How do cells encode spatial information?
All cells, from a single bacterium to the neurons in our own bodies, must sense their environments and tune their behaviors accordingly. What solutions have evolved to overcome this universal biological problem? Cell polarity is one answer, allowing individual cells to interpret, encode, utilize, and propagate spatial information within single cells and among cellular collectives. In the Muroyama lab, we are inspired by the growing consensus that polarity has evolved independently in the major branches of life and are, therefore, interrogating the mechanisms that link polarity across biological scales in developing plant tissues.
Plant development relies on many of the same processes that pattern animal tissues, including regulation of cell identity, morphological elaboration, and short- and long-range mobile signals. However, plants have evolved unique protein repertoires to execute these behaviors consistent with their sessile lifestyle and uniquely flexible and environmentally responsive development. What gene networks have plants evolved to create cell polarity and control morphogenesis? In our lab, we are focused on this fundamental question. As our foundation, we study patterning of the leaf surface, which depends on polarity-mediated control of stem cell behaviors.
Why plants?
We have thus far identified two independent mechanisms that link cell polarity to asymmetric cell division in the Arabidopsis thaliana stomatal lineage. Intriguingly, both pathways shared commonalities with polarity-mediated pathways that are widely deployed during animal development. However, our work has defined how unique genes and regulatory logic have rewired these pathways to control plant morphogenesis. With this precedent, our lab currently has two long-term goals for this work:
1) Harness polarity pathways for control of plant stem cell function for manipulating tissue architecture.
Just as our understanding of mammalian stem cells has transformed human health, we believe that similar understanding of pathways controlling plant stem cells can be harnessed to help plants thrive in a changing climate. As such, we are interested in translating our findings from the leaf epidermis to other plant tissues and species to identify tissue-specific and ubiquitous polarity pathways that can be used to control plant architecture.
2) Engineer key polarity modules into animal cells for orthogonal control of cell behavior.
Polarity is at the heart of both plant and animal development. Accordingly, defects in polarity pathways have been linked to developmental and oncogenic disease in humans. However, as the same highly conserved polarity genes are widely deployed in all our cells, it is difficult to create precision methods to ameliorate polarity defects in specific cellular populations. In recent years, orthogonal plant pathways have been successfully ported to animal cells for control of functions like protein abundance. We propose that understanding plant polarity could similarly unlock new methods to exert spatial control in animal cells for bioengineering applications.
Interrogate the basis of polarity-cytoskeleton interactions in plants
Polarity-mediated effects on the microtubule and F-actin cytoskeletons are the foundation of many morphological processes. We identified that polarity in the leaf epidermis locally sculpts the topology of the microtubule cytoskeleton (Muroyama et al., 2022 bioRxiv), leading to a host of new questions about how polarity controls the cytoskeleton in plants. We are coupling high-resolution imaging that allows us to monitor individual cytoskeletal filaments in developing plants with genetic and proteomic approaches to delineate these pathways in detail.
Pathways that shape organelle topography in plant stem cells
Executing complex cellular behaviors in a spatially defined manner depends on a cell’s ability to organize its own contents. We previously identified two pathways that couple polarization to nuclear positioning to regulate asymmetric cell division. We are currently using a range of approaches, including single-cell tracking across an entire developmental trajectory, to understand how subcellular organization contributes to physiologically relevant outcomes during leaf morphogenesis.
Divergent principles to coordinate tissue patterning
To be a productive member of an organ, a cell must coordinate its behaviors with those of its neighboring cells. How is this coordination achieved to regulate patterning at the tissue scale? We are using reverse genetics, morphometric data, and evolutionarily distant plant species to understand the regulatory mechanisms that determine organ patterning and shape.