Dissecting the pathways coordinating patterning and growth by plant boundary domains

Boundary domains play important roles during morphogenesis in plants and animals, but how they contribute to patterning and growth coordination in plants is not understood. The CUC genes determine the boundary domains in the aerial part of the plants and, in particular, they have a conserved role in regulating leaf complexity across Angiosperms. Here, we used tooth formation at the Arabidopsis leaf margin controlled by the CUC2 transcription factor to untangle intertwined events during boundary-controlled morphogenesis in plants. Combining conditional restoration of CUC2 function with morphometrics as well as quantification of gene expression and hormone signaling, we first established that tooth morphogenesis involves a patterning phase and a growth phase. These phases can be separated, as patterning requires CUC2 while growth can occur independently of CUC2. Next, we show that CUC2 acts as a trigger to promote growth through the activation of three functional relays. In particular, we show that KLUH acts downstream of CUC2 to modulate auxin response and that expressing KLUH can compensate for deficient CUC2 expression during tooth growth. Together, we reveal a genetic and molecular network that allows coordination of patterning and growth by CUC2-defined boundaries during morphogenesis at the leaf margin.

边界域（boundary domains）在动植物形态发生（morphogenesis）过程中发挥关键作用，但目前学界尚未明确其如何参与植物的模式建成（patterning）与生长协调（growth coordination）。CUC基因（CUC genes）决定植物地上部分的边界域，且在调控被子植物（Angiosperms）的叶复杂性（leaf complexity）方面具有保守功能。本研究以拟南芥（Arabidopsis）叶缘（leaf margin）受CUC2转录因子（CUC2 transcription factor）调控的齿状突起形成（tooth formation）为模型，解析植物边界域控制的形态发生过程中相互交织的分子事件。通过将CUC2功能的条件性恢复与形态计量学（morphometrics）、基因表达（gene expression）及激素信号（hormone signaling）定量分析相结合，我们首先明确齿状突起的形态发生包含模式建成阶段与生长阶段。这两个阶段可被独立分离：模式建成过程依赖CUC2的表达，而生长过程则可脱离CUC2独立进行。后续研究表明，CUC2可通过激活三类功能通路作为生长的触发因子。具体而言，我们发现KLUH蛋白（KLUH）作用于CUC2下游以调控生长素响应（auxin response），且过表达KLUH可弥补齿状突起生长过程中CUC2表达不足的缺陷。综上，本研究揭示了一套遗传与分子网络，该网络可使拟南芥叶缘形态发生过程中，由CUC2定义的边界域实现模式建成与生长的协同调控。