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The Plant Cell, Vol. 29: 199, February 2017, www.plantcell.org ã 2017 American Society of Plant Biologists. All rights reserved.
IN BRIEF
Photodamaged Chloroplasts Are Targets of Cellular
Garbage Disposal
OPEN
Autophagy, or “self eating,” is the process
cells use to consume unwanted intracellular
structures such as damaged organelles,
excess membranes, and unneeded proteins
(Mizushima and Komatsu, 2011). Typically, the
unwanted structure becomes surrounded by
an autophagosomal membrane, which then
fuses with the membrane of either the vacuole
(yeast and plants) or the lysosome (animals) to
deliver its contents for destruction by hydrolytic enzymes (Nakatogawa et al., 2009).
Mitochondria can be damaged by excess
oxidation and thus may need to be destroyed. Mitophagy, the process by which
cells consume defective mitochondria, is
well characterized in both animals and yeast
(Green et al., 2011; Youle and Narendra, 2011).
Defects in mitophagy in humans can cause
Parkinson’s-like symptoms, perhaps because
impaired mitophagy results in accumulation of
reactive oxygen species (ROS) and mutation
of mitochondrial DNA.
During photosynthesis, excess natural or
artificiallightcancausephotooxidativedamage
to chloroplasts. Izumi et al. (2017) now show
thatchlorophagy, the intracellular destructionof
chloroplasts, is induced by exposure to UV-B
irradiation (280–315 nm) and high light. They
also demonstrate that entire photodamaged
chloroplasts are transported to the plant cell
vacuole for destruction. Duringleaf senescence
and energy starvation, chloroplast stroma proteins are degraded by a type of autophagosome known as the Rubisco-containing body
(Ishida et al., 2008). Whether a similar process
operates in autophagy of photodamaged chloroplasts is a key focus of this work.
The authors first examine the relationship
between UV-B-induced damage and autophagy in wild-type versus atg mutants, which
are deficient in core proteins required for autophagy. Mutant plants irradiated with a UV-B
treatment as short as 1 h had <40% the shoot
fresh weight than similarly treated wild-type
plants, and they showed a similar reduction in
photosyntheticperformance.Thisdemonstrates
that Arabidopsis plants are more damaged by
UV-B when the autophagy process is defective.
OPEN
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Chlorophagy is inhibited in autophagy mutants.
UV-B irradiation of leaves has only a moderate effect
on chloroplast ultrastructure in wild-type plants (left
panels). In autophagy-deficient atg mutants, UV-B
exposure leads to accumulation of grossly abnormal
chloroplasts (right panels) that would otherwise be
destroyed by chlorophagy. Bar 5 2 mm. (Reprinted
from Izumi et al. [2017], Figure 5C.)
Chloroplast location was monitored via
expression of a chloroplast stroma-targeted
GFP fusion protein (CT-GFP). Chloroplasts in
untreated control leaves contained CT-GFP,
but UV-B exposure caused the appearance of
CT-GFP-deficient chloroplasts in the central
area of mesophyll cells where the vacuole is
typically found. Simultaneous expression of
a vacuolar membrane marker protein and
a stromal RFP fusion protein showed that
RFP-deficient chloroplasts were indeed found
inside the vacuole. This was not the case in atg
mutant plants, showing that their movement to
the vacuole depends on the presence of
a functional autophagy pathway.
In wild-type leaves, the number of chloroplasts in UV-B-exposed leaves decreased
;30% by 3 d following exposure. By contrast,
no decrease was seen in UV-B-exposed atg
mutant leaves, which instead accumulated
abnormal chloroplasts. In untreated control
plants, chloroplast morphology in atg mutant
leaves was similar to wild-type morphology
(see figure). However, following UV-B exposure, the chloroplasts of atg mutant leaves
hadgrosslyalteredultrastructure andenhanced
ROS production. This strongly suggests
that, in normally functioning cells, chloro-
phagy removes photodamaged chloroplasts
following excessive UV-B exposure.
The authors showed the involvement of
ROS such as H2O2 in the initiation of autophagy following UV-B-induced photodamage to chloroplasts. Using concanamycin A,
which inhibits the vacuolar H1-ATPase and
thus suppresses hydrolytic enzymes, plus
an autophagosomal membrane marker, the
authors were able to stabilize and visualize
tubular autophagosomal structures surrounding individual chloroplasts in the vacuoles of
UV-B-exposed leaves. Further experiments
described in the article showed that strong
visible light as well as UV-B will induce chlorophagy and that photodamage-induced
chlorophagy involves a pathway distinct from
starvation-induced chlorophagy. These findings not only help to elucidate the process of
chloroplast turnover in the plant cell but also
provide insights into the process of autophagy
and organelle turnover in cells.
Gregory Bertoni
Science Editor
[email protected]
ORCID ID: 0000-0001-7977-3724
REFERENCES
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Izumi, M., Ishida, H., Nakamura, S., and Hidema,
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Mizushima, N., and Komatsu, M. (2011). Autophagy: renovation of cells and tissues. Cell
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Photodamaged Chloroplasts Are Targets of Cellular Garbage Disposal
Gregory Bertoni
Plant Cell 2017;29;199; originally published online February 10, 2017;
DOI 10.1105/tpc.17.00054
This information is current as of August 9, 2017
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References
This article cites 6 articles, 3 of which can be accessed free at:
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