Transcriptome profiles of sturgeon lateral line electroreceptor and mechanoreceptor during regeneration

Abstract

Background The electrosensory ampullary organs (AOs) and mechanosensory neuromasts (NMs) found in sturgeon and some other non-neopterygian fish or amphibians are both originated from lateral line placodes. However, these two sensory organs have characteristic morphological and physiological differences. The molecular mechanisms for the specification of AOs and NMs are not clearly understood. Results We sequenced the transcriptome for neomycin treated sturgeon AOs and NMs in the early regeneration stages, and de novo assembled a sturgeon transcriptome. By comparing the gene expression differences among untreated AOs, NMs and general epithelia (EPs), we located some specific genes for these two sensory organs. In sturgeon lateral line, the voltage-gated calcium channels and voltage-gated potassium channels were predominant calcium and potassium channel subtypes, respectively. And by correlating gene expression with the regeneration process, we predicated several candidate key transcriptional regulation related genes might be involved in AOs and NMs regeneration. Conclusions Genes with specific expression in the two lateral line sensory organs suggests their important roles in mechanoreceptor and electroreceptor formation. The candidate transcriptional regulation related genes may be important for mechano- and electro- receptor specification, in a “dosage-related” manner. These results suggested the molecular basis for specification of these two sensory organs in sturgeon.

Identification of multiple transcription factor genes potentially involved in the development of electrosensory versus mechanosensory lateral line organs

“…Conversely, the neuromast-enriched dataset (Wang et al, 2020) included Insm1, which we found in sterlet to be ampullary organrestricted. Furthermore, the 'common' dataset (Wang et al, 2020) included genes whose expression in sterlet and paddlefish was either ampullary organ-specific (e.g., the voltagegated K + channel genes Kcna5 and Kcnab3, as well as Neurod4; this study; Modrell et al, 2017a), or mechanosensory-specific (e.g., Foxg1 and Isl1; this study). Overall, we think that the stage 45 Siberian sturgeon tissue dissections (Wang et al, 2020) were unable to separate ampullary organs and neuromasts completely.…”

“…Furthermore, the 'common' dataset (Wang et al, 2020) included genes whose expression in sterlet and paddlefish was either ampullary organ-specific (e.g., the voltagegated K + channel genes Kcna5 and Kcnab3, as well as Neurod4; this study; Modrell et al, 2017a), or mechanosensory-specific (e.g., Foxg1 and Isl1; this study). Overall, we think that the stage 45 Siberian sturgeon tissue dissections (Wang et al, 2020) were unable to separate ampullary organs and neuromasts completely. Like our own stage 46 paddlefish lateral line organ-enriched dataset (Modrell et al, 2017a), the stage 45 Siberian sturgeon datasets are not exhaustive (Wang et al, 2020): some of the genes whose expression we have validated in stage 45-46 sterlet and/or paddlefish lateral line organs were missing (e.g., Satb2, Sox2 and Sox8; this study; Modrell et al, 2017a).…”

“…While this work was ongoing, a differential RNA-seq study of regenerating ampullary organs and neuromasts in the Siberian sturgeon ( Acipenser baerii ) was published (Wang et al, 2020). This study compared dissected tissue samples containing stage 45 ampullary organs or neuromasts relative to general epidermis, which identified 2074 lateral line organ-enriched genes, of which 1418 were shared by ampullary organs and neuromasts; 539 were ampullary organ-enriched, and 117 were neuromast-enriched (Wang et al, 2020). The ’common’ stage 45 lateral line-organ dataset from the Siberian sturgeon (Wang et al, 2020) included many of the candidate genes encoding transcription factors and differentiation markers whose expression we have validated in both ampullary organs and neuromasts at stage 45-46 in paddlefish and/or sterlet, e.g.…”

“…This study compared dissected tissue samples containing stage 45 ampullary organs or neuromasts relative to general epidermis, which identified 2074 lateral line organ-enriched genes, of which 1418 were shared by ampullary organs and neuromasts; 539 were ampullary organ-enriched, and 117 were neuromast-enriched (Wang et al, 2020). The ’common’ stage 45 lateral line-organ dataset from the Siberian sturgeon (Wang et al, 2020) included many of the candidate genes encoding transcription factors and differentiation markers whose expression we have validated in both ampullary organs and neuromasts at stage 45-46 in paddlefish and/or sterlet, e.g. Six1 , Eya1 , Atoh1 , Pou4f3 , Gfi1 , Otof, and Cacna1d (Modrell et al, 2011b; Modrell et al, 2011a; Modrell et al, 2017a; this study).…”

“…Conversely, the neuromast-enriched dataset (Wang et al, 2020) included Insm1, which we found in sterlet to be ampullary organrestricted on the head (though expressed in trunk neuromasts). Furthermore, the 'common' dataset (Wang et al, 2020) included genes whose expression in sterlet and paddlefish was either ampullary organ-specific (e.g., the voltage-gated K + channel genes Kcna5 and Kcnab3, as well as Neurod4; this study; Modrell et al, 2017a), or mechanosensory-specific (e.g., Foxg1…”