The scientific study of plants has evolved from fundamental examinations of physiology and the inherited characteristics of Mendelian peas to sophisticated applications using molecular biology and genomics. Peter H. Quail's scientific career has run parallel with the most recent interdisciplinary advances in plant biology research. Over the past 40 years, he has made numerous contributions in the areas of cell signaling and mechanisms of plant development and the environmental cues involved.
Currently the research director of the Plant Gene Expression Center (U.S. Department of Agriculture/University of California, Berkeley) and a professor in the Department of Plant and Microbial Biology at Berkeley, Quail has been a pioneer in the study of phytochromes, photoreceptor proteins that play a major regulatory role in plant growth and development. Quail was elected to the National Academy of Sciences in 2004, and his Inaugural Article appears in this issue of PNAS (1). In the article, Quail and colleagues describe how a phytochrome-interacting transcription factor, PIF3, acts early, selectively, and positively in light-mediated chloroplast development. Using transgenic GUS:PIF3 fusion-protein constructs in Arabidopsis, Quail and his team also demonstrate that PIF3 levels are rapidly and reversibly modulated by phytochrome during daily light-dark cycles. PIF3 was found to decrease rapidly to basal steady-state levels upon light exposure but return to higher levels in darkness at night. The article's results suggest that PIF3 functions in early phytochrome signaling at the daily dark-to-light transition.
From Farmhouse to Schoolhouse
Quail was born in 1944 and grew up in Cooma, a location he fondly describes as “a small rural town surrounded by sheep farms” near the Snowy Mountains of southeast Australia. Part of Quail's childhood was spent on a farm that produced wool and had some cattle. “I was very interested in natural things around me,” he says. “I used to love to go out and just wander around in the bush or camp out. I was very interested in farming... just the rural life, living on a farm, nature.”
As a youth, Quail also possessed a keen interest in chemistry and “the `mad scientist' kind of thing,” as he describes it. “Test tubes of colored liquids, bubbling. I think that was my goal,” Quail says with a laugh. “I used to pester this pharmacist in our local town... for some kind of chemistry kit, so I could go home and do experiments with it,” he explains. “Fortunately he never gave me anything.”
Fig. 1.
Quail inspects mutant Arabidopsis plants at the Plant Gene Expression Center in Albany, CA. Quail is research director of the center, a joint venture of the University of California (Berkeley) and the U.S. Department of Agriculture.
Quail attended an agricultural high school and “developed a general interest in plants and how they work.” He adds, “I was always interested in plant growth and things around the farm.” After high school, Quail began his collegiate studies at the University of Sydney (Sydney, Australia). His undergraduate curriculum included specialized subjects such as agronomy, plant physiology, plant pathology, soil science, and agricultural economics. In 1964 Quail earned his B.Sc. degree in agriculture.
Continuing at the University of Sydney, Quail began his doctoral studies under Owen Carter. It was during his undergraduate and graduate studies that Quail first studied the mechanisms of plant development and the environmental signals involved, such as light. Quail's interests in chemistry and plant biology “must have converged at some point. I slowly became aware of the chemical basis of life and the fact that molecules must signal to each other.” Quail's thesis centered on defining the hormonal mechanisms behind the control of seed dormancy in the weed Avena fatua, a serious threat to wheat in Australia (2, 3). “My Ph.D. was technically in agronomy, but the actual research discipline was really plant physiology,” Quail explains. He received his Ph.D. in 1968.
Lighting the Way and Seeing the World
Quail left Australia for the U.S. in 1968 and began his first postdoctoral position under the mentorship of the late Joseph Varner at the Michigan State University/Atomic Energy Commission Plant Research Laboratory (East Lansing). As a research associate there, Quail studied the de novo synthesis of peroxidases and catalases in young seedlings, using biochemical techniques such as density labeling (4). He credits Varner, whom Quail cites as his “single most important mentor,” with providing him with invaluable biochemical training. More importantly, Varner “really taught me how to think about science, how to conceptualize and critique things,” says Quail. “He taught me how to think.”
After a successful fellowship with Varner at Michigan State, Quail moved to Germany in 1971 to begin a second postdoctoral position, where his research “evolved from hormones to light but still look[ed] at plant responses.” He accepted a research associate position in the Biologisches Institut at the Universität Freiburg, where Quail began to work on phytochrome, the protein which would be the focus of his research for the next three decades. Quail became interested in the general effects of light and collaborated closely with Eberhard Schäfer, a fellow postdoctoral researcher who “taught [Quail] a lot about photobiology.”
In 1973, Quail returned to Australia to join the Photobiology Laboratory of the Research School of Biological Sciences at Australian National University (Canberra). As a research fellow and group leader of the laboratory, Quail continued subcellular localization studies of phytochrome that he had started in Germany. In 1977, Quail then traveled to Israel for a 3-month stint at the Weizmann Institute of Science (Rehovot), working as a visiting scientist in plant genetics. Later in 1977, Quail moved to the U.S. to join the Carnegie Institution at Stanford University (Stanford, CA). As a senior fellow in the Department of Plant Biology, Quail was mentored by Winslow Briggs. Says Quail, “He was a big influence on the photobiology part of my research, [especially] as I got more advanced.”
Quail left Stanford in 1979 and accepted his first faculty position as an associate professor of botany at the University of Wisconsin (Madison). There, Quail collaborated with Eldon Newcomb, who had been instrumental in recruiting him to Wisconsin. As a senior colleague and collaborator, Newcomb was a guiding force during Quail's first tenure position and taught him much about cell biology. In 1984, Quail became a professor of botany and genetics. At Wisconsin, Quail began to use molecular biology and genetic approaches to study the phytochrome system. With the help of colleagues, he cloned the first phytochrome gene (5), defined the primary sequence of the phytochrome protein (6), detailed autoregulation of phytochrome gene expression (7), and raised monoclonal antibodies against phytochrome (8).
Molecular Mechanisms
In 1987, Quail began his current position as research director of the U.S. Department of Agriculture/University of California Berkeley Plant Gene Expression Center and a professor in the Department of Molecular Plant Biology (which became the Department of Plant and Microbial Biology in 1989). Quail continued to use forward and reverse genetic methods in his research and began to utilize newer genomic technologies. At Berkeley, Quail achieved some of his most noteworthy scientific contributions, including finding that “there are multiple phytochromes, five in Arabidopsis,” encoded by a small family of genes (9-11). He and his team cloned and sequenced these genes. Furthermore, they contributed “to determining that each has a partially differential function in the plant,” he says.
Quail's most important scientific contribution came in 1998, with the discovery of PIF3, a “direct signaling partner” of phytochrome following photoactivation (12-14). This phytochrome-interacting factor was found to be a basic helix-loop-helix (bHLH) transcription factor. “[This] discovery, together with the discovery from other labs that the phytochromes are transported into the nucleus,... changed the whole direction of the concepts at the time,” he says. “It was a redirection of thinking in the field about how the signaling process takes place.” Previous models of signaling invoked a second messenger-based system, whereas the discovery of light-induced phytochrome nuclear translocation and PIF3 suggested a direct signaling pathway from the photoreceptor to the transcriptional machinery.
Quail's research has also contributed to the development of some practical applications. In the context of agricultural biotechnology (15), Quail describes how it may be possible to “manipulate part of the phytochrome system to produce crop plants that are potentially able to produce high yields.” Also, Quail and his team have harnessed phytochrome's highly specific interaction with PIF3 to create “an artificial promoter that we can turn on and off with light.” This light-switchable promoter system has potential for use in any light-accessible cell type to induce or repress gene expression (16). For example, if fused to a regulatory gene in a light-penetrable model organism such as Caenorhabditis elegans or zebrafish, the expression of that gene could be conditionally induced, precisely and reversibly, at any chosen developmental stage by simple exposure to light.
“At the biological level, we're trying to understand how plants respond to their light environment.”
The current research goals of Quail and his team can be viewed on two fundamental levels: “At the biological level, we're trying to understand how plants respond to their light environment.” Quail likens the phytochrome system to a type of primitive system of color vision. “The plants use the color of the incoming light to tell them about the nature of the environment so that they can respond appropriately,” he explains. “The second level, which is our real interest,... is the mechanistic level,” says Quail. “This is where we're trying to understand the molecular mechanisms by which the plants perceive and transduce the incoming light signals.” Regarding phytochromes, he hopes to further elucidate “how those molecules, once they've become excited by the light, transfer that information downstream in the signaling network.”
By Quail's own account, his research has “evolved from biochemistry, through molecular biology, to genetics and, most recently, to genomics.” He says, “The important thing is the question you're asking. The technology evolves and enables you to ask more and more sophisticated and more rigorous questions.” When asked to identify any major hurdles facing his future research, Quail simply answers, “Complexity.” Newer genomics technologies examine experimental problems globally, involve high-throughput analyses, and require interpretation of complex patterns of interaction between multiple networks. Says Quail, “Once you scale up using genomic approaches, you run into obvious complexities that you didn't have there before, not only because the biological system is complex, but the analytical capabilities have to be much more sophisticated and complex.”
Personal Professionalism
Aside from his own research goals, Quail has been involved with the Rockefeller Foundation for more than 15 years, initially with the International Program on Rice Biotechnology. “I feel very proud about that [program] because I think it got rice into the mainstream of molecular biology and genetics, and at the same time I think we were doing something that would help developing countries, help with their food supply,” says Quail. Presently he is involved in a new program in Africa, the Rockefeller Foundation's Program on Biotechnology, Breeding, and Seed Systems for African Crops, focused on achieving disease and drought resistance and greater crop yields through biotechnology. The program centers on regional crops, such as bananas, cassava, corn, and cowpeas. In both programs, the goal has been to use “biotechnology to help underdeveloped countries and people to feed themselves,” says Quail.
Quail's research and varied professional experiences have allowed him to travel extensively. An avid skier and folk music guitarist, he is married and the proud father of a daughter and a son. He has received numerous fellowships and awards, including an American Society of Photobiologists Research Award in 1988, a LI-COR Award for Distinguished Contributions to Photochemistry/Photobiology in 1995, and an Institute for Scientific Information award in 2002 for being among the top 15 most-cited authors in the plant and animal science discipline. He attributes much of his career success to those with whom he has worked. “I've been very fortunate to have really, enormously talented students and postdocs,” Quail says. “They're the ones who have really done the work.” Many would argue that he has done the work too.
This is a Biography of a recently elected member of the National Academy of Sciences to accompany the member's Inaugural Article on page 16091.
References
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