SoxB1 transcription factors are essential for initiating and maintaining the neural plate border gene expression

Schock, Elizabeth N.; York, Joshua R.; Li, Austin P.; Tu, Ashlyn Y.; LaBonne, Carole

doi:10.1101/2023.09.28.560033

Cited by 2 publications

(2 citation statements)

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“…For example, in Drosophila , SoxNeuro (ortholog of SoxB1) takes part in shaping the denticles in the embryonic epidermis ( Rizzo and Bejsovec, 2017 ). In Xenopus , Sox3 (one of SoxB1 orthologs in vertebrates) is an important factor in the differentiation of non-neural ectodermal cells in the neural plate border ( Schock et al, 2023 ). However, unlike in the gastropod, these events take place in limited sites of the embryonic ectoderm only, and do not expand to the later developmental stages.…”

Section: Discussionmentioning

confidence: 99%

Expanded expression of pro-neurogenic factor SoxB1 during larval development of gastropod Lymnaea stagnalis suggests preadaptation to prolonged neurogenesis in Mollusca

Kurtova,

Finoshin,

Aparina

et al. 2024

Front. Neurosci.

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IntroductionThe remarkable diversity observed in the structure and development of the molluscan nervous system raises intriguing questions regarding the molecular mechanisms underlying neurogenesis in Mollusca. The expression of SoxB family transcription factors plays a pivotal role in neuronal development, thereby offering valuable insights into the strategies of neurogenesis.MethodsIn this study, we conducted gene expression analysis focusing on SoxB-family transcription factors during early neurogenesis in the gastropod Lymnaea stagnalis. We employed a combination of hybridization chain reaction in situ hybridization (HCR-ISH), immunocytochemistry, confocal microscopy, and cell proliferation assays to investigate the spatial and temporal expression patterns of LsSoxB1 and LsSoxB2 from the gastrula stage to hatching, with particular attention to the formation of central ring ganglia.ResultsOur investigation reveals that LsSoxB1 demonstrates expanded ectodermal expression from the gastrula to the hatching stage, whereas expression of LsSoxB2 in the ectoderm ceases by the veliger stage. LsSoxB1 is expressed in the ectoderm of the head, foot, and visceral complex, as well as in forming ganglia and sensory cells. Conversely, LsSoxB2 is mostly restricted to the subepithelial layer and forming ganglia cells during metamorphosis. Proliferation assays indicate a uniform distribution of dividing cells in the ectoderm across all developmental stages, suggesting the absence of distinct neurogenic zones with increased proliferation in gastropods.DiscussionOur findings reveal a spatially and temporally extended pattern of SoxB1 expression in a gastropod representative compared to other lophotrochozoan species. This prolonged and widespread expression of SoxB genes may be interpreted as a form of transcriptional neoteny, representing a preadaptation to prolonged neurogenesis. Consequently, it could contribute to the diversification of nervous systems in gastropods and lead to an increase in the complexity of the central nervous system in Mollusca.

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Section: Discussionmentioning

confidence: 99%

Expanded expression of pro-neurogenic factor SoxB1 during larval development of gastropod Lymnaea stagnalis suggests preadaptation to prolonged neurogenesis in Mollusca

Kurtova,

Finoshin,

Aparina

et al. 2024

Front. Neurosci.

View full text Add to dashboard Cite

show abstract

“…For example, in Drosophila , SoxNeuro (ortholog of SoxB1) takes part in shaping the denticles in the embryonic epidermis (Rizzo and Bejsovec, 2017). In Xenopus , Sox3 (one of SoxB1 orthologs in vertebrates) is an important factor in the differentiation of non-neural ectodermal cells in the neural plate border (Schock et al, 2023). However, unlike in the gastropod, these events take place in limited sites of the embryonic epithelium only, and don’t expand to the later developmental stages.…”

Section: Discussionmentioning

confidence: 99%

Expanded Expression of Pro-Neurogenic Factor SoxB1 during Larval Development of GastropodLymnaea stagnalisSuggests Preadaptation to Prolonged Neurogenesis in Mollusca

Kurtova,

Finoshin,

Aparina

et al. 2023

Preprint

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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 gastropodLymnaea 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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SoxB1 transcription factors are essential for initiating and maintaining the neural plate border gene expression

Cited by 2 publications

References 73 publications

Expanded expression of pro-neurogenic factor SoxB1 during larval development of gastropod Lymnaea stagnalis suggests preadaptation to prolonged neurogenesis in Mollusca

Expanded expression of pro-neurogenic factor SoxB1 during larval development of gastropod Lymnaea stagnalis suggests preadaptation to prolonged neurogenesis in Mollusca

Expanded Expression of Pro-Neurogenic Factor SoxB1 during Larval Development of GastropodLymnaea stagnalisSuggests Preadaptation to Prolonged Neurogenesis in Mollusca

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