Departamento de Biologia, Centro de Ciências Humanas e Biológicas, Universidade Federal de São Carlos, Sorocaba, SP, Brazil.
Programa de Pós-Graduação em Botânica, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil.
Ann Bot. 2023 Nov 25;132(4):771-786. doi: 10.1093/aob/mcad098.
Plastid genomes (plastomes) have long been recognized as highly conserved in their overall structure, size, gene arrangement and content among land plants. However, recent studies have shown that some lineages present unusual variations in some of these features. Members of the cactus family are one of these lineages, with distinct plastome structures reported across disparate lineages, including gene losses, inversions, boundary movements or loss of the canonical inverted repeat (IR) region. However, only a small fraction of cactus diversity has been analysed so far.
Here, we investigated plastome features of the tribe Opuntieae, the remarkable prickly pear cacti, which represent one of the most diverse and important lineages of Cactaceae. We assembled de novo the plastome of 43 species, representing a comprehensive sampling of the tribe, including all seven genera, and analysed their evolution in a phylogenetic comparative framework. Phylogenomic analyses with different datasets (full plastome sequences and genes only) were performed, followed by congruence analyses to assess signals underlying contentious nodes.
Plastomes varied considerably in length, from 121 to 162 kbp, with striking differences in the content and size of the IR region (contraction and expansion events), including a lack of the canonical IR in some lineages and the pseudogenization or loss of some genes. Overall, nine different types of plastomes were reported, deviating in the presence of the IR region or the genes contained in the IR. Overall, plastome sequences resolved phylogenetic relationships within major clades of Opuntieae with high bootstrap values but presented some contentious nodes depending on the dataset analysed (e.g. whole plastome vs. genes only). Congruence analyses revealed that most plastidial regions lack phylogenetic resolution, while few markers are supporting the most likely topology. Likewise, alternative topologies are driven by a handful of plastome markers, suggesting recalcitrant nodes in the phylogeny.
Our study reveals a dynamic nature of plastome evolution across closely related lineages, shedding light on peculiar features of plastomes. Variation of plastome types across Opuntieae is remarkable in size, structure and content and can be important for the recognition of species in some major clades. Unravelling connections between the causes of plastome variation and the consequences for species biology, physiology, ecology, diversification and adaptation is a promising and ambitious endeavour in cactus research. Although plastome data resolved major phylogenetic relationships, the generation of nuclear genomic data is necessary to confront these hypotheses and assess the recalcitrant nodes further.
质体基因组(质体基因组)在陆地植物中的整体结构、大小、基因排列和内容方面一直被认为高度保守。然而,最近的研究表明,一些谱系在这些特征中的一些方面表现出异常的变化。仙人掌科是这些谱系之一,不同谱系报道了明显不同的质体结构,包括基因丢失、反转、边界运动或经典反向重复(IR)区的丢失。然而,到目前为止,只有一小部分仙人掌多样性得到了分析。
在这里,我们研究了 Opuntieae 族的质体特征,该族是奇异的仙人掌仙人掌,是仙人掌科中最多样化和最重要的谱系之一。我们从头组装了 43 种物种的质体,代表了该族的全面采样,包括所有 7 个属,并在系统发育比较框架中分析了它们的进化。使用不同数据集(完整质体序列和仅基因)进行了系统基因组分析,然后进行了一致性分析,以评估有争议节点的潜在信号。
质体在长度上差异很大,从 121 到 162 kbp,IR 区(收缩和扩张事件)的内容和大小差异很大,包括一些谱系中缺乏典型的 IR 和一些基因的假基因化或丢失。总的来说,报道了九种不同类型的质体,在 IR 区或 IR 中包含的基因存在差异。总体而言,质体序列以高自举值解决了 Opuntieae 主要分支内的系统发育关系,但根据分析的数据集(例如,完整质体与仅基因)存在一些有争议的节点。一致性分析表明,大多数质体区域缺乏系统发育分辨率,而少数标记支持最可能的拓扑结构。同样,替代拓扑结构是由少数几个质体标记驱动的,这表明系统发育中存在顽固节点。
我们的研究揭示了密切相关谱系中质体进化的动态性质,为质体的特殊特征提供了线索。Opuntieae 中质体类型的变化在大小、结构和内容上都非常显著,这对一些主要分支中物种的识别很重要。揭示质体变异的原因与物种生物学、生理学、生态学、多样化和适应的后果之间的联系,是仙人掌研究中一项有前途和雄心勃勃的工作。尽管质体数据解决了主要的系统发育关系,但生成核基因组数据对于检验这些假设和进一步评估顽固节点是必要的。