Methylglyoxal detoxification by a DJ-1 family protein provides dual abiotic and biotic stress tolerance in transgenic plants
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.
KeywordsHeat shock proteins DJ-1 family members Methylglyoxal Abiotic stress Plant stress responses
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.
PVS and PD designed all experiments, discussed results and wrote the manuscript. MP performed most of the experiments. KB designed constructs and performed microscopy.
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.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict interests.
- Griffiths H, Parry MAJ, Hsiao T (2002) Plant responses to water stress. Annu Rev Plant Physiol 89:801–802Google Scholar
- 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
- 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
- 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