Interspecific plastome recombination in Picea (Pinaceae) reveals ancient reticulate evolution

Plastid sequences are a cornerstone in plant evolutionary inference and their interpretation is often guided by strong assumptions. Biparental inheritance, heteroplasmy, and sexual recombination appear rare, but detecting exceptions to these rules requires extensive taxon sampling and abundant sequence data. Utilizing advancements in high-throughput sequencing, we analyzed the whole plastomes of 65 accessions of Picea, a genus of ~35 coniferous forest trees, to test for violations of canonical plastome evolution. Using complementary hypothesis and data-driven tests, we found evidence for plastomes generated by interspecific hybridization and sexual recombination in the clade comprising Norway spruce (P. abies) and ten other species. Support for interspecific recombination remained after controlling for sequence saturation, positive selection, and potential alignment artifacts. These results resolve conflicting plastid-based phylogenies reported in previous studies and strengthen the inference of reticulate evolution in Picea. Given the relatively high frequency of biparental plastid inheritance and hybridization in plants, we suggest interspecific plastome recombination may be more widespread than currently appreciated and could underlie reported cases of discordant plastid phylogenies.

质体序列（plastid sequences）是植物进化推断研究的基石，其解读往往依托一系列严格假设。双亲遗传（biparental inheritance）、异质性（heteroplasmy）与有性重组（sexual recombination）在质体中较为罕见，但要检测这些规律的例外情况，需开展大范围类群采样并获取充足的序列数据。本研究依托高通量测序（high-throughput sequencing）技术的最新进展，对约35种针叶林树种所属的云杉属（Picea）的65份种质材料（accessions）的完整质体基因组（whole plastomes）进行分析，以检验是否存在违背经典质体基因组进化模式的情况。通过结合互补的假设驱动与数据驱动检验方法，本研究在包含欧洲云杉（P. abies）及其余10个物种的演化支（clade）中，发现了由种间杂交（interspecific hybridization）与有性重组产生质体基因组的证据。在控制序列饱和（sequence saturation）、正选择（positive selection）以及潜在比对误差（alignment artifacts）等干扰因素后，种间重组的支持信号依然显著。本研究结果解决了以往研究中基于质体序列的系统发育树（plastid-based phylogenies）之间的矛盾，并强化了云杉属存在网状进化（reticulate evolution）的推断。鉴于植物中双亲质体遗传与杂交事件的发生频率相对较高，本研究认为种间质体基因组重组的分布范围可能比目前认知的更广，且其或为此前报道的诸多不一致的质体系统发育树（discordant plastid phylogenies）案例的潜在成因。