Groups of diverse plant species often produce more seeds than monocultures. But whether plants ramp up yield in response to genetically distinct, direct neighbors, as opposed to a broader neighborhood of diverse plants, remains an open question in ecology. “It’s very hard to test this in natural settings because there are so many things that are uncontrolled,” says Erica McGale, a molecular ecologist at the Max Planck Institute for Chemical Ecology in Jena, Germany.
Now, McGale and colleagues have taken many of those uncontrolled variables out of the equation. Working with two lines of wild coyote tobacco plants (Nicotiana attenuata) that are identical but for a single gene, the team found that diversity could increase yield at the broader group level, not at the neighbor level. The findings, recently reported in eLife, could one day influence how farmers plant their fields.
McGale and colleagues focused on a single gene, MPK4, which codes for an enzyme critical to properly functioning stomata—the tiny openings in the leaf that allow gas and water vapor to pass through. They began with two lines of plants, one with a functioning MPK4 gene and the other with the gene silenced. Previous greenhouse experiments showed that plants with the silenced MPK4 gene had malfunctioning stomata that tended to release excess water vapor into the air.
The team planted the tobacco in groups of four in a field, varying the number of plants that carried the silenced MPK4 gene in each group. They found that groups produced the most seeds and biomass when one of the plants had the silenced MPK4 gene—any more or less of this line and the group became less productive. Plants with the silenced gene didn’t contribute to the higher yield. But their presence in low numbers seemed to trigger the other plants to produce more. The researchers then conducted an analogous experiment in the greenhouse with groups of a dozen plants in each pot and again found that groups produced the most yield when about a quarter of the plants carried the silenced gene.
But when they planted one of each of the two lines together in pairs within a single pot in the greenhouse, they discovered that a single neighboring plant with the silenced MPK4 gene was not enough to prompt the same growth response. It seemed that genetic diversity at the group level—not the neighbor level—was key for upping yield.
Still, a big question remained: How could a silenced gene that lowers water use efficiency cause an increase in group yield when a full quarter of the group carries it? The question became even more perplexing when the team directly measured the water-use efficiency of each plant line in the field and discovered that, unlike in the previous greenhouse study, they were the same. The silenced gene was influencing the group through some other mechanism altogether.
The researchers ruled out a series of hypotheses for how this gene might affect the productivity of the group. By crossing each of their lines with a mutant line that lacked the ability to interact with arbuscular mycorrhizal fungi, they determined that the silenced MPK4 gene was not affecting the symbiotic relationship with these microorganisms in the soil. By controlling water availability in the greenhouse, they determined that the silenced gene was not somehow drawing more water to the group. Hence, despite their efforts, the mechanism remains elusive.
“They did very sophisticated experiments,” says Bernhard Schmid, plant ecologist and biodiversity scientist at the University of Zurich in Switzerland, who was not involved in the research. “In the end, there is a bit of suspense,” he says. “We are left in the dark about the exact mechanism.”
“My best guess is that, at the population scale, I believe that there’s probably some sort of signal—I would guess something volatile related—that transfers between the plants,” says McGale.
Regardless of the mechanism, the finding that diversity at the level of a single gene potentially has an impact on yield at the group level could have implications for agriculture—especially considering the gene studied is common across plant species. “I think that it would be interesting to try out a blend similar to the Nicotiana experiment in a crop species and see how it performs over a number of environments,” says Jim Myers, a geneticist and vegetable breeder at Oregon State University in Corvallis, who was not involved in the study. Myers does question, however, whether crops already bred for high yields would still respond with even higher yields. “It’s a very interesting piece of work,” says Myers. “And definitely worth following up on in cultivated crops.”