Global Analysis of Transcriptome and Translatome Revealed That Coordinated WNT and FGF Regulate the Carapacial Ridge Development of Chinese Soft-Shell Turtle

Zhang, Jun; Yu, Peng; Zhao, Yang; Zhou, Qinyan; Yang, Jiayu; Hu, Qingxi; Liu, Tiantian; Bao, Chuanhe; Su, Shiping; Gui, Jian‐Fang

doi:10.3390/ijms222212441

Cited by 4 publications

(5 citation statements)

References 78 publications

(137 reference statements)

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“…A comprehensive analysis of growth performance, physiology, and transcriptomics can effectively evaluate the responses of P. sinensis to environmental factors [ 43 , 44 , 45 ]. Genes such as IGF1, IGF2, SLC27A2, GHRL, GHSR, MyoD1, WNT, and FGF have been demonstrated to be closely related to somatic growth [ 46 , 47 , 48 , 49 ]. The DEGs in the GH-IGF 1 axis genes and the Jak-STAT signaling pathway might play important roles in the growth differences of P. sinensis [ 50 ].…”

Section: Discussionmentioning

confidence: 99%

Comparative Analysis of the Growth, Physiological Responses, and Gene Expression of Chinese Soft-Shelled Turtles Cultured in Different Modes

Wu,

Huang,

et al. 2024

Animals

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The Chinese soft-shelled turtle (Pelodiscus sinensis) is an important freshwater aquaculture turtle due to its taste and nutritional and medicinal value. More ecological culturing modes, such as rice–turtle co-culture, should be developed to meet the ecological benefit demand. We compared growth, physiological parameters, and transcriptome data to detect the physiological responses and regulatory mechanisms of pond-cultured turtles as compared to co-cultured turtles. The co-cultured turtles grew slower than pond-cultured turtles. The gonadosomatic index of co-cultured male turtles was lower than that of pond-cultured male turtles, and both the mesenteric fat index and limb fat index were lower in co-cultured turtles than in pond-cultured turtles (p < 0.05). The blood GLU of the co-cultured turtles was significantly lower than the GLU of the pond-cultured turtles (p < 0.05), while the values of CRE, UA, BUN, AKP, ACP, GOT, and CAT were higher in the co-cultured turtles than in the pond-cultured turtles (p < 0.05). In total, 246 and 598 differentially expressed genes (DEGs) were identified in the brain and gut from turtles cultured in the two different modes, respectively. More DEGs were related to environmental information processing, metabolism, and human diseases. In the brain, the top enriched pathways of DEGs included the longevity regulating pathway, glycerolipid metabolism, cytokine–cytokine receptor interaction, Toll-like receptor signaling pathway, and PI3K-Akt signaling pathway, while in the gut, the top enriched pathways of DEGs included the cell cycle, DNA replication, cellular senescence, and p53 signaling pathway. The turtles acclimated to the different culturing conditions by adjusting their growth, physiological, and biochemical characteristics and related gene expression during a short culture period.

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Section: Discussionmentioning

confidence: 99%

Comparative Analysis of the Growth, Physiological Responses, and Gene Expression of Chinese Soft-Shelled Turtles Cultured in Different Modes

Wu,

Huang,

et al. 2024

Animals

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“…FZD7 mediates Wnt11 activity for the shape change and migration of cells in convergent extension movements during vertebrate gastrulation [ 49 ]. Wnt5a regulates the CR development in Chinese soft-shell turtles through the Wnt5a/JNK pathway [ 24 ]. Notably, in this study, Dkk1 was upregulated in the CR development of M. reevesii after stage 15 ( Figure 5 ).…”

Section: Discussionmentioning

confidence: 99%

“…Therefore, we suggest that the Wnt signaling pathways might regulate the CR development of M. reevesii through interacting with Fgfs , which interacts with Bmps and Shh to form a complex network. Previously, we have reported that FGFs and Wnts co-regulate the CR development in Chinese soft-shell turtles [ 24 ], which suggested that the molecular mechanisms of CR development between hard-shell and soft-shell turtles might be conserved.…”

Section: Discussionmentioning

confidence: 99%

“…Wang identified that Wnt5a (encoding Wnt family member 5A) was the only Wnt gene that was expressed in the CR region of a soft-shell turtle, and Pascual-Anaya identified the same turtle-specific Wnt5a expression in hard-shell turtles [ 22 , 23 ]. Studies on the CR of Chinese soft-shell turtles revealed that Wnt5a regulates the CR development through the Wnt5a/JUN N -terminal Kinase (JNK) pathway [ 24 ]. In addition, an in situ hybridization showed that Fgf8 and Fgf10 (encoding Fibroblast growth factor 8 and 10) are expressed in the distal tip of the ribs and the mesenchyme beneath the CR ectoderm, respectively, possibly forming a feedback loop [ 25 ].…”

Section: Introductionmentioning

confidence: 99%

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Gene Regulation during Carapacial Ridge Development of Mauremys reevesii: The Development of Carapacial Ridge, Ribs and Scutes

Yang

Xia

Shaohu

et al. 2022

Genes

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The unique topological structure of a turtle shell, including the special ribs–scapula relationship, is an evolutionarily novelty of amniotes. The carapacial ridge is a key embryonic tissue for inducing turtle carapace morphologenesis. However, the gene expression profiles and molecular regulatory mechanisms that occur during carapacial ridge development, including the regulation mechanism of rib axis arrest, the development mechanism of the carapacial ridge, and the differentiation between soft-shell turtles and hard-shell turtles, are not fully understood. In this study, we obtained genome-wide gene expression profiles during the carapacial ridge development of Mauremys reevesii using RNA-sequencing by using carapacial ridge tissues from stage 14, 15 and 16 turtle embryos. In addition, a differentially expressed genes (DEGs) analysis and a gene set enrichment analysis (GSEA) of three comparison groups were performed. Furthermore, a Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis was used to analyze the pathway enrichment of the differentially expressed genes of the three comparative groups. The result displayed that the Wnt signaling pathway was substantially enriched in the CrTK14 vs. the CrTK15 comparison group, while the Hedgehog signaling pathway was significantly enriched in the CrTK15 vs. the CrTK16 group. Moreover, the regulatory network of the Wnt signaling pathway showed that Wnt signaling pathways might interact with Fgfs, Bmps, and Shh to form a regulatory network to regulate the carapacial ridge development. Next, WGCNA was used to cluster and analyze the expression genes during the carapacial ridge development of M. reevesii and P. sinensis. Further, a KEGG functional enrichment analysis of the carapacial ridge correlation gene modules was performed. Interesting, these results indicated that the Wnt signaling pathway and the MAPK signaling pathway were significantly enriched in the gene modules that were highly correlated with the stage 14 and stage 15 carapacial ridge samples of the two species. The Hedgehog signaling pathway was significantly enriched in the modules that were strongly correlated with the stage 16 carapacial ridge samples of M. reevesii, however, the PI3K-Akt signaling and the TGF-β signaling pathways were significantly enriched in the modules that were strongly correlated with the stage 16 carapacial ridge samples of P. sinensis. Furthermore, we found that those modules that were strongly correlated with the stage 14 carapacial ridge samples of M. reevesii and P. sinensis contained Wnts and Lef1. While the navajo white 3 module which was strongly correlated with the stage 16 carapacial ridge samples of M. reevesii contained Shh and Ptchs. The dark green module strongly correlated with the stage 16 carapacial ridge samples of P. sinensis which contained Col1a1, Col1a2, and Itga8. Consequently, this study systematically revealed the signaling pathways and genes that regulate the carapacial ridge development of M. reevesii and P. sinensis, which provides new insights for revealing the molecular mechanism that is underlying the turtle’s body structure.

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“…Notably, it was reported that the "calcium signaling pathway", "Wnt signaling pathway", and "tyrosine metabolism pathway" probably play significant roles in the biomineralization process (Shi M. et al, 2013;Liu et al, 2015). Among these three pathways, calmodulin, tyr, b-catenin, TCF, and wnt5 are supposed to be related to calcium signal transduction and the shell formation process Gao et al, 2016;Zhang et al, 2021).…”

Section: Gene Functional Annotation Of Full-length Transcriptsmentioning

confidence: 99%

Full-length transcriptome analysis provides insights into larval shell formation in Mulinia lateralis

Guo

Zhao

et al. 2023

Front. Mar. Sci.

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Mollusca is the second largest animal phylum and represents one of the most evolutionarily successful animal groups. Mulinia lateralis, a small bivalve, is a promising model organism to facilitate studies of mollusc development. However, because of the lack of published genomic and transcriptomic resources, integrated research on the formation of larval shells in this species, which is a representative developmental process of molluscs and of great importance for larva survival, is hindered. In this study, the blastula, gastrula, trochophore larva, and D-shaped larva of M. lateralis were utilized for generating a comprehensive full-length transcriptome through Pacific BioSciences (PacBio) isoform sequencing (Iso-seq) and Illumina RNA-Seq. A total of 238,919 full-length transcripts with an average length of 3,267 bp and 121,424 annotated genes were obtained. Illumina RNA-Seq data analysis showed that 4,512, 10,637, and 17,829 differentially expressed genes (DEGs) were obtained between the two adjacent developmental stages. Functional annotation and enrichment analysis revealed the specific function of genes in shell biomineralization during different developmental stages. Twelve genes that may be involved in the formation of the larval shell of M. lateralis were identified, including insoluble shell matrix protein-encoding gene 1 (ISMP1), ISMP2, ISMP5, chitin synthase, tyrosinase, chitin-binding protein, collagen and pu14 involved in shell matrix deposition, and carbonic anhydrase, solute carrier family 4 member 8 (slc4a8), EF-hand, and a calmodulin coding gene C-2442 participated in ion transportation. In addition, calcium ion binding function, calcium signaling pathway, and endocrine and other factor-regulated calcium reabsorption pathways were significantly enriched. Weighted gene correlation network analysis (WGCNA) identified two modules related to biomineralization and larval shell formation, and slc4a8 and ring finger protein 41 (rnf41) were key hub genes that may be involved in this process. Moreover, it could be implied that the process of ion transport occurs earlier than the deposition of the shell matrix. This work provided a clear view of the transcriptome for M. lateralis and will be valuable in elucidating the mechanisms of larval shell formation as well as other developmental processes in molluscs.

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Global Analysis of Transcriptome and Translatome Revealed That Coordinated WNT and FGF Regulate the Carapacial Ridge Development of Chinese Soft-Shell Turtle

Cited by 4 publications

References 78 publications

Comparative Analysis of the Growth, Physiological Responses, and Gene Expression of Chinese Soft-Shelled Turtles Cultured in Different Modes

Comparative Analysis of the Growth, Physiological Responses, and Gene Expression of Chinese Soft-Shelled Turtles Cultured in Different Modes

Gene Regulation during Carapacial Ridge Development of Mauremys reevesii: The Development of Carapacial Ridge, Ribs and Scutes

Full-length transcriptome analysis provides insights into larval shell formation in Mulinia lateralis

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