Endoribonuclease DNE1 Promotes Ethylene Response by Modulating EBF1/2 mRNA Processing in Arabidopsis

Int J Mol Sci. 2024 Feb 10;25(4):2138. doi: 10.3390/ijms25042138.

Abstract

The gaseous phytohormone ethylene plays a crucial role in plant growth, development, and stress responses. In the ethylene signal transduction cascade, the F-box proteins EIN3-BINDING F-BOX 1 (EBF1) and EBF2 are identified as key negative regulators governing ethylene sensitivity. The translation and processing of EBF1/2 mRNAs are tightly controlled, and their 3' untranslated regions (UTRs) are critical in these regulations. However, despite their significance, the exact mechanisms modulating the processing of EBF1/2 mRNAs remain poorly understood. In this work, we identified the gene DCP1-ASSOCIATED NYN ENDORIBONUCLEASE 1 (DNE1), which encodes an endoribonuclease and is induced by ethylene treatment, as a positive regulator of ethylene response. The loss of function mutant dne1-2 showed mild ethylene insensitivity, highlighting the importance of DNE1 in ethylene signaling. We also found that DNE1 colocalizes with ETHYLENE INSENSITIVE 2 (EIN2), the core factor manipulating the translation of EBF1/2, and targets the P-body in response to ethylene. Further analysis revealed that DNE1 negatively regulates the abundance of EBF1/2 mRNAs by recognizing and cleaving their 3'UTRs, and it also represses their translation. Moreover, the dne1 mutant displays hypersensitivity to 1,4-dithiothreitol (DTT)-induced ER stress and oxidative stress, indicating the function of DNE1 in stress responses. This study sheds light on the essential role of DNE1 as a modulator of ethylene signaling through regulation of EBF1/2 mRNA processing. Our findings contribute to the understanding of the intricate regulatory process of ethylene signaling and provide insights into the significance of ribonuclease in stress responses.

Keywords: EBF1/2; EIN2; Endoribonuclease DNE1; mRNA processing; plant hormone ethylene.

MeSH terms

  • Arabidopsis Proteins* / genetics
  • Arabidopsis Proteins* / metabolism
  • Arabidopsis* / metabolism
  • DNA-Binding Proteins / metabolism
  • Endoribonucleases / genetics
  • Endoribonucleases / metabolism
  • Ethylenes / metabolism
  • Ethylenes / pharmacology
  • F-Box Proteins* / genetics
  • Gene Expression Regulation, Plant
  • Nuclear Proteins / genetics
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Transcription Factors / metabolism

Substances

  • Transcription Factors
  • DNA-Binding Proteins
  • Arabidopsis Proteins
  • Endoribonucleases
  • Nuclear Proteins
  • ethylene
  • Ethylenes
  • RNA, Messenger
  • EBF1 protein, Arabidopsis
  • F-Box Proteins