in A. thaliana, providing insight into the ABA signaling involved in the oxidative stress responses induced by paraquat in plants.

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

Similar content being viewed by others

References

  • Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249

    Article  PubMed  Google Scholar 

  • Babbs CF, Pham JA, Coolbaugh RC (1989) Lethal hydroxyl radical production in paraquat-treated plants. Plant Physiol 90:1267–1270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benavides MP, Gallego SM, Comba ME, Tomaro ML (2000) Relationship between polyamines and paraquat toxicity in sunflower leaf discs. Plant Growth Regul 31:215–224

    Article  CAS  Google Scholar 

  • Benina M, Ribeiro DM, Gechev TS, Mueller-Roeber B, Schippers JHM (2014) A cell type-specific view on the translation of mRNAs from ROS-responsive genes upon paraquat treatment of Arabidopsis thaliana leaves. Plant Cell Environ 38:349–363

    Article  PubMed  Google Scholar 

  • Bors W, Langebartels C, Michel C, Sandermann H (1989) Polyamines as radical scavengers and protectants against ozone damage. Phytochemistry 28:1589–1595

    Article  CAS  Google Scholar 

  • Bus JS, Gibson JE (1984) Paraquat: model for oxidant-initiated toxicity. Environ Health Perspect 55:37–46

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen RQ, Sun SL, Wang C, Li YS, Liang Y, An FY, Li C, Dong HL, Yang XH, Zhang J, Zuo JR (2009) The Arabidopsis PARAQUAT RESISTANT2 gene encodes an S-nitrosoglutathione reductase that is a key regulator of cell death. Cell Res 19:1377–1387

    Article  CAS  PubMed  Google Scholar 

  • Childs AC, Mehta DJ, Gerner EW (2003) Polyamine-dependent gene expression. Cell Mol Life Sci 60:1394–1406

    Article  CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Das KC, Misra HP (2004) Hydroxyl radical scavenging and singlet oxygen quenching properties of polyamines. Mol Cell Biochem 262:127–133

    Article  CAS  PubMed  Google Scholar 

  • Davies KJ (1995) Oxidative stress: the paradox of aerobic life. Biochem Soc Symp 61:1–31

    Article  CAS  PubMed  Google Scholar 

  • Ding HD, Zhang XH, Xu SC, Sun LL, Jiang MY, Zhang AY, Jin YG (2009) Induction of protection against paraquat-induced oxidative damage by abscisic acid in maize leaves is mediated through mitogen-activated protein kinase. J Integr Plant Biol 51:961–972

    Article  CAS  PubMed  Google Scholar 

  • Dinis-Oliveira RJ, Duarte JA, Sánchez-Navarro A, Remião F, Bastos ML, Carvalho F (2008) Paraquat poisonings: mechanisms of lung toxicity, clinical features, and treatment. Crit Rev Toxicol 38:13–71

    Article  CAS  PubMed  Google Scholar 

  • DiTomaso JM, Hart JJ, Kochian LV (1993) Compartmentation analysis of paraquat fluxes in maize roots as a means of estimating the rate of vacuolar accumulation and translocation to shoots. Plant Physiol 102:467–472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drolet G, Dumbroff EB, Legge RL, Thompson JE (1986) Radical scavenging properties of polyamines. Phytochemistry 25:367–371

    Article  CAS  Google Scholar 

  • Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446

    Article  CAS  PubMed  Google Scholar 

  • Fujii T, Yokoyama E, Inoue K, Sakurai H (1990) The sites of electron donation of photosystem I to methyl viologen. Biochim Biophys Acta (BBA)–Bioener 1015:41–48

    Article  CAS  Google Scholar 

  • Fujita M, Shinozaki K (2014) Identification of polyamine transporters in plants: paraquat transport provides crucial clues. Plant Cell Physiol 55:855–861

    Article  CAS  PubMed  Google Scholar 

  • Fujita M, Fujita Y, Iuchi S, Yamada K, Kobayashi Y, Urano K, Kobayashi M, Yamaguchi-Shinozaki K, Shinozki K (2012) Natural variation in a polyamine transporter determines paraquat tolerance in Arabidopsis. Proc Natl Acad Sci USA 109:6343–6347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fukuda H (2000) Programmed cell death of tracheary elements as a paradigm in plants. Plant Mol Bio 44:245–253

    Article  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Polyamines and abiotic stress tolerance in plants. Plant Signal Behav 5:26–33

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guan L, Scandalios JG (1998) Two structurally similar maize cytosolic superoxide dismutase genes, Sod4 and Sod4A, respond differentially to abscisic acid and high osmoticum. Plant Physiol 117:217–224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guan LM, Zhao J, Scandalios JG (2000) Cis—elements and transfactors that regulate expression of themaize Catl antioxidant gene in response to ABA and osmotic stress: H202 is the likely intermediary signaling molecule for the response. Plant J 22:87–95

    Article  CAS  PubMed  Google Scholar 

  • Han HJ, Peng RH, Zhu B, Fu XY, Zhao W, Shi B, Yao QH (2014) Gene expression profiles of Arabidopsis under the stress of methyl viologen: a microarray analysis. Mol Biol Rep 41:7089–7102

    Article  CAS  PubMed  Google Scholar 

  • Hart JJ, Ditomaso JM, Linscott DL, Kochian LV (1992) Transport interactions between paraquat and polyamines in roots of intact maize seedlings. Plant Physiol 99:1400–1405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Igarashi K, Kashiwagi K (2010) Modulation of cellular function by polyamines. Int J Biochem Cell Biol 42:39–51

    Article  CAS  PubMed  Google Scholar 

  • Jena NR (2012) DNA damage by reactive species: mechanisms, mutation and repair. J Biosci 37:503–517

    Article  CAS  PubMed  Google Scholar 

  • Kaminaka H, Morita S, Tokumoto M, Masumura T, Tanaka K (1999) Differential gene expression of rice superoxide dismutase isoforms to oxidative and environmental stresses. Free Radic Res 31:219–225

    Article  Google Scholar 

  • Kubiś J (2008) Exogenous spermidine differentially alters activities of some scavenging system enzymes, H2O2 and superoxide radical levels in water-stressed cucumber leaves. J Plant Physiol 165:397–406

    Article  PubMed  Google Scholar 

  • Kumar D, Datta R, Hazra S, Sultana A, Mukhopadhyay R, Chattopadhyay S (2015) Transcriptomic profiling of Arabidopsis thaliana mutant pad2.1 in response to combined cold and osmotic stress. PLoS One 10:e0122690

    Article  PubMed  PubMed Central  Google Scholar 

  • Kurepa J, Smalle J, Montagu MV, Inzé D (1998) Polyamines and paraquat toxicity in Arabidopsis thaliana. Plant Cell Physiol 39:987–992

    Article  CAS  PubMed  Google Scholar 

  • Kwak JM (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623–2633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li CZ, Jiao J, Wang GX (2004) The important role of reactive oxygen species in the relationship between ethylene and polyamines in leaves of spring wheat seedlings under root osmotic stress. Plant Sci 166:303–315

    Article  CAS  Google Scholar 

  • Li JY, Mu JY, Bai JT, Fu FY, Zou TT, An FY, Zhang J, Jing HW, Wang Q, Li Z, Yang SH, Zuo JR (2013) Paraquat resistant 1, a golgi-localized putative transporter protein, is involved in intracellular transport of paraquat. Plant Physiol 162:470–483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marco F, Alcázar R, Tiburcio AF, Carrasco P (2011) Interactions between polyamines and abiotic stress pathway responses unraveled by transcriptome analysis of polyamine overproducers. OMICS 15:775–781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mittler R, Blumwald E (2015) The roles of ROS and ABA in systemic acquired acclimation. Plant C 27:64–70

    Article  CAS  Google Scholar 

  • Mulangi V, Chibucos MC, Phuntumart V, Morris PF (2012) Kinetic and phylogenetic analysis of plant polyamine uptake transporters. Planta 236:1261–1273

    Article  CAS  PubMed  Google Scholar 

  • Nayyar H, Chander S (2004) Protective effects of polyamines against oxidative stress induced by water and cold stress in chickpea. J Agron Crop Sci 190:355–365

    Article  CAS  Google Scholar 

  • Pottosin I, Velarde-Buendía AM, Bose J, Zepeda-Jazo I, Shabala S, Dobrovinskaya O (2014) Cross-talk between reactive oxygen species and polyamines in regulation of ion transport across the plasma membrane: implications for plant adaptive responses. J Exp Bot 65:1271–1283

    Article  CAS  PubMed  Google Scholar 

  • Seiler N, Raul F (2005) Polyamines and apoptosis. J Cell Mol Med 9:623–642

    Article  CAS  PubMed  Google Scholar 

  • Shi LH, Bielawski J, Mu JY, Dong HL, Teng C, Zhang J, Yang XH, Tomishige N, Hanada K, Hannun YA, Zuo JR (2007) Involvement of sphingoid bases in mediating reactive oxygen intermediate production and programmed cell death in Arabidopsis. Cell Res 17:1030–1040

    Article  CAS  PubMed  Google Scholar 

  • Sies H (1997) Oxidative stress: oxidants and antioxidants. Exp Physiol 82:291–295

    Article  CAS  PubMed  Google Scholar 

  • Soar CJ, Preston C, Karotam J, Powles SB (2004) Polyamines can inhibit paraquat toxicity and translocation in the broadleaf weed Arctotheca calendula. Pestic Biochem Physiol 80:94–105

    Article  CAS  Google Scholar 

  • Stadtman E (1992) Protein oxidation and aging. Science 257:1220–1224

    Article  CAS  PubMed  Google Scholar 

  • Szigeti Z (2005) Mechanism of paraquat resistance—from the antioxidant enzymes to the transporters. Acta Biologica Szegediensis 49:177–179

    Google Scholar 

  • Tang W, Newton RJ (2005) Polyamines reduce salt-induced oxidative damage by increasing the activities of antioxidant enzymes and decreasing lipid peroxidation in Virginia pine. Plant Growth Regul 46:31–43

    Article  CAS  Google Scholar 

  • Tanou G, Ziogas V, Belghazi M, Christou A, Filippou P, Job D, Fotopoulos V, Molassiotis A (2014) Polyamines reprogram oxidative and nitrosative status and the proteome of citrus plants exposed to salinity stress. Plant Cell Environ 37:864–885

    Article  CAS  PubMed  Google Scholar 

  • Tiburcio AF, Altabella T, Bitrián M, Alcázar R (2014) The roles of polyamines during the lifespan of plants from development to stress. Planta 240:1–18

    Article  CAS  PubMed  Google Scholar 

  • Tsuji K, Hosokawa M, Morita S, Miura R, Tominaga T (2013) Resistance to paraquat in Mazus pumilus. Weed Res 53:176–182

    Article  CAS  Google Scholar 

  • Valko M, Leibfritz D, Moncol J, Cronin MTD, Mazur M, Telser J (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39:44–84

    Article  CAS  PubMed  Google Scholar 

  • Xi J, Xu P, Xiang CB (2012) Loss of AtPDR11, a plasma membrane-localized ABC transporter, confers paraquat tolerance in Arabidopsis thaliana. Plant J 69:782–791

    Article  CAS  PubMed  Google Scholar 

  • Ye B, Muller HH, Zhang J, Gressel J (1997) Constitutively elevated levels of putrescine and putrescine-generating enzymes correlated with oxidant stress resistance in Conyza bonariensis and wheat. Plant Physiol 115:1443–1451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou J, Li X, Xia XJ, Zhou YH, Shi K, Chen Z, Yu JQ (2014) H2O2 mediates the crosstalk of brassinosteroid and abscisic acid in tomato responses to heat and oxidative stresses. J Exp Bot 65:4371–4383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu D, Scandalios JG (1994) Differential accumulation of manganese-superoxide dismutase transcripts in maize in response to abscisic acid and high osmoticum. Plant Physiol 106:173–178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zuo JR, Niu QW, Chua NH (2000) An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J 24:265–273

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the 111 Project (B08032), and the Fundamental Research Funds for the Central Universities (2013QC042). We thank the Institute of Genetics and Developmental Biology, Chinese Academy of Sciences for kindly providing the XVE inducible activation lines.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shengqiu Feng.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dong, S., Hu, H., Wang, Y. et al. A pqr2 mutant encodes a defective polyamine transporter and is negatively affected by ABA for paraquat resistance in Arabidopsis thaliana . J Plant Res 129, 899–907 (2016). https://doi.org/10.1007/s10265-016-0819-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-016-0819-y

Keywords

Navigation