Highly oxidized peroxisomes are selectively degraded via autophagy in Arabidopsis

Michitaro Shibata, Kazusato Oikawa, Kohki Yoshimoto, Maki Kondo, Shoji Mano, Kenji Yamada, Makoto Hayashi, Wataru Sakamoto, Yoshinori Ohsumi, Mikio Nishimura

Research output: Contribution to journalArticle

109 Citations (Scopus)

Abstract

The positioning of peroxisomes in a cell is a regulated process that is closely associated with their functions. Using this feature of the peroxisomal positioning as a criterion, we identified three Arabidopsis thaliana mutants (peroxisome unusual positioning1 [peup1], peup2, and peup4) that contain aggregated peroxisomes. We found that the PEUP1, PEUP2, and PEUP4 were identical to Autophagy-related2 (ATG2), ATG18a, and ATG7, respectively, which are involved in the autophagic system. The number of peroxisomes was increased and the peroxisomal proteins were highly accumulated in the peup1 mutant, suggesting that peroxisome degradation by autophagy (pexophagy) is deficient in the peup1 mutant. These aggregated peroxisomes contained high levels of inactive catalase and were more oxidative than those of the wild type, indicating that peroxisome aggregates comprise damaged peroxisomes. In addition, peroxisome aggregation was induced in wild-type plants by exogenous application of hydrogen peroxide. The cat2 mutant also contained peroxisome aggregates. These findings demonstrate that hydrogen peroxide as a result of catalase inactivation is the inducer of peroxisome aggregation. Furthermore, an autophagosome marker, ATG8, frequently colocalized with peroxisome aggregates, indicating that peroxisomes damaged by hydrogen peroxide are selectively degraded by autophagy in the wild type. Our data provide evidence that autophagy is crucial for quality control mechanisms for peroxisomes in Arabidopsis.

Original languageEnglish
Pages (from-to)4967-4983
Number of pages17
JournalPlant Cell
Volume25
Issue number12
DOIs
Publication statusPublished - Dec 2013

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Peroxisomes
autophagy
Autophagy
peroxisomes
Arabidopsis
protein aggregates
Hydrogen Peroxide
hydrogen peroxide
mutants
Catalase
catalase

ASJC Scopus subject areas

  • Plant Science
  • Cell Biology

Cite this

Shibata, M., Oikawa, K., Yoshimoto, K., Kondo, M., Mano, S., Yamada, K., ... Nishimura, M. (2013). Highly oxidized peroxisomes are selectively degraded via autophagy in Arabidopsis. Plant Cell, 25(12), 4967-4983. https://doi.org/10.1105/tpc.113.116947

Highly oxidized peroxisomes are selectively degraded via autophagy in Arabidopsis. / Shibata, Michitaro; Oikawa, Kazusato; Yoshimoto, Kohki; Kondo, Maki; Mano, Shoji; Yamada, Kenji; Hayashi, Makoto; Sakamoto, Wataru; Ohsumi, Yoshinori; Nishimura, Mikio.

In: Plant Cell, Vol. 25, No. 12, 12.2013, p. 4967-4983.

Research output: Contribution to journalArticle

Shibata, M, Oikawa, K, Yoshimoto, K, Kondo, M, Mano, S, Yamada, K, Hayashi, M, Sakamoto, W, Ohsumi, Y & Nishimura, M 2013, 'Highly oxidized peroxisomes are selectively degraded via autophagy in Arabidopsis', Plant Cell, vol. 25, no. 12, pp. 4967-4983. https://doi.org/10.1105/tpc.113.116947
Shibata M, Oikawa K, Yoshimoto K, Kondo M, Mano S, Yamada K et al. Highly oxidized peroxisomes are selectively degraded via autophagy in Arabidopsis. Plant Cell. 2013 Dec;25(12):4967-4983. https://doi.org/10.1105/tpc.113.116947
Shibata, Michitaro ; Oikawa, Kazusato ; Yoshimoto, Kohki ; Kondo, Maki ; Mano, Shoji ; Yamada, Kenji ; Hayashi, Makoto ; Sakamoto, Wataru ; Ohsumi, Yoshinori ; Nishimura, Mikio. / Highly oxidized peroxisomes are selectively degraded via autophagy in Arabidopsis. In: Plant Cell. 2013 ; Vol. 25, No. 12. pp. 4967-4983.
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