Institute for Biochemistry and Biology, University of Potsdam, Potsdam-Golm D-14476, Germany.
Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm D-14476, Germany.
Plant Cell. 2024 Oct 3;36(10):4637-4657. doi: 10.1093/plcell/koae232.
Duplicated genes are thought to follow one of three evolutionary trajectories that resolve their redundancy: neofunctionalization, subfunctionalization, or pseudogenization. Differences in expression patterns have been documented for many duplicated gene pairs and interpreted as evidence of subfunctionalization and a loss of redundancy. However, little is known about the functional impact of such differences and about their molecular basis. Here, we investigate the genetic and molecular basis for the partial loss of redundancy between the two BLADE-ON-PETIOLE genes BOP1 and BOP2 in red shepherd's purse (Capsella rubella) compared to Arabidopsis (Arabidopsis thaliana). While both genes remain almost fully redundant in A. thaliana, BOP1 in C. rubella can no longer ensure wild-type floral organ numbers and suppress bract formation, due to an altered expression pattern in the region of the cryptic bract primordium. We use two complementary approaches, transgenic rescue of A. thaliana atbop1 atbop2 double mutants and deletions in the endogenous AtBOP1 promoter, to demonstrate that several BOP1 promoter regions containing conserved noncoding sequences interact in a nonadditive manner to control BOP1 expression in the bract primordium and that changes in these interactions underlie the evolutionary divergence between C. rubella and A. thaliana BOP1 expression and activity. Similarly, altered interactions between cis-regulatory regions underlie the divergence in functional promoter architecture related to the control of floral organ abscission by BOP1. These findings highlight the complexity of promoter architecture in plants and suggest that changes in the interactions between cis-regulatory elements are key drivers for evolutionary divergence in gene expression and the loss of redundancy.
新功能化、亚功能化或假基因化。许多复制基因对的表达模式差异已经被记录下来，并被解释为亚功能化和冗余丧失的证据。然而，对于这些差异的功能影响及其分子基础知之甚少。在这里，我们研究了红色荠菜（Capsella rubella）中两个叶片状叶柄基因 BOP1 和 BOP2 之间部分冗余丧失的遗传和分子基础，与拟南芥（Arabidopsis thaliana）相比。虽然这两个基因在拟南芥中仍然几乎完全冗余，但 BOP1 在 C. rubella 中由于在隐性苞片原基区域的表达模式改变，不再能够确保野生型花器官数量并抑制苞片形成。我们使用两种互补的方法，即转基因拯救拟南芥 atbop1 atbop2 双突变体和内源性 AtBOP1 启动子缺失，证明包含保守非编码序列的几个 BOP1 启动子区域以非加性方式相互作用，以控制 BOP1 在苞片原基中的表达，并且这些相互作用的变化是 C. rubella 和 A. thaliana BOP1 表达和活性进化分歧的基础。类似地，与 BOP1 控制花器官脱落相关的功能启动子结构的顺式调控区之间的相互作用的改变，导致了功能启动子结构的差异。这些发现强调了植物启动子结构的复杂性，并表明顺式调控元件之间相互作用的改变是基因表达和冗余丧失进化分歧的关键驱动因素。
