Polarity is a fundamental feature of cells and can manifest itself both in overall morphology and in the unequal distribution of molecular components. Cell polarity, in both animals and plants, is of paramount importance for many developmental and physiological processes. The establishment and maintenance of cell polarity are required for asymmetric cell division (ACD), an indispensable mechanism for multi-cellular organisms to generate cellular diversity by producing daughter cells with distinctive identities from a single mother cell. Extensive studies in animal systems have revealed a set of conserved proteins that link cell polarization to asymmetric division control. Plant genomes do not seem to encode these “polarity” proteins and the molecular components and mechanical basis for plant asymmetric division has been an enigma for decades. Studies on the novel plant protein BASL (Breaking of Asymmetry in the Stomatal Lineage) provided strong evidence that plant cells also have the capability to polarize non-transmembrane proteins and utilize polarized protein distribution to regulate asymmetric cell division (Dong, et al., 2009).

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During the past years, we established a positive feedback loop between BASL and a mitogen-activated protein kinase (MAPK) signaling cascade that promotes cell polarity. During stomatal development, the canonical MAPK signaling cascade, comprising of the MAPKK Kinase YODA (YDA), the MAPK Kinase 4/5, and MAPK 3/6, plays pivotal roles in stomatal development and patterning. We found that MPK3/6 phosphorylates BASL, causing BASL to exit the nucleus and become polarized on the cell cortex, where BASL acts as a scaffold protein to recruit YDA and MPK3/6 into the cortical polarity site. We demonstrated that the polarized YDA-MPK3/6 cascade provides a key mechanism for cell specification, as it is asymmetrically inherited into the large daughter cell that undergoes pavement cell differentiation. MPK3/6 directly phosphorylate the master stomatal lineage transcription factor SPCH, leading to asymmetric degradation of SPCH, thus asymmetric daughter cell fates (Zheng et al., Dev Cell 2015; Zhang et al., Curr Bio 2016).

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Our research interests are to 1) uncover the fundamental principles that govern cell polarization and ACD and 2) elucidate the mechanisms underpinning the connections among cell polarization, ACD, and cell differentiation using the stomatal system as a model. To achieve these goals, we are addressing several major gaps in the field, including (i) how cell polarity is initiated and established, (ii) how cellular asymmetry is maintained, (iii) how asymmetric division plane orientation is directed by polarity, (iv) how cell division and differentiation potentials are balanced, and (v) how cell fate asymmetry is specified. In the next few years, we aim to g advance our mechanistic understanding of cell polarity, ACD, and cell differentiation by 1) delineating new pathways of endosomal trafficking that determine cell polarization and ACD and 2) establishing new functions of cell signaling in balancing self-renewal division and terminal cell fate differentiation during stomatal ACD.

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