Abstract

Amphioxus is used to investigate the origin and evolution of vertebrates. To better understand the characteristics of genome evolution from cephalochordates to Osteichthyes, we conducted a genome-wide pairwise comparison of protein-coding genes within amphioxus (a comparable group) and parallel analyses within Osteichthyes (two comparable groups). A batch of fast-evolving genes in each comparable group was identified. Of these genes, the most fast-evolving genes (top 20) were scrutinized, most of which were involved in immune system. An analysis of the fast-evolving genes showed that they were enriched into gene ontology (GO) terms and pathways primarily involved in immune-related functions. Similarly, this phenomenon was detected within Osteichthyes, and more well-known and abundant GO terms and pathways involving innate immunity were found in Osteichthyes than in cephalochordates. Next, we measured the expression responses of four genes belonging to metabolism or energy production-related pathways to lipopolysaccharide challenge in the muscle, intestine or skin of B. belcheri; three of these genes (HMGCL, CYBS and MDH2) showed innate immune responses. Additionally, some genes involved in adaptive immunity showed fast evolution in Osteichthyes, such as those involving “intestinal immune network for IgA production” or “T-cell receptor signaling pathway”. In this study, the fast evolution of immune-related genes in amphioxus and Osteichthyes was determined, providing insights into the evolution of immune-related genes in chordates.

Highlights

  • Jawed vertebrates, such as Osteichthyes and mammals, have developed an elaborate adaptive immune system with diversified B-cell and T-cell antigen receptors (BCRs and TCRs) [1, 2]

  • We found that 130 and 138 gene ontology (GO) categories were significantly enriched for PFEG sets in Bf vs Bb based on the values of Ka and Ka/Ks, respectively (Table 1, Supplementary Tables 2 and 3); for the MFEG sets, 227 and 166 terms were significantly enriched

  • We found that 21 and 23 GO terms were overrepresented in the PFEG and MFEG sets of Dr vs Lc, respectively (Table 1, Supplementary Tables 6 and 7)

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Summary

Introduction

Jawed vertebrates, such as Osteichthyes and mammals, have developed an elaborate adaptive immune system with diversified B-cell and T-cell antigen receptors (BCRs and TCRs) [1, 2]. Jawless vertebrates, such as cyclostomes, have variable lymphocyte receptors (VLRs) with somatically rearranged LRR ectodomains [3, 4]. The adaptive immunity may be traced to an early stage of vertebrate evolution (Figure 1). Antigen receptors with naturally adaptive immune activity have not been found in amphioxus. The assumption is that cephalochordates strongly rely on the innate immune system according to our current knowledge [1, 7]

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