Research determines how plants tell which way is up

February 17, 2001

After being knocked over by wind or hail, many plants quickly grow upward again. Scientists at North Carolina State University and the University of Michigan have discovered that oats and maize use a chemical, also present in the human brain, to "perceive" almost instantly that something is amiss - and then bend in the proper direction within minutes or hours.

Those findings, which expand our understanding of how gravity affects plant growth, have implications for agriculture and space travel, the researchers explain.

"If humans are going to go on sustained space missions, we'll need to use plants to turn carbon dioxide into oxygen, to cleanse water and to provide food," said Dr. Wendy Boss, an NC State professor of botany who is one of 10 principal investigators on the project. "Before we create such long-term life-support systems, we need to know how gravity affects the growth of plants."

Boss will present the group's findings at 9 a.m. Sunday, Feb. 18, at the American Association for the Advancement of Science (AAAS) annual meeting in San Francisco. The AAAS meeting is the year's largest and most important science conference.

The presentation,"Signal Transduction Pathways and Early Responses of Plants to Gravistimulation," is part of a symposium titled "Biology Into Space: A Matter of Some Gravity." The symposium is being organized by Dr. Nina Strömgren Allen, NC State professor of botany, and Dr. Christopher Brown, director of the NASA Specialized Center of Research and Training (NSCORT) in Gravitational Biology at NC State. Brown is also director of space programs at NC State's Kenan Institute for Engineering, Technology and Science.

Boss says scientists don't know how plants will react to the lack of gravity and other conditions imposed by space flight. Plants won't necessarily need to grow vertically, she explains, but they have adapted to earth's environment - including gravity - to move nutrients, water and sugars between their roots and shoots.

Now that the International Space Station is in orbit, researchers can plan experiments to determine how micro gravity affects plant growth and development, Boss says.

The research by Boss and her colleagues focuses on inositol trisphosphate (InsP3), a molecule used in a wide variety of life forms to transmit chemical signals between an organism's cells. Human brain cells, for example, are a rich source of inositol trisphosphate and contain some of the highest levels of receptors for the chemical found in the human body.

"Why would plants have a signaling pathway similar to brain cells?" Boss asked. "We can't answer that, but we can explain how the chemical signaling pathway functions in plants and how that compares to the pathway found in animal cells."

While plants have not evolved to contain the sophisticated, multifaceted signaling pathways of human brain cells, Boss explains, they do contain some of the more basic components, which help plants sense and respond to changes in their environment. Specifically, the NC State researchers have found that inositol trisphosphate appears essential for plants to "perceive" a change in their orientation relative to gravity, and to respond by growing in the proper direction.

Boss and three colleagues - Dr. Imara Perera and Dr. Ingo Heilmann, NC State botany research associates, and Dr. Peter B. Kaufman, professor emeritus of plant physiology and plant biotechnology at the University of Michigan - analyzed the amount of InsP3 present in specialized cells at the base of maize and oat stems. Those cells are in the pulvinus, a specialized region of a plant stem which causes a stem to bend upward after a plant has fallen over.

The researchers found that, within 15 seconds after the plants are placed on their sides, the amount of the chemical surges fivefold in the pulvinus cells.

Additionally, the researchers discovered that the amount of InsP3 fluctuates between the upper and lower halves of the plant's pulvinus. The scientists believe that's because the pulvinus cells are communicating about whether cell organelles called amyloplasts have fallen to the bottom of the cells, pulled there by gravity. Boss says that the continued increase in InsP3 may allow a plant to determine whether it has been knocked to the ground, or is merely swaying in the wind.

That signaling continues for about 30 minutes in oats and between two to four hours in maize. During that time, the amount of InsP3 gradually increases in the lower half of the pulvinus. Then, the cells nearest the ground begin to elongate, the plant's pulvinus begins to bend like an elbow, and the plant starts to curl toward a vertical position.

"That delay makes sense. If a plant is on its side for a only few seconds, it doesn't need to grow upward," explained Perera, the NC State research associate. "Because the cell elongation is irreversible, the continued increase in inositol trisphosphate may be essential for the plants to differentiate between a transient stimulus - swaying in the wind - and a long-term stimulus - falling down."

To test the role of InsP3 in this process, the researchers added a chemical to the plants to inhibit the plants' ability to make InsP3. As expected, the oat and maize plants placed on their side showed significantly less upward bending (about 60 percent less) than untreated plants without the chemical inhibitor added.
-end-
The research was funded by NASA, the National Science Foundation and the USDA's Binational Agricultural Research Development (BARD) program. In addition to Boss, the other principal investigators on the NASA-funded project who are studying responses of maize to gravity are Kaufman; Allen; Brown; Dr. Eric Davies, NC State professor of botany; Dr. Steven C. Huber, NC State professor of botany and crop science; Dr. Ross Whetten, NC State associate professor of forestry; and Dr. Gloria Muday, professor of biology at Wake Forest University.

More information about this and other research sponsored by NSCORT is on the Web at www.cals.ncsu.edu/nscort.

Editor's note: Boss' AAAS presentation abstract follows. To reach Boss during the AAAS conference, contact Kevin Potter, NC State News Services, at 919-515-3470.

Media Contacts:
Dr. Imara Perera, 919-515-3544 or imara_perera@ncsu.edu
Kevin Potter, NC State News Services, 919-515-3470 or kevin_potter@ncsu.edu

"Signal Transduction Pathways and Early Responses of Plants to Gravistimulation" by Wendy F. Boss, North Carolina State University Feb. 18, 2001, American Association for the Advancement of Science annual meeting

Abstract: In shoots of grasses, such as maize and oats, the pulvinus is the site of both gravi-perception and response. When a plant is placed horizontally, the pulvinal cells perceive a change in orientation and the cells on the lower side begin to elongate. The resulting differential elongation of cells on the lower side relative to the upper causes the pulvinus to bend upward returning the shoot to a vertical position. We asked if the phosphoinositide signal transduction pathway was involved in the perception of or response to a change in orientation with respect to the gravity vector. Phosphoinositide signaling is initiated by hydrolysis of the inositol lipid, phosphatidylinositol (4,5)bisphosphate (PtdIns(4,5)P2) to produce the second messenger, inositol(1,4,5)trisphosphate (InsP3). When maize or oat plants are placed horizontally, there is a rapid (within 15 seconds) increase in InsP3. The levels of InsP3 oscillate up and down between the lower and upper side until the cells begin to make a commitment to elongate, at which time, there is a long-term increase in InsP3 and up regulation of PtdIns(4,5)P2 biosynthesis in the cells on the lower side, both InsP3 and PtdIns(4,5)P2 decrease to basal levels prior to visible bending. The changes in InsP3 are specific for the gravi-responsive pulvinus tissue and are not detected in internodal tissue immediately above the pulvinus. Furthermore, inhibiting the sustained increase in InsP3 inhibits gravitropic bending of the pulvinus but does not inhibit internodal growth. These data indicate that a steady state increase in InsP3 on the lower side of the pulvinus is necessary for differential cell elongation. We conclude that the phosphoinositide signaling pathway is a part of the mechanism by which cells perceive a positional change relative to the gravity vector.

North Carolina State University

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