Regulatory module WRKY33-ATL31-IRT1 mediates cadmium tolerance in Arabidopsis

Plant Cell Environ. 2023 May;46(5):1653-1670. doi: 10.1111/pce.14558. Epub 2023 Feb 14.

Abstract

Cadmium (Cd) is one of the most dangerous environmental pollutants among heavy metals, and threatens food safety and human health by accumulating in plant sink tissues. Here, we report a novel regulatory cascade that profoundly influences Cd tolerance in Arabidopsis. Phenotypic analysis showed that an insertional knockdown mutation at the Arabidopsis Tóxicos en Levadura 31 (ATL31) locus resulted in hypersensitivity to Cd stress, most likely due to a significant increase in Cd accumulation. Consistently, ATL31-overexpressing lines exhibited enhanced Cd stress tolerance and reduced Cd accumulation. Further, IRON-REGULATED TRANSPORTER 1 (IRT1) was identified, and yeast two-hybrid, co-immunoprecipitation and bimolecular fluorescence complementation assays demonstrated its interaction with ATL31. Biochemical, molecular, and genetic analyses showed that IRT1 is targeted by ATL31 for ubiquitin-conjugated degradation in response to Cd stress. Intriguingly, transcription of ATL31 was strongly induced by Cd stress. In addition, transgenic and molecular analyses showed that WRKY33 directly activated the transcription of ATL31 in response to Cd stress and positively regulated Cd tolerance. Genetic analysis indicated that ATL31 acts upstream of IRT1 and downstream of WRKY33 to regulate Cd tolerance. Our study revealed that the WRKY33-ATL31-IRT1 module plays a crucial role in timely blocking Cd absorption to prevent metal toxicity in Arabidopsis.

Keywords: Arabidopsis thaliana; IRT1; WRKY33; cadmium tolerance.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis Proteins* / metabolism
  • Arabidopsis* / metabolism
  • Cadmium / metabolism
  • Cadmium / toxicity
  • Cation Transport Proteins* / genetics
  • Cation Transport Proteins* / metabolism
  • Gene Expression Regulation, Plant
  • Humans
  • Membrane Transport Proteins / metabolism
  • Metals, Heavy* / metabolism
  • Saccharomyces cerevisiae / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / metabolism

Substances

  • Arabidopsis Proteins
  • Cadmium
  • Cation Transport Proteins
  • IRT1 protein, Arabidopsis
  • Membrane Transport Proteins
  • Metals, Heavy
  • Transcription Factors
  • WRKY33 protein, Arabidopsis
  • ATL31 protein, Arabidopsis