Abstract
Paired box genes are conserved across animals and encode transcription factors playing key roles in development, especially neurogenesis.Pax6is a chief example for functional conservation required for eye development in most bilaterian lineages except chelicerates.Pax6is ancestrally linked and was shown to have interchangeable functions withPax2.Drosophila melanogaster Pax2plays an important role in the development of sensory hairs across the whole body. In addition, it is required for the differentiation of compound eyes, making it a prime candidate to study the genetic basis of arthropod sense organ development and diversification, as well as the role of Pax genes in eye development. Interestingly, in previous studies identification of cheliceratePax2was either neglected or failed. Here we report the expression of twoPax2orthologs in the common house spiderParasteatoda tepidariorum, a model organism for chelicerate development. The twoPax2orthologs most likely arose as a consequence of a whole genome duplication in the last common ancestor of spiders and scorpions.Pax2.1is expressed in the peripheral nervous system, including developing lateral eyes and external sensilla, as well as the ventral neuroectoderm ofP. tepidariorumembryos. This not only hints at a conserved dual role ofPax2/5/8orthologs in arthropod sense organ development but suggests that in chelicerates,Pax2could have acquired the role usually played byPax6. For the other paralog,Pt-Pax2.2, expression was detected in the brain, but not in the lateral eyes and the expression pattern associated with sensory hairs differs in timing, pattern, and strength. To achieve a broader phylogenetic sampling, we also studied the expression of bothPax2genes in the haplogyne cellar spiderPholcus phalangioides. We found that the expression difference between paralogs is even more extreme in this species, sincePp-Pax2.2shows an interesting expression pattern in the ventral neuroectoderm while the expression in the prosomal appendages is strictly mesodermal. This expression divergence indicates both sub- and neofunctionalization afterPax2duplication in spiders and thus presents an opportunity to study the evolution of functional divergence after gene duplication and its impact on sense organ diversification.
Highlights
Paired box (Pax) family transcription factors are among the oldest genetic toolkit components required for animal development, as they were likely already present in the last common ancestor of metazoans (Hoshiyama et al, 1998)
The high sequence conservation between these distant groups was pointedly proven when murine Pax6 was shown to be able to induce ectopic eye formation in the fruit fly Drosophila melanogaster (Halder et al, 1995). While these findings suggest that Pax6 was involved in sense organ development in the last common ancestor of bilaterians, the subsequent discovery of a Pax6-related gene expressed in the developing eyes of a cubozoan jellyfish points to an even deeper conservation (Kozmik et al, 2003)
We find a Pax2.1 specific change from Valine to Methionine following the highly conserved GRPLPD sequence
Summary
Paired box (Pax) family transcription factors are among the oldest genetic toolkit components required for animal development, as they were likely already present in the last common ancestor of metazoans (Hoshiyama et al, 1998) Among their diverse functions, Pax genes are best known for their involvement in neurogenesis. Current phylogenetic analyses group bilaterian Pax genes into seven main subfamilies: Pax1/9, Pax2/5/8, Pax3/7, Pax4/6/10, Pox neuro, Pax eyegone, and Paxa/β (Hill et al, 2010; Franke et al, 2015; Friedrich, 2015) They are all characterized by the presence of a unique N-terminal sequence, encoding the DNA-binding Paired domain (PD) (Bopp et al, 1986). The octapeptide sequence, a highly conserved stretch of eight amino acids of unknown function, is located in between the two binding domains of Pax1/9, Pax2/5/8, and Pax3/7 group genes (Burri et al, 1989; Dressler et al, 1990)
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