CAS Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, 430074, Hubei, China.
Center of Conservation Biology, Core Botanical Gardens, Chinese Academy of Sciences, Wuhan, 430074, Hubei, China.
BMC Plant Biol. 2020 Jul 17;20(1):340. doi: 10.1186/s12870-020-02518-w.
Plastome-scale data have been prevalent in reconstructing the plant Tree of Life. However, phylogenomic studies currently based on plastomes rely primarily on maximum likelihood inference of concatenated alignments of plastid genes, and thus phylogenetic discordance produced by individual plastid genes has generally been ignored. Moreover, structural and functional characteristics of plastomes indicate that plastid genes may not evolve as a single locus and are experiencing different evolutionary forces, yet the genetic characteristics of plastid genes within a lineage remain poorly studied.
We sequenced and annotated 10 plastome sequences of Gentianeae. Phylogenomic analyses yielded robust relationships among genera within Gentianeae. We detected great variation of gene tree topologies and revealed that more than half of the genes, including one (atpB) of the three widely used plastid markers (rbcL, atpB and matK) in phylogenetic inference of Gentianeae, are likely contributing to phylogenetic ambiguity of Gentianeae. Estimation of nucleotide substitution rates showed extensive rate heterogeneity among different plastid genes and among different functional groups of genes. Comparative analysis suggested that the ribosomal protein (RPL and RPS) genes and the RNA polymerase (RPO) genes have higher substitution rates and genetic variations among plastid genes in Gentianeae. Our study revealed that just one (matK) of the three (matK, ndhB and rbcL) widely used markers show high phylogenetic informativeness (PI) value. Due to the high PI and lowest gene-tree discordance, rpoC2 is advocated as a promising plastid DNA barcode for taxonomic studies of Gentianeae. Furthermore, our analyses revealed a positive correlation of evolutionary rates with genetic variation of plastid genes, but a negative correlation with gene-tree discordance under purifying selection.
Overall, our results demonstrate the heterogeneity of nucleotide substitution rates and genetic characteristics among plastid genes providing new insights into plastome evolution, while highlighting the necessity of considering gene-tree discordance into phylogenomic studies based on plastome-scale data.
质体基因组规模的数据在重建植物系统发育树方面已经很普遍。然而，目前基于质体基因组的系统发育基因组学研究主要依赖于质体基因联合排列的最大似然推断，因此单个质体基因产生的系统发育分歧通常被忽略。此外，质体基因组的结构和功能特征表明，质体基因可能不会作为一个单一的基因座进化，并受到不同的进化力量的影响，但谱系内质体基因的遗传特征仍未得到充分研究。
我们对龙胆科的 10 个质体基因组进行了测序和注释。系统发育基因组学分析在龙胆科内各属之间产生了稳健的关系。我们检测到基因树拓扑结构的巨大变化，并揭示出超过一半的基因，包括三个广泛用于龙胆科系统发育推断的质体标记（rbcL、atpB 和 matK）中的一个（atpB），可能导致龙胆科的系统发育模糊性。核苷酸取代率的估计显示不同质体基因之间以及不同功能基因组之间存在广泛的速率异质性。比较分析表明，核糖体蛋白（RPL 和 RPS）基因和 RNA 聚合酶（RPO）基因在龙胆科的质体基因中具有较高的取代率和遗传变异。我们的研究表明，在龙胆科的三个广泛使用的标记（matK、ndhB 和 rbcL）中，只有一个（matK）显示出较高的系统发育信息量（PI）值。由于较高的 PI 和最低的基因树分歧，rpoC2 被提倡作为龙胆科分类学研究的有前途的质体 DNA 条形码。此外，我们的分析揭示了进化率与质体基因遗传变异之间的正相关，与纯化选择下的基因树分歧之间的负相关。
总的来说，我们的研究结果表明，质体基因之间的核苷酸取代率和遗传特征存在异质性，这为质体基因组的进化提供了新的见解，同时强调了在基于质体基因组规模数据的系统发育基因组学研究中考虑基因树分歧的必要性。
