Callose deficiency modulates plasmodesmata frequency and extracellular distance in rice pollen mother and tapetal cells

Ann Bot. 2024 Dec 31;134(6):1013-1026. doi: 10.1093/aob/mcae137.

Abstract

Background and aims: Fertilization relies on pollen mother cells able to transition from mitosis to meiosis to supply gametes. This process involves remarkable changes at the molecular, cellular and physiological levels, including (but not limited to) remodelling of the cell wall. During the onset of meiosis, the cellulose content in the pollen mother cell walls gradually declines, with the concurrent deposition of the polysaccharide callose in anther locules. We aim to understand the biological significance of cellulose-to-callose turnover in pollen mother cells walls.

Methods: We carried out electron microscopic, aniline blue and renaissance staining analyses of rice flowers.

Key results: Our observations indicate that in wild-type rice anthers, the mitosis-to-meiosis transition coincides with a gradual reduction in the number of cytoplasmic connections called plasmodesmata. A mutant in the Oryza sativa callose synthase GSL5 (Osgsl5-3), impaired in callose accumulation in premeiotic and meiotic anthers, displayed a greater reduction in plasmodesmata frequency among pollen mother cells and tapetal cells, suggesting a role for callose in maintenance of plasmodesmata. In addition, a significant increase in extracellular distance between pollen mother cells and impaired premeiotic cell shaping was observed in the Osgsl5-3 mutant.

Conclusions: The results suggest that callose-to-cellulose turnover during the transition from mitosis to meiosis is necessary to maintain cell-to-cell connections and optimal extracellular distance among the central anther locular cells. The findings of this study contribute to our understanding of the regulatory influence of callose metabolism during initiation of meiosis in flowering plants.

Keywords: Oryza sativa; Anther; callose; cell wall; cellulose; extracellular distance; meiosis; plasmodesmata; pollen mother cells.

MeSH terms

  • Cell Wall / metabolism
  • Cellulose / metabolism
  • Flowers / genetics
  • Flowers / metabolism
  • Flowers / physiology
  • Glucans* / metabolism
  • Glucosyltransferases / genetics
  • Glucosyltransferases / metabolism
  • Meiosis / physiology
  • Mutation
  • Oryza* / genetics
  • Oryza* / metabolism
  • Oryza* / physiology
  • Plasmodesmata* / metabolism
  • Plasmodesmata* / physiology
  • Pollen* / metabolism
  • Pollen* / physiology
  • Pollen* / ultrastructure

Substances

  • Glucans
  • callose
  • Cellulose
  • Glucosyltransferases