Two decades ago, cell and developmental plant biologist Dominique Bergmann was starting her lab at Stanford University with the goal of understanding cell development and fate using stomata, plants’ pore-like structures, as a model system. By venturing into the unexplored molecular biology of plants, Bergmann and her team described key transcription regulators that drive stomatal development and proposed a model for how these molecules guide that process.1,2 Her pioneering work was recognized with scientific awards in 2010 and a profile in The Scientist in 2011, highlighting her achievements.
In honor of The Scientist’s 40th anniversary, we reached back out to Bergmann to find out how her research has evolved since we featured her work 15 years ago. In the past decade and a half, she has embraced novel technologies to push the boundaries of what is known about stomatal development, uncovering new roles for the core regulators she described more than a decade ago and identifying new players involved in plant pore development.3-5
Looking Back to Move Forward: Rethinking the Sequential Model of Plant Pore Formation
Stomata are essential for transpiration and gas exchange between plants and their environments. The development of these leaf structures requires a series of asymmetric cell divisions followed by a single symmetric division that leads to the formation of two guard cells that flank the stomatal pore.6
By the mid-2000s, researchers had described many signals necessary to halt stomatal development, but factors that contributed to the formation of the kidney bean-shaped structures remained elusive, Bergmann explained.
To address this gap, her team performed a series of gain-and-loss-of-function experiments in the plant model Arabidopsis thaliana and described how three transcription factors—SPEECHLESS, MUTE, and FAMA—were essential for stomatal development and differentiation.1,2 The team’s findings also suggested that these plant developmental regulators work in tandem, with one factor setting the stage for the next one. ”Everyone was like, ‘You need the first one, and then [the cell] turns on the second one, and then turns on the third one. That's how you go.’ People made beautiful cartoons in the review literature [about it],” she said.
While the sequential model for the transcription factors’ actions held true most of the time, Bergmann recalled experiments in which SPEECHLESS, the factor that kickstarts the asymmetric cell divisions in stomata development, did not behave as expected.
To solve this riddle, her team needed a more detailed understanding of the cells as they progressed during stomatal development, which they achieved with the advent of single-cell transcriptomics. By combining the high-throughput sequencing technique with microRNAs to disrupt SPEECHLESS expression only at a later stage of stomata formation, Bergmann’s team showed that not only did cells at this late stage express the transcription regulator, but that SPEECHLESS was also essential for the final differentiation into guard cells. These findings led Bergmann to revisit her team’s initial model of stomatal cell development and propose a new one in which SPEECHLESS acts as the initiator of asymmetric cell divisions and complements the functions of MUTE and FAMA at later stages, contributing to cell fate commitment and the differentiation into guard cells.3
“Basically, we were wrong at the beginning, but we have refined it, and now we are finding out how these factors might actually work together,” she said.
The “Dark Side” of the Stomatal Cell
Technical advancements in proteomics and proximity labeling methods were essential to help Bergmann solve another unsettling question in the plant developmental cell biology field: how cells orient their cargo to the right location as they divide.
The leaves of plants contain pore-like structures called stomata. Dominique Bergmann studies these structures to understand how polarity proteins like BRXL2 (green) orient cells’ cargo to the right location during cell division.
Dominique Bergmann’s lab
Cells rely on a property known as polarity to direct cellular components during their divisions. The importance of cell polarity, Bergmann explained, is that once a cell divides, it sets what each daughter cell inherits.
Polarity proteins are major players in this process. For years, Bergmann and others identified these proteins and described how they contributed to asymmetric cell divisions during stomatal development.7,8 Yet, during plant pore formation, all these molecules important for cell polarity moved only to one side of the cell, an observation that intrigued Bergmann.
Evidence that some proteins did go to the opposite or “dark” side of the stomatal cell started to emerge in 2023. Bergmann’s team identified a group of molecules dubbed OCTOPUS-LIKE (OPL) proteins that moved to the opposite side from the polarity proteins previously described during stomata development.4 These findings suggested, for the first time, that the stomatal cells have two regions to which polarity proteins go during plant pore formation, with these regions affecting the subsequent cell divisions and differentiation of daughter cells into guard cells or epidermal cells.
To identify other protein players working on these oppositely positioned polarity domains, Bergmann and her team used a TurboID proximity labeling technique they had previously adapted for use in plants.9 This method enabled the researchers to identify proteins in close proximity with a protein of interest, producing spatially localized proteomes of the two opposing polarity regions in the stomatal lineage. They identified previously unknown partners of the polarity protein OPL2 and uncovered how these molecules may interact with cytoskeletal components to facilitate cellular cargo shuttling during both asymmetric and symmetric cell divisions in plant pore formation.5
While the scientific discoveries her team has made over the years are a source of contentment, Bergmann is most fond of her lab’s ability to launch the careers of many young scientists. “I’m really proud of being able to have this sort of incubator lab, a place where people are attracted to come and to spend some time in a very collaborative way, and then launch themselves someplace else,” she explained. “I'm actually most proud of being able to look at 30 postdocs that have done amazing things after they have come out.”
- Ohashi-Ito K, Bergmann DC. Arabidopsis FAMA controls the final proliferation/differentiation switch during stomatal development. Plant Cell. 2006;18(10):2493-2505.
- MacAlister CA, et al. Transcription factor control of asymmetric cell divisions that establish the stomatal lineage. Nature. 2007;445(7127):537-540.
- Lopez-Anido CB, et al. Single-cell resolution of lineage trajectories in the Arabidopsis stomatal lineage and developing leaf. Dev Cell. 2021;56(7):1043-1055.e4.
- Wallner ES, et al. Arabidopsis stomatal lineage cells establish bipolarity and segregate differential signaling capacity to regulate stem cell potential. Dev Cell. 2023;58(18):1643-1656.e5.
- Wallner ES, et al. Spatially resolved proteomics of the Arabidopsis stomatal lineage identifies polarity complexes for cell divisions and stomatal pores. Dev Cell. 2024;59(9):1096-1109.e5.
- Lee LR, Bergmann DC. The plant stomatal lineage at a glance. J Cell Sci. 2019;132(8):jcs228551.
- Dong J, et al. BASL controls asymmetric cell division in Arabidopsis. Cell. 2009;137(7):1320-1330.
- Pillitteri LJ, et al. Molecular profiling of stomatal meristemoids reveals new component of asymmetric cell division and commonalities among stem cell populations in Arabidopsis.Plant Cell. 2011;23(9):3260-3275.
- Mair A, et al. Proximity labeling of protein complexes and cell-type-specific organellar proteomes in Arabidopsis enabled by TurboID. Elife. 2019;8:e47864.
