What we thought we knew about photosynthesis was wrong

You’ve probably never heard of them. Not even discovered until the 1960s, C4 plants have been found in just 18 of the approximately 500 families of vascular plants. They make up only about 10,000 of the approximately 300,000 species of terrestrial plants. But because they are so good at photosynthesis under adverse conditions, they represent 30 percent of the world’s terrestrial plant productivity. Many of the world’s worst weeds are C4.

Photosynthesis is the mechanism by which plants use light energy to convert water and atmospheric carbon dioxide (CO2) into organic plant matter and oxygen. Plants that use C4 photosynthesis are much more efficient at using atmospheric CO2 and are more productive—up to 40 percent better at both. In addition, they are particularly successful in growing conditions of intense light, high soil salt content, warm climate, and drought, and high soil salt content.

Unfortunately, most crop species use a less efficient form of photosynthesis called C3. Among crop species, only maize, millet, sorghum, and sugar cane are C4. If more crop species could be persuaded to perform like C4, feeding a burgeoning world population would be considerably simpler—and a great deal of research has gone into trying to do so, though without much success. Now Gerry Edwards and Vince Franceschi may have made this task simpler.

Recent work by the two Washington State University School of Biological Sciences researchers and their colleagues will force botanists to reexamine what has long been thought mandatory for C4 photosynthesis. Not only does their work have implications for genetic engineering, it revises our understanding of how plants organize functions within their cells and of the evolution of photosynthetic mechanisms. When you upset a scientific paradigm, you expect a reaction, and that’s exactly what Edwards and Franceschi have gotten. As one expert in their field wrote, “Is nothing sacred?”

Over the years, Edwards’s research has helped to explain the mechanism of C4 photosynthesis, and Franceschi has used antibodies and cell biology to probe the relationship between C4 plant structure and function. The two have been colleagues for 20 years.

Until Edwards and Franceschi put their talents together on C4, it was considered dogma that plants using C4 photosynthesis always contained a specialized cellular organization known as “Kranz anatomy.” The name “Kranz,” German for “wreath,” was applied in 1884, long before C4 photosynthesis was discovered in the 1960s. It was given to the distinctive arrangement of cells seen in some species of grasses by G. Haberlandt, a German plant anatomist. Kranz anatomy is characterized by two cells that sit side by side in the leaf. One cell traps atmospheric CO2, then shuttles it to another cell, where it is concentrated and incorporated into plant matter.

Separation of the two parts of C4 photosynthesis is considered critical for the system to operate at maximum efficiency.

“It was spelled out in concrete that for C4 photosynthesis to occur in higher plants you have to have this dual cell system referred to as Kranz anatomy,” says Franceschi. Kranz often was used as an example of the tight association between structure and function.

But then Edwards and Franceschi ran across Borszczowia aralocaspica. B. Aralocaspica performs C4 photosynthesis within a single cell and without Kranz anatomy. Within that one cell, spatial separation of the functions takes place just as it does in the two cell types in plants with Kranz anatomy. Most important, B. aralocaspica’s photosynthesis is as efficient as that of Kranz plants.

But the Kranz dogma is so strong that the two scientists at first thought that what they saw in B. aralocaspica was an oddity of the plant’s development. Because its one cell looks like that of the two Kranz cells without the cell wall that separates them, Franceschi and collaborator Elena V. Voznesenskaya looked at specimens from throughout the plant’s developmental cycle to be certain that such a cell wall hadn’t disappeared during maturation.

B. aralocaspica’s unusual anatomy was first detected by German scientist Helmut Freitag. Freitag had studied its genealogical family, the Chenopodiaceae, for some time. His paper on B. aralocaspica’s anatomy caught the attention of Edwards and Franceschi, who also thought its anatomy looked unusual. It didn’t look like either a C3 or a C4 plant, but rather like something between the two, says Franceschi. He and Edwards set out to determine what kind of photosynthesis the plant was doing, and where the parts of the photosynthetic system were located. After talking with Freitag, they began a collaboration that led to the discovery of the single-cell C4 photosynthesis.

About five years ago Edwards and Franceschi began a research collaboration on photosynthesis with two Russian scientists, Voznesenskaya and Vladimir I. Pyankov. That collaboration was initially funded by the Civilian Research Development Foundation (CRDF). CRDF grants come from a pool of federal and private moneys set up after the breakup of the Soviet Union to encourage collaboration between U.S. and Russian scientists. Voznesenskaya is a plant anatomist and Pyankov, a plant physiologist. Both had worked for years on species that grow in Central Asia. Voznesenskaya returned to WSU several times after the CRDF grants were finished, and the collaboration with Freitag began during her last visit.

Initially the Russian and U.S. scientists worked together to characterize the range of both C3 and C4 photosynthesis in the Chenopodiaceae. It is an interesting family photosynthetically and shows a high diversity in its evolution of C4 photosynthesis, says Edwards.

Three distinct types of C4 cycles have evolved among the C4 plants. In addition, C4 plants exhibit a variety of Kranz anatomies, variations in the arrangement of the two characteristic cells. The Chenopodiaceae family contains plants that have five different variations of Kranz anatomy and two of the three C4 pathways.

These biochemical and anatomical variations indicate that C4 photosynthesis has evolved multiple times, says Edwards. Current data suggest that it has done so up to 31 separate times, even more than once in some families. In one genus there is so much variation in photosynthetic mechanisms that you feel as if you can see the entire evolutionary process from C3 to C4, says Franceschi. “It’s like looking at a snapshot in time.”

Edwards and Franceschi expect that more C4 plants without Kranz anatomy will be found. In the past, the quick and easy method for determining whether a plant was C4 was to look at a cross-section of leaf under a microscope. Obviously that method can no longer be considered completely accurate, and other ways will have to be used to test for C4 photosynthesis.

The collaboration with Freitag already has turned up a species from the deserts of Central Asia that Edwards and Franceschi have shown also has C4 photosynthesis without Kranz anatomy. Though it’s from the same sub-family as B. aralocaspica, its anatomy is distinct. Finding it verifies that B. aralocaspica is not just a freak of genetic engineering by nature, says Franceschi.

A good deal of basic science will be done over the next several years to determine just how the B. aralocaspica photosynthetic cell operates. These cells contain two types of chloroplasts, something not previously reported, says Edwards. “We need to learn how the cell produces and segregates these chloroplasts.”

On the more practical side, it’s clear that B. aralocaspica changes the whole idea of what’s required for C4 photosynthesis, says Franceschi.

It should be much easier to genetically engineer C3 plants to perform C4 photosynthesis if Kranz anatomy isn’t necessary. Not easy, just easier.

Because there are C4 plants without Kranz anatomy, we know there’s potential for us to do it, says Edwards.

Adds Franceschi, “Obviously, the plant can do single-celled C4 photosynthesis if it wants to. We only need to figure out how to do it ourselves.”


For more information on Ku’s work, click here.