Institute of Ecology and Evolutionary Biology, National Taiwan University, Taipei, Taiwan.
Department of Life Science, National Taiwan University, Taipei, Taiwan.
PLoS One. 2019 Jan 30;14(1):e0210054. doi: 10.1371/journal.pone.0210054. eCollection 2019.
Floral bilateral symmetry is one of the most important acquisitions in flower shape evolution in angiosperms. Members of Gesneriaceae possess predominantly zygomorphic flowers yet natural reversal to actinomorphy have independently evolved multiple times. The development of floral bilateral symmetry relies greatly on the gene CYCLOIDEA (CYC). Our reconstructed GCYC phylogeny indicated at least five GCYC duplication events occurred over the evolutionary history of Gesneriaceae. However, the patterns of GCYC expression following the duplications and the role of natural selection on GCYC copies in relation to floral symmetry remained largely unstudied. The Asiatic tribe Trichosporeae contains most reversals to actinomorphy. We thus investigated shifts in GCYC gene expression among selected zygomorphic species (Hemiboea bicornuta and Lysionotus pauciflorus) and species with reversals to actinomorphy (Conandron ramondioides) by RT-PCR. In the actinomorphic C. ramondioides, none of the three copies of GCYC was found expressed in petals implying that the reversal was a loss-of-function event. On the other hand, both zygomorphic species retained one GCYC1 copy that was expressed in the dorsal petals but each species utilized a different copy (GCYC1C for H. bicornuta and GCYC1D for L. pauciflorus). Together with previously published data, it appeared that GCYC1C and GCYC1D copies diversified their expression in a distinct species-specific pattern. To detect whether the selection signal (ω) changed before and after the duplication of GCYC1 in Asiatic Trichosporeae, we reconstructed a GCYC phylogeny using maximum likelihood and Bayesian inference algorithms and examined selection signals using PAML. The PAML analysis detected relaxation from selection right after the GCYC1 duplication (ωpre-duplication = 0.2819, ωpost-duplication = 0.3985) among Asiatic Trichosporeae species. We propose that the selection relaxation after the GCYC1 duplication created an "evolutionary window of flexibility" in which multiple copies were retained with randomly diverged roles for dorsal-specific expressions in association with floral symmetry changes.
花的两侧对称是被子植物花形进化中最重要的获得特征之一。苦苣苔科的成员主要具有左右对称的花，但花的左右对称的反转已独立进化了多次。花的两侧对称的发育很大程度上依赖于 CYCLOIDEA（CYC）基因。我们重建的 GCYC 系统发育表明，在苦苣苔科的进化历史中至少发生了五次 GCYC 复制事件。然而，复制后 GCYC 表达模式以及自然选择对与花对称性相关的 GCYC 副本的作用在很大程度上仍未得到研究。亚洲的苣苔族（Trichosporeae）包含了大多数花左右对称的反转。因此，我们通过 RT-PCR 研究了选定的左右对称物种（Hemiboea bicornuta 和 Lysionotus pauciflorus）和左右对称反转物种（Conandron ramondioides）中 GCYC 基因表达的变化。在左右对称的 C. ramondioides 中，三个 GCYC 拷贝都没有在花瓣中表达，这表明反转是一个功能丧失事件。另一方面，两个左右对称的物种都保留了一个 GCYC1 拷贝，该拷贝在背侧花瓣中表达，但每个物种都使用了不同的拷贝（H. bicornuta 用 GCYC1C，L. pauciflorus 用 GCYC1D）。结合之前发表的数据，似乎 GCYC1C 和 GCYC1D 拷贝以一种独特的物种特异性模式多样化了它们的表达。为了检测 GCYC1 在亚洲苣苔族中的复制前后选择信号（ω）是否发生变化，我们使用最大似然法和贝叶斯推断算法重建了 GCYC 系统发育，并使用 PAML 检查了选择信号。PAML 分析检测到 GCYC1 复制后选择松弛（ω复制前=0.2819，ω复制后=0.3985）。我们提出，GCYC1 复制后的选择松弛在花对称性变化相关的背侧特异性表达中创造了一个“进化灵活性窗口”，其中多个拷贝被保留下来，随机发散作用。
