SpringerLink
Log in

The accumulation of endogenous proline induces changes in gene expression of several antioxidant enzymes in leaves of transgenic Swingle citrumelo

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Plant exposure to abiotic stresses leads to an accumulation of reactive oxygen species with the concomitant increase in antioxidant defense mechanisms. Previous studies showed that exogenous application of proline mitigate the deleterious effects caused by oxidative stress due to its ability to increase the activity of antioxidant enzymes. However, there are no reports of the effects of high endogenous accumulation of proline in the transcriptional pattern of antioxidant enzymes genes under normal conditions of water supply or in response to water deficit. Here, we show that isoforms of four antioxidant enzymes genes (Ascorbate peroxidase—APX, Catalase—CAT, Superoxide dismutase—SOD and Glutathione reductase—GR) were differentially regulated in leaves of Swingle citrumelo transgenic plants with high endogenous proline accumulation submitted to water deficits and also under normal water supply condition. Proline per se caused a two-fold change in the transcription activity of APX1, APXcl, CAT2 and Cu/ZnSOD2, while during water deficit proline influenced mRNAs levels in APXs and Cu/ZnSODs isoforms, MnSODmit and GRcl. This study adds new information on the role of proline during drought conditions and, more important, without the potential confounding effects imposed by water deficiency. We showed that, in addition to its known effects on diverse plant physiological and biochemical processes, high endogenous proline can also acts as a regulatory/signalling molecule capable of altering the transcript levels of stress-related genes.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417

    Article  PubMed  CAS  Google Scholar 

  2. Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58

    Article  CAS  Google Scholar 

  3. **ong L, Lee H, Ishitani M, Zhu JK (2002) Regulation of osmotic stress-responsive gene expression by the LOS6/ABA1 locus in Arabidopsis. J Biol Chem 277:8588–8596

    Article  PubMed  CAS  Google Scholar 

  4. Ober ES et al (2005) Evaluation of physiological treats as indirect selection criteria for drought tolerance in sugar beet. Field Crop Res 91:231–249

    Article  Google Scholar 

  5. Mahajan S, Tujeta N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158

    Article  PubMed  CAS  Google Scholar 

  6. Kishor PBK, Sangam S, Amrutha RN, Sri Laxmi P, Naidu KR, Rao KRSS, Rao S, Reddy KJ, Theriappan P, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr Sci 88:424–438

    CAS  Google Scholar 

  7. Kiyosue T, Yoshiba Y, Yamaguchi-Shinozaki K, Shinozaki K (1996) A nuclear encoding mitochondrial proline dehydrogenase: an enzyme involved in proline metabolism, is upregulated by proline but down regulated by dehydration in Arabidopsis. Plant Cell 8:1323–1335

    PubMed  CAS  Google Scholar 

  8. Lehmann S, Funck D, Szabados L (2010) Proline metabolism and transport in plant development. Amino Acids 39(4):949–962

    Article  PubMed  CAS  Google Scholar 

  9. Maggio A, Miyazaki S, Veronese P, Fujita T, Ibeas JI, Damsz B, Narasimhan ML, Hasegawa PM, Joly RJ, Bressan RA (2002) Does proline accumulation play an active role in stress-induced growth reduction? Plant J 31:699–712

    Article  PubMed  CAS  Google Scholar 

  10. Alia JM, Mohanty P, Matysik J (2001) Effect of proline on the production of singlet oxygen. Amino Acids 21:195–200

    Article  PubMed  CAS  Google Scholar 

  11. Khedr AHA, Abbas MA, Wahid AAA, Quick WP, Abogadallah GM (2003) Proline induces the expression of salt stress responsive proteins and may improve the adaptation of Pancratium maritimum L. to salt stress. J Exp Bot 54:2553–2562

    Article  PubMed  CAS  Google Scholar 

  12. Ozden M, Demirel U, Kahraman A (2009) Effects of proline on antioxidant system in leaves of grapevine (Vitis vinifera L.) exposed to oxidative stress by H2O2. Scientia Hortic 119:163–168

    Article  CAS  Google Scholar 

  13. De Campos MKF, Carvalho K, Souza FS, Marur CJ, Pereira LFP, Bespalhok Filho JC, Vieira LGE (2011) Drought tolerance and antioxidant enzymatic activity in transgenic Swingle citrumelo plants over-accumulating proline. Environ Exp Bot 72:242–250

    Article  Google Scholar 

  14. Melchiorre M, Robert G, Trippi V, Racca R, Lascano HR (2009) Superoxide dismutase and glutathione reductase overexpression in wheat protoplast: photooxidative stress tolerance and changes in cellular redox state. Plant Growth Regul 57:57–68

    Article  CAS  Google Scholar 

  15. Lu Z, Liu D (2007) Two Rice cytosolic ascorbate peroxidase differentially improve salt tolerance in transgenic Arabidopsis. Plant Cell Rep 26:1909–1917

    Article  PubMed  CAS  Google Scholar 

  16. Teixeira FK, Menezes-Benavente L, Galvão VC, Margis R, Margis-Pinheiro R (2006) Rice ascorbate peroxidase gene family encodes functionally diverse isoforms localized in different subcellular compartments. Planta 224:300–314

    Article  PubMed  CAS  Google Scholar 

  17. Meneguzzo S, Sgherri CLM, Navarizzo F, Izzo R (1998) Stromal and thylakoid-bound ascorbate peroxidases in NaCl-treated leaves. Physiol Plantarum 104:735–740

    Article  CAS  Google Scholar 

  18. Ogawa K, Kanematsu S, Asada K (1997) Generation of superoxide anion and localization of CuZn-superoxide dismutase in the vascular tissue of spinach hypocotyls: their association with lignifications. Plant Cell Physiol 38:1118–1126

    Article  PubMed  CAS  Google Scholar 

  19. Sandalio LM, Palma JM, Del Rio LA (1987) Localization of manganese superoxide dismutase in peroxissomes isolated from Pisum sativum L. Plant Sci 51:1–8

    Article  CAS  Google Scholar 

  20. Mhamdi A, Queval G, Chaouch S, Vanderauwera S, Van Breusegem F, Noctor G (2010) Catalase function in plants: a focus on Arabidopsis mutants as stress-mimic models. J Exp Bot 61(1):4197–4220

    Article  PubMed  CAS  Google Scholar 

  21. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Phys 50:601–639

    Article  CAS  Google Scholar 

  22. Creissen G, Reynolds H, Xue YB, Mullineaux P (1995) Simultaneous targeting of pea glutathione reductase and of a bacterial fusion protein to chloroplasts and mitochondria. Plant J 8:167–175

    Article  PubMed  CAS  Google Scholar 

  23. Chew O, Whelan J, Millar AH (2003) Molecular definition of the ascorbate glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J Biol Chem 278:46869–46877

    Article  PubMed  CAS  Google Scholar 

  24. Kocsy G, Laurie R, Szalai G, Szilagyi V, Simon-Sarkadi L, Galiba G, De Ronde JA (2005) Genetic manipulation of proline levels affects antioxidants in soybean subjected to simultaneous drought and heat stress. Physiol Plantarum 124:227–235

    Article  CAS  Google Scholar 

  25. Molinari HBC, Marur CJ, Daros E, Campos MKF, Carvalho JFPR, Bespalhok Filho JC, Pereira LFP, Vieira LGE (2007) Evaluation of the stress-inducible production of proline in transgenic sugarcane (Saccharum spp.): osmotic adjustment, chlorophyll fluorescence and oxidative stress. Physiol Plantarum 130:218–229

    Article  CAS  Google Scholar 

  26. Popisilova J, Haisel D, Vankova R (2011) Responses of transgenic tobacco plants with increased proline content to drought and/or heat stress. Am J Plant Sci 2:318–324

    Article  Google Scholar 

  27. Nolte KD, Hanson AD (1997) Proline accumulation and methylation to proline betaine in citrus: implications for genetic engineering of stress resistance. J Am Soc Hortic Sci 22(1):8–13

    Google Scholar 

  28. Molinari HBC (2003) Transformação genética de porta-enxertos para Citrus spp. visando obter maior tolerância ao estresse hídrico. Dissertation, State University of Londrina

  29. Molinari HBC, Marur CJ, Bespalhok Filho JC, Kobayashi AK, Pileggi M, Leite Júnior RP, Pereira LFP, Vieira LGE (2004) Osmotic adjustment in transgenic citrus rootstock Carrizo citrange (Citrus sinensis Obs. × Poncirus trifoliata L. Raf.) overproducing proline. Plant Sci 167:1375–1381

    Article  CAS  Google Scholar 

  30. Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:585–587

    Article  Google Scholar 

  31. Emanuelsson O, Brunak S, Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP, and related tools. Nat Protoc 2:953–971

    Article  PubMed  CAS  Google Scholar 

  32. Carvalho K, de Campos MKF, Pereira LFP, Vieira LGE (2010) Reference gene selection for real-time quantitative polymerase chain reaction normalization in Swingle citrumelo under drought stress. Anal Biochem 402:197–199

    Article  PubMed  CAS  Google Scholar 

  33. Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolation RNA for pine trees. Plant Mol Biol 11:113–116

    Article  CAS  Google Scholar 

  34. Livak JK, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  35. Sečenji M, Hideg E, Bebes A, Györgyey J (2010) Transcriptional differences in gene families of the ascorbate–glutathione cycle in wheat during mild water deficit. Plant Cell Rep 29:37–50

    Article  PubMed  Google Scholar 

  36. Lu Y-Y, Deng X-P, Kwak S-S (2010) Over expression of CuZn superoxide dismutase (CuZn SOD) and ascorbate peroxidase (APX) in transgenic sweet potato enhances tolerance and recovery from drought stress. Afr J Biotech 9(49):8378–8391

    CAS  Google Scholar 

  37. Faize M, Burgos L, Faize L, Piqueras A, Nicolas E, Barba-Espin G, Clemente-Moreno MJ, Alcobendas R, Artlip T, Hernandez JA (2011) Involvement of cytosolic ascorbate peroxidase and Cu/Zn-superoxide dismutase for improved tolerance against drought stress. J Exp Bot 62(8):2599–2613

    Article  PubMed  CAS  Google Scholar 

  38. Ashraf M (2009) Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnol Adv 27:84–93

    Article  PubMed  CAS  Google Scholar 

  39. Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:861–905

    Article  PubMed  CAS  Google Scholar 

  40. Pompelli MF, Martins SCV, Antunes WC, Chaves ARM, DaMatta FM (2010) Photosynthesis and photo protection in coffee leaves is affected by nitrogen and light availabilities in winter conditions. J Plant Physiol 167:1052–1060

    Article  PubMed  CAS  Google Scholar 

  41. Hong Z, Lakkineni K, Zhang Z, Verma DPS (2000) Removal of feedback inhibition of 1-pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress. Plant Physiol 122:1129–1136

    Article  PubMed  CAS  Google Scholar 

  42. Okuma E, Soeda K, Tada M, Murata Y (2000) Exogenous proline mitigates the inhibition of growth of Nicotiana tabacum cultured cells under saline conditions. Soil Sci Plant Nutr 46:257–263

    Article  CAS  Google Scholar 

  43. Hoque MA, Okuma E, Banu MNA, Nakamura K, Shimoishi Y, Murata Y (2007) Exogenous proline mitigates the detrimental effects of salt stress more than exogenous betaine by increasing antioxidant enzyme activities. J Plant Physiol 164:553–561

    Article  PubMed  CAS  Google Scholar 

  44. Bhatnagar-Mathur P, Devi MJ, Vadez V, Sharma KK (2009) Differential antioxidative responses in transgenic peanut bear no relationship to their superior transpiration efficiency under drought stress. J Plant Physiol 166:1207–1217

    Article  PubMed  CAS  Google Scholar 

  45. Zhang CS, Lu Q, Verma DPS (1995) Removal of feedback inhibition of delta-1- pyrroline-5-carboxylate synthetase, a bifunctional enzyme catalyzing the first 2 steps of proline biosynthesis in plants. J Biol Chem 270:20491–20496

    Article  PubMed  CAS  Google Scholar 

  46. Nakashima K, Yamaguchi-Shinozaki K (2010) Promoters and transcription factors in abiotic stress-responsive gene expression. Abiotic Stress Adapt Plants 2:199–216

    Google Scholar 

  47. Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35:753–759

    Article  PubMed  CAS  Google Scholar 

  48. Eltayeb AE, Kawano N, Badawi GH, Kaminaka H, Sanekata T, Shibahara T, Inanaga S, Tanaka K (2007) Overexpression of monodehydroascorbate reductase in transgenic tobacco confers enhanced tolerance to ozone, salt and polyethylene glycol stresses. Planta 225:1255–1264

    Article  PubMed  CAS  Google Scholar 

  49. Panchuk II, Volkov RA, Schöffl F (2002) Heat stress- and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiol 129:838–853

    Article  PubMed  CAS  Google Scholar 

  50. Lin K-H, Huang H-C, Lin C-Y (2010) Cloning, expression and physiological analysis of broccoli catalase gene and Chinese cabbage ascorbate peroxidase gene under heat stress. Plant Cell Rep 29:575–593

    Article  PubMed  CAS  Google Scholar 

  51. Kitajima S, Tomizawa K, Shigeoka S, Yokota A (2006) An inserted loop region of stromal ascorbate peroxidase is involved in its hydrogen peroxide-mediated inactivation. FEBS J 273:2704–2710

    Article  PubMed  CAS  Google Scholar 

  52. Matysik J, Alia Bhalu B, Mohanty P (2002) Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Curr Sci 82:525–532

    CAS  Google Scholar 

  53. Kaul S, Sharma SS, Mehta IK (2008) Free radical scavenging potential of l-proline: evidence from in vitro assays. Amino Acids 34:315–320

    Article  PubMed  CAS  Google Scholar 

  54. Lin KH, Pu SF (2010) Tissue- and genotype-specific ascorbate peroxidase expression in sweet potato in response to salt stress. Biol Plantarum 54(4):664–670

    Article  CAS  Google Scholar 

  55. Du YY, Wang PC, Chen J, Song CP (2008) Comprehensive functional analysis of the catalase gene family in Arabidopsis thaliana. J Integrat Plant Biol 50:1318–1326

    Article  CAS  Google Scholar 

  56. Banu NA, Hoque A, Watanabe-Sugimoto M, Matsuoka K, Nakamura Y, Shimoishi Y, Murata Y (2009) Proline and glycinebetaine induce antioxidant defense gene expression and suppress cell death in cultured tobacco cells under salt stress. J Plant Physiol 166:146–156

    Article  PubMed  CAS  Google Scholar 

  57. Vandenabeele S, Vandeauwera S, Vuylsteke M, Rombauts S, Langebartels C, Seiditz HK (2004) Catalase deficiency drastically affects gene expression induced by high light in Arabidopsis thaliana. Plant J 39:45–58

    Article  PubMed  CAS  Google Scholar 

  58. Luna CM, Pastori GM, Driscoll S, Groten K, Bernard S, Foyer CH (2005) Drought controls on H2O2 accumulation, catalase (CAT) activity and CAT gene expression in wheat. J Exp Bot 56:417–423

    Article  PubMed  CAS  Google Scholar 

  59. Sunkar R, Kapoor A, Zhu JK (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18:2051–2065

    Article  PubMed  CAS  Google Scholar 

  60. Qu C-P, Xu Z-R, Liu G-J, Liu C, Li Y, Wei Z-G, Liu G-F (2010) Differential expression of copper-zinc superoxide dismutase gene of Polygonum sibiricum leaves, stems and underground stems, subjected to high-salt stress. Inter J Mol Sci 11:5234–5245

    Article  CAS  Google Scholar 

  61. Pilon M, Ravet K, Tapken W (2011) The biogenesis and physiological function of chloroplast superoxide dismutases. Biochem Biophys Acta 1807:989–998

    Article  PubMed  CAS  Google Scholar 

  62. Morita S, Nakatani S, Koshiba T, Masumura T, Ogihara Y, Tanaka K (2011) Differential expression of two cytosolic ascorbate peroxidases and two superoxide dismutase genes in response to abiotic stress in rice. Rice Sci 18(3):157–166

    Article  Google Scholar 

  63. Fernández-Ocaña A, Chaki M, Luque F, Gómez-Rodríguez MV, Carreras A, Valderrama R, Begara-Morales JC, Hernández LE, Corpas FJ, Barroso JB (2011) Functional analysis of superoxide dismutases (SODs) in sunflower under biotic and abiotic stress conditions: identification of two new genes of mitochondrial Mn-SOD. J Plant Physiol 168:1303–1308

    Article  PubMed  Google Scholar 

  64. Ishikawa T, Shigeoka S (2008) Recent advances in ascorbate biosynthesis and the physiological significance of ascorbate peroxidase in photosynthesizing organisms. Biosci Biotechnol Biochem 72:1143–1154

    Article  PubMed  CAS  Google Scholar 

  65. Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155:93–100

    Article  PubMed  CAS  Google Scholar 

  66. Pang CH, Wang BS (2010) Role of ascorbate peroxidase and glutathione reductase in ascorbate–glutathione cycle and stress tolerance in plants. In: Anjum NA, Chan MT, Umar S (eds) Ascorbate-glutathione pathway and stress tolerance in plants. Springer, Dordrecht, 91–112

    Google Scholar 

  67. Hong C-Y, Chao C-Y, Yang M-Y, Cho S-C, Kao CH (2009) Na+ but not Cl− or osmotic stress is involved in NaCl-induced expression of Glutathione reductase in roots of rice seedlings. J Plant Physiol 166:1598–1606

    Article  PubMed  CAS  Google Scholar 

  68. Miller G, Stein H, Honig A, Kapulnik Y, Zilberstein A (2005) Responsive modes of Medicago sativa proline dehydrogenase genes during salt stress and recovery dictate free proline accumulation. Planta 222:70–79

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Celso J. Marur and Fábio S. Souza for plant water status evaluation. This work was supported by a grant from EMBRAPA/OEPAS. KC gratefully acknowledges CAPES for scholarship. LGEV and LFPP are CNPq research fellows.

Author information

Authors and Affiliations

  1. Plant Biotechnology Laboratory, Instituto Agronômico do Paraná, CP 481, Londrina, PR, 86047-902, Brazil

    Kenia de Carvalho, Marília Kaphan Freitas de Campos, Douglas Silva Domingues, Luiz Filipe Protasio Pereira & Luiz Gonzaga Esteves Vieira

  2. Programa de Pós-graduação em Genética e Biologia Molecular, Universidade Estadual de Londrina, CP 6001, Londrina, PR, 86051-990, Brazil

    Kenia de Carvalho

  3. Embrapa Café, PqEB, Brasília, DF, 70770-901, Brazil

    Luiz Filipe Protasio Pereira

Authors
  1. Kenia de Carvalho
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marília Kaphan Freitas de Campos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Douglas Silva Domingues
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Luiz Filipe Protasio Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Luiz Gonzaga Esteves Vieira
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Luiz Gonzaga Esteves Vieira.

Electronic supplementary material

Below is the link to the electronic supplementary material.

11033_2012_2402_MOESM1_ESM.jpg

Fig. S1 UPGMA dendrogram of the deduced amino acid sequence of APXs. Bootstrap values are indicated for each branch divergence. Sequences are GenBank accession numbers: Citrus spp. (CsAPX1, CsAPX2, CsAPXcl); Arabidopsis thaliana (NP_172267 – AtAPX1; NP_177873 - AtAPXcl); Gossypium hirsutum (ABR18607 - GhAPX1); Oryza sativa (NP_001049769 - OsAPX1; NP_001047111); Populus trichocarpa (ABK93180 - PtAPX2); Solanum lycopersicum (AXX84654 - SlAPX1); Vitis vinifera (ABX79340 - VvAPX2; CA061885 – VvAPXcl) (JPG 41 kb)

11033_2012_2402_MOESM2_ESM.jpg

Fig. S2 UPGMA dendrogram of the deduced amino acid sequence of CATs. Bootstrap values are indicated for each branch divergence. Sequences are GenBank accession numbers: Citrus spp. (CsCAT1; CsCAT2); Arabidopsis thaliana (NP_564120 – AtCAT2; CAA_64220 - AtCAT1); Gossypium hirsutum (P17598 - GhCAT2); Oryza sativa (NP_001048861 - OsCAT1); Prunus persica (CAD42908 – PpCAT2; CAD42909 - PpCAT1) Populus trichocarpa (CAI43948 - PtCAT2); Solanum lycopersicum (Q9XHH3 - SlCAT1); Vitis vinifera (CA066235 - VvCAT2; AAL83720 – VvCAT1) (JPG 32 kb)

11033_2012_2402_MOESM3_ESM.jpg

Fig. S3 UPGMA dendrogram of the deduced amino acid sequence of GRs. Bootstrap values are indicated for each branch divergence. Sequences are GenBank accession numbers: Citrus spp. (CsGR; CsGRcl); Arabidopsis thaliana (AAK25938 – AtGR; NP_191026 - AtGRcl); Oryza sativa (NP_001048485 - OsGR; NP_001049057 - OsGRcl); Populus trichocarpa (EEE84081 – PtGR; EEF05642 - PtGRcl); Vitis vinifera (CAO71585 - VvGR; CAN66042 – VvGRcl) (JPG 33 kb)

11033_2012_2402_MOESM4_ESM.jpg

Fig. S4 UPGMA dendrogram of the deduced amino acid sequence of SODs. Bootstrap values are indicated for each branch divergence. Sequences are GenBank accession numbers: Citrus spp. (CsCu/ZnSOD2; CsCu/ZnSODcl; CsCu/ZnSOD1; CsMnSODmit; CsFeSODcl); Arabidopsis thaliana (NP_172360 – AtCu/ZnSOD2 ; NP_565666 - AtCu/ZnSODcl; NP_199923 – AtFeSODcl; AAM62550 - AtMnSODmit); Citrus limon (AAQ14591 - ClCu/ZnSOD2); Gossypium hirsutum (ABA00453 - GhCu/ZnSOD2; ABA00454 - GhCu/ZnSODcl; ABA00456 – GhFeSODcl; ABA00455 - GhMnSODmit); Oryza sativa (NP_001060564 - OsCu/ZnSOD2; ABF95937 - OsCu/ZnSOD2; EAZ43665 - OsCu/ZnSODcl; NP_001056612 – OsFeSODcl; NP_001055195 - OsMnSODmit); Prunus persica (Q9SM64 – PpMnSODmit); Populus trichocarpa (ABK95956 PtCu/ZnSOD2; ABK96672 - PtCu/ZnSODcl; EEF06442 – PtFeSODcl; EEE95255 - PtMnSODmit); Solanum lycopersicum (AAQ09007 - SlCu/ZnSODcl; AAQ18699 - SlFeSODcl); Vitis vinifera (CAO15111 - VvCu/ZnSOD2; CAN59834 – VvCu/ZnSODcl; CAO62292 – VvFeSODcl; CAN61687 - VvMnSODmit) (JPG 85 kb)

11033_2012_2402_MOESM5_ESM.jpg

Fig. S5 Differences in leaf rolling symptoms between non-transformed (A) and transgenic (B) “Swingle” citrumelo plants after twenty days without irrigation (JPG 29 kb)

Supplementary material 6 (DOC 36 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

de Carvalho, K., de Campos, M.K.F., Domingues, D.S. et al. The accumulation of endogenous proline induces changes in gene expression of several antioxidant enzymes in leaves of transgenic Swingle citrumelo. Mol Biol Rep 40, 3269–3279 (2013). https://doi.org/10.1007/s11033-012-2402-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-012-2402-5

Keywords

Search

Navigation