BZU2/ZmMUTE controls symmetrical division of guard mother cell and specifies neighbor cell fate in maize

First author: Hongliang Wang; Affiliations: Henan University (河南大学): Kaifeng, China

Corresponding author: Chun-Peng Song

Intercellular communication in adjacent cell layers determines cell fate and polarity, thus orchestrating tissue specification and differentiation. Here we use the maize stomatal apparatus as a model to investigate cell fate determination. Mutations in ZmBZU2 (bizui2, bzu2) confer a complete absence of subsidiary cells (SCs) and normal guard cells (GCs), leading to failure of formation of mature stomatal complexes. Nuclear polarization and actin accumulation at the interface between subsidiary mother cells (SMCs) and guard mother cells (GMCs), an essential pre-requisite for asymmetric cell division, did not occur in Zmbzu2 mutants. ZmBZU2 encodes a basic helix-loop-helix (bHLH) transcription factor, which is an ortholog of AtMUTE in Arabidopsis (BZU2/ZmMUTE). We found that a number of genes implicated in stomatal development are transcriptionally regulated by BZU2/ZmMUTE. In particular, BZU2/ZmMUTE directly binds to the promoters of PAN1 and PAN2, two early regulators of protodermal cell fate and SMC polarization, consistent with the low levels of transcription of these genes observed in bzu2-1 mutants. BZU2/ZmMUTE has the cell-to-cell mobility characteristic similar to that of BdMUTE in Brachypodium distachyon. Unexpectedly, BZU2/ZmMUTE is expressed in GMC from the asymmetric division stage to the GMC division stage, and especially in the SMC establishment stage. Taken together, these data imply that BZU2/ZmMUTE is required for early events in SMC polarization and differentiation as well as for the last symmetrical division of GMCs to produce the two GCs, and is a master determinant of the cell fate of its neighbors through cell-to-cell communication.

相邻细胞之间的通信决定了细胞的命运与极性，因此塑造了组织的特化和分化。本文中，作者利用植物的气孔器作为模式对象研究了细胞的命运决定。玉米ZmBZU2基因的突变使得植株的副卫细胞和正常的保卫细胞均消失，进而导致植物不能形成成熟的气孔复合体。副卫母细胞和保卫母细胞接触面上核的极化以及肌动蛋白的积累是不对称分裂的基础，但这些在Zmbzu2突变体中并未发生。ZmBZU2基因编码一个碱性螺旋-环-螺旋bHLH转录因子，其是拟南芥中AtMUTE的同源物。作者发现参与气孔发育的很多基因在转录上受到BZU2蛋白的调控。尤其是，BZU2会直接结合到PAN1和PAN2基因的启动子区，而这两个基因是表皮原细胞命运以及副卫母细胞极化的早期调控因子，这与这两个基因在bzu2-1突变体中转录水平比较低的情况相一致。与短柄草中的BdMUTE蛋白性能类似，玉米中的BZU2蛋白同样具有在细胞和细胞间移动的能力。令人没想到的是，玉米BZU2蛋白从不对称分裂时期到保卫母细胞分裂时期均在保卫母细胞中表达，尤其是副卫母细胞的建立时期。综上，本文的数据显示了玉米的BZU2蛋白参与了副卫母细胞极化和分化的早期进程，并且也参与了保卫母细胞最后的形成两个保卫细胞的对称性分裂，另外该蛋白还通过细胞间的通信在邻细胞的命运决定过程中发挥主要调控作用。

通讯：宋纯鹏（http://bio.henu.edu.cn/info/1011/1822.htm)

个人简介：1990年，北京大学，硕士；1997年，中国农业大学，博士。

研究方向：1. 氧化还原信号的感受和信号转导；2. 植物应答干旱胁迫的气孔调节机制；3. 环境胁迫调节根系构型形态建成的分子机制。

doi: https://doi.org/10.1371/journal.pgen.1008377

Journal: PLOS Genetics

Published date: August 29, 2019