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(plastid)序列是植物演化推断的基石，其相关解读往往基于诸多严格假设。双亲遗传、异质性与有性重组的现象看似罕见，但要检测这些规律的例外情况，需要开展大范围的类群取样并获取充足的序列数据。借助高通量测序(high-throughput sequencing)技术的进步，我们对65份云杉属(Picea，包含约35种针叶林树种)的全质体基因组(plastome)进行了分析，以此检验经典质体基因组演化规律是否存在例外。通过互补的假设驱动与数据驱动检验方法，我们在包含欧洲云杉(P. abies)及其余10个物种的演化支中，发现了由种间杂交与有性重组产生质体基因组的证据。在控制序列饱和、正选择以及潜在比对伪影等干扰因素后，种间重组的支持信号依然显著。本研究结果解决了既往研究中基于质体的系统发育树存在的冲突问题，并强化了云杉属存在网状演化的推断。考虑到植物中双亲质体遗传与杂交事件的发生频率相对较高，我们认为种间质体基因组重组的分布范围可能比当前认知更广，且或许是诸多已报道的质体系统发育树不一致现象的潜在成因。