Recent laboratory findings paint a new picture of how plant cells communicate, suggesting that they engage in a sophisticated conversation using a greater variety of proteins and hormones than once thought.
"It's a totally new concept," says Bill Lucas, a professor of plant biology at the University of California, Davis, and co-author of a research paper in the Dec. 22 issue of the weekly journal Science. "We plant scientists had no idea that plants had the capacity to traffic their own proteins from cell to cell. This sets in place a whole new way of understanding how plants control the development and fate of cells during tissue growth."
"These findings imply there's a whole lot more communicating than we assumed," says Patricia Zambryski, a professor of plant biology at the University of California, Berkeley, who reviews two related reports in the Dec. 22 issue of Science. She is co-author of another two reports in the Dec. 30 of the monthly journal Plant Cell.
Until now, a rudimentary form of communication between plant cells was assumed to take place through narrow portals called plasmodesmata, which connect the cells of a plant into one network that allows easy passage of nutrients such as sugars.
Because plasmodesmata appeared too narrow and rigid for any but the smallest molecules to traverse, cell-to-cell signaling was thought to be mediated by small molecules only -- growth hormones and small proteins called peptides.
Instead, plasmodesmata now appear to be flexible conduits that, at the proper signal, expand to allow the passage of large molecules. Moreover, these large molecules appear to use the cell's skeleton, the cytoskeleton, as a highway to and from the plasmodesmata.
How protein trafficking works is still far from understood, but the fact that it exists has broad implications for agriculture, biotechnology and nutrition, and for understanding plant evolution, Lucas says.
For example, understanding the transport of proteins to and through the plasmodesmata could help scientists devise ways to stop the spread of viruses, which have hijacked the protein transport system that plant cells use to communicate.
The revised picture of plant cell communication has emerged primarily from four California laboratories involved in the cluster of December findings.
The first hint of these new developments came in 1989 when two groups -- one at UC Davis led by Lucas and a second led by Roger Beachy at Washington University in St. Louis (now at Scripps Research Institute in La Jolla, Calif., where he is co-director of the International Laboratory for Tropical Agricultural Biotechnology) -- teamed up to look at a protein from tobacco mosaic virus, a major problem for growers of tomatoes and tobacco. Using transgenic tobacco plants produced by Beachy's group to express this protein, the team found the protein somehow increased the size limit of plasmodesmata to let the virus -- which is much larger than the normal size limit of plasmodesmata -- slip from one cell to the next.
This finding suggested that plant cells themselves may be able to increase the size of the plasmodesmata to control which molecules get through, and that the virus had stolen the "key" for opening the plasmodesmata channel.
The key pirated by these viruses to open the plasmodesmata and slip from cell to cell was identified as viral movement protein. Before long, researchers had shown that movement proteins can open plasmodesmata to allow large molecules -- 20-to-30 times bigger than once thought possible -- to squeeze between cells.
Two years ago, Lucas' group reported that plasmodesmata opened not only for the large-movement protein of an RNA virus -- a major type of virus -- but also for the virus's much larger genetic material to pass through rapidly. In a separate study they found that the movement proteins of a geminivirus, another type of plant virus, also allowed rapid spread of the viral agents.
About the same time, Zambryski's research team, using the microinjection system at the Lucas lab in Davis, reported similar results for the movement protein of tobacco mosaic virus, which opened the plasmodesmata within minutes to allow large sugars and proteins to pass through.
The papers in this week's Science and in this month's Plant Cell add exciting new details to this picture. In one of the Science papers, Lucas and colleagues show how controlling plasmodesmata can be important in the developing plant. The findings came from a collaboration with Sarah Hake and postdoctoral fellow David Jackson, researchers at the U.S. Department of Agriculture-Agricultural Research Service/UC Berkeley Plant Gene Expression Center in Albany, Calif. The study was supported in part by a grant from the National Science Foundation Integrative Plant Biology Program.
They demonstrated that a large protein called KNOTTED1, which is important to the development of the growing tips of plants, or meristems, moves through the plasmodesmata.
Surprisingly, the large protein also opens the plasmodesmata wide enough for its larger RNA to squeeze through, along with other molecules, implicating the protein as a natural regulator equivalent to the movement proteins of viruses.
"This is the first evidence that the plant's own RNA molecule can be transported through the plasmodesmata," Lucas says.
USDA researcher Hake says this supports the notion that plasmodesmata play a role in the growing plant by determining which growth factors and regulatory proteins get to which cells.
"The demonstration that a plant protein moves between cells presents a new paradigm for thinking about plants and plant development," Hake says.
In the second Science paper, Beachy and colleagues at the Scripps Research Institute show that viral movement protein can often be found attached to the cell skeleton or cytoskeleton. Zambryski and her group, including postdoctoral researcher Gail McLean, report similar evidence for this in a second article in Plant Cell. By marking movement protein with fluorescent stain, the researchers showed that the proteins "decorate the cytoskeleton" like ornaments.
The implication is that movement proteins move large molecules along the cytoskeleton to the plasmodesmata and shove them though.
Another layer of complexity has been added by the Zambryski group in work published in Plant Cell. She and postdoctoral researcher Elisabeth Waigmann report different size limits for the plasmodesmata of hair cells and other cells in the leaf. The limits are larger for hair cells, but movement proteins do not increase them, as happens in other leaf cells. "This implies that plasmodesmata in different cell types are not equivalent," Zambryski says.
Zambryski also showed that movement proteins can cluster around actin, another protein component of the cytoskeleton. She thinks the door at the entrance to the plasmodesmata may contain actin and suggests that movement proteins track along the microtubules through the cell to the plasmodesmata, where they latch onto actin and are kicked through the door.
The current goal of all the researchers is to find more of these naturally occurring proteins that regulate plant function throughout the plant. KNOTTED1 is one such regulator, Lucas says, but no doubt there are others.
"Insights gained from studies of the plant's information superhighway may well allow us to understand the way a plant controls such important events as flowering," Lucas says.
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Andy Fell, Research news (emphasis: biological and physical sciences, and engineering), 530-752-4533, ahfell@ucdavis.edu