One hundred million years ago, long before human intervention, ancestors of grasses, like wheat, rice and maize generated "bypasses" of chemical pathways that are used to create two critical compounds: lignin and starch. These more efficient pathways could explain why grass plants are so successful in nature and agriculture, according to a new paper publishing in Science on Aug. 20 by researchers from the University of Wisconsin–Madison and their collaborators.
Like a beltway that creates a more flexible traffic flow in a city, these metabolic bypasses led to efficient and robust synthesis of both lignin and starch, chemical compounds that are critical for plants.
Grasses and cereal grains make up the majority of global human caloric intake. However, it remains a mystery how these grasses became dominant and successful in both nature and later in agriculture. The lab of Hiroshi Maeda, a professor of botany at UW–Madison, teamed up with researchers from around the world to address this question.
The team was particularly interested in the metabolism of grasses, focusing on genes that are needed to make starch and lignin. Grasses are rich in starch, a complex carbohydrate that acts as the plant's energy storage, and their rapid growth requires the efficient production of lignin, a major component of plant biomass.
Just as scientists use the chimpanzee's genome as a comparison tool to study how humans evolved, Maeda's group and their collaborators, James Leebens-Mack from University of Georgia, turned to the closest relatives of grasses, such as Joinvillea ascendens.
This long-leafed plant is found in wet forests of the South Pacific islands and grows much more slowly than many grasses.
Only two out of over 100 seeds obtained from the National Tropical Botanical Garden in Hawaii germinated initially. It took another two years for these plants to grow large enough to be harvested for genomic sequencing. Then, they were finally able to sequence the genomes of Joinvillea, along with three related species.
Comparing thousands of genes found in these genomes, they revealed that Joinvillea has only one pathway to create starch. All grasses, though, have two.
This means that an additional starch synthesis pathway, or a bypass route, emerged at the common ancestor of all grasses and now allows grasses to produce double the amount of energy than Joinvillea and other non-grass plants.
In the natural world, a seed with more energy packed inside can germinate, sprout out of the ground, and begin the process of photosynthesis sooner. That allows the plant to grow taller quickly, outcompeting surrounding slower growing plants.
"That likely gave a competitive advantage to grasses to grow in open habitat, where a lot of plants would love to grow because of all the sun," Maeda says. "That's one potential reason why grasses ended up maintaining this highly efficient starch pathway. That same metabolic trait was also very beneficial to agriculture."
The researchers, including Maeda's postdoctoral researcher, Yuri Takeda-Kimura, were also interested in how grasses and Joinvillea produced lignin, a chemical compound that gives strong structural support to plants. Plants with high lignin content, like woody plants, tend to grow slowly. Grasses, however, are an exception; they can grow rapidly despite having relatively high lignin contents.
Tracing back the history of lignin synthesis pathways, the team found that both grasses and Joinvillea had two pathways for lignin synthesis. This time, Joinvillea had two.
"It turned out, this unique feature of grasses, capable of synthesizing lignin by two routes, evolved even before grasses existed", Maeda says.
Knowing when this critical change happened, the team further discovered how the dual lignin pathways were generated.
"We found two mutations in their DNA that are critical and sufficient to create this new bypass pathway," Maeda says. "So, that means, we can actually introduce similar mutations in other plants to create this second lignin pathway."
Maeda says that understanding what makes grasses unique opens doors for future improvements to cereal and bioenergy crops and other plants, whether it be augmented energy stores through additional starch synthesis pathways or improved structure strength and resilience through increased production of lignin and other related compounds.
Maeda and his collaborators are using this basic science knowledge for potential applications in plant biotechnology to improve sustainable production of beneficial nutrients and other useful chemicals in agricultural and bioenergy crops.
This work was supported by the U.S. National Science Foundation (NSF) Plant Genome Research Program (IOS-1836824) and the U.S. Department of Agriculture (NIFA-2024-67013-42518). Funding was also provided by the Oversea research fellow of the Japan Society for the Promotion of Science (JSPS), United Kingdom Research and Innovation-Biotechnology and Biological Sciences Research Council, Norwich Research Park Doctoral Training Partnership (grant no. BB/M011216/1), Institute Strategic Programme (grant no.BB/P012574/1 and BBS/E/J/000PR9795), Gatsby Charitable Foundation, United States Department of Agriculture-Agricultural Research Service CRIS #5062-21220-025-000D, the U.S. Department of Energy Joint Genome Institute (https://ror.org/04xm1d337; proposal:10.46936/10.25585/60001405), the Office of Science of the U.S. Department of Energy, the U.S. National Science Foundation (NSF) EPSCoR (OIA-1920858), Rules of Life (DEB-2001190) programs, and U.S. Army Corp of Engineers (USACE) Sustainable Rivers (W9126G-23-2-0018).
