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

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.

Dynamic and Differential Expression of Duplicated Cxcr4/Cxcl12 Genes Facilitates Antiviral Response in Hexaploid Gibel Carp

“…In gibel carp, both paralogous and homoeologous pairs of cxcr4b and cxcl12a show dynamic and differential expression patterns and antiviral responses. Our results indicate that cxcr4bs and cxcl12as should play a dominant role in immune response and confirm the specific ligand-receptor recognitions of Cxcl12b and Cxcr4a ( 48 , 70 ). Although derived from the common ancestor ( 71 ), the expression patterns of duplicated genes evolved divergently after separation.…”

“…More abundant Cgcxcr4a-A transcripts than Cgcxcr4a-B were detected in head kidney, kidney, gill and heart, while reversely differential expression patterns were observed in spleen, thymus, and intestine ( Figure 3A). Consistent with the specific chemotactic interaction of grouper Cxcr4b-Cxcl12a (48), Cgcxcl12a was the mainly expressed paralog in most analyzed immune-related tissues, as well as Cgcxcr4b (Figure 3B). Except in intestine and brain, Cgcxcl12a-B showed significantly higher expression than Cgcxcl12a-A ( Figure 3B).…”

Functional Divergence of Multiple Duplicated Foxl2 Homeologs and Alleles in a Recurrent Polyploid Fish

“…One microgram plasmids were transfected into HEK293T cells. The cell culture, transfection, fixation, and nuclear staining with 4′, 6-diamidino-2-phenylindole (DAPI) were performed as previously described ( Lu et al. 2018 ).…”

Crosstalk Between Retinoic Acid and Sex-Related Genes Controls Germ Cell Fate and Gametogenesis in Medaka

“…The SDF1/CXCR4 signaling is known to be required for the maintenance of mouse spermatogonial stem cells, and inhibition of CXCR4 signaling increases the responsiveness of the germ cells to RA (Yang et al, 2013 ). In addition, study in Orange-spotted grouper demonstrated that the expression of cxcr4b gene is sharply decreased in mature ovary (Lu et al, 2018 ). In cyp26a1 mutant testis, the orphan nuclear receptor 4A1 ( nr4a1 ) was strongly upregulated.…”