A thyroid hormone regulated asymmetric responsive centre is correlated with eye migration during flatfish metamorphosis

Abstract

Flatfish metamorphosis is a unique post-embryonic developmental event in which thyroid hormones (THs) drive the development of symmetric pelagic larva into asymmetric benthic juveniles. One of the eyes migrates to join the other eye on the opposite side of the head. Developmental mechanisms at the basis of the acquisition of flatfish anatomical asymmetry remain an open question. Here we demonstrate that an TH responsive asymmetric centre, determined by deiodinase 2 expression, ventrally juxtaposed to the migrating eye in sole (Solea senegalensis) correlates with asymmetric cranial ossification that in turn drives eye migration. Besides skin pigmentation that is asymmetric between dorsal and ventral sides, only the most anterior head region delimited by the eyes becomes asymmetric whereas the remainder of the head and organs therein stay symmetric. Sub-ocular ossification is common to all flatfish analysed to date, so we propose that this newly discovered mechanism is universal and is associated with eye migration in all flatfish.

The Role of the Thyroid Axis in Fish

“…In flatfish, pelagic larvae develop symmetrically with eyes on each side of the head, and morph into asymmetric benthic juveniles following the migration of one eye to the opposite side of the head to become right- or left-eyed, a species-specific distinction [e.g., right-eyed Atlantic halibut ( 187 ), left-eyed Japanese flounder ( 100 ) and left- or right-eyed Starry flounder ( 188 )]. In Senegalese sole ( Solea senegalensis ), increases in TH circulating levels, pituitary TSHβ, and whole body thyroglobulin and TR transcript levels ( 189 ) coincide with metamorphic climax and activity in thyroid follicles ( 190 ). Similarly, during Atlantic halibut metamorphosis, the vast majority of transcripts expressed in the head transcriptome are related to the thyroid axis ( 187 ).…”

Teleost Metamorphosis: The Role of Thyroid Hormone

“…The most likely scenario is that in some cells/tissues, metamorphic morphogenetic events are regulated by thraa, thrab , or thrb or even a combination of all or some TH receptors in a given cell/tissue. Nonetheless, in sole metamorphosis, the asymmetric development of the pseudomesial bone (discussed below) is correlated only with the asymmetric expression of thrb , strongly suggesting that, at least for this metamorphic event, thrb is the main effector of TH function (45). The actual scenario on the TH receptors mediating each metamorphic event is not clear and more work is necessary to elucidate this question in teleost metamorphosis.…”

“…During the larval stage, most cartilaginous structures are already present, but most of the dermal derived bones are still absent. Most dermal derived bones develop as metamorphosis starts, and most of the cartilaginous derived bone starts to transit from their cartilaginous scaffold into an ossified definitive structure during metamorphosis (11, 45, 105–118).…”

New Insights on Vitamin K Metabolism in Senegalese sole (Solea senegalensis) Based on Ontogenetic and Tissue-Specific Vitamin K Epoxide Reductase Molecular Data

“…Senegalese sole (Solea senegalensis) is a marine flatfish used to understand the molecular mechanisms of asymmetrical morphology [29,30], to conduct biomonitoring programs of coastal ecosystems [31,32], and is an important fish species for European aquaculture diversification [33]. As a result of the interest of both the industry and academia, the knowledge on optimal husbandry practices and environmental conditions, genetic background, and/or nutrition, has recently been improved (reviewed in Muñoz-Cueto et al [34]).…”