NUA positively regulates plant immunity by coordination with ESD4 to deSUMOylate TPR1 in Arabidopsis

New Phytol. 2024 Jan;241(1):363-377. doi: 10.1111/nph.19287. Epub 2023 Oct 2.

Abstract

Nuclear pore complex (NPC) is composed of multiple nucleoporins (Nups). A plethora of studies have highlighted the significance of NPC in plant immunity. However, the specific roles of individual Nups are poorly understood. NUCLEAR PORE ANCHOR (NUA) is a component of NPC. Loss of NUA leads to an increase in SUMO conjugates and pleiotropic developmental defects in Arabidopsis thaliana. Herein, we revealed that NUA is required for plant defense against multiple pathogens. NUCLEAR PORE ANCHOR associates with the transcriptional corepressor TOPLESS-RELATED1 (TPR1) and contributes to TPR1 deSUMOylation. Significantly, NUA-interacting protein EARLY IN SHORT DAYS 4 (ESD4), a SUMO protease, specifically deSUMOylates TPR1. It has been previously established that the SUMO E3 ligase SAP AND MIZ1 DOMAIN-CONTAINING LIGASE 1 (SIZ1)-mediated SUMOylation of TPR1 represses the immune-related function of TPR1. Consistent with this notion, the hyper-SUMOylated TPR1 in nua-3 leads to upregulated expression of TPR1 target genes and compromised TPR1-mediated disease resistance. Taken together, our work uncovers a mechanism by which NUA positively regulates plant defense responses by coordination with ESD4 to deSUMOylate TPR1. Our findings, together with previous studies, reveal a regulatory module in which SIZ1 and NUA/ESD4 control the homeostasis of TPR1 SUMOylation to maintain proper immune output.

Keywords: Arabidopsis; ESD4; NUA; TPR1; deSUMOylation; nuclear pore complex; plant immunity.

MeSH terms

  • Arabidopsis Proteins* / metabolism
  • Arabidopsis* / metabolism
  • Gene Expression Regulation, Plant
  • Ligases / metabolism
  • Nuclear Pore / metabolism
  • Plant Immunity*
  • Sumoylation
  • Ubiquitin-Protein Ligases / metabolism

Substances

  • Arabidopsis Proteins
  • Ligases
  • SIZ1 protein, Arabidopsis
  • Ubiquitin-Protein Ligases
  • NUA protein, Arabidopsis
  • ESD4 protein, Arabidopsis
  • topless-related 1 protein, Arabidopsis