Hao Jing, Liang Yingyi, Wang Ting, Su Yingjuan
School of Life Sciences, Sun Yat-sen University, Guangzhou, 510275, China.
College of Life Sciences, South China Agricultural University, Guangzhou, 510642, China.
BMC Plant Biol. 2025 Feb 1;25(1):134. doi: 10.1186/s12870-025-06157-x.
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.
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).
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.
线粒体对于植物组织中的能量产生至关重要，但其数量和活性在不同组织和发育过程中有所不同。确定分子进化速率差异背后的因素长期以来一直是进化生物学的核心问题，表达水平已成为主要预测指标。尽管我们之前在叶绿体基因中观察到表达水平（E）与进化速率（R）之间存在负相关，但尚不清楚这种负相关在植物线粒体基因中是否存在。瓶尔小草是一种属于瓶尔小草科的典型植物，其特征是形态独特，地上只有一片叶子。它具有重要的科学和药用价值。利用瓶尔小草的线粒体基因组和转录组数据，我们首先分析了不同组织中线粒体基因表达、密码子使用偏好和进化速率之间的相关性。
我们的研究结果表明，线粒体基因表达水平在茎和叶之间最强，而在孢子囊和根之间最弱。Kruskal-Wallis检验显示不同组织类型之间存在显著差异。密码子使用偏好受突变和选择的影响，其中选择的影响更大。孢子囊、茎、叶和根的密码子适应指数与表达水平之间的Spearman等级相关系数分别为0.1178、0.3926、0.4463和0.2945，在茎和叶中具有显著性（P < 0.05）。非同义替换率（dN）与孢子囊、茎、叶和根的表达水平之间的相关系数分别为-0.0840、-0.1786、-0.1714和-0.0857，但均无统计学显著性。同义替换率（dS）与孢子囊表达水平之间的相关系数为负，而dS与茎、叶和根之间的相关系数为正，尽管不显著。dN/dS比值在叶和根中与表达水平均呈现显著负相关（P < 0.05）。
我们的研究首次揭示了瓶尔小草不同组织中线粒体基因表达与密码子使用偏好以及进化速率之间相关性的差异。此外，我们还为理解植物线粒体基因表达对进化模式的影响提供了新的见解。
