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High nucleotide divergence in developmental regulatory genes contrasts with the structural elements of olfactory pathways in caenorhabditis.

ABSTRACT: Almost all organismal function is controlled by pathways composed of interacting genetic components. The relationship between pathway structure and the evolution of individual pathway components is not completely understood. For the nematode Caenorhabditis elegans, chemosensory pathways regulate critical aspects of an individual's life history and development. To help understand how olfaction evolves in Caenorhabditis and to examine patterns of gene evolution within transduction pathways in general, we analyzed nucleotide variation within and between species across two well-characterized olfactory pathways, including regulatory genes controlling the fate of the cells in which the pathways are expressed. In agreement with previous studies, we found much higher levels of polymorphism within C. remanei than within the related species C. elegans and C. briggsae. There are significant differences in the rates of nucleotide evolution for genes across the two pathways but no particular association between evolutionary rate and gene position, suggesting that the evolution of functional pathways must be considered within the context of broader gene network structure. However, developmental regulatory genes show both higher levels of divergence and polymorphism than the structural genes of the pathway. These results show that, contrary to the emerging paradigm in the evolution of development, important structural changes can accumulate in transcription factors.

SUBMITTER: Jovelin R

PROVIDER: S-EPMC2666507 | biostudies-literature | 2009 Apr

REPOSITORIES: biostudies-literature

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High nucleotide divergence in developmental regulatory genes contrasts with the structural elements of olfactory pathways in caenorhabditis.

Jovelin Richard R Dunham Joseph P JP Sung Frances S FS Phillips Patrick C PC

Genetics 20081110 4

Almost all organismal function is controlled by pathways composed of interacting genetic components. The relationship between pathway structure and the evolution of individual pathway components is not completely understood. For the nematode Caenorhabditis elegans, chemosensory pathways regulate critical aspects of an individual's life history and development. To help understand how olfaction evolves in Caenorhabditis and to examine patterns of gene evolution within transduction pathways in gene ...[more]

PMID: 19001295

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Project description: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.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.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.

Dataset Information

High nucleotide divergence in developmental regulatory genes contrasts with the structural elements of olfactory pathways in caenorhabditis.

Publications

High nucleotide divergence in developmental regulatory genes contrasts with the structural elements of olfactory pathways in caenorhabditis.

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