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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.

Divergent Expression Patterns and Function of Two cxcr4 Paralogs in Hermaphroditic Epinephelus coioides