Abstract
Chemokine receptor Cxcr4 evolved two paralogs in the teleost lineage. However, cxcr4a and cxcr4b have been characterized only in a few species. In this study, we identified two cxcr4 paralogs from the orange-spotted grouper, Epinephelus coioides. The phylogenetic relationship and gene structure and synteny suggest that the duplicated cxcr4a/b should result from the teleost-specific genome duplication (Ts3R). The teleost cxcr4 gene clusters in two paralogous chromosomes exhibit a complementary gene loss/retention pattern. Ec_cxcr4a and Ec_cxcr4b show differential and biased expression patterns in grouper adult tissue, gonads, and embryos at different stages. During embryogenesis, Ec_cxcr4a/b are abundantly transcribed from the neurula stage and mainly expressed in the neural plate and sensory organs, indicating their roles in neurogenesis. Ec_Cxcr4a and Ec_Cxcr4b possess different chemotactic migratory abilities from the human SDF-1α, Ec_Cxcl12a, and Ec_Cxcl12b. Moreover, we uncovered the N-terminus and TM5 domain as the key elements for specific ligand–receptor recognition of Ec_Cxcr4a-Ec_Cxcl12b and Ec_Cxcr4b-Ec_Cxcl12a. Based on the biased and divergent expression patterns of Eccxcr4a/b, and specific ligand–receptor recognition of Ec_Cxcl12a/b–Ec_Cxcr4b/a, the current study provides a paradigm of sub-functionalization of two teleost paralogs after Ts3R.
Highlights
Chemokine receptors belong to the largest rhodopsin family of G-protein coupled receptors (GPCR) [1,2] and are considered an evolutionary innovations in vertebrate [3]
In addition to the two rounds of whole genome duplication (WGD) that occurred at the root of vertebrate lineage, the fish-specific genome duplication that occurred in a teleost ancestor gave dramatic rise and rapid radiation to teleost fish [50,51,52,53,54,55]
Coelacanth and spotted gar diverged from teleosts before Ts3R [51,56], and have only a single cxcr4 gene that falls outside the branches of teleost cxcr4s (Figure 2)
Summary
Chemokine receptors belong to the largest rhodopsin family of G-protein coupled receptors (GPCR) [1,2] and are considered an evolutionary innovations in vertebrate [3]. Accompanied by the emergence of thymopoiesis in jawed vertebrates, CXCL12-CXCR4 is one of the most ancient chemokine ligand–receptor in vertebrates [3,10,11] and it participates in angiogenesis, lymphopoiesis, neurogenesis, myelopoiesis, germ cell development, and so on [12,13,14,15,16,17,18]. The expression and function of cxcl12s-cxcr4s have been well documented in zebrafish [4]. Detailed research on comparative synteny and evolution analysis, and divergent expression patterns and function of the two cxcr paralogs in teleost is scarce
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