The PRK/Rubisco shunt strongly influences Arabidopsis seed metabolism and oil accumulation, affecting more than carbon recycling

Deslandes-Hérold, Gabriel; Zanella, Martina; Solhaug, Erik; Fischer-Stettler, Michaela; Sharma, Mayank; Buergy, Léo; Herrfurth, Cornelia; Colinas, Maite; Feussner, Ivo; Abt, Melanie R; Zeeman, Samuel C (2023). The PRK/Rubisco shunt strongly influences Arabidopsis seed metabolism and oil accumulation, affecting more than carbon recycling. The Plant Cell, 35(2), pp. 808-826. American Society of Plant Biologists 10.1093/plcell/koac338

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Background: Light promotes the accumulation of storage lipids during development of oilseeds with green embryos. This has been explained by embryonic photosynthesis generating cofactors that can power an energy-consuming metabolic pathway known as the PRK/Rubisco shunt that is distinct from the Calvin cycle operating in leaves. There is good biochemical evidence for the existence of this pathway in Brassicaceae; however, the extent of its biological significance has not been assessed genetically. Here, we use a refined genetic complementation approach in Arabidopsis to study the role of PRK, specifically in the proposed pathway in its green seeds.

Questions: How can we study the PRK/Rubisco shunt genetically, and what is its quantitative influence on storage oil accumulation in green, developing Arabidopsis seeds?

Findings: As an enzyme integral to the Calvin cycle, the complete loss of PRK is detrimental to plant growth. However, because heterozygous PRK/prk plants are phenotypically normal, we used them to establish a plant line generating prk embryos in parallel with complemented siblings, which can be differentiated using a fluorescent marker. The absence of PRK throughout embryogenesis reduced the oil content in the embryo by one-third; more than expected from theoretical calculations of the contribution of the PRK/Rubisco shunt. Several lines of evidence further indicate tight metabolic integration of the shunt into green embryo photosynthesis and metabolism.

Next steps: Our observations provide insight into the integration of the PRK/Rubisco shunt into Arabidopsis embryo metabolism. We would like to understand better how it is coordinated with pathways leading to other storage compounds, how it is regulated genetically and biochemically, and how this knowledge can help oil crop improvement.

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