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

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.

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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

    CAS  Article  PubMed  Google 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

    CAS  Article  PubMed  Google 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

    CAS  Article  PubMed  Google Scholar 

  4. Allaman I, Bélanger M, Magistretti PJ (2015) Methylglyoxal, the dark side of glycolysis. Front Neurosci. doi:10.3389/fnins.2015.00023

    PubMed  PubMed Central  Google 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

    CAS  Article  PubMed  Google 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

    Article  PubMed  PubMed Central  Google 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. Baulcombe D (2004) RNA silencing in plants. Nature 431:356–363. doi:10.1079/IVP2004619

    CAS  Article  PubMed  Google Scholar 

  9. Bevan M (1984) Binary Agrobacterium vectors for plant transformation. Nucleic Acids Res 12:8711–8721. doi:10.1093/nar/12.22.8711

    CAS  Article  PubMed  PubMed Central  Google 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

    CAS  Article  PubMed  Google Scholar 

  11. Boyland E, Chasseaud LF (1967) Enzyme-catalysed conjugations of glutathione with unsaturated compounds. Biochem J 104:95–102

    CAS  Article  PubMed  PubMed Central  Google 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

    Article  PubMed  PubMed Central  Google 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

    CAS  Article  PubMed  PubMed Central  Google 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

    CAS  Article  Google 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

    CAS  Article  PubMed  Google 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

    Article  Google 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

    CAS  Article  PubMed  Google 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

    Article  PubMed  PubMed Central  Google 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

    CAS  Article  PubMed  PubMed Central  Google 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

    CAS  Article  PubMed  Google 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 89:801–802

    Google 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

    CAS  Article  PubMed  PubMed Central  Google 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

    CAS  Article  PubMed  Google 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

    Article  Google 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

    CAS  Article  PubMed  Google 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

    CAS  Article  PubMed  PubMed Central  Google 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

    CAS  Article  PubMed  Google 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

    CAS  Article  Google 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

    PubMed  PubMed Central  Google 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

    CAS  Article  PubMed  Google 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

    CAS  Article  Google 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

    CAS  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

    CAS  Article  PubMed  Google 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

    CAS  Article  Google 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

    CAS  Article  PubMed  Google 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

    Article  PubMed  PubMed Central  Google 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

    CAS  Article  Google 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

    CAS  Article  PubMed  Google 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

    CAS  Article  PubMed  PubMed Central  Google 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

    Article  PubMed  Google 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

    CAS  Article  PubMed  Google 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

    CAS  Article  PubMed  PubMed Central  Google 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

    CAS  Article  PubMed  Google 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

    CAS  Article  PubMed  Google 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

    CAS  Article  PubMed  Google 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

    CAS  Article  PubMed  Google 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

    Article  PubMed  PubMed Central  Google 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

    CAS  Article  PubMed  Google 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

    CAS  Article  Google 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

    CAS  Article  PubMed  PubMed Central  Google 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

    Article  PubMed  Google Scholar 

  58. Thornalley PJ (1990) The glyoxalase system: new developments towards functional characterization of a metabolic pathway fundamental to biological life. Biochem J 269:1–11

    CAS  Article  PubMed  PubMed Central  Google 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

    CAS  Article  PubMed  Google 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

    CAS  Article  PubMed  PubMed Central  Google 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

    CAS  Article  PubMed  PubMed Central  Google 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

    CAS  Article  PubMed  Google 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

    CAS  Article  PubMed  PubMed Central  Google 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

    CAS  Article  PubMed  Google 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

    CAS  Article  PubMed  Google 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

    CAS  Article  PubMed  PubMed Central  Google 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

    CAS  Article  Google 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

    CAS  Article  PubMed  PubMed Central  Google 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

    CAS  Article  PubMed  PubMed Central  Google 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

    CAS  Article  PubMed  PubMed Central  Google 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

    CAS  Article  PubMed  Google 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

    CAS  Article  PubMed  Google 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

    CAS  Article  PubMed  Google 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

    CAS  Article  PubMed  Google 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

    CAS  Article  PubMed  Google Scholar 

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Acknowledgements

The authors acknowledge access to Imaging, greenhouse and sequencing facilities from their respective institutions. Thanks to Prof. K. Veluthambi for pBIN19 vector, viral clones and Agrobacterium strain LBA4404 (pSB1), Dr. Radhika Venkatesan for P. syringae DC3000, Prof. Janardhana for Alternaria Spp., Swetha Chenna for help in structure prediction and N. D. Sunitha for comments.

Author contributions

PVS and PD designed all experiments, discussed results and wrote the manuscript. MP performed most of the experiments. KB designed constructs and performed microscopy.

Funding

PVS acknowledges support from Ramanujan Fellowship (SR/S2/RJN-109/2012; Department of Science and Technology, Government of India). PVS lab is supported by NCBS-TIFR core funding and a grant (BT/PR12394/AGIII/103/891/2014) from Department of Biotechnology, Government of India. PDS acknowledges support from Swarnajayanti Fellowship (DST/SJF/LS-01/2011–2012), DBT-IISc partnership program (DBT/BF/PR/INS/2011-12/IISc) and UGC-CAS SAP-II program (UGC LT. No. F. 5-2/2012. SAP-II). KB acknowledges research fellowship from CSIR.

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Correspondence to P. V. Shivaprasad.

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Melvin, P., Bankapalli, K., D’Silva, P. et al. Methylglyoxal detoxification by a DJ-1 family protein provides dual abiotic and biotic stress tolerance in transgenic plants. Plant Mol Biol 94, 381–397 (2017). https://doi.org/10.1007/s11103-017-0613-9

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Keywords

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