Regulatory elements of Caenorhabditis elegans ribosomal protein genes

BMC Genomics. 2012 Aug 28:13:433. doi: 10.1186/1471-2164-13-433.

Abstract

Background: Ribosomal protein genes (RPGs) are essential, tightly regulated, and highly expressed during embryonic development and cell growth. Even though their protein sequences are strongly conserved, their mechanism of regulation is not conserved across yeast, Drosophila, and vertebrates. A recent investigation of genomic sequences conserved across both nematode species and associated with different gene groups indicated the existence of several elements in the upstream regions of C. elegans RPGs, providing a new insight regarding the regulation of these genes in C. elegans.

Results: In this study, we performed an in-depth examination of C. elegans RPG regulation and found nine highly conserved motifs in the upstream regions of C. elegans RPGs using the motif discovery algorithm DME. Four motifs were partially similar to transcription factor binding sites from C. elegans, Drosophila, yeast, and human. One pair of these motifs was found to co-occur in the upstream regions of 250 transcripts including 22 RPGs. The distance between the two motifs displayed a complex frequency pattern that was related to their relative orientation.We tested the impact of three of these motifs on the expression of rpl-2 using a series of reporter gene constructs and showed that all three motifs are necessary to maintain the high natural expression level of this gene. One of the motifs was similar to the binding site of an orthologue of POP-1, and we showed that RNAi knockdown of pop-1 impacts the expression of rpl-2. We further determined the transcription start site of rpl-2 by 5' RACE and found that the motifs lie 40-90 bases upstream of the start site. We also found evidence that a noncoding RNA, contained within the outron of rpl-2, is co-transcribed with rpl-2 and cleaved during trans-splicing.

Conclusions: Our results indicate that C. elegans RPGs are regulated by a complex novel series of regulatory elements that is evolutionarily distinct from those of all other species examined up until now.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Base Sequence
  • Binding Sites
  • Caenorhabditis elegans / genetics*
  • Caenorhabditis elegans Proteins / genetics*
  • Conserved Sequence
  • DNA-Binding Proteins / genetics*
  • Gene Expression
  • Genes, Helminth*
  • High Mobility Group Proteins / genetics*
  • Promoter Regions, Genetic
  • RNA Interference
  • RNA, Small Interfering
  • Regulatory Elements, Transcriptional*
  • Regulatory Sequences, Nucleic Acid
  • Ribosomal Proteins / genetics*
  • Transcription Initiation Site

Substances

  • Caenorhabditis elegans Proteins
  • DNA-Binding Proteins
  • High Mobility Group Proteins
  • RNA, Small Interfering
  • Ribosomal Proteins
  • pop-1 protein, C elegans
  • ribosomal protein L2