Platanthera zijinensis and Platanthera guangdongensis Genome sequencing and assembly

Mycoheterotrophs exist in almost every major lineage of terrestrial plants, but the majority of them are found in the family Orchidaceae. To improve our understanding of the origin and evolution of mycoheterotrophic plants, we here present the genome sequences of two sibling orchid species, estimated to have diverged approximately 22 Mya, namely the leafy, partially mycoheterotrophic Platanthera zijinensi with roots, and the leafless, fully mycoheterotrophic P. guangdongensis without roots. For both species we obtained chromosome-scale assemblies and found that their large genome sizes are mainly due to the expansion of retrotransposons Gypsy and Copia. Comparative analysis with other, previously sequenced orchids shows that mycoheterotrophy in Orchidaceae is associated with increased substitution rates and gene loss. Specifically, the fully mycoheterotrophic orchids P. guangdongensis and Gastrodia elata have lost many, if not most genes involved in photosynthesis. Also, deletion of most photoreceptor genes and auxin transporter genes might be linked to the unique leafless and rootless phenotypes of fully mycoheterotrophic orchids. Conversely, trehalase genes that catalyse the conversion of trehalose into glucose have expanded in most sequenced orchids, in line with the fact that the germination of orchid non-endosperm seeds needs carbohydrates from fungi during the protocorm stage. We further show that the mature plant of the fully mycoheterotrophic P. guangdongensis, different from photosynthetic orchids, keep expressing trehalase genes to hijack trehalose from fungi. Therefore, we propose that mycoheterotrophy in mature orchids is a continuation of the protocorm stage by sustaining the expression of trehalase genes. Our results shed light on the molecular mechanism underlying initial, partial and full mycoheterotrophy.

真菌异养植物（Mycoheterotrophs）几乎存在于所有陆生植物的主要演化支中，但其中绝大多数类群隶属于兰科（Orchidaceae）。为深化我们对菌异养植物起源与演化的认知，本研究报道了两个姊妹兰科物种的基因组序列——二者预估约于2200万年前发生分化，具体为具根、带叶的兼性菌异养植物紫金舌唇兰（Platanthera zijinensi），以及无叶、无根的专性菌异养植物广东舌唇兰（P. guangdongensis）。针对这两个物种，我们均获得了染色体级别的基因组组装结果，并发现其较大的基因组尺寸主要源于反转录转座子（retrotransposons）Gypsy与Copia的扩张。通过与已发表全基因组测序的其他兰科物种开展比较分析，我们发现兰科的菌异养特性与更高的碱基替换速率及基因丢失事件显著相关。具体而言，专性菌异养兰科植物广东舌唇兰（P. guangdongensis）与天麻（Gastrodia elata）已丢失了绝大多数参与光合作用的基因。此外，多数光受体基因与生长素转运基因的缺失，可能与专性菌异养兰科植物特有的无叶、无根表型存在关联。与之相反，在多数已测序兰科物种中，催化海藻糖（trehalose）转化为葡萄糖的海藻糖酶基因（trehalase genes）发生了扩张，这与兰科无胚乳种子在原球茎（protocorm）阶段需依赖真菌提供碳水化合物以完成萌发的事实相符。我们进一步发现，与光合兰科植物不同，专性菌异养的广东舌唇兰成熟植株仍持续表达海藻糖酶基因，以此从真菌中截获海藻糖。据此，我们提出：成熟兰科植物的菌异养特性，是通过维持海藻糖酶基因的表达，延续了原球茎阶段的营养获取策略。本研究结果为阐释初始型、兼性型及专性型菌异养的分子机制提供了重要见解。