A glutathione-independent DJ-1/PfpI domain-containing tomato glyoxalaseIII2, SlGLYIII2, confers enhanced tolerance under salt and osmotic stresses

Plant Cell Environ. 2023 Feb;46(2):518-548. doi: 10.1111/pce.14493. Epub 2022 Nov 26.

Abstract

In plants, glyoxalase enzymes are activated under stress conditions to mitigate the toxic effects of hyperaccumulated methylglyoxal (MG), a highly reactive carbonyl compound. Until recently, a glutathione-dependent bi-enzymatic pathway involving glyoxalase I (GLYI) and glyoxalase II (GLYII) was considered the primary MG-detoxification system. Recently, a new glutathione-independent glyoxalase III (GLYIII) mediated direct route was also reported in plants. However, the physiological significance of this new pathway remains to be elucidated across plant species. This study identified the full complement of 22 glyoxalases in tomato. Based on their strong induction under multiple abiotic stresses, SlGLYI4, SlGLYII2 and SlGLYIII2 were selected candidates for further functional characterisation. Stress-inducible overexpression of both glutathione-dependent (SlGLYI4 + SlGLYII2) and independent (SlGLYIII2) pathways led to enhanced tolerance in both sets of transgenic plants under abiotic stresses. However, SlGLYIII2 overexpression (OE) plants outperformed the SlGLYI4 + SlGLYII2 OE counterparts for their stress tolerance under abiotic stresses. Further, knockdown of SlGLYIII2 resulted in plants with exacerbated stress responses than those silenced for both SlGLYI4 and SlGLYII2. The superior performance of SlGLYIII2 OE tomato plants for better growth and yield under salt and osmotic treatments could be attributed to better GSH/GSSG ratio, lower reactive oxygen species levels, and enhanced antioxidant potential, indicating a prominent role of GLYIII MG-detoxification pathway in abiotic stress mitigation in this species.

Keywords: GSH/GSSG; ROS; abiotic stress; glyoxalase; methylglyoxal; overexpression; tomato transgenics.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Glutathione / metabolism
  • Lactoylglutathione Lyase* / genetics
  • Lactoylglutathione Lyase* / metabolism
  • Osmotic Pressure
  • Plant Proteins / genetics
  • Plant Proteins / metabolism
  • Plants, Genetically Modified / metabolism
  • Pyruvaldehyde / metabolism
  • Sodium Chloride / pharmacology
  • Solanum lycopersicum* / genetics
  • Stress, Physiological

Substances

  • Lactoylglutathione Lyase
  • Sodium Chloride
  • Glutathione
  • Plant Proteins
  • Pyruvaldehyde