A novel class of PTEN protein in Arabidopsis displays unusual phosphoinositide phosphatase activity and efficiently binds phosphatidic acid

Anne Pribat, Rodnay Sormani, Mathieu Rousseau-Gueutin, Magdalena M. Julkowska, Christa Testerink, Jerôme Joubès, Michel Castroviejo, Michel Laguerre, Christian Meyer, Véronique Germain*, Christophe Rothan

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

28 Citations (Scopus)

Abstract

PTEN (phosphatase and tensin homologue deleted on chromosome ten) proteins are dual phosphatases with both protein and phosphoinositide phosphatase activity. Theymodulate signalling pathways controlling growth, metabolism and apoptosis in animals and are implied in several human diseases. In the present paper we describe a novel class of PTEN proteins in plants, termed PTEN2, which comprises the AtPTEN (Arabidopsis PTEN) 2a and AtPTEN2b proteins in Arabidopsis. Both display low in vitro tyrosine phosphatase activity. In addition, AtPTEN2a actively dephosphorylates in vitro the 3′phosphate group of PI3P (phosphatidylinositol 3-phosphate), PI(3,4)P 2 (phosphatidylinositol 3,4-bisphosphate) and PI(3,5)P 2(phosphatidylinositol 3,5-bisphosphate). In contrast with animal PTENs, PI(3,4,5)P 3 (phosphatidylinositol 3,4,5-trisphosphate) is a poor substrate. Site-directed mutagenesis of AtPTEN2a and molecular modelling of protein-phosphoinositide interactions indicated that substitutions at the PTEN2 core catalytic site of the Lys 267 and Gly 268 residues found in animals, which are critical for animal PTENactivity, by Met 267 and Ala 268 found in the eudicot PTEN2 are responsible for changes in substrate specificity. Remarkably, the AtPTEN2a protein also displays strong binding activity for PA (phosphatidic acid), a major lipid second messenger in plants. Promoter::GUS (β-glucuronidase) fusion, transcript and protein analyses further showed the transcriptional regulation of the ubiquitously expressed AtPTEN2a and AtPTEN2b by salt and osmotic stress. The results of the present study suggest a function for this novel class of plant PTEN proteins as an effector of lipid signalling in plants.

Original languageEnglish
Pages (from-to)161-171
Number of pages11
JournalBiochemical Journal
Volume441
Issue number1
DOIs
Publication statusPublished - Jan 2012
Externally publishedYes

Keywords

  • Expression in planta
  • Phosphatidic acid (PA) binding
  • Phosphoinositide phosphatase
  • Phylogenetics
  • Site-directed mutagenesis

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