Spo1, a phospholipase B homolog, is required for spindle pole body duplication during meiosis in Saccharomyces cerevisiae

Chromosoma. 2000;109(1-2):72-85. doi: 10.1007/s004120050414.

Abstract

The SPO1 gene was cloned and shown to encode an early meiotic transcript specifying a nuclear protein with extensive similarity to fungal and vertebrate phospholipase enzymes. Alteration of a conserved serine residue in the putative phospholipase active site, and presence of the spo1-1 temperature-sensitive mutation, which resides near this site, each result in loss of SPO1 function. The phenotype of a complete deletion indicates that SPO1 is dispensable for vegetative growth, premeiotic DNA synthesis and meiotic recombination. In contrast, it is required for Meiosis I (MI) and Meiosis II (MII) chromosome segregation and spore formation. In a null mutant approximately 75% of cells arrest early at MI spindle pole body (SPB) duplication, approximately 20% arrest at MII, and approximately 5% arrest at spore formation. Progression beyond the first arrest point suggests the existence of functions partially redundant to Spo1 and that Spo1 is required at multiple stages. At present SPO1 is the only known gene required for SPB duplication in meiosis but not in mitosis. Its product may thus play a regulatory (rather than a structural) role in SPB function. The transcriptional program in the spo1 null is similar to the wild type early in meiosis but is significantly delayed at later stages of sporulation. A single gene, CWP1, was recovered as a multicopy suppressor of the spo1 null. CWP1 encodes a cell wall protein with a glycolipid moiety. We propose that, when modified by other lipases, this moiety may substitute for the product(s) of Spo1p lipase activity in meiosis. Based on the similarity of Spo1p to phospholipase B enzymes, its unique role in SPB duplication, and pleiotropic effects on MII, late gene expression and spore formation, we propose that the Spo1 protein participates in a novel meiotic pathway that functions through the SPB to coordinate nuclear division with spore development.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Cell Nucleus / metabolism
  • DNA / biosynthesis
  • Fungal Proteins / antagonists & inhibitors
  • Fungal Proteins / biosynthesis
  • Fungal Proteins / genetics*
  • Gene Dosage
  • Gene Expression
  • Genes, Reporter
  • Lysophospholipase / genetics*
  • Meiosis / genetics*
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism
  • Mitosis / genetics
  • Molecular Sequence Data
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / metabolism
  • Recombination, Genetic
  • Saccharomyces cerevisiae / enzymology
  • Saccharomyces cerevisiae / genetics*
  • Saccharomyces cerevisiae Proteins*
  • Sequence Homology, Amino Acid
  • Spindle Apparatus / genetics*
  • Spores, Fungal / metabolism

Substances

  • CWP1 protein, S cerevisiae
  • Fungal Proteins
  • Membrane Glycoproteins
  • Recombinant Fusion Proteins
  • Saccharomyces cerevisiae Proteins
  • DNA
  • Lysophospholipase
  • SPO1 protein, S cerevisiae

Associated data

  • GENBANK/L39372