Selective elimination of membrane-damaged chloroplasts via microautophagy

Sakuya Nakamura, Jun Hidema, Wataru Sakamoto, Hiroyuki Ishida, Masanori Izumi

Research output: Contribution to journalArticle

10 Citations (Scopus)

Abstract

Plant chloroplasts constantly accumulate damage caused by visible wavelengths of light during photosynthesis. Our previous study revealed that entire photodamaged chloroplasts are subjected to vacuolar digestion through an autophagy process termed chlorophagy; however, how this process is induced and executed remained poorly understood. In this study, we monitored intracellular induction of chlorophagy in Arabidopsis (Arabidopsis thaliana) leaves and found that mesophyll cells damaged by high visible light displayed abnormal chloroplasts with a swollen shape and 2.5 times the volume of normal chloroplasts. In wild-type plants, the activation of chlorophagy decreased the number of swollen chloroplasts. In the autophagy-deficient autophagy mutants, the swollen chloroplasts persisted, and dysfunctional chloroplasts that had lost chlorophyll fluorescence accumulated in the cytoplasm. Chloroplast swelling and subsequent induction of chlorophagy were suppressed by the application of exogenous mannitol to increase the osmotic pressure outside chloroplasts or by overexpression of VESICLE INDUCING PROTEIN IN PLASTID1, which maintains chloroplast envelope integrity. Microscopic observations of autophagy-related membranes showed that swollen chloroplasts were partly surrounded by autophagosomal structures and were engulfed directly by the tonoplast, as in microautophagy. Our results indicate that an elevation in osmotic potential inside the chloroplast due to high visible light-derived envelope damage results in chloroplast swelling and serves as an induction factor for chlorophagy, and this process mobilizes entire chloroplasts via tonoplast-mediated sequestering to avoid the cytosolic accumulation of dysfunctional chloroplasts.

Original languageEnglish
Pages (from-to)1007-1026
Number of pages20
JournalPlant Physiology
Volume177
Issue number3
DOIs
Publication statusPublished - Jun 1 2018

Fingerprint

Chloroplasts
chloroplasts
Membranes
autophagy
Autophagy
tonoplast
osmotic pressure
Arabidopsis
Light
Mesophyll Cells
Osmotic Pressure
Photosynthesis
Mannitol
Chlorophyll
mannitol
mesophyll
wavelengths
Digestion
Cytoplasm

ASJC Scopus subject areas

  • Physiology
  • Genetics
  • Plant Science

Cite this

Selective elimination of membrane-damaged chloroplasts via microautophagy. / Nakamura, Sakuya; Hidema, Jun; Sakamoto, Wataru; Ishida, Hiroyuki; Izumi, Masanori.

In: Plant Physiology, Vol. 177, No. 3, 01.06.2018, p. 1007-1026.

Research output: Contribution to journalArticle

Nakamura, Sakuya ; Hidema, Jun ; Sakamoto, Wataru ; Ishida, Hiroyuki ; Izumi, Masanori. / Selective elimination of membrane-damaged chloroplasts via microautophagy. In: Plant Physiology. 2018 ; Vol. 177, No. 3. pp. 1007-1026.
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