Coelimination and Survival in Gene Network Evolution: Dismantling the RA-Signaling in a Chordate

Abstract

The bloom of genomics is revealing gene loss as a pervasive evolutionary force generating genetic diversity that shapes the evolution of species. Outside bacteria and yeast, however, the understanding of the process of gene loss remains elusive, especially in the evolution of animal species. Here, using the dismantling of the retinoic acid metabolic gene network (RA-MGN) in the chordate Oikopleura dioica as a case study, we combine approaches of comparative genomics, phylogenetics, biochemistry, and developmental biology to investigate the mutational robustness associated to biased patterns of gene loss. We demonstrate the absence of alternative pathways for RA-synthesis in O. dioica, which suggests that gene losses of RA-MGN were not compensated by mutational robustness, but occurred in a scenario of regressive evolution. In addition, the lack of drastic phenotypic changes associated to the loss of RA-signaling provides an example of the inverse paradox of Evo-Devo. This work illustrates how the identification of patterns of gene coelimination-in our case five losses (Rdh10, Rdh16, Bco1, Aldh1a, and Cyp26)-is a useful strategy to recognize gene network modules associated to distinct functions. Our work also illustrates how the identification of survival genes helps to recognize neofunctionalization events and ancestral functions. Thus, the survival and extensive duplication of Cco and RdhE2 in O. dioica correlated with the acquisition of complex compartmentalization of expression domains in the digestive system and a process of enzymatic neofunctionalization of the Cco, while the surviving Aldh8 could be related to its ancestral housekeeping role against toxic aldehydes.

De novo draft assembly of the Botrylloides leachii genome provides further insight into tunicate evolution

“…Components of this pathway have been found in non-chordate animals, suggesting a more ancient origin 80 . This pathway is required for B. leachii WBR 25 and Ciona development, yet several genes essential for RA signalling appear to be missing in O. dioica 80 , 81 .

Figure 8 Evolution of the RA pathway in tunicates.

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“…Tunicate proteins are shown in bold. No Cyp26 gene has been identified in the O. dioica genome 81 . Values for the approximate likelihood-ratio test (aLRT) are indicated.…”

“…Rdh10 is the major dehydrogenase associated with the first steps of RA production, although the Rdh16 and RdhE2 enzymes can also substitute this function 82 – 84 . The O. dioica genome has no orthologs for either Rdh10 or Rdh16 but it does have four genes that encode for RdhE2 proteins 81 . O. dioica also lacks both an Aldh1- type gene, as well as a Cyp26 gene, but has one single RXR-ortholog 81 (Fig.…”

Metallothioneins of the urochordateOikopleura dioicahave Cys-rich tandem repeats, large size and cadmium-binding preference

“…14 Appendicularians are also ecologically relevant because they contribute to the vertical transport of carbon to deep ocean through the rapid sinking of fecal pellets and discarded houses. [15][16][17] Among Appendicularians, Oikopleura dioica is the most studied species, and it is becoming a new laboratory model for comparative genetic and genomic analyses, [18][19][20][21][22] developmental biology studies, [23][24][25][26][27][28][29][30] as well as ecological and toxicological investigations. [31][32][33][34] The ecological relevance of Appendicularians together with the potential of O. dioica as an experimental model [35][36][37][38] prompted us to survey the MTs of O. dioica to characterize the MT system of an Appendicularian species.…”

A genome database for a Japanese population of the larvacean Oikopleura dioica

“…We thus adopted the OSKA2016 as the best genome assembly for Japanese O. dioica. It is reasonable that less than 90% of BUSCO was recovered, because O. dioica is shown to have the smallest and most highly rearranged genome amongst non-parasitic metazoans (Seo et al, 2001;Denoeud et al, 2010), and often lacks evolutionarily conserved genes, such as those for retinoic acid signal (Martí-Solans et al, 2016), Nodal signal (Onuma et al, 2020), and the non-homologous DNA end-joining pathway (Deng et al, 2018).…”