State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China.
University of Chinese Academy of Sciences, Beijing, 100049, China.
Plant J. 2020 Dec;104(6):1657-1672. doi: 10.1111/tpj.15028. Epub 2020 Nov 17.
Plastids and mitochondria are endosymbiotic organelles that store genetic information. The genomes of these organelles generally exhibit contrasting patterns regarding genome architecture and genetic content. However, they have similar genetic features in Selaginellaceae, and little is known about what causes parallel evolution. Here, we document the multipartite plastid genomes (plastomes) and the highly divergent mitochondrial genomes (mitogenomes) from spikemoss obtained by combining short- and long-reads. The 188-kb multipartite plastome has three ribosomal operon copies in the master genomic conformation, creating the alternative subgenomic conformation composed of 110- and 78-kb subgenomes. The long-read data indicated that the two different genomic conformations were present in almost equal proportions in the plastomes of Selaginella nipponica. The mitogenome of S. nipponica was assembled into 27 contigs with a total size of 110 kb. All contigs contained directly arranged repeats at both ends, which introduced multiple conformations. Our results showed that plastomes and mitogenomes share high tRNA losses, GC-biased nucleotides, elevated substitution rates and complicated organization. The exploration of nuclear-encoded organelle DNA replication, recombination and repair proteins indicated that, several single-targeted proteins, particularly plastid-targeted recombinase A1, have been lost in Selaginellaceae; conversely, the dual-targeted proteins remain intact. According to the reported function of recombinase A1, we propose that the plastomes of spikemoss often fail to pair homologous sequences during recombination, and the dual-targeted proteins play a key role in the convergent genetic features of plastomes and mitogenomes. Our results provide a distinctive evolutionary pattern of the organelle genomes in Selaginellaceae and evidence of their convergent evolution.
质体和线粒体是内共生细胞器，它们储存遗传信息。这些细胞器的基因组在基因组结构和遗传内容方面通常表现出相反的模式。然而，在卷柏科中它们具有相似的遗传特征，对于导致平行进化的原因知之甚少。在这里，我们通过结合短读长和长读长，记录了从石松属植物中获得的多部分质体基因组（质体基因组）和高度分化的线粒体基因组（线粒体基因组）。188kb 的多部分质体基因组在主基因组构象中有三个核糖体操纵子拷贝，从而产生由 110-和 78-kb 亚基因组组成的替代亚基因组构象。长读长数据表明，两种不同的基因组构象在石松属植物的质体中几乎以相等的比例存在。石松属植物的线粒体基因组组装成 27 个重叠群，总大小为 110kb。所有重叠群的两端都含有直接排列的重复序列，这引入了多种构象。我们的结果表明，质体基因组和线粒体基因组具有高度的 tRNA 丢失、GC 偏向核苷酸、高替代率和复杂的组织。对核编码细胞器 DNA 复制、重组和修复蛋白的探索表明，几种单靶向蛋白，特别是质体靶向重组酶 A1，在卷柏科中已经丢失；相反，双靶向蛋白保持完整。根据报道的重组酶 A1 的功能，我们提出石松属植物的质体在重组过程中经常无法配对同源序列，双靶向蛋白在质体基因组和线粒体基因组的趋同遗传特征中发挥关键作用。我们的研究结果为卷柏科细胞器基因组的独特进化模式提供了证据，并证明了它们的趋同进化。
