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980-8578

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112-86102-1-1

3819-0395744

4

606-8502

Dawn of Chloroplastology: On the Frontiers between Cell and Organelle
Where Plant Science Pioneers to Find New Homes for Biologists
Shinichiro Maruyama1,2, Juntaro Negi3 Yoshiki Nishimura4
1
Department of Ecological Developmental Adaptability Life Sciences, Graduate School ofLife Sciences, Tohoku University,
6- 3 Aramaki-aza-Aoba, Aobaku, Sendai 980-8578, Japan
2
Graduate School of Humanities and Sciences, Ochanomizu University, 2-1-1 Otsuka,
Bunkyo-ku, Tokyo 112-8610, Japan3
Department of Biology, Faculty of Sciences, Kyushu University,
744 Motooka, Nishi-Ku, Fukuoka, 819-0395, Japan
4
Department of Botany, Graduate School of Science, Kyoto University
Oiwake-cho, Kita-Shirakawa, Sakyo-ku, Kyoto 606-8502, Japan
DOI: 10.24480/bsj-review.12a1.00194:

S. Maruyama et al. - 1
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2020

9

84

:

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:
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Meta-Organellar Network (MONet)
Claude Monet
MONet
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606-8502

The division cycle of chloroplast nucleoids
Yoshiki Nishimura, Mari Takusagawa
Laboratory of Plant Molecular Genetics, Department of Botany, Graduate School of Science,
Kyoto University
Oiwake-cho, Kita-Shirakawa, Sakyo-ku, Kyoto 606-8502, Japan
Keywords: chloroplast nucleoids, Holliday junction resolvase
DOI: 10.24480/bsj-review.12a2.00195_TÞ^Qµ ~}&³D´ÉÃÒÓÅÎØÃ³vV´9E@¢RZ

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(Sakai et al., 1991)(Nemoto et al., 1988)(Sulfite
Reductase: SiR) (Sato et al., 2001)
Chloroplast Nucleoid DNA binding protein (CND) 41 (Nakano et al., 1997; Murakami et al.,
2000; Nakano et al., 1993)

Plastid-envelope DNA-binding protein (PEND)(Sato et al., 1998, 1993)

2000(Matsuzaki et al., 2004)
Cyanidioschyzon merolae

Heat unstable(HU)(Kobayashi

et al., 2002)

HU

Chlamydomonas reinhardtii(Karcher et al., 2009)

Klebsormidium flaccidum

Marchantia polymorpha

HU
HU(Kobayashi et al., 2016b)
SiR

in vitro

DNA(Sekine et al., 2002)
SiR

SiR

C

50

C-terminally encoded peptide (CEP
CEP

SiR
SiR

CEP

SiR

CEP
(Kobayashi et al., 2016a)

DNA-RNA-

Plastid Transcriptionally Active Chromosome (pTAC)(Hallick et al., 1976; Melonek et al., 2016; Pfalz andPfannschmidt, 2015)
RNA polymerase (PEP)

2

1

Plastid-encodedRNA

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Nuclear-encoded plastid RNA polymerase (NEP)
RNA
5’/3’

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Pentatricopeptide repeat (PPR)
mRNA

mRNA

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DNA

DNA
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pTAC

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(Hallick et al., 1976; Pfalz et al., 2006)

pTAC

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al., 1982)(Briat et

pTAC

DNA
DNA

2006

Pfalz

18

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pTAC1

Whirly(ss)DNA(AtWHY1)(Desveaux et al., 2002)(Yoo et al., 2007)
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3

AtWhy2(Krause et al., 2005) 2008
WhirlyatpF

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(Maréchal et al., 2009)
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DNA

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DNA

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m
c

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n

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y

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(Kobayashi et al., 2017)

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DNA

(single strand break: SSB)DNA

Holliday junction

DNA

HJR
HJR MOC1
HJR
2019)(Yan et al., 2020; Lin et al.,

MOC1
(Kobayashi et al., 2020)

3
DNA

DNA

(Odahara et al., 2016)
DNA gyrase (Cho et al., 2004; Itoh et al., 1997)

RNaseH(Yang et al., 2020)
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DNA
DNA

18H02460

201910032

sA
Bennett-Lovsey, R., Hart, S.E., Shirai, H., and Mizuguchi, K. 2002. The SWIB and the MDM2
domains are homologous and share a common fold. Bioinformatics 18: 626–630.
Blomme, J. et al. 2017. The Mitochondrial DNA (mtDNA)-Associated Protein SWIB5 Influences
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Briat, J.F., Gigot, C., Laulhere, J.P., and Mache, R. 1982. Visualization of a Spinach Plastid
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69: 1205–1211.
Cho, H.S., Lee, S.S., Kim, K.D., Hwang, I., Lim, J.-S., Park, Y.-I., and Pai, H.-S. 2004. DNA gyrase isinvolved in chloroplast nucleoid partitioning. Plant Cell 16: 2665–82.
Desveaux, D., Allard, J., Brisson, N., and Sygusch, J. 2002. A new family of plant transcription factors
displays a novel ssDNA-binding surface. Nat. Struct. Biol. 9: 512–517.
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Commun. Biol.: 1–7.
Y. Nishimura & M. Takusagawa - 7
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:@K!4Uw ~~}wx}~yw

Karcher, D., Köster, D., Schadach, A., Klevesath, A., and Bock, R. 2009. The chlamydomonas
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2: 1223–1232.
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:@K!4Uw ~~~wx}~yw

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:@K!4Uw ~~wx}~yw

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AtWHY1 modulates telomere length homeostasis in Arabidopsis. Plant J. 49: 442–451.

Y. Nishimura & M. Takusagawa - 10
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444-0874

38

Protective responses of photosynthesis
Ryutaro Tokutsu1
1
National Institute for Basic Biology, 38 Nishigo-Naka, Miyodaiji, Okazaki, Aichi, 444-0874,
Japan
Keywords: Photoprotection, Non-Photochemical-Quenching (NPQ), Green algae
DOI: 10.24480/bsj-review.12a3.00196
4

C 4

2

P2
28
(Photosystem [PS] I

PSII)

R. Tokutsu - 1
             

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(

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” (Takahashi and Murata 2008))(Non-Photochemical Quenching

NPQ)

(

1)

(Horton, Ruban, and Walters 1996; Niyogi 1999)

C 4

.

L
(NPQ)

NPQ

2016

(

2016)

NPQ
(

)

4
NPQ
NPQ

(Demmig-Adams and Adams 1992; El Bissati et al. 2000; Wilson et al.

2006; Peers et al. 2009; Bailleul et al. 2010; Alboresi et al. 2010)
NPQ
1990

(Arabidopsis thaliana)(Niyogi, Grossman, and Bjorkman 1998)

PsbS

NPQ
R. Tokutsu - 2
             (Li et al. 2000)

PsbS
PsbS

NPQ
PsbS
(Alboresi et al. 2008; Bonente et al. 2008)

PsbS

NPQ

(Bonente et al. 2008; Tibiletti et al. 2016;

Alboresi et al. 2010)

NPQ

2009

(Peers et al. 2009) 2010

(Alboresi et al. 2010)
LHCSR

LHCSR

NPQ

PsbS
LHCSR1LHCSR1LHCSR1LHCSR3LHCSR22

LHCSR2LHCSR12

LHCSR

LHCSR1LHCSR

LHCSR1LHCSR3(Alboresi et al. 2008)
LHCSR

NPQ

(Peers et al. 2009; Allorent et al. 2016)
LHCSR1NPQ(Alboresi et al. 2010)

LHCSR(Alboresi et al. 2008; Niyogi and Truong 2013)

LHCSR

PsbS

LHCSR

(

2)

LHCSR

PsbS
OrangeCarotenoid Protein OCP

NPQ(Wilson et al. 2006;

Wilson et al. 2007)
PsbS

LHCSR
PsbS

N

NPQ
NPQ

S

4 .

1
NPQ
(

PsbS
)

LHCSR
NPQ

R. Tokutsu - 3
             

PsbS

“

”

(Li et al. 2000; Alboresi et al. 2010)
”

LHCSR

(Alboresi et al. 2010)

PsbS

“

LHCSR

(Allorent and Petroutsos 2017)
NPQ

NPQ

NPQ
(Peers et al. 2009; Maruyama, Tokutsu, and Minagawa
2014)
NPQ

(

)
LHCSR

LHCSR3

Phototropin((Petroutsos et al. 2016))
LHCSR1

PsbS

UVR8(Allorent et al. 2016; Tokutsu et al. 2019b)
NPQ
(

3)

4 .

H3

NPQ
CONSTANS

Nuclear Transcription Factor Y(Tokutsu et al. 2019a)
E3
(

(

2020)

)

NPQ

LHCSR

R. Tokutsu - 4
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L

R
NPQ
(
(

PsbS

NPQ

2016)

)

NPQ

(Li et al. 2000;

Li et al. 2004) PsbS

NPQ

PsbS

NPQ

PsbS
macro organization(LHCII)NPQ(Li et al.

2004; Kiss, Ruban, and Horton 2008; Kereïche et al. 2010; Goral et al. 2012)
NPQ

in vivo

LHCII

PsbS

LHCII

LHCII

NPQ
in vitro
NPQ
NPQ

NPQ

NPQ

NPQ

LHCSR1PsbS

NPQ(Kondo et al. 2019; Kondo et al. 2017)

1

(

)

in vitro

NPQ

NPQ
LHCSR1NPQ

LHCSR

LHCSR3in vitroin vitro
LHCSR3LHCSR3

NPQ(Bonente et al. 2011; de la Cruz Valbuena et al. 2019)
LHCSR1LHCSR3

NPQ(Troiano et al. 2020)
LHCSR3

NPQ
2013

LHCSR3(Tokutsu and Minagawa 2013)
PSII

LHCSR3

PSII-LHCSR3

NPQ

PSII-LHCSR3LHCSR3
BonenteNPQ(Bonente et al. 2011)

PSII-LHCSR3LHCSR3
PSII-LHCSR3LHCSR3NPQ
R. Tokutsu - 5
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PsbS
LHCSR3LHCSR1

NPQ
NPQ

NPQ

(
) LHCSR1LHCSR3PSII

LHCSR3LHCSR1LHCSR1LHCSR1NPQPSI
LHCSR1PSII

NPQ(Kosuge et al. 2018)

PSI

PSII

NPQ
LHCSR1NPQPSI

LHCSR1NPQ
PSII(LHCII)PSILHCSR1LHCSR1
PSI
PSI

NPQ

PSII

PSI

PSII

(Krieger-Liszkay 2005; Savikhin 2006; Croce and van Amerongen 2013)
LHCSR1

LHCII

3

PSI

PSII

(

4 .

4)

1

LHCSR3LHCSR1PSI

PSII

R. Tokutsu - 6
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4
LHCSR

PsbS

NPQ

NPQ
PsbS

LHCSR
LHCSR3LHCSR

LHCSR (LHCSR1

)
NPQ

II
NPQ

I
(Ballottari et al. 2014; Pinnola et al. 2015;

Tian et al. 2017; Girolomoni et al. 2019)

NPQ

NPQ
NPQ

(

)

NPQ

NPQ

Q
Alboresi, A., S. Caffarri, F. Nogue, R. Bassi, and T. Morosinotto. 2008. In silico and biochemical
analysis of Physcomitrella patens photosynthetic antenna: identification of subunits which evolved
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R. Bassi. 2011. Analysis of LhcSR3, a protein essential for feedback de-excitation in the green alga
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Cosimo D’Andrea, Matteo Ballottari, and Giulio Cerullo. 2019. Molecular Mechanisms ofNonphotochemical Quenching in the LHCSR3 Protein of Chlamydomonas reinhardtii, J. Phys. Chem.
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Girolomoni, L., S. Cazzaniga, A. Pinnola, F. Perozeni, M. Ballottari, and R. Bassi. 2019. LHCSR3 is anonphotochemical quencher of both photosystems in Chlamydomonas reinhardtii, Proc. Natl. Acad.
Sci. U. S. A., 116: 4212-4217
Goral, T. K., M. P. Johnson, C. D. Duffy, A. P. Brain, A. V. Ruban, and C. W. Mullineaux. 2012. Lightharvesting antenna composition controls the macrostructure and dynamics of thylakoid membranes in
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FEBS Lett., 584: 759-764
Kiss, A. Z., A. V. Ruban, and P. Horton. 2008. The PsbS protein controls the organization of thephotosystem II antenna in higher plant thylakoid membranes, J. Biol. Chem., 283: 3972-3978
Kondo, T., A. Pinnola, W. J. Chen, L. Dall'Osto, R. Bassi, and G. S. Schlau-Cohen. 2017. Singlemolecule spectroscopy of LHCSR1 protein dynamics identifies two distinct states responsible formulti-timescale photosynthetic photoprotection, Nat. Chem., 9: 772-778
Kondo, Toru, Jesse B. Gordon, Alberta Pinnola, Luca Dall’Osto, Roberto Bassi, and Gabriela S. SchlauCohen. 2019. Microsecond and millisecond dynamics in the photosynthetic protein LHCSR1 observedby single-molecule correlation spectroscopy, Proc. Natl. Acad. Sci. U. S. A., 116: 11247
Kosuge, K., R. Tokutsu, E. Kim, S. Akimoto, M. Yokono, Y. Ueno, and J. Minagawa. 2018. LHCSR1dependent fluorescence quenching is mediated by excitation energy transfer from LHCII tophotosystem I in Chlamydomonas reinhardtii, Proc. Natl. Acad. Sci. U. S. A., 115: 3722-3727
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             Krieger-Liszkay, A. 2005. Singlet oxygen production in photosynthesis, J. Exp. Bot., 56: 337-346
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Biol. Chem., 279: 22866-22874
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1

75

,

88

26

: 36-42. 2020.
2

,

,

,

30

: 73-83

Tokutsu, R., K. Fujimura-Kamada, T. Matsuo, T. Yamasaki, and J. Minagawa. 2019a. The CONSTANS
flowering complex controls the protective response of photosynthesis in the green alga
R. Tokutsu - 9
            Chlamydomonas, Nat. Commun., 10
Tokutsu, R., K. Fujimura-Kamada, T. Yamasaki, T. Matsuo, and J. Minagawa. 2019b. Isolation ofphotoprotective signal transduction mutants by systematic bioluminescence screening inChlamydomonas reinhardtii, Sci. Rep., 9
Tokutsu, R., and J. Minagawa. 2013. Energy-dissipative supercomplex of photosystem II associatedwith LHCSR3 in Chlamydomonas reinhardtii, Proc. Natl. Acad. Sci. U. S. A., 110: 10016-10021
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reinhardtii, bioRxiv: 2020.2007.2010.197483
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R. Tokutsu - 10          

1

,

2

1
2

599-8531

1-1

Evolution and diversity of chloroplasts from the viewpoint of lipid
metabolism
Koichi Kobayashi1, Akiko Yoshihara2
1
Faculty of Liberal Arts and Sciences, Osaka Prefecture University,
1-1 Gakuen-cho, Naka-ku, Sakai, Osaka 599-8531, Japan2
Department of Biological Sciences, School of Science, Osaka Prefecture University,
1-1 Gakuen-cho, Naka-ku, Sakai, Osaka 599-8531, Japan
Keywords: Chloroplast, Cyanobacteria, Endosymbiosis, Glycolipid
DOI: 10.24480/bsj-review.12a4.00197

K. Kobayashi & A. Yoshihara - 1
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02 (Yoshida & Uemura, 1986)tiq}i\ Synechocystis sp. PCC 6803 (Wada &Murata, 1989) \19*g#TJPA; vh{uBCL; num PC; vh{usPE; vh{ulziPI; vh{ujt~PG; vh{urx
SQDG; vptuitrxDGDG; uoq~tuitrx
MGDG; oq~tuitrxJ
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2

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(Awai et al., 2014, 2006)

MgdE
UDP-

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3

MgdA

MGD1
MgdA

3

(Shimojima et al., 1997)

MgdE

MGD1
(Sato, 2020)
MGD1

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DGDG

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DGDG
dgdA

DGDG
DGD1

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2007)

DGD1
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DGD1

(Sato, 2020)

4
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2015

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K. Kobayashi & A. Yoshihara - 4
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MGDG
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(Shipley et al., 1973) MGDG
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1982)

MGDG
MGDG
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MGDG(Kobayashi et al., 2013, 2007)
MGDG

DGDG

MGDG

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MGDG

MGDG
Synechocystis sp. PCC 6803

GlcDG

MgdE

(Awai et al., 2014)
MGDG

mgdE

GlcDG

MGDG

DGDG

GlcDG
GlcDG
GlcDG

1

MGDG
DGDG

Synechocystis sp. PCC 6803
(Dörmann et al., 1995;

Hölzl et al., 2009; Mizusawa et al., 2009; Sakurai et al., 2007)
Synechococcus elongatus PCC 7942

DGDG

(Maida& Awai, 2016)

DGDG(Dörmann et al., 1995; Hölzl et al., 2009)

SQDG(Yu & Benning, 2003)

Chlamydomonas reinhardtii

SQDG(Sato et al., 1995)
SQDG
S. elongatus PCC 7942

DGDG

Synechocystis sp. PCC 6803 (Aoki et al., 2004)
Thermosynechococcus elongatus BP-1

al., 1996)

Gloeobacter violaceus PCC

7421
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SQDG
SQDG

(Selstam & Campbell, 1996) SQDG
PG
(Kobayashi, 2016)

PG

PG
PG

PG
PG

PG

PG
PG

PG
PG

2015

K. Kobayashi & A. Yoshihara - 6
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PG

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SQDG
S. elongatus PCC 7942

SQDG

T. elongatus BP-1

SQDG

SQDG

PG

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PG

SQDG

SQDG

PG
(Yu

& Benning, 2003) PG

SQDG

T. elongatus BP-1
II

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PG

SQDG
(Nakajima et al., 2018)

SQDG

PG
(Sugimoto et al., 2008)
PG
SQDG
SQDG
SQDG

PG
(Endo et al., 2016; Güler et al., 1996; Riekhof etal., 2003; Yu et al., 2002)

SQDG

PG

PG
PG
SQDG
SQDG
PG
(Kobayashi et al., 2015)

SQDG

PG

K. Kobayashi & A. Yoshihara - 7
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SQDG
PG

DGDG

DGDG

(Härtel et al., 2000)

DGDG

20%

al., 2004)(Jouhet et

4
50%

70%

DGDG

(Andersson et al., 2003)(Russo et al., 2007)
DGDG
DGDG

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MGDG
MGD1

AtMGD2

AtMGD3

AtMGD1(Kobayashi et al., 2004)
DGDG(Kobayashi et al., 2009) AtMGD2

AtMGD3

MGDG

MGDG
DGDG

AtMGD2

AtMGD3(Kobayashi et al., 2009)
DGDG

DGDG

AtMGD2

AtMGD3(Kobayashi et al., 2004)
in vitro

MGDG(Nakamura et al., 2009)

DGDG

DGDG
DGDG

(Botté et al., 2011)

AtMGD2MGDG
AtMGD1

AtMGD2

AtMGD3
AtMGD1

AtMGD3

MGDG

K. Kobayashi & A. Yoshihara - 8
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OsMGD2(Basnet et al., 2019b)
OsMGD2DGDG

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MGDG

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(Gasulla et al., 2019; Kelly& Dörmann, 2004)2010
sfr2 sensitive to freezing 2)

galactolipid:galactolipid galactosyltransferase, GGGT(Moellering et al., 2010)
MGDG

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2

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DGDG

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TGDG

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MGDG

MGDG
GGGT
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SFR2
1

K. Kobayashi & A. Yoshihara - 9
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MGDG
SFR2
(Wang et al., 2016)

SFR2
SFR2

Klebsormidium nitens

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SFR2
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α

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GGGT

G
SQDG

SQD1

UDP-

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DAG

3
SQD1

SQD2

SQDG
sqd1

sqd2

(Okazaki et al., 2013)(GlcADG)
Okazaki et al. 2013
GlcADG

SQDG

sqd1

GlcADG
sqd2

SQDG

sqd2
GlcADG

sqd1

SQDG

GlcADG
6

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GlcADG(Okazaki et al., 2015)
SQD2
GlcADG

SQD2

GlcADG

GlcADG

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Sato
2020

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Agrobacterium
tumefaciens /Rhizobium radiobacter

GlcDG

DGDG GlcADG(Semeniuk et al., 2014)
MGD1

SQD2

MGDG

DGDG

SQDG

GlcADG
MGDG

SFR2
SFR2

β

Alban, C., Joyard, J., & Douce, R. 1988. Preparation and characterization of envelope membranes from
nongreen plastids. Plant Physiol. 88: 709–717.
Andersson, M.X., Stridh, M.H., Larsson, K.E., Liljenberg, C., & Sandelius, A.S. 2003. PhosphateK. Kobayashi & A. Yoshihara - 11         

deficient oat replaces a major portion of the plasma membrane phospholipids with the galactolipid
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819-0395

744

A new perspective on the feature and function of guard cell chloroplasts
Juntaro Negi, Tomoki Obata, Boseok SongDepartment of Biology, Faculty of Sciences, Kyushu University,
744 Motooka, Nishi-Ku, Fukuoka, 819-0395, Japan
Keywords: Arabidopsis, Guard cell chloroplasts, Lipid metabolism, Stomatal movement
DOI: 10.24480/bsj-review.12a5.00198

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819-0395

744

Role of chloroplast movement in adaption to ambient light environment
Eiji Gotoh
Faculty of Agriculture, Kyushu University
744 Motooka, Nishi-ku, Fukuoka, 819-0395, Japan
Keywords: chloroplast movements, light adaptation, photoprotection, phototropin, plantbiomass production
DOI: 10.24480/bsj-review.12a6.00199

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E. Gotoh - 7
          CLF

669-1337

2-1

Chloroplast proteolysis - between organellar homeostasis and cellular signaling
Kenji Nishimura
Department of Bioscience, School of Science and Technology, Kwansei Gakuin University,
2-1 Gakuen, Sanda, Hyogo 669-1337, Japan
Keywords: chloroplast, homeostasis, peptide, protease, signaling
DOI: 10.24480/bsj-review.12a7.00200

3000

20
AAA+ (ATPases associated with diverse cellular activities)

Clp FtsH Lon
ATP

AAA+
(Gottesman, 1996; Gottesman and Maurizi, 1992) (

1A)

ATP

(

)

K. Nishimura - 1
         (Thompson et al., 1994)
ATPATP

Clp FtsH Lon
3

Clp

FtsH Lon

Clp

ATP
FtsH

Lon

(

B)

Clp
(Nishimura and van Wijk, 2015)

Clp

ClpC1/ClpC2/ClpD
6(Nishimura and van Wijk, 2015)

3

ClpC1
Clp
ClpS1
ClpF

2

ClpS1/FClp

K. Nishimura - 2
         (Nishimura et al., 2013, 2015)

ClpS

N
N-end rule

(Varshavsky, 2011) N-

end ruleNN-degron

ClpSN-

end rule(Bouchnak and van Wijk, 2019)

N-degron

ClpS

ClpS1

(Colombo et al., 2018;

Montandon et al., 2019) ClpS/F
N-end rule
(Nishimura et al., 2015)
Clp

ClpP3/ClpP4/ClpP5/ClpP6
P

4

1:2:3:1

ClpP1/ClpR1/ClpR2/ClpR3/ClpR4

R

14

3:1:1:1:1(Olinares et al., 2011)

ClpP1(Shikanai et al., 2001)(Nishimura and van Wijk, 2015)

Clp

ClpP/R

ClpP

3
ClpR
Clp

10

2

P/R

2

ClpT1/T2(Clarke, 2012; Kim et al., 2015; Sjögren and Clarke, 2011)
P

ClpT1

ClpT2
Clp

R
P

R

ClpT
(Colombo et al., 2014)
FtsH

ATP

(Zn)

N
FtsH
12

FtsH1/2/5/6/7/8/9/11/12

9

3(Sakamoto et al., 2003)

FtsH

FtsH1/2/5/8
FtsH6

FtsH
(FtsH1/5)

4
B (FtsH2/8)

2:4

6

FtsH7/9/11/12(Nishimura et al., 2017)

FtsH

A

(Yu et al., 2004, 2005; Zaltsman et al., 2005)(Moldavski et al., 2012) (

B)

FtsH

N
6

K. Nishimura - 3
         (Nishimura et al., 2017) FtsH5

FtsH2

yellow variegated1/2 (var1/var2)
Sakamoto, 2018)

FtsH1(Kato and

FtsH8
var1

var2

(Putarjunan et al., 2013)

Clp

ClpP1
Clp-FtsH

FtsH

GTPase2018) EngA

1

EngA

(Kato et al.,

FtsH5/2

EngA
FtsH

FtsH

FtsH

EngA

FtsH

FtsH5/2
FtsH(Kato and Sakamoto, 2019)

FtsH11

FtsH(Adam et al., 2019)

CPN20
FtsH7

FtsH9
(Wagner et al., 2012)

FtsH12

FtsH

FtsHi1/2/4/5

Ycf2

NAD

2-MD
TIC

1-MD

ATP
(Kikuchi et al., 2018) FtsH12

Zn
FtsHi

FtsHi3

Ycf2/FtsHi

TIC

1-MD

Lon

ATP

(Pinti et al., 2016)
6

Lon

(

B)

2
LonA

N

LonB

(Rotanova et al., 2004)
2

Lon (Lon1/4)(Rigas et al., 2014)

Lon

LonA
Lon

N

N

4

3

K. Nishimura - 4
         (van Wijk, 2015) Lon1/4
αLon

Lon1/4
Lon1

Lon4(Daras et al., 2014)

C
(

2)

N
(TP)

TOC

TIC-Ycf2/FtsHi
al., 2020)(Thomson et

Zn
TP

SPP
(

)
TP

(Teixeira and Glaser, 2013) TP
SPP

C(Richter and Lamppa, 1999, 2002) SPP(Trösch and Jarvis, 2011; Zhong et al.,2003) SPP
II (PSII)(LHCII)

10(Yue et al., 2010)
TP

(TTS)

(

)

TAT

SEC

K. Nishimura - 5
         (Jarvis and Lopez-Juez, 2013)

TTS

Plsp1

(Midorikawa et al., 2014; Shipman and Inoue, 2009) Plsp1
2(Midorikawa et al., 2014) Plsp1

SEC

PsbO
(Frielingsdorf and Klösgen, 2007; Midorikawa and Inoue, 2013;
Shackleton and Robinson, 1991)

TAT

PsbP

TTS

TAT

Plsp1
(Frielingsdorf andKlösgen, 2007; Midorikawa and Inoue, 2013; Shipman-Roston et al., 2010)b (Chlb)
a

(CAO)

Chlb

Clp

(Nakagawara et al., 2007; Yamasato et al., 2005) CAO
Chlb
Chlb

N
CAO

CAO

ClpC
(Sakuraba et al., 2007, 2009)tRNA
ClpS1/F(GluTR)(Richter et al., 2019)

GluTR

N

(GBP)
2011)

GluTR
(Czarnecki et al.,

GBP

GBP-GluTR(Richter et al., 2019)

N

GBP

ClpS1
GBP

GluTR

Clp

PAA2
Clp
PAA2

(Tapken et al., 2015)

ClpS1

ClpC
PAA2

N
CAO

Clp

Clp
Tic110(Flores-Pérez et al., 2016; Sjögren et al., 2014)
TIC(Flores-Pérez et al., 2016)(PHY)

Tic110

DnaJ

ORANGE (OR)K. Nishimura - 6
         (Welsch et al., 2018;
Yuan et al., 2020)

PHY

ClpS1/F

ClpC/D(Welsch et al., 2018)

4-

(MEP)

5J20

(DXS)

Hsp70

ClpB3

Clp

(Pulido et al., 2016)
DXS

Hsp40/DnaJ

J20

Hsp70

DXS

ClpB3

Hsp70

Hsp70
DXS
Hsp70
Hsp70

ClpC1

ClpB3

ClpC1

ClpC1

Clp
(Pulido et al., 2017)
PSII

D1

(Kato and Sakamoto, 2018)

PSII
D1

D1
DEG

FtsH
D1

PSII

PSII
PSII

D1/D2

CP43

(Kato and Sakamoto, 2014; Puthiyaveetil and Kirchhoff, 2013; Samol et al., 2012) STN8

DEG

PsbH

STN8
D1

PBCP

PBCP

D1

SPP

TP

Clp/FtsH

Zn
PreP1/2
26

146 aa

12 aa

10

OOP

(Kmiec et al., 2014) TP(Zybailov et al., 2008)

20 aa

PreP1/2

Clp

FtsH

5

(Choi and Licht, 2005; Ito and Akiyama, 2005)

OOP

10

65 aa

8

23 aa

(Kmiec et al., 2014; Moberg et al., 2003; Ståhl et al., 2005)
PreP/OOP

3 4 aaPreP/OOP2

M1

M17-20TP(Teixeira et al., 2017)

CFH

K. Nishimura - 7
         ()
GENOME UNCOUPLED1 (GUN1)

Clp(Wu et al., 2018) GUN1
(PPR)

GUN1

Clp

(LIN)
GUN1

ClpP1
Clp

GUN1

GUN1

PPR

GUN1
(Shimizu et al., 2019)

(ROS)

(O)
1

2

FtsH

1

O

EXECUTER1 (EX1)2(Dogra et al., 2017; Wang et al., 2016)
EX1

1

FtsH

O

2

EX1
(Dogra et al.,2017, 2019a)(unfolded protein response)(UPRmt)
RNAi

(UPR)

(Haynes et al., 2013; Walter and Ron, 2011)
LIN

Clp

ClpB3
UPR

(cpUPR) (Llamas et al., 2017; Ramundo et al., 2014)
GUN1

cpUPR

HsfA2

(Llamas et al., 2017)

FtsH

PSII
ROS
(Dogra et al., 2019b)
UPR

UPR(damaged protein response, DPR)
FtsH
FtsH

PSII
(SA)

(Duan et al., 2019)

SA

K. Nishimura - 8
          

SA

FtsH

(Dogra and Kim, 2019)
PreP/OOP

3

TP(Kmiec et al., 2018)

RubiscoRubisco

LHCII D1

CP47

3

(Fesenko et al., 2015; Mamaeva
et al., 2020)

TAP (transporter associated with antigen processing)(Parcej and Tampé, 2010)
MHC (major histocompatibility complex)
UPRmt

I
Clp

HAF-1
(Haynes and Ron, 2010)
HAF-1

TAP
2

1

(Huang et al., 2013)

TAP

K. Nishimura - 9
           

JSPS

(

19K23734)

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K. Nishimura - 16         

1

1

1

351-0198

2-1

Study on chloroplast autophagy for the development of cell biology
Sakuya Nakamura & Masanori Izumi
Center for Sustainable Resource Science (CSRS), RIKEN
2-1 Hirosawa, Wako, Saitama 351-0198, Japan
Keywords: autophagy; chlorophagy; chloroplasts, organelle dynamics, ubiquitination
DOI: 10.24480/bsj-review.12a8.00201
1

1

1

2020

9

84

S. Nakamura & M. Izumi - 1
         (

1; Dikic, 2017)
2004
2016

(
)

(
(

)

1B; Nakatogawa, 2020)
8.6 kDa
E1

E2

E3
(
1A)

1.

48

(A)
E1
E3

26S

E2
48

(Chau etal., 1989)

26S
(B)
(ATG

)
/
/

(

(Dikic,
2017)

)

(C)

PINK1/Parkin
PINK1
E3 Parkin

S. Nakamura & M. Izumi - 2
          (Shaid et al., 2013)
PTEN-induced kinase 1 (PINK1)/Parkin(

1C; Pickles et al., 2018)
PINK1
PINK1
E3

ParkinPINK1(Koyano et al., 2014; Lazarou et al., 2015)

ATP(Izumi et al., 2017)(

2A; Nakamura et al., 2018)

(O)
1

E3

2

PLANT U-BOX4 (PUB4)(

2B; Woodson et al., 2015)

PUB4

2.
(A)

PUB4

1

(B) PUB4

FERROCHELATASE 2

O2

E3 PUB4(fc2)

S. Nakamura & M. Izumi - 3
           

PUB4

PUB4
pub4-6(Kikuchi etal., 2020)
pub4-6(3A)

pub4-6(Kikuchi et al., 2020)

E3

of PPI1 locus 1 (SP1)(Ling et al., 2012) sp1

Suppressor

sp1 pub4-6
PUB4(Kikuchi et al., 2020)
PUB4
2ParkinE3

SP1

Translocon

on the outer chloroplast membrane (TOC)

26S(Ling et al., 2012; Ling et al., 2019)

PUB4

PUB4
pub4-6

AUTOPHAGY5 (ATG5)(Kikuchi et al., 2020)

3.

PUB4

(A)

GFP (CT-GFP)
pub4-6((B)
atg5 pub4-6 atg5

pub4-6)pub4-6
PUB4(pub4-6 atg5)


S. Nakamura & M. Izumi - 4
          

(
(

)
)

(

3B)
(

)

PUB4
PUB4
E3

(Oku and Sakai, 2018)
(ATG

)

ATG

Endosomal Sorting Complex Required for Transport (ESCRT)(

4.
(A) ESCRT

4A B)

ESCRT

(B) ATG

ATG

(C)

ATG8
ATG8

S. Nakamura & M. Izumi - 5

         (Schuck, 2020)(Nakamura et al., 2018)
ATG8

Phosphatidylethanolamine (PE)ATG5 ATG7

ATG(GFP) -ATG8
Nakamura et al., 2018
(

4C)

ATG
(Oku and Sakai, 2018)

Rubiscocontaining body
(Ishida et al., 2008; Izumi et al., 2015; Hirota et al., 2018)
H -ATPase

Concanamycin A

+

CO

2

Rubisco
(

1 µm
5A)

S. Nakamura & M. Izumi - 6
         5.
(A) GFP
Rubisco (Rubisco-GFP)
Rubisco-GFP
concanamycin A(B, C) Drp1
Drp1

H+-ATPase
Rubisco-GFP(Yamashita et al., 2016)(
2011)

5B; Twig and Shirihai,

DRP1 (Dynamin-related protein 1)
Hela(Yamashita et al., 2016)
( 5C)

2

PINK1/Parkin(Hypoxia)
FUN14 domain–containing protein 1 (FUDC1)
B-cell lymphoma 2 (BCL2)

BCL2 / adenovirus E1B 19

kDa-interacting protein 3 (BNIP3), BNIP3L / Nix(Bellot et al., 2009; Liu et al., 2012)
PINK1 / Parkin

S. Nakamura & M. Izumi - 7
         

Rubisco-containing body

JSPS
, JP20H04916

JP17H05050, JP20K21322

JP19H04712

JP19J01681, JP20K15501, JP20H05352
GFP
Cornell

atg5

Maureen R. Hanson

pub4-6
Arizona

Jesse D. Woodson

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S. Nakamura & M. Izumi - 10     