Characterizing the role of PP2A B'' family subunits in mechanical stress response and plant development through calcium and ABA signaling in Arabidopsis thaliana

PLoS One. 2024 Nov 14;19(11):e0313590. doi: 10.1371/journal.pone.0313590. eCollection 2024.

Abstract

Protein phosphatase 2AB'' (PP2A B'') family subunits have calcium-binding EF-hand motifs, facilitating interaction with PP2A substrates. In Arabidopsis thaliana, the PP2A B'' family subunits consist of six members, AtB''α-ε and FASS. These subunits can interact with a basic leucine zipper transcription factor, VIP1, and its close homologs. Mechanical stress triggers PP2A-mediated dephosphorylation of VIP1 and its close homologs, leading to nuclear localization and gene upregulation to alleviate touch-induced root bending and leaf damage. However, the physiological roles of PP2A B'' family subunits in the mechanical stress response in Arabidopsis remain unclear. This study aims to characterize such roles. A quadruple knockout mutant with T-DNA insertions in AtB''α, AtB''β, AtB''γ, and AtB''δ was generated. atb''αβγδ mutants exhibited no significant damage upon brushing or touch-induced root bending compared to the wild type. Transcriptome analysis showed a significant decrease in the expression of CYP707A3, a gene potentially targeted by VIP1 that regulates abscisic acid (ABA) catabolism, in the atb''αβγδ mutant compared to wild type leaves. However, other genes, including XTH23, EXLA1, and CYP707A1, also VIP1 targets, exhibited similar induction in both brushed atb''αβγδ mutants and wild type leaves. We observed an enrichment of the CAMTA motif, CGCG(C/T) in the promoters of genes showing downregulated expression levels in brushed atb''αβγδ leaves compared to brushed wild type leaves. These findings suggest that PP2A B'' family subunits exhibit functional redundancy in the VIP1-dependent pathway but influence CAMTA-dependent gene expression under mechanical stress. Under calcium-deficient and ABA-supplemented conditions, growth of atb''αβγδ seedlings was retarded when compared to wild type and single knockout mutants, atb''γ and atb''δ, indicating a crucial role in plant development by modulating calcium or ABA signaling.

MeSH terms

  • Abscisic Acid* / metabolism
  • Arabidopsis Proteins* / genetics
  • Arabidopsis Proteins* / metabolism
  • Arabidopsis* / genetics
  • Arabidopsis* / growth & development
  • Arabidopsis* / metabolism
  • Arabidopsis* / physiology
  • Basic-Leucine Zipper Transcription Factors / genetics
  • Basic-Leucine Zipper Transcription Factors / metabolism
  • Calcium / metabolism
  • Calcium Signaling
  • Gene Expression Regulation, Plant*
  • Plant Roots / genetics
  • Plant Roots / growth & development
  • Plant Roots / metabolism
  • Protein Phosphatase 2 / genetics
  • Protein Phosphatase 2 / metabolism
  • Protein Subunits / genetics
  • Protein Subunits / metabolism
  • Signal Transduction
  • Stress, Mechanical

Substances

  • Abscisic Acid
  • Arabidopsis Proteins
  • Calcium
  • Protein Phosphatase 2
  • PP2A protein, Arabidopsis
  • VIP1 protein, Arabidopsis
  • Protein Subunits
  • Basic-Leucine Zipper Transcription Factors

Grants and funding

This work was supported by a Kakenhi grant (grant number: 23K19293) from Japan Society for the Promotion of Science (JSPS).