Soil microbes remember drought and help plants survive

"The bacteria and fungi and other organisms living in the soil can actually end up having important effects on things that matter, like carbon sequestration, nutrient movement and what we're particularly interested in -- the legacy effects on plants," said co-author Maggie Wagner, associate professor of ecology & evolutionary biology at the University of Kansas.

"We got interested in this because other researchers, for years, have been describing this type of ecological memory of soil microbes having some way to remember from their ancestors' past," she said. "We thought this was really fascinating. It has a lot of important implications for how we can grow plants, including things like corn and wheat. Precipitation itself has a big influence on how plants grow, but also the memory of the microbes living in those soils could also play a role."

According to Wagner, legacy effects have been observed before, yet the details remain unclear. A clearer picture could eventually assist farmers and agricultural biotechnology companies that aim to leverage beneficial microbes.

"We don't really understand how legacy effects work," she said. "Like, which microbes are involved at the genetic level, and how does that work? Which bacterial genes are being influenced? We also don't understand how that legacy of climate moves through the soil to the microbes, and then eventually to the plant."

The team sampled soils from six Kansas locations, spanning the wetter eastern region to the higher, drier High Plains in the west, which receive less rain because of the Rocky Mountains' rain shadow. The goal was to compare how legacy effects varied along this climate gradient.

"This was a collaboration with a team at the University of Nottingham in England," Wagner said. "We divided up the work, but the bulk of the experiment -- actually, the entire experiment -- was conducted here at KU, and we also focused on soils from Kansas for this work."

At KU, Wagner and colleagues evaluated how the microbial communities from these soils influenced plants.

"We used a kind of old-school technique, treating the microbes as a black box," she said. "We grew the plant in different microbial communities with different drought memories and then measured plants' performance to understand what was beneficial and what was not."

The researchers exposed the microbial communities to either ample water or very limited water for five months to reinforce contrasting histories of moisture availability.

"Even after many thousands of bacterial generations, the memory of drought was still detectable," Wagner said. "One of the most interesting aspects we saw is that the microbial legacy effect was much stronger with plants that were native to those exact locales than plants that were from elsewhere and planted for agricultural reasons but weren't native."

To begin testing how plant identity interacts with microbial legacy, the team compared one crop (corn) with one native grass (gamagrass). They note that additional species will be needed to confirm the pattern, yet the early results suggest that native plants may align more strongly with local microbial histories.

"We think it has something to do with the co-evolutionary history of those plants, meaning that over very long periods, gamagrass has been living with these exact microbial communities, but corn has not," she said. "Corn was domesticated in Central America and has only been in this area for a few thousand years."

Beyond plant performance, the researchers examined gene activity in both microbes and plants to explore potential mechanisms behind legacy effects at the molecular scale.

"The gene that excited us most was called nicotianamine synthase," Wagner said. "It produces a molecule mainly useful for plants to acquire iron from the soil but has also been recorded to influence drought tolerance in some species. In our analysis, the plant expressed this gene under drought conditions, but only when grown with microbes with a memory of dry conditions. The plant's response to drought depended on the memory of the microbes, which we found fascinating."

Wagner noted that gamagrass is being considered as a source of useful genes for improving corn under stress.

"The gene I mentioned earlier could be of interest," she said. "For biotech firms focused on microbial additions to crops, this gives hints about where to look for microbes with beneficial properties. Microbial commercialization in agriculture is a multibillion dollar industry and still growing."

Wagner's KU collaborators were lead author Nichole Ginnan, now of the University of California-Riverside, and Natalie Ford, now of Pennsylvania State University; Valéria Custódio, David Gopaulchan, Dylan Jones, Darren Wells and Gabriel Castrillo of the University of Nottingham; Isai Salas-González of the Universidad Nacional Autónoma de México; and Ângela Moreno of the Ministério da Agricultura e Ambiente in Cabo Verde.

"One of the things that makes this work valuable is how interdisciplinary it was," Wagner said. "We brought together genetic analysis, plant physiology and microbiology, allowing us to ask and answer questions that couldn't have been addressed before."

This work was funded by the National Science Foundation's Division of Integrative Organismal Systems.