The genome and transcriptome of Japanese flounder provide insights into flatfish asymmetry

Abstract

9 l e t t e r sFlatfish have the most extreme asymmetric body morphology of vertebrates. During metamorphosis, one eye migrates to the contralateral side of the skull, and this migration is accompanied by extensive craniofacial transformations and simultaneous development of lopsided body pigmentation 1-5 . The evolution of this developmental and physiological innovation remains enigmatic. Comparative genomics of two flatfish and transcriptomic analyses during metamorphosis point to a role for thyroid hormone and retinoic acid signaling, as well as phototransduction pathways. We demonstrate that retinoic acid is critical in establishing asymmetric pigmentation and, via cross-talk with thyroid hormones, in modulating eye migration. The unexpected expression of the visual opsins from the phototransduction pathway in the skin translates illumination differences and generates retinoic acid gradients that underlie the generation of asymmetry. Identifying the genetic underpinning of this unique developmental process answers long-standing questions about the evolutionary origin of asymmetry, but it also provides insight into the mechanisms that control body shape in vertebrates.

Highly dense linkage maps from 31 full-sibling families of turbot (Scophthalmus maximus) provide insights into recombination patterns and chromosome rearrangements throughout a newly refined genome assembly

“…The 1:1 macrosyntenic pattern observed between Acanthopterygii 38 was confirmed when comparing the available flatfish genomes: turbot, tongue sole and Japanese flounder 9 , 21 , 42 . The integration of our data with previous information, which includes the recently assembled genome of P. olivaceus , 43 enabled us to confirm and refine the suggested chromosome fusions along flatfish evolution 9 . Our results highlight that the fusion of ancestral chromosomes in the evolution of turbot genome resulted in the formation of new chromosomes, whose centromeres should correspond to the ancestral centromere of one of the fusing chromosomes, as reported in the origin of human chromosome 2 75 .…”

“…For this, we compared the improved turbot genome with those of Japanese flounder ( Paralichthys olivaceus 43 ) and half-smooth tongue sole ( Cynoglossus semilaevis 42 ) at chromosome level using LASTZ 54 (using options ‘–notransition – step = 400 – nogapped – format = rdotplot’) and compared each turbot chromosome with the orthologues of the other two species. Further, in order to assess the relation between flatfish megascaffolds to a model fish genome outside Pleuronectiformes, an additional LASTZ analysis was carried out with stickleback ( Gasterosteus aculeatus ) using the same parameters.…”

Vitamin A Affects Flatfish Development in a Thyroid Hormone Signaling and Metamorphic Stage Dependent Manner

“…More recently, it has been suggested that, through the control of histone modifications, an elevated TH signaling might stimulate RA signaling genes, while RA signaling might de-repress TH signaling (Li et al, 2015). In fish, metamorphosis is a largely known THs signaling driven process (Campinho et al, 2010; Gomes et al, 2015); while RA and THs signaling pathways crosstalk in flatfish metamorphosis (eye migration and adult pigmentation acquisition) has been recently hypothesized (Shao et al, 2016). Nevertheless, although transcriptomic approaches have been previously used to uncover the underlying VA signaling pathways activated or inhibited in fish species (Oliveira et al, 2013; Lie et al, 2016), little is known about the interaction between RA and TH signaling pathways determining the skeletal development in fish.…”

“…Nevertheless, skeletal deformities might be also indirectly induced through VA action on: (i) digestive system maturation, by perturbing nutrient uptake (Fernández et al, 2008); (ii) muscle development (Hamade et al, 2006), through the mechanostat theory (Fiaz et al, 2010); (iii) pituitary cells (Sternberg and Moav, 1999), by altering the synthesis and secretion of growth factors (Fernández et al, 2011); or (iv) thyroid follicles, by modifying homeostasis of thyroid hormones (THs; Fernández et al, 2009). The latter have been demonstrated to have a direct role on skeletal development and bone mineral density in mammals (reviewed in Gogakos et al, 2010), while in fish species it is known to control metamorphosis (Manchado et al, 2008a,b; Campinho et al, 2010; Gomes et al, 2015; Shao et al, 2016). The RA and THs signaling pathways crosstalk in flatfish metamorphosis (eye migration and adult pigmentation acquisition) has been recently hypothesized, being the basis for the generation of asymmetry in flatfish (Shao et al, 2016).…”

“…The latter have been demonstrated to have a direct role on skeletal development and bone mineral density in mammals (reviewed in Gogakos et al, 2010), while in fish species it is known to control metamorphosis (Manchado et al, 2008a,b; Campinho et al, 2010; Gomes et al, 2015; Shao et al, 2016). The RA and THs signaling pathways crosstalk in flatfish metamorphosis (eye migration and adult pigmentation acquisition) has been recently hypothesized, being the basis for the generation of asymmetry in flatfish (Shao et al, 2016). However, little is known about the interaction between VA and TH signaling pathways on the skeletal development.…”