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

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

BMC Evol Biol. 2019 Jul 1;19(1):136. doi: 10.1186/s12862-019-1463-7.

Authors

Jianfeng Ren^{1

2

3}, Yu-Wen Chung-Davidson⁴, Liang Jia¹, Weiming Li⁵

Affiliations

¹ International Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, 201306, China.
² Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai, 201306, China.
³ Key Laboratory of Freshwater Aquatic Genetic Resources, Ministry of Agriculture, Shanghai Ocean University, Shanghai, 201306, China.
⁴ Department of Fisheries and Wildlife, Michigan State University, East Lansing, MI, 48824, USA.
⁵ Department of Fisheries and Wildlife, Michigan State University, East Lansing, MI, 48824, USA. liweim@msu.edu.

Abstract

Background: Nuclear 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.

Results: In 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.

Conclusions: Non-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.

Keywords: Evolution; Lamprey; Membrane associated progesterone receptor; Membrane progesterone receptor; Metazoan; Nuclear progesterone receptor.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Evolution, Molecular*
Genomics*
Petromyzon / genetics*
Phylogeny
Receptors, Progesterone / genetics*
Sequence Homology, Nucleic Acid*

Substances

Receptors, Progesterone