Abstract

BackgroundIntraflagellar transport (IFT) genes, which are critical for the development and function of cilia and flagella in metazoans, are tightly regulated by the Regulatory Factor X (RFX) transcription factors (TFs). However, how and when their evolutionary relationship was established remains unknown.ResultsWe have identified evidence suggesting that RFX TFs and IFT genes evolved independently and their evolution converged before the first appearance of metazoans. Both ciliary genes and RFX TFs exist in all metazoans as well as some unicellular eukaryotes. However, while RFX TFs and IFT genes are found simultaneously in all sequenced metazoan genomes, RFX TFs do not co-exist with IFT genes in most pre-metazoans and thus do not regulate them in these organisms. For example, neither the budding yeast nor the fission yeast possesses cilia although both have well-defined RFX TFs. Conversely, most unicellular eukaryotes, including the green alga Chlamydomonas reinhardtii, have typical cilia and well conserved IFT genes but lack RFX TFs. Outside of metazoans, RFX TFs and IFT genes co-exist only in choanoflagellates including M. brevicollis, and only one fungus Allomyces macrogynus of the 51 sequenced fungus genomes. M. brevicollis has two putative RFX genes and a full complement of ciliary genes.ConclusionsThe evolution of RFX TFs and IFT genes were independent in pre-metazoans. We propose that their convergence in evolution, or the acquired transcriptional regulation of IFT genes by RFX TFs, played a pivotal role in the establishment of metazoan.

Highlights

  • Intraflagellar transport (IFT) genes, which are critical for the development and function of cilia and flagella in metazoans, are tightly regulated by the Regulatory Factor X (RFX) transcription factors (TFs)

  • Ciliary defects have been associated with defective development in the nematode Caenorhabditis elegans [3] as well as a growing list of devastating human genetic disease conditions collectively called ciliopathies, including polycystic kidney disease (PKD), Bardet-Biedl syndrome (BBS), Alstrome syndrome, Jou* Correspondence: chenn@sfu.ca

  • In addition to the RFX TFs that have been reported previously, including seven RFX TFs found in mammals [16], DAF-19 in C. elegans [3], and dRFX [13], we found many RFX genes that have not been described previously

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Summary

Introduction

Intraflagellar transport (IFT) genes, which are critical for the development and function of cilia and flagella in metazoans, are tightly regulated by the Regulatory Factor X (RFX) transcription factors (TFs). All metazoans and many unicellular eukaryotes have functional cilia ( known as flagella) [1]. Both motile and immotile cilia ( known as sensory or primary cilia) hold many receptors for sensing environmental signals. It is not surprising that cilia and most ciliary genes are deeply conserved, both in structure and function, in the "tree of life". Such high levels of conservation suggest a common evolutionary origin [1].

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