Correlations of gene expression, codon usage bias, and evolutionary rates of the mitochondrial genome show tissue differentiation in Ophioglossum vulgatum
Abstract Background Mitochondria are crucial for energy production in plant tissues, but their quantity and activity vary in different tissues and developmental processes. Determining the factors underlying differential molecular evolutionary rates has long been a central question in evolutionary bi...
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2025-02-01
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| Series: | BMC Plant Biology |
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| Online Access: | https://doi.org/10.1186/s12870-025-06157-x |
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| author | Jing Hao Yingyi Liang Ting Wang Yingjuan Su |
| author_facet | Jing Hao Yingyi Liang Ting Wang Yingjuan Su |
| author_sort | Jing Hao |
| collection | DOAJ |
| description | Abstract Background Mitochondria are crucial for energy production in plant tissues, but their quantity and activity vary in different tissues and developmental processes. Determining the factors underlying differential molecular evolutionary rates has long been a central question in evolutionary biology, with expression level emerging as the prime predictor. Although we have previously observed an anti-correlation between expression level (E) and evolutionary rate (R) in chloroplast genes, it remains unclear whether such an anti-correlation exists in plant mitochondrial genes. Ophioglossum vulgatum is a typical plant belonging to the Ophioglossaceae, characterized by its unique morphology with only a single leaf above ground. It holds significant scientific and medicinal value. Using the mitochondrial genome and transcriptome data of O. vulgatum, we first analyzed the correlation between mitochondrial gene expression, codon usage bias, and evolutionary rates in different tissues. Results Our findings indicated that mitochondrial gene expression level was the strongest between stem and leaf, while the weakest was between sporangium and root. Kruskal-Wallis tests revealed significant differences across various tissue types. Codon usage bias was influenced by both mutation and selection, with selection exerting a greater impact. The Spearman’s rank correlation coefficients between codon adaptation index and expression levels of sporangium, stem, leaf, and root were 0.1178, 0.3926, 0.4463, and 0.2945, respectively, with significance in stem and leaf (P < 0.05). The correlation coefficients between the nonsynonymous substitution rate (dN) and expression levels in sporangium, stem, leaf, and root were -0.0840, -0.1786, -0.1714, and -0.0857, respectively, yet none are statistically significant. The correlation coefficient between the synonymous substitution rate (dS) and expression levels in sporangium was negative, whereas those between dS and the stem, leaf, and root were positive, although they were not significant. The dN/dS ratio exhibited a significant negative correlation with expression levels in both leaf and root (P < 0.05). Conclusions For the first time, our study revealed differences in the correlation between mitochondrial gene expression and codon usage bias, as well as evolutionary rates, across various tissues of O. vulgatum. Moreover, we also provide novel insights into understanding the effects of plant mitochondrial gene expression on evolutionary patterns. |
| format | Article |
| id | doaj-art-039e71dc171b4257a75fbf1df3e9c0c7 |
| institution | Kabale University |
| issn | 1471-2229 |
| language | English |
| publishDate | 2025-02-01 |
| publisher | BMC |
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| series | BMC Plant Biology |
| spelling | doaj-art-039e71dc171b4257a75fbf1df3e9c0c72025-02-02T12:15:30ZengBMCBMC Plant Biology1471-22292025-02-0125111510.1186/s12870-025-06157-xCorrelations of gene expression, codon usage bias, and evolutionary rates of the mitochondrial genome show tissue differentiation in Ophioglossum vulgatumJing Hao0Yingyi Liang1Ting Wang2Yingjuan Su3School of Life Sciences, Sun Yat-sen UniversityCollege of Life Sciences, South China Agricultural UniversityCollege of Life Sciences, South China Agricultural UniversitySchool of Life Sciences, Sun Yat-sen UniversityAbstract Background Mitochondria are crucial for energy production in plant tissues, but their quantity and activity vary in different tissues and developmental processes. Determining the factors underlying differential molecular evolutionary rates has long been a central question in evolutionary biology, with expression level emerging as the prime predictor. Although we have previously observed an anti-correlation between expression level (E) and evolutionary rate (R) in chloroplast genes, it remains unclear whether such an anti-correlation exists in plant mitochondrial genes. Ophioglossum vulgatum is a typical plant belonging to the Ophioglossaceae, characterized by its unique morphology with only a single leaf above ground. It holds significant scientific and medicinal value. Using the mitochondrial genome and transcriptome data of O. vulgatum, we first analyzed the correlation between mitochondrial gene expression, codon usage bias, and evolutionary rates in different tissues. Results Our findings indicated that mitochondrial gene expression level was the strongest between stem and leaf, while the weakest was between sporangium and root. Kruskal-Wallis tests revealed significant differences across various tissue types. Codon usage bias was influenced by both mutation and selection, with selection exerting a greater impact. The Spearman’s rank correlation coefficients between codon adaptation index and expression levels of sporangium, stem, leaf, and root were 0.1178, 0.3926, 0.4463, and 0.2945, respectively, with significance in stem and leaf (P < 0.05). The correlation coefficients between the nonsynonymous substitution rate (dN) and expression levels in sporangium, stem, leaf, and root were -0.0840, -0.1786, -0.1714, and -0.0857, respectively, yet none are statistically significant. The correlation coefficient between the synonymous substitution rate (dS) and expression levels in sporangium was negative, whereas those between dS and the stem, leaf, and root were positive, although they were not significant. The dN/dS ratio exhibited a significant negative correlation with expression levels in both leaf and root (P < 0.05). Conclusions For the first time, our study revealed differences in the correlation between mitochondrial gene expression and codon usage bias, as well as evolutionary rates, across various tissues of O. vulgatum. Moreover, we also provide novel insights into understanding the effects of plant mitochondrial gene expression on evolutionary patterns.https://doi.org/10.1186/s12870-025-06157-xOphioglossum vulgatumMitochondrial gene expressionCodon usage biasEvolutionary ratesTissue differentiation |
| spellingShingle | Jing Hao Yingyi Liang Ting Wang Yingjuan Su Correlations of gene expression, codon usage bias, and evolutionary rates of the mitochondrial genome show tissue differentiation in Ophioglossum vulgatum BMC Plant Biology Ophioglossum vulgatum Mitochondrial gene expression Codon usage bias Evolutionary rates Tissue differentiation |
| title | Correlations of gene expression, codon usage bias, and evolutionary rates of the mitochondrial genome show tissue differentiation in Ophioglossum vulgatum |
| title_full | Correlations of gene expression, codon usage bias, and evolutionary rates of the mitochondrial genome show tissue differentiation in Ophioglossum vulgatum |
| title_fullStr | Correlations of gene expression, codon usage bias, and evolutionary rates of the mitochondrial genome show tissue differentiation in Ophioglossum vulgatum |
| title_full_unstemmed | Correlations of gene expression, codon usage bias, and evolutionary rates of the mitochondrial genome show tissue differentiation in Ophioglossum vulgatum |
| title_short | Correlations of gene expression, codon usage bias, and evolutionary rates of the mitochondrial genome show tissue differentiation in Ophioglossum vulgatum |
| title_sort | correlations of gene expression codon usage bias and evolutionary rates of the mitochondrial genome show tissue differentiation in ophioglossum vulgatum |
| topic | Ophioglossum vulgatum Mitochondrial gene expression Codon usage bias Evolutionary rates Tissue differentiation |
| url | https://doi.org/10.1186/s12870-025-06157-x |
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