Developmental Systems Drift and the Evolution of Redundancy in Plants

真核生物的发育在很大程度上是由一组保守的调控基因控制的，这些基因在相关物种中发挥着非常相似的功能。然而，在酵母和动物中已经描述了许多例子，其中表型保守的性状由不同的分子途径控制。当相关物种的同源基因突变导致不同的表型时，这种所谓的发育系统漂移变得明显。一个可能的原因是同一物种的两个基因之间存在差异冗余，而其他物种则没有。我们最近在红荠菜风疹中发现了一个相关的例子，其中叶片ON PETIOLE2 （BOP2）基因的功能缺失突变导致异位苞片的完全渗透形成，这在密切相关的模式植物拟南芥的BOP2突变中没有看到；在后者中，苞片的形成只在bop1 bop2双突变体中看到，以及许多其他突变表型。我们假设这种差异反映了BOP1和BOP2在两个物种之间的差异冗余，这两个基因在拟南拟南拟中仍然完全冗余，但在风疹中不是，在大多数过程中都可以看到冗余，但在抑制苞片形成方面没有。这种冗余的部分解决反映了两个基因的亚功能化的第一步，这是冗余进化的一个重要过程。虽然从理论角度对发育系统漂移和亚功能化进行了深入研究，但对植物早期亚功能化突变的分子基础、群体遗传学和发育后果知之甚少。因此，建议的项目将利用BOP1/2的例子，从进化和功能的角度经验地解决这些问题。具体而言，我们将努力实现以下主要目标。(1)我们将详细定义拟南芥和风疹C. BOP1之间的分子差异，这可能是导致BOP1在苞片抑制中功能丧失的原因。这将确定植物中两个冗余基因之间的第一个早期亚功能突变之一。(2)我们将分析Capsella中这个亚功能化突变的群体遗传学，以验证它在风疹衣原体中由于漂移而固定的假设。此外，我们将通过实验检测BOP1/2冗余在其他芸花科植物中的状态，以确定该基因对之间的冗余分解是否也在其他分类群中进行。(3)我们将通过比较芥和拟南芥在苞片抑制方面的发育错误频率，来验证冗余有助于使发育过程更加稳健的假设。总之，这些研究将为亚功能化的早期阶段和植物发育系统漂移提供前所未有的见解。

Development in eukaryotes is controlled to a large extent by a conserved set of regulatory genes that fulfil very similar functions in related species. However, a number of examples have been described in yeast and animals where a phenotypically conserved trait is controlled by divergent molecular pathways. This so-called developmental systems drift becomes apparent, when mutations in orthologous genes in related species cause different phenotypes. One possible reason for this is differential redundancy between two genes in one, but not the other species. We have recently identified a pertinent example in the Red Shepherd’s Purse Capsella rubella, where a loss-of-function mutation in the BLADE ON PETIOLE2 (BOP2) gene leads to a fully penetrant formation of ectopic bracts, which is not seen in bop2 mutants in the closely related model plant Arabidopsis thaliana; in the latter, bract formation is only seen in bop1 bop2 double mutants, together with a host of additional mutant phenotypes. We hypothesize that this difference reflects differential redundancy between BOP1 and BOP2 between the two species, with the two genes still fully redundant in A. thaliana for all of their functions, but not in C. rubella, where redundancy is seen for most processes, but not for the suppression of bract formation. This partial resolution of redundancy reflects a first step towards subfunctionalization of the two genes, an important process in the evolution of redundancy. While both developmental systems drift and subfunctionalization have been studied intensively from a theoretical perspective, little is known about the molecular basis, population genetics and developmental consequences of early-stage subfunctionalizing mutations in plants. Therefore, the proposed project will exploit the example of BOP1/2 to empirically address these issues from an evolutionary and functional perspective. In particular, we will pursue the following main objectives. (1) We will define in detail the molecular difference between A. thaliana and C. rubella BOP1 that is responsible for the presumed loss of BOP1 function in bract suppression. This will identify one of the first early subfunctionalizing mutations between two redundant genes in plants. (2) We will analyze the population genetics of this subfunctionalizing mutation in Capsella to test the hypothesis that it became fixed in C. rubella due to drift. In addition, we will experimentally test the status of BOP1/2 redundancy in other Brassicaceae to determine whether resolution of redundancy between this gene pair is also ongoing in other taxa. (3) We will test the hypothesis that redundancy serves to render developmental processes more robust by comparing the frequency of developmental errors regarding bract suppression between Capsella and Arabidopsis. Together, these studies will provide unprecedented insight into the early stages of subfunctionalization and into developmental systems drift in plants.