Physical interaction between peroxisomes and chloroplasts elucidated by in situ laser analysis

A Corrigendum to this article was published on 01 January 2015

Abstract

Life on earth relies upon photosynthesis, which consumes carbon dioxide and generates oxygen and carbohydrates. Photosynthesis is sustained by a dynamic environment within the plant cell involving numerous organelles with cytoplasmic streaming. Physiological studies of chloroplasts, mitochondria and peroxisomes show that these organelles actively communicate during photorespiration, a process by which by-products produced by photosynthesis are salvaged. Nevertheless, the mechanisms enabling efficient exchange of metabolites have not been clearly defined. We found that peroxisomes along chloroplasts changed shape from spherical to elliptical and their interaction area increased during photorespiration. We applied a recent femtosecond laser technology to analyse adhesion between the organelles inside palisade mesophyll cells of Arabidopsis leaves and succeeded in estimating their physical interactions under different environmental conditions. This is the first application of this estimation method within living cells. Our findings suggest that photosynthetic-dependent interactions play a critical role in ensuring efficient metabolite flow during photorespiration.

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Figure 1: Light enhances the peroxisome–chloroplast interaction and peroxisome movement.
Figure 2: Estimation of the force required to detach peroxisomes from chloroplasts.
Figure 3: Photosynthetic regulation of peroxisome–chloroplast interactions and peroxisome movements.
Figure 4: Interactions between peroxisomes and F-actin in leaf palisade mesophyll cells.
Figure 5: Light-dependent formation of the three-organelle complex under photosynthetic conditions.

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Acknowledgements

We thank Drs S. Arimura (The University of Tokyo) for providing the Mt-GFP plants, S. Takahashi (The Australian National University; ANU) for providing shmt1, and M.R. Badger (ANU) and S. Takahashi (ANU) for kindly discussing and suggesting experiments. This work was supported by MEXT KAKENHI (Grant-in-Aid for Scientific Research on Innovative Areas) to M.N. (no. 22120007) and Y.H. (no. 22120010).

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K.O., Y.H., and M.N. designed the entire study; K.O. performed most of the experiments; K.O., S. Matsunaga, S. Mano, K.Y., M.H., A.K., T.K., W.S., T.M., S.H., and M.W. performed the physiological and fluorescence microscopic experiments; Y.H., T.I., and A.S. performed the adhesion analysis using femtosecond laser and AFM; S. Matsunaga performed analyses of peroxisome movement; M.K. performed transmission electron microscopic analysis; K.O., Y.H., S. Mano, K.Y., and M.N. wrote the paper; Y.H. supervised femtosecond laser analysis; and M.N. supervised and supported the entire study.

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Correspondence to Yoichiroh Hosokawa or Mikio Nishimura.

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Oikawa, K., Matsunaga, S., Mano, S. et al. Physical interaction between peroxisomes and chloroplasts elucidated by in situ laser analysis. Nature Plants 1, 15035 (2015). https://doi.org/10.1038/nplants.2015.35

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