An orphan gene BOOSTER enhances photosynthetic efficiency and plant productivity

Biruk A Feyissa; Elsa M de Becker; Coralie E Salesse-Smith; Jin Zhang; Timothy B Yates; Meng Xie; Kuntal De; Dhananjay Gotarkar; Margot S S Chen; Sara S Jawdy; Dana L Carper; Kerrie Barry; Jeremy Schmutz; David J Weston; Paul E Abraham; Chung-Jui Tsai; Jennifer L Morrell-Falvey; Gail Taylor; Jin-Gui Chen; Gerald A Tuskan; Stephen P Long; Steven J Burgess; Wellington Muchero

doi:10.1016/j.devcel.2024.11.002

An orphan gene BOOSTER enhances photosynthetic efficiency and plant productivity

Dev Cell. 2024 Nov 28:S1534-5807(24)00667-1. doi: 10.1016/j.devcel.2024.11.002. Online ahead of print.

Authors

Biruk A Feyissa¹, Elsa M de Becker², Coralie E Salesse-Smith³, Jin Zhang¹, Timothy B Yates¹, Meng Xie⁴, Kuntal De⁵, Dhananjay Gotarkar⁶, Margot S S Chen⁷, Sara S Jawdy¹, Dana L Carper¹, Kerrie Barry⁸, Jeremy Schmutz⁹, David J Weston⁵, Paul E Abraham¹, Chung-Jui Tsai¹⁰, Jennifer L Morrell-Falvey⁵, Gail Taylor¹¹, Jin-Gui Chen¹², Gerald A Tuskan¹, Stephen P Long¹³, Steven J Burgess¹⁴, Wellington Muchero⁵

Affiliations

¹ Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37830, USA; Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, TN 37830, USA.
² Department of Plant Biology, University of Illinois Urbana-Champaign, Urbana, IL 61801, USA.
³ Center for Advanced Bioenergy and Bioproducts Innovation, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.
⁴ Biology Department, Brookhaven National Laboratory, Upton, NY 11973, USA.
⁵ Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37830, USA.
⁶ Division of Plant Sciences and Technology, University of Missouri, Columbia, MO 65201, USA.
⁷ Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, TN 37830, USA; School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, USA.
⁸ U.S. Department of Energy Joint Genome Institute, Berkeley, CA 94720, USA.
⁹ U.S. Department of Energy Joint Genome Institute, Berkeley, CA 94720, USA; HudsonAlpha Institute for Biotechnology, Huntsville, AL 35806, USA.
¹⁰ Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, TN 37830, USA; School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, USA; Department of Genetics, University of Georgia, Athens, GA 30602, USA; Department of Plant Biology, University of Georgia, Athens, GA 30602, USA.
¹¹ Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, TN 37830, USA; Department of Plant Sciences, University of California Davis, Davis, CA 95616, USA.
¹² Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37830, USA; Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, TN 37830, USA. Electronic address: chenj@ornl.gov.
¹³ Center for Advanced Bioenergy and Bioproducts Innovation, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA; Department of Plant Biology, University of Illinois Urbana-Champaign, Urbana, IL 61801, USA; Carl R Woese Institute for Genomic Biology, University of Illinois Urbana-Champaign, Urbana, IL 61801, USA.
¹⁴ Center for Advanced Bioenergy and Bioproducts Innovation, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA; Department of Plant Biology, University of Illinois Urbana-Champaign, Urbana, IL 61801, USA; Carl R Woese Institute for Genomic Biology, University of Illinois Urbana-Champaign, Urbana, IL 61801, USA. Electronic address: sjb287@illinois.edu.

PMID: 39631390
DOI: 10.1016/j.devcel.2024.11.002

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.

Keywords: Booster; EGT; NPQ; NUPT; Rubisco; anterograde signaling; biomass; horizontal gene transfer; orphan gene; photosynthesis.