The AtMINPP Gene, Encoding a Multiple Inositol Polyphosphate Phosphatase, Coordinates a Novel Crosstalk between Phytic Acid Metabolism and Ethylene Signal Transduction in Leaf Senescence

Int J Mol Sci. 2024 Aug 17;25(16):8969. doi: 10.3390/ijms25168969.

Abstract

Plant senescence is a highly coordinated process that is intricately regulated by numerous endogenous and environmental signals. The involvement of phytic acid in various cell signaling and plant processes has been recognized, but the specific roles of phytic acid metabolism in Arabidopsis leaf senescence remain unclear. Here, we demonstrate that in Arabidopsis thaliana the multiple inositol phosphate phosphatase (AtMINPP) gene, encoding an enzyme with phytase activity, plays a crucial role in regulating leaf senescence by coordinating the ethylene signal transduction pathway. Through overexpressing AtMINPP (AtMINPP-OE), we observed early leaf senescence and reduced chlorophyll contents. Conversely, a loss-of-function heterozygous mutant (atminpp/+) exhibited the opposite phenotype. Correspondingly, the expression of senescence-associated genes (SAGs) was significantly upregulated in AtMINPP-OE but markedly decreased in atminpp/+. Yeast one-hybrid and chromatin immunoprecipitation assays indicated that the EIN3 transcription factor directly binds to the promoter of AtMINPP. Genetic analysis further revealed that AtMINPP-OE could accelerate the senescence of ein3-1eil1-3 mutants. These findings elucidate the mechanism by which AtMINPP regulates ethylene-induced leaf senescence in Arabidopsis, providing insights into the genetic manipulation of leaf senescence and plant growth.

Keywords: Arabidopsis; EIN3; ethylene; leaf senescence; multiple inositol polyphosphate phosphatase; senescence-associated genes.

MeSH terms

  • Arabidopsis Proteins* / genetics
  • Arabidopsis Proteins* / metabolism
  • Arabidopsis* / genetics
  • Arabidopsis* / growth & development
  • Arabidopsis* / metabolism
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Ethylenes* / metabolism
  • Gene Expression Regulation, Plant*
  • Phosphoric Monoester Hydrolases / genetics
  • Phosphoric Monoester Hydrolases / metabolism
  • Phytic Acid* / metabolism
  • Plant Leaves* / genetics
  • Plant Leaves* / growth & development
  • Plant Leaves* / metabolism
  • Plant Senescence / genetics
  • Promoter Regions, Genetic
  • Signal Transduction*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism

Substances

  • Ethylenes
  • Arabidopsis Proteins
  • ethylene
  • Phytic Acid
  • Phosphoric Monoester Hydrolases
  • Transcription Factors
  • EIN3 protein, Arabidopsis
  • DNA-Binding Proteins