Molecular Framework of a Regulatory Circuit Initiating Two-Dimensional Spatial Patterning of Stomatal Lineage.
Molecular Framework of a Regulatory Circuit Initiating Two-Dimensional Spatial Patterning of Stomatal Lineage.
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DOI：
10.1371/journal.pgen.1005374
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发表时间：
2015-07
期刊：
影响因子：
4.5
通讯作者：
Torii KU
中科院分区：
文献类型：
--
作者：
Horst RJ;Fujita H;Lee JS;Rychel AL;Garrick JM;Kawaguchi M;Peterson KM;Torii KU
气孔是植物表皮上的阀门，对植物的生长和生存至关重要，气孔的存在影响着全球的水和碳循环。尽管调控气孔发育的转录因子和细胞-细胞信号成分已被鉴定，但它们的调控相互作用如何转化为气孔起始细胞的二维模式仍不清楚。利用分子遗传学、成像和数学模拟，我们报道了一个启动气孔细胞谱系的调节电路。该电路包括一个正反馈回路，构成需要无言以对的尖叫的自我激活。这个转录因子模块直接与启动子结合，激活一个分泌信号，表皮图案化因子2和受体修饰物太多的嘴，而受体ERECTA位于这个模块的外部。这进而抑制了SPCH，从而抑制了SCRM，从而构成了负反馈回路。我们的数学模型通过在电路中加入两个额外的组件来准确预测所有已知的气孔表型：一个独立于EPF2的负反馈环和一个位于SPCH·SCRM模块之外的信号。我们的工作揭示了控制植物表皮中自组织二维图案的复杂分子框架。自组织、功能性组织模式的产生对多细胞生物体的发育和再生至关重要。陆地植物表皮上的小阀门，称为气孔，在调节气体交换的同时将水分损失降至最低。气孔的密度和间距受驱动分化的转录因子以及调节气孔谱系细胞进入和间距的细胞-细胞信号成分的调节。为了揭示这些成分的相互作用如何转化为气孔的二维模式，我们采取了一种综合的方法，利用分子遗传学、成像和数学模型。在这篇文章中，我们已经确定了一个控制气孔细胞谱系启动的调节电路。该电路的关键元件是构成转录因子Scream/SCREAM2(SCRMS)自我激活的正反馈环(需要无言语(SPCH))，以及涉及信号配体EPF2、受体修饰物太多张口和SPCH·SCRMS模块的负反馈环。另一方面，受体ERECTA位于调控环路之外。我们的数学模型概括了所有已知的气孔表型，增加了两个调节节点。这项工作突出了植物中自组织模式系统的分子框架。
Stomata, valves on the plant epidermis, are critical for plant growth and survival, and the presence of stomata impacts the global water and carbon cycle. Although transcription factors and cell-cell signaling components regulating stomatal development have been identified, it remains unclear as to how their regulatory interactions are translated into two-dimensional patterns of stomatal initial cells. Using molecular genetics, imaging, and mathematical simulation, we report a regulatory circuit that initiates the stomatal cell-lineage. The circuit includes a positive feedback loop constituting self-activation of SCREAMs that requires SPEECHLESS. This transcription factor module directly binds to the promoters and activates a secreted signal, EPIDERMAL PATTERNING FACTOR2, and the receptor modifier TOO MANY MOUTHS, while the receptor ERECTA lies outside of this module. This in turn inhibits SPCH, and hence SCRMs, thus constituting a negative feedback loop. Our mathematical model accurately predicts all known stomatal phenotypes with the inclusion of two additional components to the circuit: an EPF2-independent negative-feedback loop and a signal that lies outside of the SPCH•SCRM module. Our work reveals the intricate molecular framework governing self-organizing two-dimensional patterning in the plant epidermis. Generation of self-organized, functional tissue patterns is critical for development and regeneration in multicellular organisms. Small valves on the epidermis of land plants, called stomata, mediate gas-exchange while minimizing water loss. Density and spacing of stomata are regulated by transcription factors that drive differentiation as well as by cell-cell signaling components that regulate entry and spacing of stomatal lineage cells. To unravel how interaction of these components translates into two-dimensional patterning of stomata, we have taken an integrative approach employing molecular genetics, imaging, and mathematical modeling. In this paper we have identified a regulatory circuit controlling the initiation of the stomatal cell lineage. The key elements of the circuit are a positive feedback loop constituting self-activation of the transcription factors SCREAM / SCREAM2 (SCRMs) that requires SPEECHLESS (SPCH), and a negative feedback loop involving the signaling ligand EPF2, the receptor modifier TOO MANY MOUTHS, and the SPCH•SCRMs module. The receptor ERECTA, on the other hand, lies outside of the regulatory loop. Our mathematical modeling recapitulated all known stomatal phenotypes with the addition of two regulatory nodes. This work highlights the molecular framework of a self-organizing patterning system in plants.