Plastid gene loss and pseudogenization has been widely documented in parasitic and mycoheterotrophic plants, which have relaxed selective constraints on photosynthetic function. More enigmatic are sporadic reports of pseudogenization and loss of important photosynthesis genes in lineages thought to be fully photosynthetic. Here we report the complete plastid genome of Saniculiphyllum guangxiense, a critically endangered and phylogenetically isolated plant lineage, along with genomic evidence of reduced chloroplast function. We also report 22 additional plastid genomes representing the diversity of its containing clade Saxifragales, characterizing gene content and placing variation in a broader phylogenetic context. We find that the plastid genome of Saniculiphyllum has experienced pseudogenization of five genes of the ndh complex (ndhA, ndhB, ndhD, ndhF, and ndhK), previously reported in flowering plants with an aquatic habit, as well as the surprising pseudogenization of two genes more central to photosynthesis (ccsA and cemA), contrasting with strong phylogenetic conservatism of plastid gene content in all other sampled Saxifragales. These genes participate in photooxidative protection, cytochrome synthesis, and carbon uptake. Nuclear paralogs exist for all seven plastid pseudogenes, yet these are also unlikely to be functional. Saniculiphyllum appears to represent the greatest degree of plastid gene loss observed to date in any fully photosynthetic lineage, perhaps related to its extreme habitat specialization, yet plastid genome length, structure, and substitution rate are within the variation previously reported for photosynthetic plants. These results highlight the increasingly appreciated dynamism of plastid genomes, otherwise highly conserved across a billion years of green plant evolution, in plants with highly specialized life history traits.

中文翻译：

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极度濒危半水生开花植物广西虎耳草科（Saxifragaceae）关键光合基因的退化。

在寄生植物和真菌异养植物中，质体基因丢失和假基因化已被广泛记录，这些植物放松了对光合功能的选择性限制。更神秘的是，在被认为完全光合作用的谱系中，有零星的假发生和重要光合作用基因丢失的报道。在这里，我们报告了广西 Saniculiphyllum guangxiense（一种极度濒危且系统发育分离的植物谱系）的完整质体基因组，以及叶绿体功能降低的基因组证据。我们还报告了 22 个额外的质体基因组，代表了其包含的虎耳草目分支的多样性，表征了基因内容并将变异置于更广泛的系统发育背景中。我们发现 Saniculiphyllum 的质体基因组经历了 ndh 复合体的五个基因（ndhA、ndhB、ndhD、ndhF 和 ndhK）的假基因化，这两个基因先前在水生习性的开花植物中报道过，以及两个基因的令人惊讶的假基因化对光合作用（ccsA 和 cemA）更为重要，这与所有其他虎耳草样本中质体基因含量的强烈系统发育保守性形成鲜明对比。这些基因参与光氧化保护、细胞色素合成和碳吸收。所有七个质体假基因都存在核旁系同源物，但它们也不太可能发挥作用。Saniculiphyllum 似乎代表了迄今为止在任何完全光合作用谱系中观察到的最大程度的质体基因丢失，可能与其极端栖息地的特化有关，但质体基因组长度、结构和替代率仍在先前报道的光合植物的变异范围内。这些结果凸显了质体基因组的活力日益受到重视，而在数十亿年的绿色植物进化过程中，质体基因组在具有高度特化的生活史性状的植物中高度保守。