Function and Evolution of Nuclear Receptors in Environmental-Dependent Postembryonic Development

Abstract

Nuclear receptors (NRs) fulfill key roles in the coordination of postembryonal developmental transitions in animal species. They control the metamorphosis and sexual maturation in virtually all animals and by that the two main environmental-dependent developmental decision points. Sexual maturation and metamorphosis are controlled by steroid receptors and thyroid receptors, respectively in vertebrates, while both processes are orchestrated by the ecdysone receptor (EcR) in insects. The regulation of these processes depends on environmental factors like nutrition, temperature, or photoperiods and by that NRs form evolutionary conserved mediators of phenotypic plasticity. While the mechanism of action for metamorphosis and sexual maturation are well studied in model organisms, the evolution of these systems is not entirely understood and requires further investigation. We here review the current knowledge of NR involvement in metamorphosis and sexual maturation across the animal tree of life with special attention to environmental integration and evolution of the signaling mechanism. Furthermore, we compare commonalities and differences of the different signaling systems. Finally, we identify key gaps in our knowledge of NR evolution, which, if sufficiently investigated, would lead to an importantly improved understanding of the evolution of complex signaling systems, the evolution of life history decision points, and, ultimately, speciation events in the metazoan kingdom.

Microbiota mediated plasticity promotes thermal adaptation in the sea anemone Nematostella vectensis

“…On the other hand, the upregulation of genes involved in steroid biosynthesis and metabolism in animals acclimated to high temperature may indicate the contribution of steroid signaling in the regulation of phenotypic plasticity 68 , 69 , e.g., in body size regulation and reproduction rate in response to different temperatures. The enhanced production of small RNAs (sRNAs) in the animals acclimated to high temperature, and the upregulation of processes involved in chromatin remodeling in animals acclimated at 15 °C, suggest a general change in transcriptional and translational regulations at these two extreme conditions, which might take part in acclimation.…”

From Dark to Light – An Overview of Over 70 Years of Endocrine Disruption Research on Marine Mollusks

“…Of course, there are also many positive lessons. For example, findings in the research area showed that there are nuclear receptors (e.g., retinoid X receptor, retinoid acid receptor) that participate in endocrine processes of mollusks and other invertebrates [reviewed by ( 94 , 100 )]. These results also highlighted the power of comparative genomics when supported by in vitro experiments.…”

“…Here, we would like to stress that there is no more evidence for endogenous synthesis of estrogens in annelids than in mollusks. The allosteric switch of the ligand-binding domain of ‘molluscan nER’ has been proposed to become stuck in the agonist position leading to constitutive transcription/ligand-independence ( 92 – 94 ), and, indeed, the investigation of C. gigas ER supported this idea by convincingly demonstrating the vestigialization of the receptor ( 95 ). Recent findings by Markov and his co-workers suggested that an aromatized sterol (i.e.…”

Studies on a widely-recognized snail model species (Lymnaea stagnalis) provide further evidence that vertebrate steroids do not have a hormonal role in the reproduction of mollusks

“…Furthermore, the protein homologues of the enzymes that catalyze these reactions (CYP21, CYP11B1, and CYP11B2) are not present in molluscan genomes ( 80 , 81 ). Also, there is no evidence that mollusks have corticoid receptors (NR3C1 and NR3C2) – the NR3C receptor family is vertebrate-specific ( 58 , 61 , 82 ). Instead of vertebrate-like steroids, we would like to highlight the potential role of sterols as hormones in molluscan endocrinology, though not necessarily in relation to reproduction.…”