Plant Molecular Biology

, Volume 94, Issue 4–5, pp 381–397 | Cite as

Methylglyoxal detoxification by a DJ-1 family protein provides dual abiotic and biotic stress tolerance in transgenic plants

  • Prasad Melvin
  • Kondalarao Bankapalli
  • Patrick D’Silva
  • P. V. Shivaprasad
Article

Abstract

Methylglyoxal (MG) is a key signaling molecule resulting from glycolysis and other metabolic pathways. During abiotic stress, MG levels accumulate to toxic levels in affected cells. However, MG is routinely detoxified through the action of DJ1/PARK7/Hsp31 proteins that are highly conserved across kingdoms and mutations in such genes are associated with neurodegenerative diseases. Here, we report for the first time that, similar to abiotic stresses, MG levels increase during biotic stresses in plants, likely contributing to enhanced susceptibility to a wide range of stresses. We show that overexpression of yeast Heat shock protein 31 (Hsp31), a DJ-1 homolog with robust MG detoxifying capabilities, confers dual biotic and abiotic stress tolerance in model plant Nicotiana tabacum. Strikingly, overexpression of Hsp31 in tobacco imparts robust stress tolerance against diverse biotic stress inducers such as viruses, bacteria and fungi, in addition to tolerance against a range of abiotic stress inducers. During stress, Hsp31 was targeted to mitochondria and induced expression of key stress-related genes. These results indicate that Hsp31 is a novel attractive tool to engineer plants against both biotic and abiotic stresses.

Keywords

Heat shock proteins DJ-1 family members Methylglyoxal Abiotic stress Plant stress responses 

Supplementary material

11103_2017_613_MOESM1_ESM.pptx (4.5 mb)
Supplementary material 1 (PPTX 4632 KB)

References

  1. Abdallah J, Mihoub M, Gautier V, Richarme G (2016) The DJ-1 superfamily members YhbO and YajL from Escherichia coli repair proteins from glycation by methylglyoxal and glyoxal. Biochem Biophys Res Commun 470:282–286. doi:10.1016/j.bbrc.2016.01.068 CrossRefPubMedGoogle Scholar
  2. Ahuja I, de Vos RCH, Bones AM, Hall RD (2010) Plant molecular stress responses face climate change. Trends Plant Sci 15:664–674. doi:10.1016/j.tplants.2010.08.002 CrossRefPubMedGoogle Scholar
  3. Ali W, Isner JC, Isayenkov SV et al (2012) Heterologous expression of the yeast arsenite efflux system ACR3 improves Arabidopsis thaliana tolerance to arsenic stress. New Phytol 194:716–723. doi:10.1111/j.1469-8137.2012.04092.x CrossRefPubMedGoogle Scholar
  4. Allaman I, Bélanger M, Magistretti PJ (2015) Methylglyoxal, the dark side of glycolysis. Front Neurosci. doi:10.3389/fnins.2015.00023 PubMedPubMedCentralGoogle Scholar
  5. Allocati N, Federici L, Masulli M, Di Ilio C (2009) Glutathione transferases in bacteria. FEBS J 276:58–75. doi:10.1111/j.1742-4658.2008.06743.x CrossRefPubMedGoogle Scholar
  6. Aslam K, Hazbun TR (2016) Hsp31, a member of the DJ-1 superfamily, is a multitasking stress responder with chaperone activity. Prion 10:103–111. doi:10.1080/19336896.2016.1141858 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bankapalli K, Saladi S, Awadia SS et al (2015) Robust glyoxalase activity of Hsp31, a ThiJ/DJ-1/PfpI family member protein, is critical for oxidative stress resistance in Saccharomyces cerevisiae. J Biol Chem 290:26491–26507. doi:10.1074/jbc.M115.673624 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Baulcombe D (2004) RNA silencing in plants. Nature 431:356–363. doi:10.1079/IVP2004619 CrossRefPubMedGoogle Scholar
  9. Bevan M (1984) Binary Agrobacterium vectors for plant transformation. Nucleic Acids Res 12:8711–8721. doi:10.1093/nar/12.22.8711 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bohnert HJ, Gong Q, Li P, Ma S (2006) Unraveling abiotic stress tolerance mechanisms-getting genomics going. Curr Opin Plant Biol 9:180–188. doi:10.1016/j.pbi.2006.01.003 CrossRefPubMedGoogle Scholar
  11. Boyland E, Chasseaud LF (1967) Enzyme-catalysed conjugations of glutathione with unsaturated compounds. Biochem J 104:95–102CrossRefPubMedPubMedCentralGoogle Scholar
  12. Canet-Avilés RM, Wilson MA, Miller DW et al (2004) The Parkinson’s disease protein DJ-1 is neuroprotective due to cysteine-sulfinic acid-driven mitochondrial localization. Proc Natl Acad Sci USA 101:9103–9108. doi:10.1073/pnas.0402959101 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Choi J, Sullards MC, Olzmann JA et al (2006) Oxidative damage of DJ-1 is linked to sporadic Parkinson and Alzheimer diseases. J Biol Chem 281:10816–10824. doi:10.1074/jbc.M509079200 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Conrath U, Beckers GJM, Flors V, et al (2006) Priming: getting ready for battle. Mol Pant-Microbe Interact 19:1062–1071. doi:10.1094/MPMI-19-1062 CrossRefGoogle Scholar
  15. Daudi A, O’Brien JA (2012) Detection of hydrogen peroxide by DAB staining in Arabidopsis leaves. Bio-protocol 2:e263. doi:10.1007/BF00139728.5. http://www.bio-protocol.org/e263
  16. Davie CA (2008) A review of Parkinson’s disease. Br Med Bull 86:109–127. doi:10.1093/bmb/ldn013 CrossRefPubMedGoogle Scholar
  17. de las Mercedes Dana M, Pintor-Toro JA, Cubero B (2006) Transgenic tobacco plants overexpressing chitinases of fungal origin show enhanced resistance to biotic and abiotic stress agents. Plant Physiol 142:722–730. doi:10.1104/pp.106.086140 CrossRefGoogle Scholar
  18. Dixon DP, Cummins I, Cole DJ, Edwards R (1998) Glutathione-mediated detoxification systems in plants. Curr Opin Plant Biol 1:258–266. doi:10.1007/s00299-002-0545-x CrossRefPubMedGoogle Scholar
  19. Eswaran N, Parameswaran S, Sathram B et al (2010) Yeast functional screen to identify genetic determinants capable of conferring abiotic stress tolerance in Jatropha curcas. BMC Biotechnol 10:23. doi:10.1186/1472-6750-10-23 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Furtado Macedo A (2012) Abiotic stress responses in plants. Springer, Berlin. doi:10.1007/978-1-4614-0634-1 Google Scholar
  21. Gill SS, Tuteja N (2010) Polyamines and abiotic stress tolerance in plants. Plant Signal Behav 5:26–33. doi:10.4161/psb.5.1.10291 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Gill SS, Anjum NA, Hasanuzzaman M et al (2013) Glutathione and glutathione reductase: a boon in disguise for plant abiotic stress defense operations. Plant Physiol Biochem 70:204–212. doi:10.1016/j.plaphy.2013.05.032 CrossRefPubMedGoogle Scholar
  23. Goyal RK, Hancock REW, Mattoo AK, Misra S (2013) Expression of an engineered heterologous antimicrobial peptide in potato alters plant development and mitigates normal abiotic and biotic responses. PLoS ONE. doi:10.1371/journal.pone.0077505 Google Scholar
  24. Griffiths H, Parry MAJ, Hsiao T (2002) Plant responses to water stress. Annu Rev Plant Physiol 89:801–802Google Scholar
  25. Hao L-Y, Giasson BI, Bonini NM (2010) DJ-1 is critical for mitochondrial function and rescues PINK1 loss of function. Proc Natl Acad Sci USA 107:9747–9752. doi:10.1073/pnas.0911175107 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Hasim S, Hussin NA, Alomar F et al (2014) A glutathione-independent glyoxalase of the DJ-1 superfamily plays an important role in managing metabolically generated methylglyoxal in candida albicans. J Biol Chem 289:1662–1674. doi:10.1074/jbc.M113.505784 CrossRefPubMedGoogle Scholar
  27. Hossain MA, Piyatida P, da Silva JAT, Fujita M (2012) Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J Bot 2012:1–37. doi:10.1155/2012/872875 CrossRefGoogle Scholar
  28. Hussain SS, Ali M, Ahmad M, Siddique KHM (2011) Polyamines: natural and engineered abiotic and biotic stress tolerance in plants. Biotechnol Adv 29:300–311. doi:10.1016/j.biotechadv.2011.01.003 CrossRefPubMedGoogle Scholar
  29. Junn E, Jang WH, Zhao X et al (2009) Mitochondrial localization of DJ-1 leads to enhanced neuroprotection. J Neurosci Res 87:123–129. doi:10.1002/jnr.21831 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Kasai H, Iwamoto-Tanaka N, Fukada S (1998) DNA modifications by the mutagen glyoxal: adduction to G and C, deamination of C and GC and GA cross-linking. Carcinogenesis 19:1459–1465. doi:10.1093/carcin/19.8.1459 CrossRefPubMedGoogle Scholar
  31. Kaur C, Singla-Pareek SL, Sopory SK (2014) Glyoxalase and Methylglyoxal as Biomarkers for Plant Stress Tolerance. Crit Rev Plant Sci 33:429–456. doi:10.1080/07352689.2014.904147 CrossRefGoogle Scholar
  32. Kaur C, Kushwaha HR, Mustafiz A et al (2015) Analysis of global gene expression profile of rice in response to methylglyoxal indicates its possible role as a stress signal molecule. Front Plant Sci 6:682. doi:10.3389/fpls.2015.00682 PubMedPubMedCentralGoogle Scholar
  33. Lee JY, Song J, Kwon K et al (2012) Human DJ-1 and its homologs are novel glyoxalases. Hum Mol Genet 21:3215–3225. doi:10.1093/hmg/dds155 CrossRefPubMedGoogle Scholar
  34. Lin J, Nazarenus TJ, Frey JL et al (2011) A plant DJ-1 homolog is essential for Arabidopsis thaliana chloroplast development. PLoS ONE. doi:10.1371/journal.pone.0023731 Google Scholar
  35. Luo M, Liu X, Singh P, et al. (2012) Chromatin modifications and remodeling in plant abiotic stress responses. Biochim Biophys Acta 1819:129–136. doi:10.1016/j.bbagrm.2011.06.008 CrossRefGoogle Scholar
  36. May MJ, Vernoux T, Leaver C et al (1998) Glutathione homeostasis in plants: implications for environmental sensing and plant development. J Exp Bot 49:649–667. doi:10.1093/jxb/49.321.649 Google Scholar
  37. Morcos M, Du X, Pfisterer F et al (2008) Glyoxalase-1 prevents mitochondrial protein modification and enhances lifespan in Caenorhabditis elegans. Aging Cell 7:260–269. doi:10.1111/j.1474-9726.2008.00371.x CrossRefPubMedGoogle Scholar
  38. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497. doi:10.1111/j.1399-3054.1962.tb08052.x CrossRefGoogle Scholar
  39. Nakabayashi R, Yonekura-Sakakibara K, Urano K et al (2014) Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids. Plant J 77:367–379. doi:10.1111/tpj.12388 CrossRefPubMedGoogle Scholar
  40. Nakahara Y, Sawabe S, Kainuma K et al (2015) Yeast functional screen to identify genes conferring salt stress tolerance in Salicornia europaea. Front Plant Sci 6:920. doi:10.3389/fpls.2015.00920 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Nakaminami K, Matsui A, Shinozaki K, Seki M (2012) RNA regulation in plant abiotic stress responses. Biochim Biophys Acta 1819:149–153. doi:10.1016/j.bbagrm.2011.07.015 CrossRefGoogle Scholar
  42. Niki E, Yoshida Y, Saito Y, Noguchi N (2005) Lipid peroxidation: mechanisms, inhibition, and biological effects. Biochem Biophys Res Commun 338:668–676. doi:10.1016/j.bbrc.2005.08.072 CrossRefPubMedGoogle Scholar
  43. Obata T, Fernie AR (2012) The use of metabolomics to dissect plant responses to abiotic stresses. Cell Mol Life Sci 69:3225–3243. doi:10.1007/s00018-012-1091-5 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Padilla-Chacón D, Cordoba E, Olivera T et al (2010) Heterologous expression of yeast Hxt2 in arabidopsis thaliana alters sugar uptake, carbon metabolism and gene expression leading to glucose tolerance of germinating seedlings. Plant Mol Biol 72:631–641. doi:10.1007/s11103-010-9602-y CrossRefPubMedGoogle Scholar
  45. Pareek A, Sopory SK, Bohnert HJ (2010) Abiotic stress adaptation in plants. Physiol Mol Genom Found. doi:10.1007/978-90-481-3112-9 Google Scholar
  46. Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:290–295. doi:10.1016/j.pbi.2011.02.001 CrossRefPubMedGoogle Scholar
  47. Raza H (2011) Dual localization of glutathione S-transferase in the cytosol and mitochondria: Implications in oxidative stress, toxicity and disease. FEBS J 278:4243–4251. doi:10.1111/j.1742-4658.2011.08358.x CrossRefPubMedPubMedCentralGoogle Scholar
  48. Rhee SG, Yang K-S, Kang SW et al (2005) Controlled elimination of intracellular H2O2: regulation of peroxiredoxin, catalase, and glutathione peroxidase via post-translational modification. Antioxid Redox Signal 7:619–626. doi:10.1089/ars.2005.7.619 CrossRefPubMedGoogle Scholar
  49. Roy SJ, Tucker EJ, Tester M (2011) Genetic analysis of abiotic stress tolerance in crops. Curr Opin Plant Biol 14:232–239. doi:10.1016/j.pbi.2011.03.002 CrossRefPubMedGoogle Scholar
  50. Shangari N, O’Brien PJ (2004) The cytotoxic mechanism of glyoxal involves oxidative stress. Biochem Pharmacol 68:1433–1442. doi:10.1016/j.bcp.2004.06.013 CrossRefPubMedGoogle Scholar
  51. Shivaprasad PV, Thillaichidambaram P, Balaji V, Veluthambi K (2006) Expression of full-length and truncated Rep genes from Mungbean yellow mosaic virus-Vigna inhibits viral replication in transgenic tobacco. Virus Genes 33:365–374. doi:10.1007/s11262-006-0077-5 CrossRefPubMedGoogle Scholar
  52. Shivaprasad PV, Dunn RM, Santos BA et al (2011) Extraordinary transgressive phenotypes of hybrid tomato are influenced by epigenetics and small silencing RNAs. EMBO J 31:257–266. doi:10.1038/emboj.2011.458 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Subedi KP, Choi D, Kim I et al (2011) Hsp31 of Escherichia coli K-12 is glyoxalase III. Mol Microbiol 81:926–936. doi:10.1111/j.1365-2958.2011.07736.x CrossRefPubMedGoogle Scholar
  54. Szabados L, Kovács H, Zilberstein A, Bouchereau A (2011) Plants in extreme environments: importance of protective compounds in stress tolerance. Adv Bot Res. doi:10.1016/B978-0-12-387692-8.00004-7 Google Scholar
  55. Szalai G, Kellos T, Galiba G, Kocsy G (2009) Glutathione as an antioxidant and regulatory molecule in plants under abiotic stress conditions. J Plant Growth Regul 28:66–80. doi:10.1007/s00344-008-9075-2 CrossRefGoogle Scholar
  56. Taira T, Saito Y, Niki T et al (2004) DJ-1 has a role in antioxidative stress to prevent cell death. EMBO Rep 5:213–218. doi:10.1038/sj.embor.7400074 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Tardieu F, Tuberosa R (2010) Dissection and modelling of abiotic stress tolerance in plants. Curr Opin Plant Biol 13:206–212. doi:10.1016/j.pbi.2009.12.012 CrossRefPubMedGoogle Scholar
  58. Thornalley PJ (1990) The glyoxalase system: new developments towards functional characterization of a metabolic pathway fundamental to biological life. Biochem J 269:1–11CrossRefPubMedPubMedCentralGoogle Scholar
  59. Thornalley PJ (1996) Pharmacology of methylglyoxal: formation, modification of proteins and nucleic acids, and enzymatic detoxification: a role in pathogenesis and antiproliferative chemotherapy. Gen Pharmacol 27:565–573. doi:10.1016/0306-3623(95)02054-3 CrossRefPubMedGoogle Scholar
  60. Thornalley PJ (2008) Protein and nucleotide damage by glyoxal and methylglyoxal in physiological systems–role in ageing and disease. Drug Metabol Drug Interact 23:125–150. doi:10.1515/DMDI.2008.23.1-2.125 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Thornalley PJ, Langborg A, Minhas HS (1999) Formation of glyoxal, methylglyoxal and 3-deoxyglucosone in the glycation of proteins by glucose. Biochem J 344:109–116. doi:10.1042/bj3440109 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Treutter D (2005) Significance of flavonoids in plant resistance and enhancement of their biosynthesis. Plant Biol 7:581–591. doi:10.1055/s-2005-873009 CrossRefPubMedGoogle Scholar
  63. Tsai CJ, Aslam K, Drendel HM et al (2015) Hsp31 is a stress response chaperone that intervenes in the protein misfolding process. J Biol Chem 290:24816–24834. doi:10.1074/jbc.M115.678367 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Urano K, Kurihara Y, Seki M, Shinozaki K (2010) “Omics” analyses of regulatory networks in plant abiotic stress responses. Curr Opin Plant Biol 13:132–138. doi:10.1016/j.pbi.2009.12.006 CrossRefPubMedGoogle Scholar
  65. Veena RVS, Sopory SK (1999) Glyoxalase I from Brassica juncea: molecular cloning, regulation and its over-expression confer tolerance in transgenic tobacco under stress. Plant J 17:385–395. doi:10.1046/j.1365-313X.1999.00390.x CrossRefPubMedGoogle Scholar
  66. Wang X, Petrie TG, Liu Y et al (2012) Parkinson’s disease-associated DJ-1 mutations impair mitochondrial dynamics and cause mitochondrial dysfunction. J Neurochem 121:830–839. doi:10.1111/j.1471-4159.2012.07734.x CrossRefPubMedPubMedCentralGoogle Scholar
  67. Wei Y, Ringe D, Wilson MA, Ondrechen MJ (2007) Identification of functional subclasses in the DJ-1 superfamily proteins. PLoS Comput Biol 3:0120–0126. doi:10.1371/journal.pcbi.0030010 CrossRefGoogle Scholar
  68. Willekens H, Chamnongpol S, Davey M et al (1997) Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J 16:4806–4816. doi:10.1093/emboj/16.16.4806 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Wilson MA (2011) The role of cysteine oxidation in DJ-1 function and dysfunction. Antioxid Redox Signal 15:111–122. doi:10.1089/ars.2010.3481 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Xu XM, Møller SG (2010) ROS removal by DJ-1: Arabidopsis as a new model to understand Parkinson’s Disease. Plant Signal Behav 5:1034–1036. doi:10.4161/psb.5.8.12298 CrossRefPubMedPubMedCentralGoogle Scholar
  71. Xu XM, Lin H, Maple J et al (2010) The Arabidopsis DJ-1a protein confers stress protection through cytosolic SOD activation. J Cell Sci 123:1644–1651. doi:10.1242/jcs.063222 CrossRefPubMedGoogle Scholar
  72. Yadav SK, Singla-Pareek SL, Ray M et al (2005a) Methylglyoxal levels in plants under salinity stress are dependent on glyoxalase I and glutathione. Biochem Biophys Res Commun 337:61–67. doi:10.1016/j.bbrc.2005.08.263 CrossRefPubMedGoogle Scholar
  73. Yadav SK, Singla-Pareek SL, Reddy MK, Sopory SK (2005b) Transgenic tobacco plants overexpressing glyoxalase enzymes resist an increase in methylglyoxal and maintain higher reduced glutathione levels under salinity stress. FEBS Lett 579:6265–6271. doi:10.1016/j.febslet.2005.10.006 CrossRefPubMedGoogle Scholar
  74. Zhou W, Freed CR (2005) DJ-1 up-regulates glutathione synthesis during oxidative stress and inhibits A53T alpha-synuclein toxicity. J Biol Chem 280:43150–43158. doi:10.1074/jbc.M507124200 CrossRefPubMedGoogle Scholar
  75. Zhou W, Zhu M, Wilson MA et al (2006) The oxidation state of DJ-1 regulates its chaperone activity toward α-synuclein. J Mol Biol 356:1036–1048. doi:10.1016/j.jmb.2005.12.030 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  1. 1.National Centre for Biological SciencesBangaloreIndia
  2. 2.Department of BiochemistryIndian Institute of ScienceBangaloreIndia

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