Abstract
Key message
By using the organelle glue technique, we artificially manipulated organelle interactions and controlled the plant metabolome at the pathway level.
Abstract
Plant cell metabolic activity changes with fluctuating environmental conditions, in part via adjustments in the arrangement and interaction of organelles. This hints at the potential for designing plants with desirable metabolic activities for food and pharmaceutical industries by artificially controlling the interaction of organelles through genetic modification. We previously developed a method called the organelle glue technique, in which chloroplast–chloroplast adhesion is induced in plant cells using the multimerization properties of split fluorescent proteins. Here, we generated transgenic Arabidopsis (Arabidopsis thaliana) plants in which chloroplasts adhere to each other and performed metabolome analysis to examine the metabolic changes in these lines. In plant cells expressing a construct encoding the red fluorescent protein mCherry targeted to the chloroplast outer envelope by fusion with a signal sequence (cTP-mCherry), chloroplasts adhered to each other and formed chloroplast aggregations. Mitochondria and peroxisomes were embedded in the aggregates, suggesting that normal interactions between chloroplasts and these organelles were also affected. Metabolome analysis of the cTP-mCherry-expressing Arabidopsis shoots revealed significantly higher levels of glycine, serine, and glycerate compared to control plants. Notably, these are photorespiratory metabolites that are normally transported between chloroplasts, mitochondria, and peroxisomes. Together, our data indicate that chloroplast–chloroplast adhesion alters organellar interactions with mitochondria and peroxisomes and disrupts photorespiratory metabolite transport. These results highlight the possibility of controlling plant metabolism at the pathway level by manipulating organelle interactions.
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Data availability
All data in this study are available from the corresponding author upon reasonable request.
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Acknowledgements
We thank Ms. Hitomi Takahashi (Utsunomiya University) and Ms. Miho Kitamura (Utsunomiya University) for technical assistance; Dr. Tsuyoshi Nakagawa (Shimane University) for providing vectors (pGWB508 and pGWB602).
Funding
This work was supported by the Japan Science and Technology Agency Exploratory Research for Advanced Technology program (JST-ERATO; Grant No. JPMJER1602) and MEXT KAKENHI (Grant No. 20H05905).
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KI, KN, and YK conceived the research plans and performed most of the experiments including data analysis; MK, MK, and KI performed metabolome analysis; KN and YK supervised the experiments; KI and YK interpreted the results and wrote the manuscript with contributions from all authors.
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Ishikawa, K., Kobayashi, M., Kusano, M. et al. Using the organelle glue technique to engineer the plant cell metabolome. Plant Cell Rep 42, 599–607 (2023). https://doi.org/10.1007/s00299-023-02982-2
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DOI: https://doi.org/10.1007/s00299-023-02982-2