Polyploidization and pseudogenization in allotetraploid frog Xenopus laevis promote the evolution of aquaporin family in higher vertebrates

Abstract

Background: Aquaporins (AQPs), as members of the major intrinsic protein (MIP) superfamily, facilitated the permeation of water and other solutes and are involved in multiple biological processes. AQP family exists in almost all living organisms and is highly diversified in vertebrates in both classification and function due to genome wide duplication. While some AQP orthologs have been lost in higher vertebrates through evolution. Result: Genome-wide comparative analyses of the AQP family between allotetraploid frog Xenopus laevis (Xla) and diploid frog Xenopus tropicalis (Xtr), based on the genome assemblies, revealed that the number of AQPs in Xla genome nearly doubled that in Xtr (32 vs. 19). Synteny analysis indicated that the distribution of the retained AQPs in Xla subgenomes (17 in Xla. L, the longer homeolog of Xla genome and 15 in Xla. S, the shorter homeolog of Xla genome) were highly symmetrical when compared with that in Xtr genome. Remarkably, two members in Xla. L and four members in Xla. S were lost through evolution. Blast analysis revealed that the lost AQPs in Xla are pseudogenized via either the deletion of some exons or some single nucleotide insertions or deletions that lead the reading frame shift. Additionally, comparative genomic analyses suggested that the orthologs of AQPs that with one copy absence in Xla are also prone to be lost in higher vertebrates. Conclusion: This study revealed that polyploidization and subsequent pseudogenization and deletion in Xla genome promote the evolution of AQP family in higher vertebrates. Besides, our results would also contribute to understanding the evolution of AQP family.

Ventx Family and Its Functional Similarities with Nanog: Involvement in Embryonic Development and Cancer Progression

“…X. laevis thus provides a model for testing theories of whole genome duplication and significance, as its tetraploidization is neither too recent for studying the functions of a duplicated locus nor too ancient for measuring the impacts of single-nucleotide polymorphisms (SNPs) [4]. In addition, a recent genome-wide comparative study of aquaporins (AQPs) in allotetraploid X. laevis and diploid X. tropicalis revealed that the number of AQPs in X. laevis was nearly double (32) that of X. tropicalis (19) [3]. Meanwhile, a synteny-based analysis showed that the L-subgenome contained 17 AQPs, while the shorter S-subgenome had 15 AQPs.…”

“…These lost members are pseudogenized via either exon deletion or frameshift insertion and deletion. The merging of two ancestral genomes in the allotetraploid Xenopus laevis and the evolution of nonfunctional gene-duplication has indicated that Xenopus laevis is a pseudo-allotetraploid organism [2,3,[5][6][7]55,57]. Consequently, the allotetraploidy of Xenopus laevis genome has become an important model in which to study polyploidy and aneuploidy formation.…”

“…Xenopus laevis is an established animal model for studying vertebrate development, neurobiology, immunology, cell biology, and toxicology [ 1 , 2 ]. Xenopus is a pseudo-tetraploidy organism [ 3 , 4 ]. Its genome tetraploidy arose from the merging of two progenitor ancestral frog genomes millions of years ago [ 3 , 4 , 5 , 6 ].…”

“…Xenopus is a pseudo-tetraploidy organism [ 3 , 4 ]. Its genome tetraploidy arose from the merging of two progenitor ancestral frog genomes millions of years ago [ 3 , 4 , 5 , 6 ]. During genome evolution, the Xenopus laevis genome was subdivided into a longer subgenome (L-subgenome) and a shorter subgenome (S-subgenome).…”

The alternative transcription and expression characterization of Dmc1 in autotetraploid Carassius auratus

“…Frontiers in Genetics frontiersin.org that given the fish-specific whole-genome duplication (FSGD) process, compared with Dmc1-1, Dmc1-2 has been structurally mutated and expression-silenced resulting in its pseudogenization in RCC. The pseudogenization has been considered a special-evolutionary "Relic" in which the retention or elimination contributed to the genome evolution (Seixas et al, 2007;Jia and Liu, 2020). Moreover, in 4nRR, beyond the two original Dmc1 (Dmc1-1 and Dmc1-2) from RCC, two duplicated Dmc1 with different DNA lengths and sequences were identified, signifying that the Dmc1-3 and Dmc1-4 were induced underlying the autotetraploidization.…”