Three foxg1 paralogues in lampreys and gnathostomes-brothers or cousins?

Galina V Ermakova; Alexander V Kucheryavyy; Nikolay S Mugue; Aleksandr V Mischenko; Andrey G Zaraisky; Andrey V Bayramov

doi:10.3389/fcell.2023.1321317

Three foxg1 paralogues in lampreys and gnathostomes-brothers or cousins?

Front Cell Dev Biol. 2024 Jan 2:11:1321317. doi: 10.3389/fcell.2023.1321317. eCollection 2023.

Authors

Galina V Ermakova¹, Alexander V Kucheryavyy², Nikolay S Mugue^{3

4}, Aleksandr V Mischenko⁵, Andrey G Zaraisky^{1

6}, Andrey V Bayramov¹

Affiliations

¹ Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, Moscow, Russia.
² Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, Russia.
³ Russian Federal Research Institute of Fisheries and Oceanography (VNIRO), Moscow, Russia.
⁴ Koltzov Institute of Developmental Biology of Russian Academy of Sciences, Moscow, Russia.
⁵ Branch for the Freshwater Fisheries of the Russian Federal Research Institute of Fisheries and Oceanography, Moscow, Russia.
⁶ Pirogov Russian National Research Medical University, Moscow, Russia.

Abstract

Foxg1 is a key regulator of the early development of the vertebrate forebrain and sensory organs. In this study, we describe for the first time three foxg1 paralogues in lamprey, representative of one of two basally diverged lineages of vertebrates-the agnathans. We also first describe three foxg1 genes in sterlet-representative of one of the evolutionarily ancient clades of gnathostomes. According to the analysis of local genomic synteny, three foxg1 genes of agnathans and gnathostomes have a common origin as a result of two rounds of genomic duplications in the early evolution of vertebrates. At the same time, it is difficult to reliably establish pairwise orthology between foxg1 genes of agnathans and gnathostomes based on the analysis of phylogeny and local genomic synteny, as well as our studies of the spatiotemporal expression of foxg1 genes in the river lamprey Lampetra fluviatilis and the sterlet Acipenser ruthenus. Thus, the appearance of three foxg1 paralogues in agnathans and gnathostomes could have occurred either as a result of two rounds of duplication of the vertebrate common ancestor genome (2R hypothesis) or as a result of the first common round followed by subsequent independent polyploidizations in two evolutionary lineages (1R hypothesis).

Keywords: forebrain development; foxg1; lamprey; sterlet; sturgeon; telencephalon.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by Russian Scientific Foundation grant No. 23-74-30005 to AZ.