Plant fertility research benefits from discovery of molecular signaling system

Pollen tubes (red tubules) from the pop2 mutant grow in a tangled mass within female tissues. Rather than efficiently growing up to an ovule (upper right), they instead gather at the ovule's base. Photo: Anna Edlund Full size image available through contact

August 4, 2003—University of Chicago researchers have found that a substance that functions as a neurotransmitter in humans also plays a crucial role in plant reproduction, guiding growth of the tube that transports sperm from a pollen grain on a flower's surface to the egg cells within a plant's ovules.

Their finding, published in the July 11, 2003, issue of the journal Cell, is a major step forward in understanding plant fertility. The discovery, which is supported in part by the DOE Office of Science, could also help researchers understand similar biological processes, such as how nerve cells find each other and make appropriate connections. It may even provide clues about repairing spinal cord injuries.

"Since agriculture, which supplies nearly 80 percent of the world's food supply, depends so profoundly on plant fertility, understanding this process is fundamentally important," said Daphne Preuss, Ph.D., professor of molecular and cell biology and an investigator in the Howard Hughes Medical Institute at the University of Chicago.

When a pollen grain is deposited on the surface of a flower, it somehow has to grow a tube from the stigma of the flower, past several different cell types to where the eggs are, digesting tissue as it grows to burrow all the way inside.

"While a few molecules involved in this process have been identified over the years," said Preuss, "we really still don't understand how this tube gets from start to finish."

Working with Arabidopsis, a popular model plant, Preuss and colleagues from her lab found that plants produce a carefully controlled gradient of gamma-amino butyric acid (GABA), a molecule best known for its role in the mammalian nervous system, to lure a pollen tube toward the egg cells. GABA acts like a light at the end of a tunnel, stimulating the initial growth of the pollen tube and shining ever brighter as the tube gets closer to its goal.

Daphne Preuss Full size image available through contact

The researchers found that the key to regulating GABA levels is an enzyme they named POP2 that degrades GABA. Arabidopsis flowers produce high levels of GABA, then eliminate varying amounts of it from different structures, so that a small amount is present at the surface of the pistil, where it stimulates pollen tube growth. Higher concentrations are found closer to the eggs, leading the tubes toward the target.

The study grew out of the team's chance finding of abnormal pollen tubes on plants that were later found to lack POP2.

"We saw the pollen tubes just winding around and totally missing their targets on one particular mutant," said Preuss. Co-author Laura Brass, a former Ph.D. student in the Preuss lab, analyzed the mutant strain and pinpointed the gene that caused the defect, which the researchers named POP2. By comparing the sequence of the defective protein produced by POP2 to other known proteins, lead author Ravishankar Palanivelu, Ph.D., a post-doctoral fellow in Preuss's laboratory, concluded that it was an enzyme called an aminotransferase. It was not until the researchers found that the mutant plant contained a hundred-fold elevation in GABA, however, that they learned which molecule the enzyme degraded.

Further studies confirmed that the chemical normally concentrates near the egg-containing ovule. In contrast, in the mutant plants, GABA is diffused throughout the tissues. In these mutants, the pollen tubes are "just overwhelmed with signal," said Preuss. Instead of a light at the end of the tunnel it was "like staring at the sun."

Finding a reproductive role for GABA in plants is a good example of nature's ability to make the most of what's available, said Preuss. GABA is a small, comparatively simple molecule. Many plants and animals use it as a source of carbon or nitrogen or to send signals from cell to cell. Animals use it to regulate hormone secretion, inhibit certain signals between nerve cells, and perhaps even to guide embryonic neurons to their destination.

GABA is only one of several substances involved in pollen tube guidance, however, said Preuss. The researchers are analyzing other mutants with altered pollen tube growth.

Media contact: John Easton, University of Chicago Media Affairs, 773-702-6241, jeaston@uchospitals.edu
Technical contact: Daphne Preuss, Professor, University of Chicago Department of Molecular Genetics and Cell Biology, 773-702-1605, dpreuss@uchicago.edu

Related Web Links
Pollen Tube Growth and Guidance Is Regulated by POP2, an Arabidopsis Gene that Controls GABA Levels. Palanivelu, R, L Brass, AF Edlund, and D Preuss. Cell 114(1):47-59, July 11, 2003 (subscription may be required)

GABA Accumulation in Arabidopsis Flowers Impairs Pollen Tube Growth and Causes Sterility. Ravishankar Palanivelu, Laura Brass, Anna Edlund, Daphne Preuss. Poster abstract from the 2nd International Conference on Plant Metabolomics, Potsdam, Germany, April 25 - 28, 2003.

Plant Sex: Pollen Tubes Caught in the Act

The Arabidopsis Information Resource

Arabidopsis thaliana Genome Center

The TIGR Arabidopsis thaliana Database

The Preuss Lab

Funding: This research was supported by the DOE Office of Science Basic Energy Sciences program, the Searle Scholars Program, and the University of Chicago.

Established in 1890 by John D. Rockefeller, the University of Chicago claims 74 Nobel Prize winners as faculty members, students, or researchers, with six Laureates currently on the faculty. In addition, faculty honors include 13 recipients of the MacArthur Fellowship (commonly known as the "genius grant"), eight recipients of the National Medal of Science, 41 members of the National Academy of Sciences, and 123 current members of the American Academy of Arts and Sciences-among many others. The university is located in Hyde Park.