The making of Delphinieae flowers through rewiring the interactions between duplicated and diversified floral organ identity and symmetry genes

Species of the tribe Delphinieae (Ranunculaceae) have long been the focus of morphological, ecological and evolutionary studies for their highly specialized, nearly zygomorphic spiral flowers with nested petal and sepal spurs and reduced petals. The mechanisms underlying the development and evolution of the Delphinieae flowers, however, remain unclear. Here, by conducting extensive phylogenetic, comparative transcriptomic, expression and functional studies, we clarify the evolutionary histories, expression patterns and functions of floral organ identity and symmetry genes in Delphinieae. We find that duplication and/or diversification of APETALA3-3 (AP3-3), AGAMOUS-LIKE6 (AGL6), CYCLOIDEA (CYC) and DIVARICATA (DIV) lineage genes were tightly associated with the origination of the Delphinieae flowers. Specifically, an AGL6-lineage member (such as the Delphinium ajacis AGL6-1a) represses sepal spur formation and petal development in the lateral and ventral parts of the flower while determining petal identity redundantly with AGL6-1b. Two CYC2-like genes, CYC2b and CYC2a, however, define the dorsal and lateral/ventral identities of the flower, respectively, and form complex regulatory links with AP3-3, AGL6-1a and DIV1. Duplication and diversification of floral symmetry genes, as well as co-option of the duplicated copies into the pre-existing floral regulatory network, therefore, have been the key to the origin of the Delphinieae flowers

翠雀族（Delphinieae）隶属毛茛科（Ranunculaceae），其植物因高度特化、近两侧对称的螺旋状花，以及嵌套分布的花瓣距与萼片距、退化花瓣的特征，长期以来一直是形态学、生态学与进化生物学研究的焦点。然而，翠雀族花发育与演化背后的分子机制仍不明晰。本研究通过开展大规模系统发育分析、比较转录组学、基因表达及功能实验研究，阐明了翠雀族花器官特征基因与花对称性基因的演化历史、表达模式及生物学功能。研究发现，APETALA3-3（AP3-3）、AGAMOUS-LIKE6（AGL6）、CYCLOIDEA（CYC）与DIVARICATA（DIV）基因家族的复制与/或功能分化，与翠雀族花的起源紧密相关。具体而言，一类AGL6家族成员（如飞燕草Delphinium ajacis的AGL6-1a）可在花的侧部与腹部抑制萼片距形成与花瓣发育，同时与AGL6-1b以功能冗余的方式共同决定花瓣身份。而两个CYC2类基因——CYC2b与CYC2a，分别决定花的背部与侧部/腹部身份，并与AP3-3、AGL6-1a及DIV1形成复杂的调控关联。综上，花对称性基因的复制与功能分化，以及将复制后的基因拷贝共招募至预先存在的花发育调控网络中，是翠雀族花起源的关键机制。