Expanded Expression of Pro-Neurogenic Factor SoxB1 during Larval Development of gastropod Lymnaea stagnalis Suggests Preadaptation to Prolonged Neurogenesis in Mollusca

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Expanded Expression of Pro-Neurogenic Factor SoxB1 during Larval Development of gastropod Lymnaea stagnalis Suggests Preadaptation to Prolonged Neurogenesis in Mollusca

Authors

Kurtova, A. I.; Finoshin, A. D.; Aparina, M. S.; Gazizova, G. R.; Kozlova, O. S.; Voronova, S. N.; Shagimardanova, E. I.; Voronezhskaya, E. E.; Ivashkin, E. G.

Abstract

The diversity in the organization of the nervous system in mollusks raises intriguing questions about its development and evolution. Our study aims to gain a deeper understanding of how the nervous system forms in Mollusca by examining the involvement of SoxB-family transcription factors in the early development of neurogenic zones. Specifically, we explore the expression patterns of two SoxB genes in the gastropod Lymnaea stagnalis, namely Ls-SoxB1 and Ls-SoxB2, across various developmental stages. Through a combination of in situ hybridization chain reaction, immunohistochemistry, and proliferation assays, we examine the dynamic spatial distribution of Ls-SoxB1 and Ls-SoxB2, with a particular emphasis on the formation of central ring ganglia and the identification of active proliferative zones. Our findings reveal that Ls-SoxB1 exhibits expanded ectodermal expression from the gastrula to the postmetamorphic stage, evident at both transcriptional and translational levels. Throughout larval development, Ls-SoxB1 is expressed in the ectoderm of the head, foot, and visceral complex, as well as in ganglia anlagen and sensory cells. In contrast, the expression of Ls-SoxB2 in the ectoderm is observed until the veliger stage, after which it persists in subepithelial layer cells and ganglia rudiments. Proliferation assay reveals a uniform distribution of dividing cells in the ectoderm at all developmental stages, indicating the absence of distinct neurogenic zones with increased proliferation in gastropods. Our findings highlight that Ls-SoxB1 exhibit widespread expression patterns in both location and time compared to other Lophotrochozoa species. This prolonged expression of SoxB genes in gastropods can be interpreted as a form of transcriptional neoteny, playing a crucial role in the diversification of nervous systems. Thus, it serves as a preadaptation to prolonged neurogenesis and an increase in the central nervous system complexity in Mollusca.

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