Genomic sequence analyses of classical and non-classical lamprey progesterone receptor genes and the inference of homologous gene evolution in metazoans

Jianfeng Ren,Yu-Wen Chung-Davidson,Liang Jia,Weiming Li

doi:10.1186/s12862-019-1463-7

Abstract

BackgroundNuclear progesterone receptor (nPR) is an evolutionary innovation in vertebrates that mediates genomic responses to progesterone. Vertebrates also respond to progesterone via membrane progesterone receptors (mPRs) or membrane associated progesterone receptors (MAPRs) through rapid nongenomic mechanisms. Lampreys are extant agnathan vertebrates, residing at the evolutionary juncture where vertebrates diverged from invertebrates. A survey of the progesterone receptor (PR) gene sequences in lamprey genomes would inform PR gene evolutionary events during the transition from invertebrates to vertebrates.ResultsIn this study, we annotated sequences of one nPR, four mPR (β, γ, δ and ε) and four MAPR genes from genomes of two lamprey species (Petromyzon marinus and Lethenteron japonicum). To infer the origin and evolutionary history of PR genes, we constructed phylogenetic trees of PR homologous sequences across representative species of metazoans. Phylogenetic analyses revealed that the mPRγ gene first appeared in non-bilaterians, and the mPRβ gene likely arose from a duplication of mPRγ. On the other hand, the mPRγ gene gave rise to the mPRδ and ε genes much later in the vertebrate lineage. In addition, the mPRα gene first appeared in cartilaginous fishes, likely derived from duplication of mPRβ after the agnathan-gnathostome divergence. All known MAPR genes were present in the lamprey genomes. Progesterone receptor membrane component 1 (PGRMC1), neudesin and neuferricin genes probably evolved in parallel in non-bilaterians, whereas two copies of PGRMC genes probably derived from duplication of ancestral PGRMC1 sequence and appeared before the speciation of lampreys.ConclusionsNon-classical mPR and MAPR genes first evolved in non-bilaterians and classical nPR genes evolved later in basal vertebrates. Sequence repertoires for membrane progesterone receptor genes in vertebrates likely originated from an ancestral metazoan sequence and expanded via several duplication events.

Highlights

Nuclear progesterone receptor is an evolutionary innovation in vertebrates that mediates genomic responses to progesterone
The 12 additional bp of the sea lamprey Nuclear progesterone receptor (nPR) gene were located in the fourth exon of the coding DNA sequence (CDS) region
Similar domains for Src homolog 2 (SH2) or Src homology 3 (SH3) interactions, kinase or kinase-binding were present in Membrane progestin receptor (mPR) or Membrane-associated progesterone receptor (MAPR) sequences. These findings indicate that mPRs, MAPRs and nPR may potentially recognize and interact with similar proteins in lampreys

Summary

Introduction

Nuclear progesterone receptor (nPR) is an evolutionary innovation in vertebrates that mediates genomic responses to progesterone. A survey of the progesterone receptor (PR) gene sequences in lamprey genomes would inform PR gene evolutionary events during the transition from invertebrates to vertebrates. Progesterone (P4) is one of the first discovered steroid hormones with known functions and subsequently pursued as a drug target [1]. It was initially discovered as a sex hormone, and later found to have broader effects, ranging from inhibition of apoptosis to regulation of cholesterol biosynthesis and axon guidance [2, 3]. The proteins encoded by mPRα, β and γ genes are typically coupled to a pertussis-sensitive inhibitory G protein (Gi) that inhibits adenylyl cyclase activity, resulting in a decrease in secondary messenger cAMP levels [18]. It is widely accepted that mPRs have specific and saturable high-affinity binding sites for P4 [19]

Methods

Results

Discussion

Conclusion