A team of scientists with two Department of Energy Bioenergy Research Centers - the Center for Bioenergy Innovation, or CBI, at Oak Ridge National Laboratory and the Center for Advanced Bioenergy and Bioproducts Innovation, or CABBI, at the University of Illinois Urbana-Champaign - identified a gene in a poplar tree that enhances photosynthesis and can boost tree height by about 30% in the field and by as much as 200% in the greenhouse.
The gene, which scientists named Booster, also increased the biomass of another plant species, Arabidopsis, or thale cress, indicating the potential for higher yields from other crops if successful on a larger scale.
Booster was identified in Populus trichocarpa, or the black cottonwood tree, a species that thrives from Baja California in Mexico into northern Canada. This tree is recognized as a leading candidate as a feedstock for making biofuels and bioproducts.
Booster is a chimeric gene that contains sequences from three originally separated genes, and has been preserved in poplar with minimal changes over evolutionary time. The gene plays an important role in photosynthesis, the process plants use to convert sunlight, carbon dioxide and water into glucose - the building block for cellulose, starch and other macromolecules related to food and fuel production.
Chimeric genes have unique origins and are thought to enable evolutionary changes that help plants adapt to new environments. In the case of Booster, the ORNL team determined that it contains three different DNA origins. One segment is from a bacteria found in the poplar tree's root system; one segment is from an ant that farms a fungus known to infect poplar; and one segment is from the large subunit of Rubisco, an abundant protein found in plant chloroplasts.
Chloroplasts are the principal cell structures that house the photosynthetic apparatus converting light energy into the chemical energy that fuels plant growth. The Rubisco protein functions as the plant's "carbon-grabber," capturing carbon dioxide from the atmosphere. Scientists have for years been working on ways to boost the amount of Rubisco in plants for greater crop yield and absorption of atmospheric CO2.
When researchers created poplar trees with greater expression of the Booster gene, their Rubisco content and subsequent photosynthetic activity soared, resulting in plants that were as much as 200% taller when grown in greenhouse conditions, as described in the journal Developmental Cell . The trees demonstrated up to 62% more Rubisco content and about a 25% increase in net leaf CO2 uptake. In field conditions, scientists found that higher expression of Booster resulted in poplar trees up to 37% taller, with as much as 88% more stem volume, increasing biomass per plant.
Scientists inserted Booster in a different plant, Arabidopsis, resulting in a similar increase in biomass and a 50% increase in seed production. This finding indicates the wider applicability of Booster to potentially trigger higher yields in other plants.
Multiple benefits from a single enhancement
Poplar and Arabidopsis are known as C3 plants, a category that includes key food crops such as soybeans, rice, wheat and oats. The Booster gene has the potential to increase bioenergy crop yields without requiring more land, water or fertilizer, supporting a robust bioeconomy. If Booster works similarly in food crops, higher yields could reduce food scarcity around the world.
"Growing high-yielding, perennial bioenergy crops on marginal lands unsuitable for conventional agriculture can help us meet rising demand for liquid biofuels for hard-to-electrify sectors like aviation," said Jerry Tuskan, CBI director and a Corporate Fellow at ORNL who coauthored the paper. "Fast-growing, resilient feedstock plants can stimulate the bioeconomy, create rural jobs, and support forecasted demand for energy."
"This discovery could be a game-changer in terms of a big stimulation of photosynthesis and plant productivity," said Stephen Long, a leading authority on plant photosynthesis and professor at the University of Illinois Urbana-Champaign, who is also a coauthor in his role with the Illinois-led CABBI. "While we need to test more widely to be sure we can reproduce the results on a large scale, the fact that it worked in a completely unrelated plant indicates that it could work over a wider range of plants."
Next steps in the research could encompass multilocation field trials of poplar and other bioenergy and food plants, with researchers recording plant productivity in varying growing conditions to analyze long-term success, Long said.
The discovery was the result of a collaboration between two DOE centers where scientists focus on developing improved bioenergy feedstock plants along with efficient methods to process plants into advanced fuels and products.
Collaboration links large genetic database, photosynthesis expertise
At the ORNL-led CBI, scientists have studied poplar for years as a fast-growing, nonfood perennial crop for feedstock production. They assembled the first genome-wide association study, or GWAS, of Populus trichocarpa by sampling from 1,500 trees in the wild and analyzing their physical characteristics and genetic makeup. The GWAS, one of the first and largest of its kind, identified more than 28 million single nucleotide polymorphisms that act as biological markers, helping scientists locate genes associated with certain traits such as plant growth; carbon, nitrogen and lignin content; and how efficiently the plants use water.
Scientists from CBI and CABBI used the GWAS population to look for two candidate genes that had been linked to photosynthetic quenching, a process that regulates how quickly plants adjust between sun and shade and dissipate excess energy from too much sun to avoid damage. CABBI scientists leveraged screening techniques they had developed to conduct rapid phenotyping of poplar in trial gardens in Davis, California. Initial screenings did not immediately turn up the genes they were looking for. But further molecular analysis of one candidate gene turned out to be Booster, which influences the two genes CABBI had predicted to be key to improved photosynthesis.
The research was supported by CBI and CABBI, both sponsored by the DOE Office of Science Biological and Environmental Research Program. The project used the high-throughput, world-leading imaging capabilities of ORNL's Advanced Plant Phenotyping Laboratory , which enabled rapid, automated measurement of leaf size changes in poplars expressing the Booster gene in a greenhouse environment. Whole-genome sequencing and other RNA analyses were conducted by the Joint Genome Institute, or JGI, a DOE Office of Science user facility at Lawrence Berkeley National Laboratory. The project used high-performance computing resources of the Oak Ridge Leadership Computing Facility, a DOE Office of Science user facility at ORNL.
Opening a new avenue of scientific thinking
"Conserved chimeric genes such as Booster are often disregarded as non-functional, evolutionary artifacts that no longer influence plant processes," said ORNL's Biruk Feyissa, who led the gene's molecular analysis and is first author on the paper. "But here we proved just the opposite. Our molecular and physiological validation confirmed that Booster enhances photosynthesis so that plants perform better under steady and fluctuating light conditions."
"The discovery opens up a new avenue of scientific thinking," Tuskan said. "We tend to think of photosynthesis as a difficult-to-improve process. But in fact, the molecular machinery surrounding photosynthesis has continued to evolve as plants adapted to their environment. In this case, the exchange of DNA with associated organisms changed a biological process in a fundamental way."
Other scientists on the project include co-lead Steven Burgess of CABBI and the Carl R. Woese Institute for Genomic Biology at Illinois; co-lead Jay Chen, ORNL Plant Systems Biology group leader; Jin Zhang, Timothy Yates, Kuntal De, Sara Jawdy, Dana Carper, David Weston, Paul Abraham and Jennifer Morrell-Falvey of CBI/ORNL; Elsa de Becker and Coralie Salesse-Smith of CABBI/Illinois; Margot SS Chen and Chung-Jui Tsai of CBI/University of Georgia; Gail Taylor of CBI/University of California, Davis; Meng Xie of Brookhaven National Laboratory; Dhananjay Gotarkar of the University of Missouri; Kerrie Barry of JGI/Lawrence Berkeley National Laboratory; and Jeremy Schmutz of JGI and HudsonAlpha. The paper is dedicated to the memory of Wellington Muchero, project co-lead and former ORNL plant scientist and geneticist.
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