Transcriptome profiles of metamorphosis in the ornamented pygmy frog Microhyla fissipes clarify the functions of thyroid hormone receptors in metamorphosis

Abstract

Anuran metamorphosis is an excellent system in which to study postembryonic development. Studies on Xenopus (Mesobatrachia) show that thyroid hormone receptors (TRs) regulate metamorphosis in a ligand-dependent manner by coordinating the action of hundreds of genes. However, whether this mechanism is conserved among amphibians is still unknown. To understand the molecular mechanism of this universal phenomenon, we report the transcriptional profiles of the three key developmental stages in Microhyla fissipes (Neobatrachia): premetamorphosis (PM), metamorphic climax (MC) and completion of metamorphosis (CM). In total, 2,293 differentially expressed genes were identified from comparisons of transcriptomes, and these genes showed stage-specific expression patterns. Unexpectedly, we found that TRα was highly expressed in Xenopus laevis and Bufo gargarizans at premetamorphosis but showed low expression in M. fissipes. In contrast, TRβ was highly expressed during metamorphosis in M. fissipes and X. laevis. This result may imply that TRβ is essential for initiating metamorphosis, at least in M. fissipes. Thus, our work not only identifies genes that are likely to be involved in Neobatrachia metamorphosis but also clarifies the roles of unliganded TRα in regulating tadpole growth and timing of metamorphosis, which may be conserved in anurans, and the role of liganded TRβ in launching metamorphosis.

Morphological and transcriptomic analyses reveal three discrete primary stages of postembryonic development in the common fire salamander, Salamandra salamandra

“…This protein is related to osmotic regulation, and is conserved in amphibians, fishes, and mammals (Howie, Lote, Cunningham, Zaccone, & Fasulo, ). We found Uromodulin downregulated in Meta for S. salamandra , as was also shown in the salamander A. mexicanum (Page et al., ) and the anurans M. fissipes (Zhao et al., ) and X. laevis (Das et al., ; Furlow, Berry, Wang, & Brown, ).…”

“…This development of coloration is mirrored by the upregulation of enzymes involved in the synthesis of pigments, such as TYRP1 and DCT for eumelanin, and SPR, TXNL5 , and XDH for pteridines in late ProM and Meta. Similarly, TYR is upregulated in Meta in M. fissipes (Zhao et al., ). This postembryonic development of pigment cells and coloration patterns in vertebrates is expected to be at least partly conserved, since it is subject to hormonal control—especially by thyroid hormones (Brown, ; McMenamin et al., ).…”

“…The tail fins of amphibians are composed of a double layer of skin and crossed fibers of collagen (Wassersug, ). The resorption of the tail in anurans, which includes the tail fins and muscle tissue, has been linked to matrix metalloproteinases (stromelysin and collagenases)—highly expressed during metamorphosis (Damjanovski, Ishizuya‐Oka, & Shi, ; Wang & Brown, ; Brinckerhoff & Matrisian ; Zhao et al., ). Some of these are upregulated in late ProM and Meta in both anurans and caudates.…”

“…Observable morphological and physiological changes are caused by the expression of underlying genes, whose differential regulation during amphibian metamorphosis is causally associated with increases in circulating thyroid hormone levels (Brown, ; Brown & Cai, ; Denver, Glennemeier, & Boorse ; Laudet, ; Norman et al., ; Sachs et al., ; Tata, ; Voss, Shaffer, Taylor, Safi, & Laudet, ; Yaoita & Brown, ). Therefore, amphibian postembryonic development is categorized using morphological characters, endogenous thyroid hormones measures, and—more recently—gene expression profiles into four primary developmental stages: premetamorphosis (PreM; according to Gosner stages 25 – 35), prometamorphosis (ProM; Gosner stages 36 – 41), metamorphic climax (Meta; Gosner stages 42 – 46), and completion of metamorphosis (PostM; Gosner stage 46) (Buchholz, Heimeier, Das, Washington, & Shi, ; Duellman & Trueb, ; Etkin, ; Gosner ; Nieuwkoop & Faber ; Tata, ; Zhao, Liu, Wang, Wang, & Jiang, ). In short, larvae develop independently of thyroid hormones during PreM, but at ProM, when thyroid hormones start to be produced, the first metamorphic changes occur.…”

Description and initial characterization of metatranscriptomic nidovirus-like genomes from the proposed new family Abyssoviridae, and from a sister group to the Coronavirinae, the proposed genus Alphaletovirus

“…In this report we describe the discovery and characterization of one of the nidoviruses prototyping a new family along with another putative nidovirus. We used BLAST searches to scan the publicly available transcriptomes and expressed sequence tag libraries available at the US National Center for Biotechnology Information, and revealed two novel nido-like virus sequences from the frog Microhyla fissipes developmental transcriptome (Zhao et al, 2016) and from several transcriptome studies dealing with the marine gastropod Aplysia californica (Fiedler et al, 2010;Heyland et al, 2011;Moroz et al, 2006). We describe the bioinformatics of the new virus-like sequences, and demonstrate that the Aplysia virus-like sequence encodes a functional proteinase, and a translational termination-suppression signal.…”