Department of Plant Sciences, University of Oxford, Oxford OX1 3RB, UK.
Mechanobiology Institute and Department of Biological Sciences, National University of Singapore, 117411 Singapore, Singapore.
Curr Biol. 2020 May 18;30(10):1905-1915.e4. doi: 10.1016/j.cub.2020.03.032. Epub 2020 Apr 2.
Lateral inhibition patterns differentiated cell types among equivalent cells during development in bacteria, metazoans, and plants. Tip-growing rhizoid cells develop among flat epidermal cells in the epidermis of the early-diverging land plant Marchantia polymorpha. We show that the majority of rhizoid cells develop individually, but some develop in linear, one-dimensional groups (chains) of between 2 and 7 rhizoid cells in wild-type plants. The distribution of rhizoid cells can be accounted for within a simple cellular automata model of lateral inhibition. The model predicted that in the absence of lateral inhibition, two-dimensional rhizoid cell groups (clusters) form. These can be larger than those formed with lateral inhibition. M. polymorpha rhizoid differentiation is positively regulated by the ROOT HAIR DEFECTIVE SIX-LIKE1 (MpRSL1) basic-helix-loop-helix (bHLH) transcription factor, which is directly repressed by the FEW RHIZOIDS1 (MpFRH1) microRNA (miRNA). To test if MpFRH1 miRNA acts during lateral inhibition, we generated loss-of-function (lof) mutants without the MpFRH1 miRNA. Two-dimensional clusters of rhizoids develop in Mpfrh1 mutants as predicted by the model for plants that lack lateral inhibition. Furthermore, two-dimensional clusters of up to 9 rhizoid cells developed in the Mpfrh1 mutants compared to a maximum number of 7 observed in wild-type groups. The higher steady-state levels of MpRSL1 mRNA in Mpfrh1 mutants indicate that MpFRH1-mediated lateral inhibition involves the repression of MpRSL1 activity. Together, the modeling and genetic data indicate that MpFRH1 miRNA mediates lateral inhibition by repressing MpRSL1 during pattern formation in the M. polymorpha epidermis.
侧向抑制模式在细菌、后生动物和植物的发育过程中区分了等同细胞的类型。在早期分化的陆地植物 Marchantia polymorpha 的表皮中，顶端生长的根状细胞在扁平的表皮细胞之间发育。我们表明，大多数根状细胞单独发育，但在野生型植物中，有些根状细胞以 2 到 7 个根状细胞的线性一维组（链）发育。根状细胞的分布可以用简单的侧向抑制细胞自动机模型来解释。该模型预测，如果没有侧向抑制，二维根状细胞群（簇）会形成。这些比具有侧向抑制形成的要大。M. polymorpha 根状分化受 ROOT HAIR DEFECTIVE SIX-LIKE1（MpRSL1）碱性-螺旋-环-螺旋（bHLH）转录因子的正调控，该转录因子直接受少数根状 1（MpFRH1）microRNA（miRNA）的抑制。为了测试 MpFRH1 miRNA 是否在侧向抑制过程中起作用，我们生成了没有 MpFRH1 miRNA 的功能丧失（lof）突变体。如缺乏侧向抑制的植物模型所预测的那样，Mpfrh1 突变体中根状细胞形成二维簇。此外，在 Mpfrh1 突变体中，二维簇中最多可发育 9 个根状细胞，而在野生型群体中最多观察到 7 个。Mpfrh1 突变体中 MpRSL1 mRNA 的稳态水平较高，表明 MpFRH1 介导的侧向抑制涉及对 MpRSL1 活性的抑制。综上所述，模型和遗传数据表明，MpFRH1 miRNA 通过在 M. polymorpha 表皮的模式形成过程中抑制 MpRSL1 来介导侧向抑制。
