Abstract

Pax genes play important roles in Metazoan development. Their evolution has been extensively studied but Lophotrochozoa are usually omitted. We addressed the question of Pax paralog diversity in Lophotrochozoa by a thorough review of available databases. The existence of six Pax families (Pax1/9, Pax2/5/8, Pax3/7, Pax4/6, Paxβ, PoxNeuro) was confirmed and the lophotrochozoan Paxβ subfamily was further characterized. Contrary to the pattern reported in chordates, the Pax2/5/8 family is devoid of homeodomain in Lophotrochozoa. Expression patterns of the three main pax classes (pax2/5/8, pax3/7, pax4/6) during Sepia officinalis development showed that Pax roles taken as ancestral and common in metazoans are modified in S. officinalis, most likely due to either the morphological specificities of cephalopods or to their direct development. Some expected expression patterns were missing (e.g. pax6 in the developing retina), and some expressions in unexpected tissues have been found (e.g. pax2/5/8 in dermal tissue and in gills). This study underlines the diversity and functional plasticity of Pax genes and illustrates the difficulty of using probable gene homology as strict indicator of homology between biological structures.

Highlights

  • Pax proteins belong to a family of transcription factors playing important roles in development of metazoans, from early specification of cell fate to body patterning through morphogenesis of various tissues and organs [1,2]

  • The sets used in these analyses were obtained by elimination of redundant sequences and sequences lacking important parts or whole paired domain (PRD) (e.g. 93 partial PRD sequences from various Cephalopoda and all putative eyg sequences)

  • The phylogenetic trees obtained with these different sets were comparable and confirmed the presence of the 6 Pax families in Lophotrochozoa proposed by Schmerer et al [12] (Fig 2)

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Summary

Introduction

Pax proteins belong to a family of transcription factors playing important roles in development of metazoans, from early specification of cell fate to body patterning through morphogenesis of various tissues and organs [1,2]. The evolution of Pax genes has been extensively studied and the availability of genomes has allowed for the identification of Pax genes in nearly 200 species of chordates in which duplication and subfunctionalization may have occurred several times [3]. Pax genes have been identified in non-chordates, but no exhaustive study of Pax gene evolution has been conducted regarding these clades. Lophotrochozoans, which comprise approximately 30% of all animal species, are usually omitted in studies of Pax gene evolution (see [4] as a recent example). Pax proteins are characterized by the presence of a DNA-binding domain of 128 aminoacids, referred to as the paired domain (PRD) (review in [5]). Other conserved domains may PLOS ONE | DOI:10.1371/journal.pone.0172719 March 2, 2017

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