CORE CONCEPTS CORE CONCEPTS Probing the phytobiome to advance agriculture Carolyn Beans, Science Writer The Colorado potato beetle had Gary Felton stumped. That something else turned out to be bacteria. If he Felton, an entomologist at Pennsylvania State Univer- applied antibiotics, the plants could launch a defense sity, has built his career on revealing how plants defend and inhibit potato beetle larvae growth (1). Bacteria in themselves against voracious insects. Plants often de- the insect’s oral secretions were tricking the plants into tect chemicals in an insect’s oral secretions and respond defending against microbial invaders instead of insect by producing proteins that wreak havoc on insect di- ones. Kill the bacteria and the cover is blown. gestion and nutrient absorption. Myriad factors affect crop health, such as genetics, But the Colorado potato beetle was different. Felton insects, microbes, weather, soil nutrients, weeds, fertilizer, found that oral secretions from its larvae actually pre- tilling. Until recently, scientists typically studied one vented potato and tomato plants from launching a proper variable at a time, says plant pathologist Jan Leach of defense. He tested chemical factors in the secretions that Colorado State University. “When a plant is sitting in the might help the beetle foil the plant, but came up short. field, it’s not just exposed to one pathogen, one tem- “Maybethereissomethingelseherethatwe’ve totally perature, one insect. It’s exposed to everything at once,” overlooked,” he recalls thinking. says Leach. “If we want to understand how plants Bacteria in the oral secretions of Colorado potato beetle larvae can trick potato and tomato plants into defending against microbes instead of the insect pest. Image courtesy of Nick Sloff (Pennsylvania State University, State College, PA). 8900–8902 | PNAS | August 22, 2017 | vol. 114 | no. 34 www.pnas.org/cgi/doi/10.1073/pnas.1710176114 Downloaded by guest on September 26, 2021 respond to a single pathogen, we really need to take the Agricultural companies are already developing whole system into account.” products that hinge on understanding the inner work- Leach calls this whole system the phytobiome, a term ings of the phytobiome. Bayer, for example, offers that encompasses plants, the environment they inhabit, BioAct, a fungal product that infects the eggs and lar- and the surrounding community of organisms. Leach vae of a broad range of parasitic nematodes that attack attached a name to this concept in 2013 during a crop roots. Indigo Agriculture, a Boston-based agri- meeting hosted by the American Phytopathological cultural start-up, is developing methods to coat seeds Society. The group had brought together scientists to with beneficial microbes that improve crop growth. address a looming global food crisis. Among the major challenges afoot: the human population will increase by Piecing Together the Parts 2.4 billion by 2050, and with increases in food crop-yields Scientists and farmers have long known that many slowing, many researchers fear food demand will soon interacting factors affect crop health. But until re- outpace supply (2). The scientists concluded that for cently, they didn’t have the technological capacity to them to optimize crop productivity to meet increasing quantify them or the analytic and computational needs in a sustainable way, researchers could no longer power to tease them all apart. “We always assumed it focus on any factor affecting plant health in isolation. would be complex,” says plant pathologist Linda They would have to contend with many interrelated fac- Kinkel of the University of Minnesota, who is also the tors. They would have to explore the phytobiome. associate editor-in-chief of Phytobiomes, a journal “ An Alliance Forms launched this year. With genomics tools, we can Following the meeting, researchers developed a Phy- begin to put these pieces together in ways we ’ ” tobiomes Roadmap, a strategic plan for “acquiring couldn tdo10or20yearsago. knowledge of what constitutes a healthy, productive, Metagenomics, for example, now enables re- and sustainable agroecosystem and translating that searchers to collect soil samples from the field and knowledge into powerful new tools in our crop man- identify the suite of bacterial and fungal residents “ agement toolbox” (3). Phytobiome researchers realized based on gene sequences. When we could only a key component of that plan in October 2016 with the identify microbes by culturing them in the [labora- launch of the Phytobiomes Alliance. tory], we didn’t know many of them were there,” says The Alliance’s vision is to empower farmers to Kinkel. Using metaproteomics, researchers can also choose the best combination of crops and manage- get a sense of how these microbes are responding to ment practices for a specific field in a specific year their environments. They could, for example, compare based on detailed knowledge of the environmental and biological components of phytobiomes, says Kellye Eversole, the Alliance’s executive director. “It’s “You can’t understand the potential to resist plant like precision agriculture in a precision medicine pathogens unless you measure all of these layers.” sense.” Some farmers already use precision agricul- tural technologies to understand the physical com- —Linda Kinkel ponents of the phytobiome (4). They might place sensors in soil to monitor moisture levels or conduct soil surveys to track nutrient levels. how different crops affect the quantities of proteins that Eversole would like to see more biological data as microbes produce in response to stress (5). part of the equation. Scientists might, for example, Drawing on these technologies, Kinkel and others design sensors that quantify microbial communities in are diagraming the working parts of the phytobiome. “ ” real-time, or produce cheaper soil and plant sampling Kinkel studies what she calls the Russian doll story of kits that can tell farmers which microbes are present. microbes and plants. She wants to understand how the Combined with detailed records of crop yield over diversity of a plant community affects how an individual ’ space and time, all of this information could help plant influences the microbes colonizing that plant s “ ’ farmers predict which crops do best under which roots. You can t understand the potential to resist abiotic and biotic conditions, and how many plants a plant pathogens unless you measure all of these lay- given plot of land can support. ers,” she says. The Phytobiomes Alliance includes academics, In one study, her laboratory explored the bacte- small agricultural start-ups, and large companies like rial communities associated with four different Monsanto and Bayer that have all agreed to collaborate prairie plants: when the plants were grown in mono- in what is known as a precompetitive space, an agree- culture versus when they were grown with 3, 7, or ment in which industry players recognize the value of 15 other species (6). The researchers found that as putting aside intellectual property interests to advance plant community richness increased, bacterial di- a fledgling idea. “It means that industry agrees that versity actually decreased, as did the proportion of we have a specific need that individually we cannot antibiotic-producing bacteria that fend off plant achieve,” says Magalie Guilhabert, head of Biologics pathogens. So the monoculture encouraged more Crop Efficiency and Seed Growth Indication in the beneficial bacteria. Kinkel is now looking for ways Crops Science division of Bayer. In principle, industry to encourage these beneficial bacteria without ac- and academic partners share data, results, and ideas. tually relying on monocultures, which can drain Beans PNAS | August 22, 2017 | vol. 114 | no. 34 | 8901 Downloaded by guest on September 26, 2021 soil nutrients and leave crops vulnerable to rapid Power in a Name disease spread. Many challenges remain. Researchers need better Building on his previous work, Felton recently dis- molecular techniques for identifying viruses and fun- covered that the bacterial community inside the guts gal species. They need standardized sampling tech- of Colorado potato beetles is shaped by the plant niques so they can compare results across studies. species on which the larvae feed (7). It turns out that And researchers need a better sense of how often for many plants, including eggplant, the bacterial they should sample organisms and environmental ’ community can t help the insect evade detection. parameters to capture a changing phytobiome. “ There is more specificity involved in the interaction Even selecting which types of data to collect is ” than we initially thought, Felton says. challenging. “Do we really need to know the soil Leach is teasing apart the complex interactions be- particle size to understand how a microbe signal im- tween plant genetics, pathogen susceptibility, and tem- pacts plant health and productivity at high versus low perature. “Traditionally, in order to protect plants from temperatures?” asks Leach. “Maybe that dataset does disease, plant breeders will introduce single resistance not significantly influence or is not useful to train a genes that recognize pathogens and mount a defense model. But we don’t yet know.” response in the plant,” Leach says. “The problem is that Kinkel, Felton, and others say that having the at high temperatures, many of those genes aren’tef- “ ” fective.” But Leach discovered that one gene in rice name phytobiome makes