Abstract
Organelle-to-nucleus DNA transfer is an ongoing process playing an important role in the evolution of eukaryotic life. Here, genome-wide association studies (GWAS) of non-photochemical quenching parameters in 743 Populus trichocarpa accessions identified a nuclear-encoded genomic region associated with variation in photosynthesis under fluctuating light. The identified gene, BOOSTER (BSTR), comprises three exons, two with apparent endophytic origin and the third containing a large fragment of plastid-encoded Rubisco large subunit. Higher expression of BSTR facilitated anterograde signaling between nucleus and plastid, which corresponded to enhanced expression of Rubisco, increased photosynthesis, and up to 35% greater plant height and 88% biomass in poplar accessions under field conditions. Overexpression of BSTR in Populus tremula × P. alba achieved up to a 200% in plant height. Similarly, Arabidopsis plants heterologously expressing BSTR gained up to 200% in biomass and up to 50% increase in seed.
Original language | English |
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Journal | Developmental Cell |
DOIs | |
State | Accepted/In press - 2025 |
Funding
The authors thank W. Patrick Bewg, Lynn Doran, Laurie Leonelli, and Brent Lieb for laboratory assistance; Berkley Walker for the gift of pure RubP for the Rubisco assays; and Mac McLennan for his assistance with the Advanced Plant Phenotyping Laboratory (APPL) instrumentation. This manuscript has been financially supported by the Center for Bioenergy Innovation (CBI), which is a US Department of Energy Bioenergy Research Center supported by the Office of Biological and Environmental Research Program in the DOE Office of Science under award number ERKP886 and by the Center for Advanced Bioenergy and Bioproducts Innovation (CABBI) at the University of Illinois and supported by the US Department of Energy, Office of Science, Biological and Environmental Research Program under award number DE-SC0018420. Oak Ridge National Laboratory is managed by UT-Battelle, LLC for the US DOE under contract number DE-AC05-00OR22725. The whole-genome sequencing and RNA-seq analysis work (proposal: 10.46936/10.25585/60001221) was conducted by the US Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, supported by the Office of Science of the US Department of Energy operated under contract no. DE-AC02-05CH11231. This research used resources of the Compute and Data Environment for Science (CADES) and the Oak Ridge Leadership Computing Facility (OLCF) at the Oak Ridge National Laboratory. D.G. was supported by the UK Foreign, Commonwealth & Development Office grant OPP11722157. M.X. is supported by the US DOE, Office of Science, Office of Biological and Environmental Research, as part of the Quantitative Plant Science Initiative (QPSI) at Brookhaven National Laboratory. S.J.B. was supported by CABBI.The United States Government retains and the publisher, by accepting the article for publication, acknowledges that the United States Government retains a nonexclusive, paid-up, irrevocable, worldwide license to publish or reproduce the published form of this manuscript, or allow others to do so, for United States Government purposes. The Department of Energy will provide public access to these results of federally sponsored research in accordance with the DOE Public Access Plan (http://energy.gov/downloads/doe-public-access-plan).
Keywords
- anterograde signaling
- biomass
- Booster
- EGT
- horizontal gene transfer
- NPQ
- NUPT
- orphan gene
- photosynthesis
- Rubisco