Investigation of cell polarity mechanisms connected to cell fate and pattern formation in Arabidopsis vascular and stomatal development
Final Report Abstract
Cell polarity combined with asymmetric cell divisions (ACDs) is key to generate cellular diversity in tissues of multicellular organisms. In animal cells, mutually inhibitory plasmamembrane associated domains can orient divisions and ensure differential segregation of fate determinants. In the Arabidopsis thaliana stomatal lineage, a cortical polarity domain marked by BASL and BRXL family members orients asymmetric cell divisions (ACD) and is consistently inherited by the bigger daughter cell that subsequently exits the lineage. This division orientation and differential inheritance of polarity factors is critical to allow uniform patterning of stomata, which are valves of gas exchange, within the epidermis of leaves. A long-standing question was whether stomatal lineage cells could support a second, reciprocal polarity domain that polarizes opposite of BASL-BRXL to regulated fate of the smaller meristemoid daughter cell, which ultimately differentiates into guard cells that form a stoma. In this project, I show that stomatal lineage cells can sustain two independent and opposing cortical polarity domains that segregate distinct proteins to each daughter cell during ACDs. This second and novel plasma membrane domain is marked by several OCTOPUS- LIKE (OPL) family members, which polarize prior to ACDs opposite of BASL-BRX and are consistently inherited to meristemoids. Through genetic and misexpression analyses I show that OPLs polarize to promote meristemoid amplifying divisions and delay stomatal fate progression independently of a reciprocal BASL-BRXL domain. Asymmetric sequestration of OPL proteins seems to be critical for differential fate determination and proliferation of stomatal daughters. By utilizing proximity labelling and comparing the plasma membrane proteomes of the reciprocal BRXL and OPL domains I identified several new protein-protein interaction partners that could act with OPLs in regulating cell division. Although OPLs are only evolutionarily conserved in seed plants, ectopic expression in the liverwort Marchantia polymorpha can also promote cell proliferation and suppress fate progression of thalli. I therefore propose that OPLs utilize an ancient signalling pathway present among widely diverged plants to regulate cell division and fate of the leaf epidermis. These findings open manifold possibilities for follow-up studies and – for the first time – allow to investigate reciprocal polarity domains during ACDs in plant development, which will help to gain a better understanding of division and fate determination in plants in general, and stomatal fate and patterning in particular.
Publications
- Quantitative and dynamic cell polarity tracking in plant cells. New Phytologist
Gong Y, Varnau R, Wallner ES, Acharya R, Bergmann DC, Cheung LS
(See online at https://doi.org/10.1111/nph.17165) - The value of asymmetry: how polarity proteins determine plant growth and morphology. The Journal of Experimental Botany
Wallner ES
(See online at https://doi.org/10.1093/jxb/eraa329)
