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. 2024 Oct 10;13(10):1217.
doi: 10.3390/antiox13101217.

Comparative Analyses of Dynamic Transcriptome Profile of Heart Highlight the Key Response Genes for Heat Stress in Zhikong Scallop Chlamys farreri

Xinyuan Wang  1 , Zujing Yang  1 , Cheng Peng  1 , Haitao Yu  1 , Chang Cui  1 , Qiang Xing  1   2 , Jingjie Hu  1   3 , Zhenmin Bao  1   2   3 , Xiaoting Huang  1   2
Affiliations

Comparative Analyses of Dynamic Transcriptome Profile of Heart Highlight the Key Response Genes for Heat Stress in Zhikong Scallop Chlamys farreri

Xinyuan Wang et al. Antioxidants (Basel). .

Abstract

Heat stress resulting from global climate change has been demonstrated to adversely affect growth, development, and reproduction of marine organisms. The Zhikong scallop (Chlamys farreri), an important economical mollusk in China, faces increasing risks of summer mortality due to the prolonged heat waves. The heart, responsible for transporting gas and nutrients, is vital in maintaining homeostasis and physiological status in response to environmental changes. In this study, the effect of heat stress on the cardiac function of C. farreri was investigated during the continuous 30-day heat stress at 27 °C. The results showed the heart rate of scallops increased due to stress in the initial phase of high temperature exposure, peaking at 12 h, and then gradually recovered, indicating an acclimatization at the end of the experiment. In addition, the levels of catalase (CAT), superoxide dismutase (SOD), and total antioxidant capacity (T-AOC) exhibited an initial increase followed by recovery in response to heat stress. Furthermore, transcriptome analysis of the heart identified 3541 differentially expressed genes (DEGs) in response to heat stress. Subsequent GO and KEGG enrichment analysis showed that these genes were primarily related to signal transduction and oxidative stress, such as the phosphatidylinositol signaling system, regulation of actin cytoskeleton, MAPK signaling pathway, FoxO signaling pathway, etc. In addition, two modules were identified as significant responsive modules according to the weighted gene co-expression network analysis (WGCNA). The upregulation of key enzymes within the base excision repair and gap junction pathways indicated that the heart of C. farreri under heat stress enhanced DNA repair and maintained cellular integrity. In addition, the variable expression of essential signaling molecules and cytoskeletal regulators suggested that the heart of C. farreri modulated cardiomyocyte contraction, intracellular signaling, and heart rate through complex regulation of phosphorylation and calcium dynamics in response to heat stress. Collectively, this study enhances our understanding of cardiac function and provides novel evidence for unraveling the mechanism underlying the thermal response in mollusks.

Keywords: Chlamys farreri; antioxidant; heart; heat stress; transcriptome.

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Conflict of interest statement

The authors declare no conflicts of interest.

Figures

Figure 1
Figure 1
Heart rate and amplitude of C. farreri under different heat stress time. (A) Heart rate (HR); (B) Heart amplitude (HA). The circle shape represents the mean ± S.D. (n = 3). (* p value < 0.05).
Figure 2
Figure 2
Antioxidant enzymes activity and total antioxidant capacity in heart of C. farreri under heat stress. (A) CAT activity; (B) SOD activity; (C) T-AOC. The triangular shape represents the mean ± S.D. (n = 3). (* p value < 0.05).
Figure 3
Figure 3
Numbers of DEGs in heart of C. farreri under heat stress. Red bar represents the number of up-regulated DEGs; blue bar represents the number of down-regulated DEGs.
Figure 4
Figure 4
Three expression trends of DEGs in heart of C. farreri under heat stress. (A) Expression trend contrary to the trend observed in HR changes; (B) expression trend similar to the trend of HR; (C) expression trend opposite to the trend of HA changes. The X-axis represents the time of heat stress. The Y-axis represents the log2FC of gene expression change.
Figure 5
Figure 5
The expressions of key genes from three trends in heart of C. farreri under heat stress.
Figure 6
Figure 6
The GO and KEGG analysis of DEGs in heart of C. farreri under heat stress. (A) GO annotation. The X-axis represents the annotated functions. The Y-axis represents the percent of enriched gene numbers. (B) KEGG enrichment. The X-axis represents the rich factor of KEGG terms. The Y-axis represents the enriched pathways. The circle shape represents the number of DGEs in the enriched pathways.
Figure 7
Figure 7
The WGCNA analysis of scallop heart transcriptome under heat stress. Dendrogram is produced by average linkage hierarchical clustering of genes based on topological overlap. Horizontal color bars represent different co-expression modules that are also numbered. Unassigned genes are labeled in grey.
Figure 8
Figure 8
Main response modules of WGCNA network of heart after heat treatment. Yellow dots belong to M1 and blue dots belong to M2.
Figure 9
Figure 9
Quantitative real time-PCR validation. Green line represents RT-qPCR results; red line represents RNA-Seq results.
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