Amphioxus SYCP1: a case of retrogene replacement and co-option of regulatory elements adjacent to the ParaHox cluster

Myles G Garstang,David E K Ferrier

doi:10.1007/s00427-017-0600-9

Abstract

Retrogenes are formed when an mRNA is reverse-transcribed and reinserted into the genome in a location unrelated to the original locus. If this retrocopy inserts into a transcriptionally favourable locus and is able to carry out its original function, it can, in rare cases, lead to retrogene replacement. This involves the original, often multi-exonic, parental copy being lost whilst the newer single-exon retrogene copy ‘replaces’ the role of the ancestral parent gene. One example of this is amphioxus SYCP1, a gene that encodes a protein used in synaptonemal complex formation during meiosis and which offers the opportunity to examine how a retrogene evolves after the retrogene replacement event. SYCP1 genes exist as large multi-exonic genes in most animals. AmphiSYCP1, however, contains a single coding exon of ~ 3200 bp and has inserted next to the ParaHox cluster of amphioxus, whilst the multi-exonic ancestral parental copy has been lost. Here, we show that AmphiSYCP1 has not only replaced its parental copy, but also has evolved additional regulatory function by co-opting a bidirectional promoter from the nearby AmphiCHIC gene. AmphiSYCP1 has also evolved a de novo, multi-exonic 5′untranslated region that displays distinct regulatory states, in the form of two different isoforms, and has evolved novel expression patterns during amphioxus embryogenesis in addition to its ancestral role in meiosis. The absence of ParaHox-like expression of AmphiSYCP1, despite its proximity to the ParaHox cluster, also suggests that this gene is not influenced by any potential pan-cluster regulatory mechanisms, which are seemingly restricted to only the ParaHox genes themselves.

Highlights

Synaptonemal complex protein 1 (SYCP1) belongs to a group of proteins that form the synaptonemal complex, which is crucial to the process of meiotic recombination (Page and Hawley 2004; Zickler and Kleckner 1999)
The single-coding-exon organisation of amphioxus SYCP1 genes is in stark contrast to the multi-exonic arrangement of SYCP1 genes in most other species (Table S1), consistent with the amphioxus gene originating via retrogene replacement
The position of amphioxus SYCP1 genes is given relative to the flanking CHIC and Gsx genes in Fig. 1 for B. floridae (Fig. 1a), B. lanceolatum (Fig. 1b) and B.belcheri (Fig. 1c)

Summary

Introduction

Synaptonemal complex protein 1 (SYCP1) belongs to a group of proteins that form the synaptonemal complex, which is crucial to the process of meiotic recombination (Page and Hawley 2004; Zickler and Kleckner 1999). Due to its crucial role in meiosis, SYCP1 expression is observed within the germ cells of vertebrates (Iwai et al 2006; Zheng et al 2009) and within the basal-most cells of the Hydra testis, highlighting this deeply conserved role of SYCP1 in meiosis (Fraune et al 2012a). This localisation of SYCP1 to the germ cells is such that a promoter fragment of

Methods

Results

Discussion

Conclusion