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An Orphan-Moonlighting Gene PRL-1 Enhances Photosynthetic Efficiency and Productivity in Plants

ABSTRACT: Increasing photosynthetic efficiency remains a major goal across the globe given its central role in CO2 assimilation. Here, we identified a nuclear genome-residing orphan gene, comprised of 3 exons, two with apparent endophytic origins and the third being a highly conserved fragment of the RIBULOSE BISPHOSPHATE CARBOXYLASE/ OXYGENASE LARGE SUBUNIT (RuBisCo). This novel gene, here-on referred to as Populus RuBisCo-like (PRL-1) gene localizes in chloroplast, endoplasmic reticulum and nuclear compartments of plant cells, acts as a transcriptional repressor and modulates adaptation to fluctuating light. P. trichocarpa genotypes with high PRL-1 expression levels quickly dissipated non-photochemical quenching (NPQ) upon transitioning from high to low light and rapidly induced NPQ upon returning to high light. The dynamic modulation of NPQ yields high quantum efficiency of linear electron transport (PSII) and 10-20% increased quantum efficiency of CO2 assimilation (CO2). The enhanced photosynthesis efficiency corresponded with increased plant height and biomass in P. trichocarpa with up to 35 % and 100% increases under field and greenhouse conditions. Transgenic Arabidopsis plants heterologously expressing the PRL-1 gene gained up to 200% in biomass and 97% in seed yield under greenhouse conditions. Taken together, PRL-1 presents a novel and trackable target for increasing photosynthetic efficiency in plants.

INSTRUMENT(S): Q Exactive Plus

ORGANISM(S): Populus Trichocarpa (ncbitaxon:3694)

SUBMITTER: Paul Abraham

PROVIDER: MSV000091785 | MassIVE | Mon Apr 24 05:32:00 BST 2023

SECONDARY ACCESSION(S): PXD041771

REPOSITORIES: MassIVE

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Project description:Heterosis, a phenomenon where hybrids exhibit superior performance in various traits such as yield, quality, and resistance compared to their parents, has long been a focus of agricultural research. Although tobacco biomass significantly affects tobacco yield and economic profitability, the underlying reasons for the dominance of tobacco biomass hybrids and their formation remain unclear. To address this, we selected 5 tobacco varieties (lines) with large differences in tobacco biomass as the parents and formulated F1 hybrids to analyze the expression of tobacco biomass heterosis. Our findings demonstrate that tobacco leaf biomass exhibits a clear heterosis advantage. In particular, the hybrid Va116×GDH94 showed strong heterosis, with 76.69% of differentially expressed genes (DEGs) displaying Overdominant expression pattern. Notably, these Overdominant DEGs were significantly enriched in biological processes such as photosynthesis and respiration. During photosynthesis, transgressive up-regulation of Lhc improved light-harvesting efficiency, while the up-regulation of Psa and Psb in the photosystem enhanced the defense of chloroplasts against strong light. Additionally, the up-regulation of rbcl promoted the increase of photosynthetic products in the hybrids. During respiration, the down-regulation of MDH, ACO, and OGDH suppressed the tricarboxylic acid cycle (TCA cycle) and weakened respiratory consumption in the hybrids. Furthermore, we observed that the net photosynthetic rate and intercellular CO2 concentration of the hybrids were significantly higher than those of the parents. Taken together, our results suggest that the overdominant expression effect of DEGs plays a crucial role in the formation of tobacco biomass hybrid advantage. The overdominant expression effect of photosynthesis and respiration-related genes enhanced the photosynthetic capacity of the hybrids, reduced respiration consumption, and promoted the increase of tobacco biomass, thus demonstrating the obvious hybrid advantage.

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An Orphan-Moonlighting Gene PRL-1 Enhances Photosynthetic Efficiency and Productivity in Plants

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