Dominique Bergmann's first experience doing science with plants was a summer internship in southern Idaho after high school. The task, which required her to count cacti all day, was so dull she quickly talked her way into a job using a backhoe to install cattle guards instead. But her curiosity about how organisms develop eventually brought Bergmann back to plants.
All multicellular organisms must create and organize a variety of specialized cells to form a complete, functioning organism, and Bergmann wants to understand how they do it.
After studying the development of the simple flatworm Caenorhabditis elegans during graduate school at the University of Colorado at Boulder, Bergmann was ready for a change. Seeking an organism whose developmental processes were more intricate, she settled on Arabidopsis thaliana, a weedy broccoli relative that's been used for decades to study development. "Every time the plant makes a new leaf, that leaf is basically a blank slate," she says. "It's starting all over again and you can watch development unfold."
Now a developmental biologist at Stanford University, Bergmann focuses her studies on the tiny holes on the bottom of plants' leaves called stomata. "Stomata are a really clever innovation on the part of plants to regulate things that really matter to them," Bergmann says. When stomata are open, carbon dioxide can diffuse into the leaf from the air and water can evaporate out of the plant. If too much water escapes, the plant wilts, but if too little carbon dioxide gets in, the plant starves—so the plant must maintain a delicate balance. "The stomata are little valves that help them do that," she explains.
Bergmann says plant stomata let her ask questions about development in different ways than she could in an animal model. In contrast to many animal stem cell populations that are tucked inside the body and whose daughters migrate away from their mothers, the plant cells Bergmann studies are readily accessible on the surface of the plant. Moreover, because plant cells do not move, when these epidermal stem cell populations divide, not only is it easy to identify stem cells, but the daughters of the stem cells remain neighbors. It's possible to follow many generations of stem cell divisions and see how different treatments, mutations, and environmental factors change the regenerative potential of these cells. Bergmann's striking microscope images of these patterns—and the ways they can be perturbed—have helped her make fundamental discoveries about the molecular forces that guide development.
A key discovery Bergmann made as a postdoctoral fellow at Stanford helped her establish stomata as a model for developmental studies. Investigating a gene called YODA, she found it to be—true to its name—a master regulator. YODA controls many of the genes that determine the identity and patterning of cells as they mature from stem cells to the specialized guard cells that make up stomata. Arabidopsis plants that lack YODA make too many stomata; when YODA is overactive, they cannot make any stomata at all.
Bergmann compared the activity of genes in plants with and without YODA and found hundreds of genes that come under its influence. Teasing out how individual genes in that set contribute to stomatal development has been a major component of her research since that discovery in 2004.
Since she set up her own lab in 2005, Bergmann has been interested in asymmetric cell division. Multicellular organisms start as a single cell, which divides, then divides again, and on and on as the organism's complex form emerges. To make that happen, there are many points where a mother cell has to divide into daughter cells of two different types. Plants lack the asymmetry-regulating proteins that researchers have discovered in animals and also face the plant-specific challenge of dividing with the constraints of a rigid cell wall—so Bergmann knew they must use their own strategy to achieve asymmetric cell division.
"I'm a little contrary," she says. "I like when people think that something is solved and done a certain way. That's fine—it can be done that way—but I can find an equally good path to the same result." Her lab has found a protein unique to plants, called BASL, that accumulates on one end of a dividing cell and winds up in only one of its daughters. When it is missing, plant cells overproliferate or differentiate into the wrong kinds of cells—similar, Bergmann says, to the defects that develop when asymmetric divisions are disrupted in animal stem cells. There are hints that, like many of the other proteins Bergmann has identified as key players in stomatal development, BASL represents the plant kingdom's solution to a developmental problem faced by both plants and animals.
"I keep one foot in the animal development world," says Bergmann, who is a familiar face at developmental biology meetings where most attendees focus on fruit flies, frogs, and worms. "I've tried to make my lab a place where we grab everything available from a wide range of sciences and throw it at a classic problem in developmental and cell biology."
With genetic techniques commonly employed by scientists studying animal development, she discovered genes that drive the formation of the pair of guard cells that surround the stomatal pore. There's one on each side of the pore—they open the pore by blowing up like balloons and close it as they deflate. A series of asymmetric divisions leads down a path from stem cells to guard cells, and Bergmann's lab has worked out a group of three regulatory genes that control that journey. "It turns out that's a really simple genetic pathway," she says. And, although it evolved independently, it's quite similar to a pathway used in animals to make neurons and muscle cells.
She hopes to take the opportunity offered by the HHMI-GBMF appointment to study stomata development in different organisms, especially grasses. Despite their agricultural importance, grasses—which include wheat, sorghum, corn, and rice—haven't been very well studied, because it takes so much time and money to start working on a new model system. But grasses intrigue Bergmann because they have a different kind of stomata than other plants. A four-cell setup lets their stomata snap open and shut much faster. With a better understanding of these structures, Bergmann says, it could be possible to create crops with the ideal number of stomata to thrive in a particular climate.