Golgi-localized APYRASE 1 is critical for Arabidopsis growth by affecting cell wall integrity under boron deficiency

Physiol Plant. 2024 May-Jun;176(3):e14320. doi: 10.1111/ppl.14320.

Abstract

Many nucleoside triphosphate-diphosphohydrolases (NTPDases/APYRASEs, APYs) play a key role in modulating extracellular nucleotide levels. However, the Golgi-localized APYs, which help control glycosylation, have rarely been studied. Here, we identified AtAPY1, a gene encoding an NTPDase in the Golgi apparatus, which is required for cell wall integrity and plant growth under boron (B) limited availability. Loss of function in AtAPY1 hindered cell elongation and division in root tips while increasing the number of cortical cell layers, leading to swelling of the root tip and abundant root hairs under low B stress. Further, expression pattern analysis revealed that B deficiency significantly induced AtAPY1, especially in the root meristem and stele. Fluorescent-labeled AtAPY1-GFP localized to the Golgi stack. Biochemical analysis showed that AtAPY1 exhibited a preference of UDP and GDP hydrolysis activities. Consequently, the loss of function in AtAPY1 might disturb the homoeostasis of NMP-driven NDP-sugar transport, which was closely related to the synthesis of cell wall polysaccharides. Further, cell wall-composition analysis showed that pectin content increased and borate-dimerized RG-II decreased in apy1 mutants, along with a decrease in cellulose content. Eventually, altered polysaccharide characteristics presumably cause growth defects in apy1 mutants under B deficiency. Altogether, these data strongly support a novel role for AtAPY1 in mediating responses to low B availability by regulating cell wall integrity.

MeSH terms

  • Apyrase* / genetics
  • Apyrase* / metabolism
  • Arabidopsis Proteins* / genetics
  • Arabidopsis Proteins* / metabolism
  • Arabidopsis* / enzymology
  • Arabidopsis* / genetics
  • Arabidopsis* / growth & development
  • Arabidopsis* / metabolism
  • Boron* / deficiency
  • Boron* / metabolism
  • Cell Wall* / metabolism
  • Gene Expression Regulation, Plant
  • Golgi Apparatus* / metabolism
  • Meristem / genetics
  • Meristem / growth & development
  • Meristem / metabolism
  • Pectins / metabolism
  • Plant Roots / genetics
  • Plant Roots / growth & development
  • Plant Roots / metabolism

Substances

  • Boron
  • Arabidopsis Proteins
  • Apyrase
  • APY1 protein, Arabidopsis
  • Pectins