The protein expression landscape of mitosis and meiosis in diploid budding yeast

J Proteomics. 2017 Mar 6;156:5-19. doi: 10.1016/j.jprot.2016.12.016. Epub 2017 Jan 3.


Saccharomyces cerevisiae is an established model organism for the molecular analysis of fundamental biological processes. The genomes of numerous strains have been sequenced, and the transcriptome and proteome ofmajor phases during the haploid and diploid yeast life cycle have been determined. However, much less is known about dynamic changes of the proteome when cells switch from mitotic growth to meiotic development. We report a quantitative protein profiling analysis of yeast cell division and differentiation based on mass spectrometry. Information about protein levels was integrated with strand-specific tiling array expression data. We identified a total of 2366 proteins in at least one condition, including 175 proteins showing a statistically significant>5-fold change across the sample set, and 136 proteins detectable in sporulating but not respiring cells. We correlate protein expression patterns with biological processes and molecular function by Gene Ontology term enrichment, chemoprofiling, transcription interference and the formation of double stranded RNAs by overlapping sense/antisense transcripts. Our work provides initial quantitative insight into protein expression in diploid respiring and differentiating yeast cells. Critically, it associates developmentally regulated induction of antisense long noncoding RNAs and double stranded RNAs with fluctuating protein concentrations during growth and development.

Biological significance: This integrated genomics analysis helps better understand how the transcriptome and the proteome correlate in diploid yeast cells undergoing mitotic growth in the presence of acetate (respiration) versus meiotic differentiation (Meiosis I and II). The study (i) provides quantitative expression data for 2366 proteins and their cognate mRNAs in at least one sample, (ii) shows strongly fluctuating protein levels during growth and differentiation for 175 cases, and (iii) identifies 136 proteins absent in mitotic but present in meiotic yeast cells. We have integrated protein profiling data using mass spectrometry with tiling array RNA profiling data and information on double-stranded RNAs (dsRNAs) by overlapping sense/antisense transcripts from an RNA-Sequencing experiment. This work therefore provides quantitative insight into protein expression during cell division and development and associates changing protein levels with developmental stage specific induction of antisense transcripts and the formation of dsRNAs.

Keywords: Budding yeast; Double stranded RNAs; Long noncoding RNAs; Meiosis; Proteome; Respiration; Sporulation; Transcriptome.

MeSH terms

  • Cell Differentiation / genetics
  • Cell Division / genetics
  • Diploidy*
  • Gene Expression Profiling*
  • Mass Spectrometry
  • Meiosis / genetics*
  • Mitosis / genetics*
  • Proteome / analysis
  • Proteome / genetics
  • Proteomics / methods
  • RNA, Messenger / analysis
  • Saccharomyces cerevisiae / chemistry
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae / physiology
  • Saccharomyces cerevisiae Proteins / analysis*
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomycetales / chemistry
  • Saccharomycetales / genetics*
  • Saccharomycetales / physiology


  • Proteome
  • RNA, Messenger
  • Saccharomyces cerevisiae Proteins