Table 1.
Summary of proteins that influence the assembly, stability, and repair of PSII in Arabidopsis.
| Name | Gene locus in Synechocystis sp. PCC 6803a | Gene locus in Arabidopsisb | Full-length Size (kDa) | Mature size (kDa) | Location | Protein classification | Function | Referencesc |
|---|---|---|---|---|---|---|---|---|
| cpSRP43 | − | At2g47450 | 41 | 35 | CS | Thylakoid protein targeting: cpSRP translocase | Insertion and assembly of PSII proteins such as D1, D2, and CP47, and LHCII subunits | Henry et al., 2007; Schunemann, 2007; Cline and Dabney-Smith, 2008; Albiniak et al., 2012 |
| cpSRP54 | slr1531 | At5g03940 | 61 | 53 | CS | Thylakoid protein targeting: cpSRP translocase | Insertion and assembly of PSII proteins such as D1, D2, and CP47, and LHCII subunits | Henry et al., 2007; Schunemann, 2007; Cline and Dabney-Smith, 2008; Albiniak et al., 2012; Walter et al., 2015 |
| cpFtsY | slr2102 | At2g45770 | 40 | 36 | CS, TM | Thylakoid protein targeting: cpSRP translocase | Insertion and assembly of PSII proteins such as D1, D2, and CP47, and LHCII subunits | Henry et al., 2007; Schunemann, 2007; Cline and Dabney-Smith, 2008; Albiniak et al., 2012; Walter et al., 2015 |
| ALB3 | slr1471 | At2g28800 | 50 | 45 | TM | Thylakoid protein targeting: cpSRP translocase | Insertion and assembly of PSII proteins such as D1, D2, and CP47, and LHCII subunits | Pasch et al., 2005; Henry et al., 2007; Ma et al., 2007; Schunemann, 2007; Cline and Dabney-Smith, 2008; Walter et al., 2015 |
| cpSecA1 | sll0616 | At4g01800 | 117 | 111 | CS, TM | Thylakoid protein targeting: cpSec translocase | Insertion and assembly of PSII proteins such as PsbO | Cline and Theg, 2007; Schunemann, 2007; Cline and Dabney-Smith, 2008; Albiniak et al., 2012 |
| cpSecA2 | At1g21650 | 203 | 203 | CS, TM | Thylakoid protein targeting: cpSec translocase | Insertion and assembly of PSII proteins such as PsbO | Cline and Theg, 2007; Schunemann, 2007; Cline and Dabney-Smith, 2008; Albiniak et al., 2012 | |
| cpSecE1 | ssl3335 | At4g14870 | 19 | 15 | TM | Thylakoid protein targeting: cpSec translocase | Insertion and assembly of PSII proteins such as PsbO | Cline and Theg, 2007; Schunemann, 2007; Cline and Dabney-Smith, 2008; Albiniak et al., 2012 |
| cpSecE2 | At4g38490 | 17 | 12 | TM | Thylakoid protein targeting: cpSec translocase | Insertion and assembly of PSII proteins such as PsbO | Cline and Theg, 2007; Schunemann, 2007; Cline and Dabney-Smith, 2008; Albiniak et al., 2012 | |
| cpSecY1 | sll1814 | At2g18710 | 59 | 51 | TM | Thylakoid protein targeting: cpSec translocase | Insertion and assembly of PSII proteins such as D1 and PsbO | Cline and Theg, 2007; Henry et al., 2007; Schunemann, 2007; Cline and Dabney-Smith, 2008; Albiniak et al., 2012; Walter et al., 2015 |
| cpSecY2 | At2g31530 | 65 | 61 | TM | Thylakoid protein targeting: cpSec translocase | Insertion and assembly of PSII proteins such as D1 and PsbO | Cline and Theg, 2007; Henry et al., 2007; Schunemann, 2007; Cline and Dabney-Smith, 2008; Albiniak et al., 2012; Walter et al., 2015 | |
| Tha4 | slr1046 | At5g28750 | 16 | 14 | TM | Thylakoid protein targeting: cpTat translocase | Insertion and assembly of PSII proteins such as PsbP and PsbQ | Cline and Theg, 2007; Schunemann, 2007; Cline and Dabney-Smith, 2008; Albiniak et al., 2012 |
| HCF106 | slr1046 | At5g52440 | 28 | 19 | TM | Thylakoid protein targeting: cpTat translocase | Insertion and assembly of PSII proteins such as PsbP and PsbQ | Cline and Theg, 2007; Schunemann, 2007; Cline and Dabney-Smith, 2008; Albiniak et al., 2012 |
| cpTatC | sll0194 | At2g01110 | 37 | 34 | TM | Thylakoid protein targeting: cpTat translocase | Insertion and assembly of PSII proteins such as PsbP and PsbQ | Cline and Theg, 2007; Schunemann, 2007; Cline and Dabney-Smith, 2008; Albiniak et al., 2012 |
| CPRabA5e | − | At1g05810 | 29 | 24 | CS, TM | Chloroplast vesicle transport | Transport of PSII proteins such as LHCB1, LHCB3, and CP47, to and from thylakoids | Karim et al., 2014; Karim and Aronsson, 2014 |
| CYO1/SCO2 | − | At3g19220 | 21 | 17 | TM | Chloroplast vesicle transport; thiol/disulfide-modulating protein | Chloroplast and thylakoid biogenesis; folding and transport of cysteine-containing proteins such as CP43, CP47, and LHCB1; stability of PSI-LHCI and PSII-LHCII supercomplexes | Shimada et al., 2007; Albrecht et al., 2008; Muranaka et al., 2012; Tanz et al., 2012 |
| THF1/PSB29 | sll1414 | At2g20890 | 34 | 27 | CE, CS, TM | Chloroplast vesicle transport | Thylakoid biogenesis; dynamics of PSII-LHCII supercomplexes | Wang et al., 2004; Keren et al., 2005; Huang et al., 2006, 2013; Shi et al., 2012; Yamatani et al., 2013 |
| TerC | − | At5g12130 | 42 | 34 | TM | Chloroplast vesicle transport | Thylakoid biogenesis; co-translational insertion of PSII proteins such as D1, D2, and CP43 | Kwon and Cho, 2008; Schneider et al., 2014 |
| VIPP1 | sll0617 | At1g65260 | 36 | 32 | ICE, TM | Chloroplast vesicle transport | Thylakoid biogenesis; transport and/or co-translational insertion of photosynthetic proteins such as D1 | Kroll et al., 2001; Zhang et al., 2012; Zhang and Sakamoto, 2012; Walter et al., 2015 |
| PPL1 | sll1418 | At3g55330 | 26 | 18 | TL | PSII subunit-like: PsbP-like | PSII repair | Ishihara et al., 2007 |
| ELIP1 | − | At3g22840 | 20 | 16 | TM | PSII subunit-like: LHCP-like | Binding of chlorophyll and/or stability of pigment-binding proteins and complexes during photoinhibition? | Hutin et al., 2003; Casazza et al., 2005; Heddad et al., 2006; Rossini et al., 2006 |
| ELIP2 | − | At4g14690 | 20 | 16 | TM | PSII subunit-like: LHCP-like | Binding of chlorophyll and/or stability of pigment-binding proteins and complexes during photoinhibition? | Hutin et al., 2003; Casazza et al., 2005; Heddad et al., 2006; Rossini et al., 2006 |
| SEP3.1/LIL3:1 | − | At4g17600 | 29 | 25 | TM | PSII subunit-like: LHCP-like | Anchoring geranylgeranyl reductase to thylakoid membranes; stabilizing LHCII | Tanaka et al., 2010; Takahashi et al., 2014; Lohscheider et al., 2015 |
| SEP3.2/LIL3:2 | − | At5g47110 | 29 | 24 | TM | PSII subunit-like: LHCP-like | Anchoring geranylgeranyl reductase to thylakoid membranes; stabilizing LHCII | Tanaka et al., 2010; Takahashi et al., 2014; Lohscheider et al., 2015 |
| HCF173 | sll1218 | At1g16720 | 66 | 57 | CS, TM | atypical SDR | Translational initiation of the psbA mRNA | Schult et al., 2007; Link et al., 2012 |
| HCF244 | slr0399 | At4g35250 | 44 | 38 | TM | atypical SDR | Translational initiation of the psbA mRNA | Link et al., 2012 |
| CtpA1 | slr0008 | At3g57680 | 56 | 47 | TL | C-terminal processing peptidase | C-terminal processing of D1 under high light | Yamamoto et al., 2001; Yin et al., 2008 |
| CtpA2 | At4g17740 | 56 | 46 | TL | C-terminal processing peptidase | C-terminal processing of D1 | Yamamoto et al., 2001; Che et al., 2013 | |
| LPA1/PratA | slr2048 | At1g02910 | 50 | 47 | TM | TPR | Biogenesis and assembly of the D1 protein | Peng et al., 2006 |
| MET1 | − | At1g55480 | 37 | 30 | TM | TPR | Supercomplex formation in PSII repair | Ishikawa et al., 2005a; Bhuiyan et al., 2015 |
| LQY1 | − | At1g75690 | 16 | 12 | TL | Thiol/disulfide-modulating protein | Dissembly, folding, and/or reassembly of cysteine-containing PSII subunits and complexes and/or D1 synthesis and turnover, during PSII repair | Lu, 2011; Lu et al., 2011 |
| PDI6/PDIL1-2 | − | At1g77510 | 56 | 54 | CS | Thiol/disulfide-modulating protein | Regulation of D1 synthesis | Houston et al., 2005; Wittenberg et al., 2014 |
| TRX-M1 | slr0623 | At1g03680 | 20 | 14 | CS | Thiol/disulfide-modulating protein | Assembly of CP47 into PSII | Cain et al., 2009; Wang et al., 2013 |
| TRX-M2 | At4g03520 | 20 | 13 | CS | Thiol/disulfide-modulating protein | Assembly of CP47 into PSII | Cain et al., 2009; Wang et al., 2013 | |
| TRX-M4 | At3g15360 | 21 | 13 | CS | Thiol/disulfide-modulating protein | Assembly of CP47 into PSII | Cain et al., 2009; Wang et al., 2013 | |
| LTO1 | slr0565 | At4g35760 | 40 | 35 | TM | Thiol/disulfide-modulating protein | Disulfide bond formation in PsbO | Feng et al., 2011; Karamoko et al., 2011; Lu et al., 2013 |
| RBD1 | slr2033 | At1g54500 | 22 | 16 | TM | Thiol/disulfide-modulating protein | PSII assembly and stability | Calderon et al., 2013 |
| CYP20-3/ROC4 | slr1251 | At3g62030 | 34 | 23 | CS | PPIase | Repair and reassembly of PSII under high light; redox regulation during stress acclimation | Lippuner et al., 1994; Cai et al., 2008; Dominguez-Solis et al., 2008; Park et al., 2013; Speiser et al., 2015 |
| CYP38/TLP40 | sll0408 | At3g01480 | 48 | 38-40 | TL | PPIase | Inhibiting dephosphorylation of PSII subunits during the PSII repair; conversion of PSII core monomers to PSII supercomplexes | Fulgosi et al., 1998; Vener et al., 1999; Rokka et al., 2000; Fu et al., 2007; Sirpiö et al., 2008; Vasudevan et al., 2012 |
| FKBP20-2 | slr1761 | At3g60370 | 27 | 20 | TM, TL | PPIase | Formation of PSII-LHCII supercomplexes under normal and high light | Lima et al., 2006 |
| STN7 | − | At1g68830 | 63 | 59 | TM | Protein kinase | Phosphorylation of LHCII; phosphorylation of D1, D2, CP43, and PsbH under low light | Bellafiore et al., 2005; Bonardi et al., 2005; Tikkanen et al., 2008; Pesaresi et al., 2011; Tikkanen and Aro, 2012 |
| STN8 | − | At5g01920 | 55 | 50 | TM | Protein kinase | Phosphorylation of D1, D2, CP43, and PsbH | Bonardi et al., 2005; Tikkanen et al., 2008; Pesaresi et al., 2011; Tikkanen and Aro, 2012; Nath et al., 2013 |
| PBCP | − | At2g30170 | 32 | 30 | CS, TM | Protein phosphatase | Dephosphorylation of D1, D2, CP43, and PsbH | Samol et al., 2012 |
| TLP18.3 | sll1390 | At1g54780 | 31 | 18 | TL, TM | Protein phosphatase | D1 degradation and PSII dimerization; dephosphorylation of PSII core proteins (e.g., D1 and D2) | Sirpiö et al., 2007; Wu et al., 2011 |
| PPH1/TAP38 | − | At4g27800 | 43 | 41 | TM | Protein phosphatase | Dephosphorylation of LHCII | Pribil et al., 2010; Shapiguzov et al., 2010; Pesaresi et al., 2011 |
| FtsH1 | slr1390, slr0228, slr1604, sll1463d | At1g50250 | 77 | 71 | TM | FtsH protease | Degradation of photodamaged D1 | Sakamoto et al., 2003; Yu et al., 2004, 2005; Zaltsman et al., 2005b |
| FtsH2/VAR2 | At2g30950 | 74 | 69 | TM | FtsH protease | Chloroplast biogenesis; thylakoid formation; degradation of photodamaged D1 | Bailey et al., 2002; Sakamoto et al., 2002, 2003; Yu et al., 2004, 2005; Zaltsman et al., 2005a,b; Kato et al., 2007, 2009, 2012; Wagner et al., 2011 | |
| FtsH5/VAR1 | At5g42270 | 75 | 69 | TM | FtsH protease | Chloroplast biogenesis; thylakoid formation; degradation of photodamaged D1 | Sakamoto et al., 2002, 2003; Yu et al., 2004, 2005; Zaltsman et al., 2005b; Kato et al., 2009; Wagner et al., 2011 | |
| FtsH6 | At5g15250 | 77 | 69 | TM | FtsH protease | Degradation of LHCII during high-light acclimation and senescence? | Sakamoto et al., 2003; Yu et al., 2004; Zelisko et al., 2005; Wagner et al., 2011 | |
| FtsH8 | At1g06430 | 73 | 69 | TM | FtsH protease | Degradation of photodamaged D1 | Sakamoto et al., 2003; Yu et al., 2004, 2005; Zaltsman et al., 2005b; Wagner et al., 2011 | |
| FtsH11 | At5g53170 | 89 | 82 | C(TM?), IMM | FtsH protease | Thermoprotection of the photosynthetic apparatus | Sakamoto et al., 2003; Yu et al., 2004; Urantowka et al., 2005; Chen et al., 2006b; Wagner et al., 2011 | |
| Deg1 | slr1204, sll1679, sll1427e | At3g27925 | 47 | 42 | TL, TM, | Deg protease | Degradation of plastocyanin and PsbO, and photodamaged D1; integration of newly synthesized PSII subunits such as D1, D2, CP43, and CP47, into PSII complexes | Chassin et al., 2002; Huesgen et al., 2005; Kapri-Pardes et al., 2007; Sun et al., 2010b; Schuhmann and Adamska, 2012 |
| Deg2 | At2g47940 | 67 | 59 | CS, TM | Deg protease | Stress-induced degradation of LHCB6; a minor protease in in vivo degradation of photodamaged D1 | Haubühl et al., 2001; Huesgen et al., 2005, 2006; Luciński et al., 2011b; Schuhmann and Adamska, 2012 | |
| Deg5 | At4g18370 | 35 | 32 | TL, TM | Deg protease | Degradation of photodamaged D1; wound-induced degradation of PsbF | Huesgen et al., 2005; Sun et al., 2007; Luciński et al., 2011a; Kato et al., 2012; Schuhmann and Adamska, 2012 | |
| Deg7 | At3g03380 | 120 | 120? | CS, TM | Deg protease | Degradation of photodamaged D1, D2, CP43, and CP47 | Huesgen et al., 2005; Sun et al., 2010a; Schuhmann et al., 2011; Schuhmann and Adamska, 2012 | |
| Deg8 | At5g39830 | 47 | 45 | TL, TM | Deg protease | Degradation of photodamaged D1 | Huesgen et al., 2005; Sun et al., 2007; Kato et al., 2012; Schuhmann and Adamska, 2012 | |
| HCF243 | − | At3g15095 | 76 | 67 | TM | Otherf | Biogenesis, C-terminal processing, and assembly of D1; possibly biogenesis of D2 | Zhang et al., 2011 |
| PSB27-H1 | slr1645 | At1g03600 | 19 | 12 | TL, TM | Other | C-terminal processing of D1 during PSII repair? | Chen et al., 2006a; Wei et al., 2010; Dietzel et al., 2011; Shi et al., 2012; Mabbitt et al., 2014 |
| PSB27-H2/LPA19 | At1g05385 | 22 | 15 | TL, TM | Other | C-terminal processing during de novo PSII assembly | Wei et al., 2010; Shi et al., 2012; Mabbitt et al., 2014 | |
| HCF136 | slr2034 | At5g23120 | 44 | 38 | TL | Other | Assembly of PSII reaction-center complexes such as RC, RC47a, and RC47b | Meurer et al., 1998; Plücken et al., 2002; Mabbitt et al., 2014 |
| PAM68 | sll0933 | At4g19100 | 24 | 20 | TM | Other | Conversion of PSII minimal reaction-center complexes into larger PSII assembly intermediates; C-terminal processing of D1 | Armbruster et al., 2010 |
| PsbN/PBF1 | smr0009 | AtCg00700 | 4.7 | 4.7 | TM | Other | Assembly of PSII minimal reaction-center complexes; regulation of PSII core and antenna protein phosphorylation | Krech et al., 2013; Torabi et al., 2014 |
| PSB28 | sll1398 | At4g28660 | 22 | 14 | TL | Other | Biogenesis of chlorophyll-binding proteins such as CP47, PsaA, and PsaB | Jung et al., 2008; Shi et al., 2012; Mabbitt et al., 2014 |
| LPA2 | − | At5g51545 | 20 | ~20 | TM | Other | Synthesis and assembly of CP43 | Ma et al., 2007; Cai et al., 2010 |
| LPA3 | − | At1g73060 | 40 | 34 | CS, TM | Other | Synthesis and assembly of CP43 | Cai et al., 2010 |
| PSB33 | − | At1g71500 | 32 | 25 | TM | Other | Association of LHCII with PSII | Fristedt et al., 2015 |
| HHL1 | − | At1g67700 | 26 | 18 | TM | Other | Reassembly of PSII core monomers and PSII-LHCII supercomplexes during PSII repair | Jin et al., 2014 |
| MPH1 | − | At5g07020 | 24 | 20 | TM | Other | Assembly and/or stability of PSII core monomers and higher order PSII complexes under high light | Liu and Last, 2015a,b |
C, chloroplast; CE, chloroplast envelope; CS, chloroplast stroma; ICE, inner chloroplast envelope; IMM, inner mitochondria membranes; TL, thylakoid lumen; TM, thylakoid membranes.
a
The gene loci in Synechocystis sp. PCC 6803 are included in this table only to distinguish between factors that are conserved in cyanobacteria and land plants and factors that are found in land plants but not in cyanobacteria. The hyphen indicates that the corresponding factor is either absent or not yet found in Synechocystis sp. PCC 6803.
b
This article focuses on the identification and roles of PSII assembly, stability, and repair factors in Arabidopsis; therefore the gene loci for factors in other land plants are not listed in this table.
c
Detailed descriptions of factors involved in the assembly, stability, and repair of PSII in cyanobacteria can be found in Nickelsen and Rengstl (2013). Therefore, references for factors in cyanobacteria are not listed in this table.
d
The Synechocystis sp. PCC 6803 genome contains four FtsH genes. Because there is no straightforward one-to-one correspondence between the 12 Arabidopsis FtsH genes and four cyanobacterial FtsH genes, the four cyanobacterial FtsH loci are listed together.
e
The Synechocystis sp. PCC 6803 genome contains three Deg genes. Because there is no straightforward one-to-one correspondence between the 16 Arabidopsis Deg genes and three cyanobacterial Deg genes, the three cyanobacterial Deg loci are listed together.
f
Factors that do not fall in the 12 well-defined classifications (see Section Proteins that influence the assembly, stability, and repair of PSII) are classified as “other proteins” that influence the assembly, stability, and repair of PSII.