Entomologist Jack Schultz and plant physiologist Eva Pell believe that important scientific questions cannot be answered without drawing on multiple disciplines.

In her first year of graduate school, Eva Pell's plant physiology professor handed the class a manuscript and said, "This is a book I'm writing on plant physiology we're going to use it in this course. But I'm not going to teach you the Calvin cycle, and I'm not going to teach you the Krebs cycle. I'm going to teach you how Krebs discovered the Krebs cycle, and I'm going to teach you how Calvin discovered the Calvin cycle. Then you can go on and discover something new."

"Everything was done by case study, in which you learn about a subject by working through real-world problems," Pell explains. "That made an enormous impression on me and influenced the way I teach my classes. We do a lot of problem solving, like specialists in a think tank." Recently, Pell has applied this educational philosophy in an innovative five-year training program, Plant Responses to the Environment: Biochemical Bases, Physiological Responses, and Ecological Consequences. Developed by Pell, a plant physiologist, and entomologist Jack Schultz, the program is supported by a $1.25 million grant from the National Science Foundation. The grant is part of a nationwide initiative to develop innovative graduate programs that will produce Ph.D.'s with the multidisciplinary backgrounds and skills necessary to meet the career demands of the future. Now in its fourth year, the program supports six Ph.D. students and six postdoctoral researchers, and also provides research opportunities for several undergraduates. Teaching strategies initiated by this program have since been incorporated into established courses and graduate programs at Penn State.

"Students of plant biology, whether they're going to be ecologists, physiologists, or molecular biologists, should have a sense of the continuity from the molecule to the ecosystem," Pell says. "We wanted to develop an educational program that would encourage a molecular scientist to say, 'I wonder what the implications of this gene are in the context of the whole plant or ecosystem?' We wanted an ecologist to say, 'I wonder what the fundamental mechanism is that allows a plant to emerge, be suppressed, or perform a certain way in a given environment?'"

To answer such questions requires knowledge that spans scientific levels from molecular biology and biochemistry to "whole plant" physiology to ecology, so Pell and Schultz formed a research training group consisting of nearly 20 faculty members from eight academic units in the Colleges of Agricultural Sciences, Engineering, and the Eberly College of Science. Participating scientists in the agricultural sciences include specialists in agronomy, biology, entomology, forest resources, horticulture, plant pathology, and veterinary science.

Schultz and Pell don't expect students to become experts at all of the scientific levels their goal is to help young scientists acquire Ph.D.-level expertise at one level and still communicate with people in others. "We all joke about how we can't read the titles of the papers from someone else's discipline in Science," Schultz says. "It seems like gobbledygook. But if you needed information from that discipline to answer one of your questions, you'd have to learn that language. That's what we're promoting. Important scientific questions can't be answered without drawing on multiple disciplines. We're coming to realize that to solve basic science problems or applied agricultural problems it's important that we work in teams. Each member may have a narrowly defined focus, but someone on the team has to be able to talk to all the other members. We're also hoping to train scientists who can lead these interdisciplinary teams."

To promote working across boundaries, each student is advised by two mentors drawn from two of the three scientific levels. "Students may work with an ecologist and molecular biologist, for instance, which means they attend lab meetings in two different places," Schultz says. "We hope this will make them think more broadly. So often, scientists attract students to their laboratories, then keep them under their wing, which limits their experiences to what happens in a single lab. Our program is designed to force students out of a single lab and to work across labs with more than one person."

An integral part of the graduate training included roundtable discussions with postdoctoral researchers and students with different scientific backgrounds. Here, Eva Pell (l) and graduate student Jennifer Tomscha (r) share a point with the rest of a discussion group.

The students also had to devise Ph.D. projects in which they worked at two of the three scientific levels. "A student who came into the program interested in ecology, for instance, had to devise a thesis project that focuses on an ecological question, but uses molecular/biochemical or physiological approaches to solve it," Schultz says. A variety of research projects have recently taken off beneath the umbrella of the training program (see page 21).

Finally, Schultz and Pell trained students to work across scientific levels by organizing courses around problem-based learning. For one year, students and postdoctoral researchers participated in roundtable discussions, in which they examined current theories on how plants respond to the environment, why those theories are good or bad, and the experiments they might carry out to test them. "We'd form groups and get assigned a problem," says graduate student Jennifer Tomscha. "We'd go off and find out everything we could about the topic, then come back and share what we found. We'd have these very interesting discussions trying to develop a strategy, for instance, on how to make plants more resistant to cold. We'd bat around ideas, brainstorming. We might use genetic engineering, ecology, or whole plant solutions. It was really great training."

"This approach forces students to seek information outside their normal discipline," Schultz explains. "Suppose you're an ecologist and you have to solve a problem relating to how plants change their growth in response to competition from neighbors. As it turns out, the presence of nearby plants changes the quality or color of the light that hits a given plant. Scientists who specialize in physiology know that plants have sensors called phytochromes, which can detect these changes in light quality. These phytochromes produce signals that alter gene expression in the plant and ultimately alter its growth. If you're an ecologist who wants to understand how competition among plants works in a natural setting, or if you're an agriculturalist who wants to know how production is altered when plants are growing in crowded conditions, these physiological mechanisms become fundamental to answering your questions."

"In these groups, I learned that I need to look beyond a narrow focus to different species, different life forms even how different kingdoms might respond to a stimulus," says graduate student Anne Walton. "How do bacteria handle cold? What kinds of genes do animals turn on in response to cold? This approach taught us that all knowledge is a resource."

The groups rotated so each student had a chance to work with everyone else in the program. The discussions revolved around a variety of plant behaviors, from responses to light, ozone, and disease to the phenomenon of plant emissions. "One of Jack's biggest contributions to science is the discovery that trees can 'talk' that is, plants emit signals that allow them to communicate," Walton says. "For instance, we know that plants emit ethylene or methyl jasmonate when insects start eating them. Recently, there's been a lot of research that indicates that when plants emit these chemicals, they are screaming 'I'm being attacked!' They send these ethylene or methyl jasmonate signals to another plant, which can then perceive it, turn on its own defenses, and protect itself. So in class, we would discuss why plants emit other compounds like isoprenes, methane, and terpenes into the atmosphere. Why do some plants do it while others do not? What does it mean for a plant to do this in nature?"

The groups would discuss topics at all levels, from the perception of the stimulus or signal, to the transduction of the signal from the outside to the inside of the cell, to the ultimate response observed. By the end of the year, they were able to draw a huge pathway on paper showing how all of the known plant responses might interconnect.

Graduate student Jeremiah Fasano feels he really benefited from the approach. "I could have stayed immersed in cell biology," he says. "But because we spent all that time wandering around in the woods and growing all these plants in growth chambers and watching them die," he says, laughing, "and wading through the library constructing all these hypotheses about things at different levels of organization, and trying to tie them together just the exercise of doing that has enabled me to communicate with ecologists and physiologists. I can understand what's important to them and explain my work in terms they'll understand."

"Really, problem-based learning is research," Tomscha adds. "By taking us through this curriculum, they prepared us to do our own research. Many graduate students don't learn that until they're in the midst of their own projects, but we were able to go into our research already knowing how to approach problem show to really dig into the literature, find out what's known, and then come up with novel approaches. Now I can go to a professor and clearly explain my work and why I'm doing it. I would've gotten here eventually, but it would've taken a whole lot longer."

Outdoor laboratories help researchers simulate the complexities plants face in forests, farms, and cities.

Besides funding new educational approaches, training grants allow faculty to train scientists in new subject areas in this case, the ways in which plants respond to their environment. "Jack and I are very interested in the universality of plant responses," Pell says. "Do plants have a finite suite of responses to the range of environmental stimuli? Researchers have identified biochemical and physiological mechanisms that appear to be common to many plant responses, such as responses to ozone, pathogens, light, and cold. You have these different environmental cues coming into cells in different ways, but once they get in, they may be triggering one of a finite number of biochemical pathways. This is a big area right now looking for the common threads in all living systems."

"We know that responses to light share characteristics with responses to diseases, and that responses to diseases share characteristics with responses to soil nutrient levels, or water stress," Schultz adds. "But how much overlap is there? And can we figure out where the overlap occurs?"

The enzyme lipoxygenase, for instance, which oxidizes fatty acids, exists in both animals and plants. This enzyme system is turned on by a variety of environmental stimuli, one of which is wounding. "Enzymes are proteins that catalyze chemical reactions," Schultz explains. "The chemical by-products of the lipoxygenase reaction act as signals that travel through the animal or plant, organizing wound responses." In animals, some of these chemical signals are involved in asthma attacks, heart disease, and even cancer. In plants, one of these signals is methyl jasmonate, which travels between plants and acts as an airborne signal that turns on defenses in unattacked plants. "You can actually spray jasmonate on plants and turn on their defenses," Schultz says. "A commercial grower has used it successfully on a tomato patch. It's an exciting prospect. It's so popular right now you can hardly buy it the chemical company is constantly out of stock."

In the real world, plants like people deal with more than one stress at a time. Graduate student Doug Bielenberg stresses plants with ozone while varying levels of soil nitrogen.

Jasmonate also is the chemical responsible for the odor of jasmine flowers. "It's the queen of aroma," Schultz says. "A recent outbreak of spider mites on some of our oak seedlings made the greenhouse smell like the perfume counter at a department store. When Steve Pechous, one of the graduate students in the program, first started working on this project, he joked about how, when he went home at night, his wife would ask him where he'd been!"

Four years since its beginnings, the program has proven fruitful. "NSF wants these training programs to be seeds for changes to be made in curricula," Pell says. "I'm happy to say that Jack and I can turn to NSF at the end of the five years and say we delivered. Penn State made a long-term commitment to this model. We developed new courses, and changed our requirements for the Plant Physiology graduate program. Our underlying vision also served as the jumping off point for Ecological and Molecular Plant Physiology, a new graduate program funded by the Life Sciences Consortium" (see page 26).

Pell relates a story from the training program's beginnings, when the ideas were still words on sheets of paper. "Before NSF decides to fund a training grant, they come out for a site visit. Jack and I orchestrated this big series of presentations. The faculty came and talked about their research programs. Jack and I talked about the educational component. And the leader of the NSF party sat there very quietly. By lunchtime, my heart was sinking. Finally, near the end of the day, he opened his eyes, looked at the two of us, and said, 'In other words, you're going to educate biologists. This is something that hasn't happened for 20 years.'" Pell laughs, recalling her relief. "When he said that, I felt like we had successfully made our case, because that's exactly what we had in mind. We wanted to prepare students by providing them with a way to think. We can't give them the techniques and facts they'll need five years from now, because they haven't even been invented yet. Instead, we're giving our students the tools they'll need to find tomorrow's facts and techniques."

— Kim Dionis

Faculty and students referenced in this article are Eva Pell, Nancy and John Steimer Professor of Agriculture and chair of the intercollege graduate program in plant physiology; Jack Schultz, professor of entomology; Jeremiah Fasano, doctoral student in biology; Jennifer Tomscha, doctoral student in plant physiology; and Anne Walton, doctoral student in entomology. The program is funded in part by The National Science Foundation.