Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

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

Nature Plants volume 1, Article number: 15035 (2015) Cite this article

Subjects

A Corrigendum to this article was published on 10 April 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.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

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.

Similar content being viewed by others

References

  1. Hayashi, M. & Nishimura, M. Arabidopsis thaliana – a model organism to study plant peroxisomes. Biochim. Biophys. Acta 1763, 1382–1391 (2006).

    Article  CAS  Google Scholar 

  2. Hu, J. et al. Plant peroxisomes: biogenesis and function. Plant Cell 24, 2279–2303 (2012).

    Article  CAS  Google Scholar 

  3. Pracharoenwattana I. & Smith S. When is a peroxisome not a peroxisome? Trends Plant Sci. 13, 522–525 (2008).

    Article  CAS  Google Scholar 

  4. Peterhansel, C. et al. Photorespiration. Arabidopsis Book 8, e0130 (2010).

    Article  Google Scholar 

  5. Takahashi, S. & Badger, M. R. Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci. 16, 53–60 (2011).

    Article  CAS  Google Scholar 

  6. Kozaki, K. & Takeba, G. Photorespiration protects C3 plants from photooxidation. Nature 384, 557–560 (1996).

    Article  CAS  Google Scholar 

  7. Hayashi, Y. et al. Direct interaction between glyoxysomes and lipid bodies in cotyledons of the Arabidopsis thaliana ped1 mutant. Protoplasma 218, 83–94 (2001).

    Article  CAS  Google Scholar 

  8. Tolbert, N. E. & Essner, E. Microbodies: peroxisomes and glyoxysomes. J. Cell Biol. 91, 271s–283s (1981).

    Article  CAS  Google Scholar 

  9. Beevers, H. Microbodies in higher plants. Annu. Rev. Plant Physiol. 30, 159–193 (1979).

    Article  CAS  Google Scholar 

  10. Corpas, F. J. et al. Trends Plant Sci. 6, 145–150 (2001).

  11. Spiess, G. M. & Zolma, B. K. Subcell. Biochem. 69, 257–281 (2013).

    Article  CAS  Google Scholar 

  12. Wada, M., Kagawa, T. & Sato, Y. Chloroplast movement. Annu. Rev. Plant Biol. 54, 455–468 (2003).

    Article  CAS  Google Scholar 

  13. Takagi, S., Islam, M. S. & Iwabuchi, K. Dynamic behavior of double-membrane-bounded organelles in plant cells. Int. Rev. Cell Mol. Biol. 286, 181–222 (2011).

    Article  CAS  Google Scholar 

  14. Wada, M. & Suetsugu, N. Plant organelle positioning. Curr. Opin. Plant Biol. 7, 626–631 (2004).

    Article  CAS  Google Scholar 

  15. Higaki, T., Sano, T. & Hasezawa, S. Actin microfilament dynamics and actin side-binding proteins in plants. Curr. Opin. Plant Biol. 10, 549–556 (2007).

    Article  CAS  Google Scholar 

  16. Mathur, J., Mathur, N. & Hulskamp, M. Simultaneous visualization of peroxisomes and cytoskeletal elements reveals actin and not microtubule-based peroxisome motility in plants. Plant Physiol. 128, 1031–1045 (2002).

    Article  CAS  Google Scholar 

  17. Mano, S. et al. Distribution and characterization of peroxisomes in Arabidopsis by visualization with GFP: dynamic morphology and actin-dependent movement. Plant Cell Physiol. 43, 331–341 (2002).

    Article  CAS  Google Scholar 

  18. Kaji, T. et al. Nondestructive micro-patterning of living animal cells using focused femtosecond laser-induced impulsive force. Appl. Phys. Lett. 91, 023904 (2007).

    Article  Google Scholar 

  19. Hosokawa, Y. et al. Non-contact estimation of intercellular breaking force using a femtosecond laser impulse quantified by atomic force microscopy. Proc. Natl Acad. Sci. USA 108, 1777–1782 (2011).

    Article  CAS  Google Scholar 

  20. Iino, T. & Hosokawa, Y. Direct measurement of femtosecond laser impulse in water by atomic force microscopy. Appl. Phys. Express 3, 107002 (2010).

    Article  Google Scholar 

  21. Oikawa, K. et al. Chloroplast outer envelope protein CHUP1 is essential for chloroplast anchorage to the plasma membrane and chloroplast movement. Plant Physiol. 148, 829–842 (2008).

    Article  CAS  Google Scholar 

  22. Vogel, A. & Venugopalan, V. Mechanisms of pulsed laser ablation of biological tissues. Chem. Rev. 103, 577–644 (2003).

    Article  CAS  Google Scholar 

  23. Vogel, A. et al. Mechanisms of femtosecond laser nanosurgery of cells and tissues. Appl. Phys. B 81, 1015–1047 (2005).

    Article  CAS  Google Scholar 

  24. Usami, T. et al. Cryptochromes and phytochromes synergistically regulate Arabidopsis root greening under blue light. Plant Cell Physiol. 45, 1798–1808 (2004).

    Article  CAS  Google Scholar 

  25. Ahmad, M. et al. Cryptochrome blue-light photoreceptors of Arabidopsis implicated in phototropism. Nature 392, 720–723 (1998).

    Article  CAS  Google Scholar 

  26. Sakai, T. et al. Arabidopsis nph1 and npl1: blue light receptors that mediate both phototropism and chloroplast relocation. Proc. Natl Acad. Sci. USA 98, 6969–6974 (2001).

    Article  CAS  Google Scholar 

  27. Campbell, W. J. & Ogren, W. L. Electron transport through photosystem I stimulates light activation of ribulose bisphosphate carboxylase/oxygenase (Rubisco) by rubisco activase. Plant Physiol. 94, 479–484 (1990).

    Article  CAS  Google Scholar 

  28. Murata, N. et al. Photoinhibition of photosystem II under environmental stress. Biochim. Biophys. Acta 1767, 414–421 (2007).

    Article  CAS  Google Scholar 

  29. Braun, G. et al. Proton flow through the ATP synthase in chloroplasts regulates the distribution of light energy between PS I and PS II. FEBS Lett. 280, 57–60 (1991).

    Article  CAS  Google Scholar 

  30. Kato, Y. et al. The variegated mutants lacking chloroplastic FtsHs are defective in D1 degradation and accumulate reactive oxygen species. Plant Physiol. 151, 1790–1801 (2009).

    Article  CAS  Google Scholar 

  31. Hayashi, M. et al. AtPex14p maintains peroxisomal functions by determining protein targeting to three kinds of plant peroxisomes. EMBO J. 19, 5701–5710 (2000).

    Article  CAS  Google Scholar 

  32. Takahashi, S., Bauwe, H. & Badger, M. Impairment of the photorespiratory pathway accelerates photoinhibition of photosystem II by suppression of repair but not acceleration of damage processes in Arabidopsis. Plant Physiol. 144, 487–494 (2007).

    Article  CAS  Google Scholar 

  33. Spector, I. et al. Latrunculins: novel marine toxins that disrupt microfilament organization in cultured cells. Science 219, 493–495 (1983).

    Article  CAS  Google Scholar 

  34. Casella, J. F., Flanagan, M. D. & Lin, S. Cytochalasin D inhibits actin polymerization and induces depolymerization of actin filaments formed during platelet shape change. Nature 293, 302–305 (1981).

    Article  CAS  Google Scholar 

  35. Oikawa, K. et al. Chloroplast unusual positioning is essential for proper chloroplast positioning. Plant Cell 15, 2805–2815 (2003).

    Article  CAS  Google Scholar 

  36. Sheahan, M. B. et al. A green fluorescent protein fusion to actin-binding domain 2 of Arabidopsis fimbrin highlights new features of a dynamic actin cytoskeleton in live plant cells. Plant Physiol. 136, 3968–3978 (2004).

    Article  CAS  Google Scholar 

  37. Ishijima, A. et al. Simultaneous observation of individual ATPase and mechanical events by a single myosin molecule during interaction with actin. Cell 92, 161–171 (1998).

    Article  CAS  Google Scholar 

  38. Piramowicz, M. O. et al. Dynamic force measurements of avidin–biotin and streptavidin–biotin interactions using AFM. Acta Biochim. Polon. 53, 93–100 (2006).

    CAS  Google Scholar 

  39. Panorchan, P. et al. Single-molecule analysis of cadherin-mediated cell-cell adhesion. J. Cell Sci. 119, 66–74 (2006).

    Article  CAS  Google Scholar 

  40. Sinclair, A. M., Trobacher, C. P., Mathur, N., Greenwood, J. S. & Mathur, J. Peroxule extension over ER-defined paths constitutes a rapid subcellular response to hydroxyl stress. Plant J. 59, 231–242 (2009).

    Article  CAS  Google Scholar 

  41. Sunil, B. et al. Optimization of photosynthesis by multiple metabolic pathways involving interorganelle interactions: resource sharing and ROS maintenance as the bases. Photosynth. Res. 117, 61–71 (2013).

    Article  CAS  Google Scholar 

  42. Hu, J. et al. A role for peroxisomes in photomorphogenesis and development of Arabidopsis. Science 297, 405–409 (2002).

    Article  CAS  Google Scholar 

  43. Takemiya, A. et al. Phototropins promote plant growth in response to blue light in low light environments. Plant Cell 17, 1120–1127 (2005).

    Article  CAS  Google Scholar 

  44. Christie, J. M. Phototropin blue-light receptors. Annu. Rev. Plant Biol. 58, 21–45 (2007).

    Article  CAS  Google Scholar 

  45. Peremyslov, V. V. et al. Two class XI myosins function in organelle trafficking and root hair development in Arabidopsis. Plant Physiol. 146, 1109–1116 (2008).

    Article  CAS  Google Scholar 

  46. Tominaga, M. et al. Higher plant myosin XI moves processively on actin with 35 nm steps at high velocity. EMBO J. 22, 1263–1272 (2003).

    Article  CAS  Google Scholar 

  47. de Brito, O. M. & Scorrano, L. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 456, 605–610 (2008).

    Article  Google Scholar 

  48. Binns, D. et al. An intimate collaboration between peroxisomes and lipid bodies. J. Cell Biol. 173, 719–731 (2006).

    Article  CAS  Google Scholar 

  49. Kagawa, T. & Wada, M. Blue light-induced chloroplast relocation in Arabidopsis thaliana as analyzed by microbeam irradiation. Plant Cell Physiol. 41, 84–93 (2000).

    Article  CAS  Google Scholar 

  50. Arimura, S., Yamamoto, J., Aida, G. P., Nakazono, M. & Tsutsumi, N. Frequent fusion and fission of plant mitochondria with unequal nucleoid distribution. Proc. Natl Acad. Sci. USA 101, 7805–7808 (2004).

    Article  CAS  Google Scholar 

Download references

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).

Author information

Author notes

  1. Kazusato Oikawa, Shigeru Matsunaga, Kenji Yamada & Makoto Hayashi

    Present address: †Present address: Department of Applied Biological Chemistry, Faculty of Agriculture, Niigata University, Niigata 950-2181, Niigata, Japan (K.O.); Central Research Laboratory, Hamamatsu Photonics K.K. (S.M.); Department of Botany, Graduate School of Science, Kyoto University, Kyoto 606-8502, Kyoto, Japan (K.Y.); Department of Bioscience, Nagahama Institute of Bioscience and Technology, Nagahama 526-0829, Shiga, Japan (M.H.),

Authors and Affiliations

  1. Department of Cell Biology, National Institute for Basic Biology, Okazaki 444-8585, Aichi, Japan

    Kazusato Oikawa, Shoji Mano, Maki Kondo, Kenji Yamada, Makoto Hayashi & Mikio Nishimura

  2. Hayama Center for Advanced Studies, SOKENDAI (The Graduate University for Advanced Studies), Hayama 240-0193, Kanagawa, Japan

    Shigeru Matsunaga & Masakatsu Watanabe

  3. Department of Basic Biology, School of Life Science, SOKENDAI (The Graduate University for Advanced Studies), Okazaki 444-8585, Aichi, Japan

    Shoji Mano, Kenji Yamada & Mikio Nishimura

  4. Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba 305-8572, Ibaraki, Japan

    Takatoshi Kagawa

  5. Department of Biological Sciences, Graduate School of Science, Tokyo Metropolitan University,

    Akeo Kadota

  6. Institute of Plant Science and Resources, Okayama University, Kurashiki 710-0046, Okayama, Japan

    Wataru Sakamoto

  7. Okazaki Large Spectrograph, National Institute for Basic Biology, Okazaki 444-8585, Aichi, Japan

    Shoichi Higashi & Masakatsu Watanabe

  8. Department of Applied Biological Chemistry, Faculty of Agriculture, Niigata University, Niigata 950-2181, Niigata, Japan

    Toshiaki Mitsui

  9. Graduate School of Materials Science, Nara Institute of Science and Technology, Ikoma 630-0192, Nara, Japan

    Akinori Shigemasa, Takanori Iino & Yoichiroh Hosokawa

Authors
  1. Kazusato Oikawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shigeru Matsunaga
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shoji Mano
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maki Kondo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kenji Yamada
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Makoto Hayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Takatoshi Kagawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Akeo Kadota
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Wataru Sakamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Shoichi Higashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Masakatsu Watanabe
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Toshiaki Mitsui
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Akinori Shigemasa
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Takanori Iino
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Yoichiroh Hosokawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Mikio Nishimura
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

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.

Corresponding authors

Correspondence to Yoichiroh Hosokawa or Mikio Nishimura.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nplants.2015.35

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing