June 6, 2003 Scientists announce in the current issue of the journal Nature their discovery that plants respond to environmental stresses with a sequence of molecular signals known in humans and other mammals as the "G-protein signaling pathway," revealing that this signaling strategy has long been conserved throughout evolution. Because a large percentage of all the drugs approved for use in humans target the G-protein signaling pathway, the team's findings could also be used in the search for plant compounds that regulate the pathway in mammals, possibly leading to new drugs for human diseases. In addition, the research identifies the enzyme in plants that triggers the production of an important molecule, S1P, in this signaling system. The enzyme in mammals is known to play a critical role in regulating the proliferation and death of cells. "Our research also indicates that the S1P-G-protein signaling pathway is the previously unknown genetic basis of characteristics that regulate a plant's ability to withstand drought," says Sarah M. Assmann, the Waller Professor of Plant Biology at Penn State University and leader of the group of researchers from Penn State and Virginia Commonwealth University. Its discovery in plants could be used to develop crop varieties with higher yields and greater drought resistance, in addition to helping to identify plant sources for new pharmaceuticals.
Like team members in a relay race, molecules in the G-protein signaling pathway, well known in human cells, swing into action one after another when activated by a hormone. However, the identities and roles of the signal relayers in the G-protein pathway in plants were essentially unknown before the current findings. Assmann and her fellow researchers did know that a molecule important in the G-protein-signaling pathway in human cells, the molecule S1P (sphingosine-1-phosphate), also exists in plants, but they did not know much about its origin and function in plant cells. "The questions we sought to answer were what is the enzyme in plants that produces S1P and does S1P cause the same kind of G-protein signaling cascade in plant cells as it does in mammals," Assmann says.
The researchers made a series of discoveries, not only identifying sphingosine kinase as the enzyme that produces S1P in plants, but also demonstrating that S1P production is triggered by the stress hormone abscisic acid. During drought, this hormone initiates a chain of cellular events that ultimately cause a leaf's pores, known as stomates, to change their shape in order to limit the amount of water lost by the plants. The researchers found that the enzyme’s product, S1P, is involved in both inhibiting the opening of the plant's pores and promoting their closure.
In addition, Assmann and her team discovered that, in plants as in humans, a G-protein signaling pathway is critical for the sensing of S1P produced by sphingosine kinase. By studying in the model plant species, Arabidopsis, plants genetically engineered to lack the G-protein alpha subunit, the researchers learned that these mutant plants were unable to close their pores in response to the abscisic acid hormone, revealing that the G-protein alpha subunit is essential for relaying this drought-alert signal.
The researchers further discovered that the ultimate targets of the relay race--from abscisic acid to S1P production to G-proteins--are proteins in the cell membrane called ion channels. "What we show in this paper is that if you knock out the G-protein alpha subunit, not only do you knock out stomatal closure, but you also knock out the ability of the S1P protein to regulate these ion channels in the cells that border the pores," Assmann says. Assmann notes that a high-yielding “Green Revolution” variety of rice also lacks the gene necessary for producing the G-protein alpha subunit, indicating that the G-protein signaling pathway may be important in controlling crop yields. "G proteins are of paramount importance and their function is well known in mammalian systems, so it is quite interesting to discover that they also play an important role in plants and are regulated similarly," Assmann says. "The more you can understand about how plants function on the molecular level, the more likely it is that you can use breeding or biotechnology to develop more drought-tolerant and productive crop species.
In addition to Assmann, other members of the research team include Sylvie Coursol, Liu-Min Fan, and Simon Gilroy at Penn State and Hervé Le Stunff and Sarah Spiegel at Virginia Commonwealth University. This research was funded by the National Science Foundation, the United States Department of Agriculture, and the National Institutes of Health.
NOTE: The research described below is published in the current issue of the journal Nature.
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