ABI3- and PIF1-mediated regulation of GIG1 enhances seed germination by detoxification of methylglyoxal in Arabidopsis

Plant J. 2022 Jun;110(6):1578-1591. doi: 10.1111/tpj.15755. Epub 2022 Apr 25.

Abstract

Methylglyoxal (MG) is a toxic by-product of the glycolysis pathway in most living organisms and was previously shown to inhibit seed germination. MG is detoxified by glyoxalase I and II family proteins in plants. MG is abundantly produced during early embryogenesis in Arabidopsis seeds. However, the mechanism that alleviates the toxic effect of MG in maturing seeds is poorly understood. In this study, by T-DNA mutant population screening, we found that mutations in a glyoxalase I gene (named GERMINATION-IMPAIRED GLYOXALASE 1, GIG1) led to significantly impaired germination compared with wild-type seeds. Transformation of full-length GIG1 cDNA under the constitutively active cauliflower mosaic virus 35S promoter in the gig1 background completely recovered the seed germination phenotype. Quantitative reverse transcription polymerase chain reaction (qRT-PCR) analyses revealed that GIG1 is uniquely expressed in seeds and is upregulated by abscisic acid (ABA) and downregulated by gibberellic acid (GA) during seed germination. An ABA signaling component, ABI3, directly activated GIG1 in maturing seeds. In addition, PHYTOCHROME INTERACTING FACTOR 1 (PIF1) also plays cooperatively with ABI3 in the regulation of GIG1 expression in the early stage of imbibed seeds. Furthermore, GIG1 expression is stably silenced by epigenetic repressors such as polycomb repressor complexes. Altogether, our results indicate that light and ABA signaling cooperate to enhance seed germination by the upregulation of GIG1 to detoxify MG in maturing seeds.

Keywords: abscisic acid; glyoxalase I; methylglyoxal; phytochrome; seed germination.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Abscisic Acid / metabolism
  • Arabidopsis Proteins* / metabolism
  • Arabidopsis* / metabolism
  • Basic Helix-Loop-Helix Transcription Factors / metabolism
  • Gene Expression Regulation, Plant
  • Germination
  • Lactoylglutathione Lyase* / genetics
  • Lactoylglutathione Lyase* / metabolism
  • Phytochrome* / metabolism
  • Pyruvaldehyde / metabolism
  • Seeds / metabolism
  • Transcription Factors / metabolism

Substances

  • ABI3 protein, Arabidopsis
  • Arabidopsis Proteins
  • Basic Helix-Loop-Helix Transcription Factors
  • PIF1 protein, Arabidopsis
  • Transcription Factors
  • Phytochrome
  • Pyruvaldehyde
  • Abscisic Acid
  • Lactoylglutathione Lyase