PSⅡ组装与修复循环机制研究进展
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摘要
PSⅡ超级复合体由反应中心和外周捕光色素复合体组成,其组装过程包括PSⅡ反应中心的形成、初级PSⅡ复合体组装完成以及捕光色素复合体的装配。在PSⅡ超级复合体的组装过程中,以TPR家族和HCF家族为代表的多种蛋白因子作为组装辅因子参与装配。光抑制是光破坏和修复的平衡,快速的蛋白降解和替换是应对光破坏的一种重要保护机制。PSⅡ的自我修复循环系统会快速降解损坏的D1蛋白及其他组分,重新合成PSⅡ超级复合体,这对于植物体快速修复光合系统,恢复光合作用起到了重要作用。
The PSⅡ super complex consists of a reaction center and a peripheral light-harvesting pigment complex. The assembly process includes the formation of a PSⅡ reaction center, the assembly of the primary PSⅡ complex, and the assembly of the light-harvesting pigment complex. In the assembly process of the PSⅡ super complex, various protein factors represented by the TPR family and the HCF family are involved in assembly as an assembly cofactor. Photoinhibition was historically described as an imbalance between PSⅡ photodamage and its subsequent repair, rapid protein degradation and replacement is an important response to photodamage and a means of photoprotection. The repair cycle system of PSⅡ rapidly degrade the damaged D1 protein and other components, and re-synthesize the PSⅡ super complex, which will restore photosynthesis from the rapid restoration of photosynthetic systems in plants.
The PSⅡ super complex consists of a reaction center and a peripheral light-harvesting pigment complex. The assembly process includes the formation of a PSⅡ reaction center, the assembly of the primary PSⅡ complex, and the assembly of the light-harvesting pigment complex. In the assembly process of the PSⅡ super complex, various protein factors represented by the TPR family and the HCF family are involved in assembly as an assembly cofactor. Photoinhibition was historically described as an imbalance between PSⅡ photodamage and its subsequent repair, rapid protein degradation and replacement is an important response to photodamage and a means of photoprotection. The repair cycle system of PSⅡ rapidly degrade the damaged D1 protein and other components, and re-synthesize the PSⅡ super complex, which will restore photosynthesis from the rapid restoration of photosynthetic systems in plants.
引文
Armbruster U,Zühlke J,Rengstl B,et al(2010).The Arabidopsis thylakoid protein PAM68 is required for efficient D1 biogenesis and photosystem Ⅱ sssembly.Plant Cell,22(10):3439-3460
Berne N,Fabryova T,Bistaz F,et al(2018).The peculiar NPQregulation in the stramenopile Phaeomonas sp.challenges the xanthophyll cycle dogma.Biochim Biophys Acta Bioenerg,1859(7):491-500
Bhuiyan NH,Friso G,Poliakov A,et al(2015).MET1 is a thylakoid-associated TPR protein involved in photosystem Ⅱ supercomplex formation and repair in Arabidopsis.Plant Cell,27(1):262-285
Boehm M,Yu J,Reisinger V,et al(2012).Subunit composition of CP43-less photosystem Ⅱ complexes of Synechocystis sp.PCC 6803:implications for the assembly and repair of photosystem Ⅱ.Philos Trans R Soc Lond B Biol Sci,367(1608):3444-3454
Bonardi V,Pesaresi P,Becker T,et al(2005).Photosystem Ⅱ core phosphorylation and photosynthetic acclimation require two different protein kinases.Nature,437(7062):1179-1182
Chen H,Zhang D,Guo J,et al(2006).A Psb27 homologue in Arabidopsis thaliana is required for efficient repair of photodamaged photosystem Ⅱ.Plant Mol Biol,61(4-5):567-575
Cormann KU,M?ller M,Nowaczyk MM(2016).Critical assessment of protein cross-linking and molecular docking:An updated model for the interaction between photosystem Ⅱ and Psb27.Front Plant Sci,7:157
Horton P,Ruban AV,Rees D,et al(1991).Control of the light-harvesting function of chloroplast membranes by aggregation of the LHCⅡ chlorophyll-protein complex.FEBS Lett,292(1-2):1-4
Huesgen PF,Schuhmann H,Adamska I(2006).Photodamaged D1 protein is degraded in Arabidopsis mutants lacking the Deg2 protease.FEBS Lett,580(30):6929-6932
Jeong J,Baek K,Kirst H,et al(2017).Loss of CpSRP54function leads to a truncated light-harvesting antenna size in Chlamydomonas reinhardtii.Biochim Biophys Acta Bioenerg,1858(1):45-55
Karamoko M,Cline S,Redding K,et al(2011).Lumen Thiol Oxidoreductase1,a disulfide bond-forming catalyst,is required for the assembly of photosystem Ⅱ in Arabidopsis.Plant Cell,23(12):4462-4475
Karim S,Aronsson H(2014).The puzzle of chloroplast vesicle transport-involvement of GTPases.Front Plant Sci,5:472
Kato Y,Sakamoto W(2009).Protein quality control in chloroplasts:a current model of D1 protein degradation in the photosystem Ⅱ repair cycle.J Biochem,146(4):463-469
Knopf RR,Adam Z(2018).Lumenal exposed regions of the D1 protein of PSⅡ are long enough to be degraded by the chloroplast Deg1 protease.Sci Rep,8(1):5230
Koivuniemi A,Aro EM,Andersson B(1995).Degradation of the D1-and D2-proteins of photosystem Ⅱ in higher plants is regulated by reversible phosphorylation.Biochemistry,34(49):16022-16029
Komenda J,KuvikováS,Granvogl B,et al(2007).Cleavage after residue Ala352 in the C-terminal extension is an early step in the maturation of the D1 subunit of photosystem Ⅱ in Synechocystis PCC 6803.Biochim Biophys Acta,1767(6):829-837
Komenda J,LupínkováL,KopeckyJ(2002).Absence of the psbH gene product destabilizes photosystem Ⅱ complex and bicarbonate binding on its acceptor side in Synechocystis PCC 6803.Eur J Biochem,269(2):610-619
Komenda J,Nickelsen J,Tichy M,et al(2008).The cyanobacterial homologue of HCF136/YCF48 is a component of an early photosystem Ⅱ assembly complex and is important for both the efficient assembly and repair of photosystem Ⅱ in Synechocystis sp.PCC 6803.J Biol Chem,283(33):22390-22399
Krishna N,Roshan Sharma P,Joon-Seob E,et al(2013).Lossof-function of osstn8 suppresses the photosystem Ⅱ core protein phosphorylation and interferes with the photosystem Ⅱ repair mechanism in rice(Oryza sativa).Plant J,76(4):675-686
Lindahl M,Spetea C,Hundal T,et al(2000).The thylakoid FtsH protease plays a role in the light-induced turnover of the photosystem Ⅱ D1 protein.Plant Cell,12(3):419-431
Liu H,Huang RY,Chen J,et al(2011b).Psb27,a transiently associated protein,binds to the chlorophyll binding protein CP43 in photosystem Ⅱ assembly intermediates.Proc Natl Acad Sci USA,108(45):18536-18541
Liu H,Roose JL,Cameron JC,et al(2011a).A genetically tagged Psb27 protein allows purification of two consecutive photosystem Ⅱ(PSⅡ)assembly intermediates in Synechocystis 6803,a cyanobacterium.J Biol Chem,286(28):24865-24871
Lu Y(2016).Identification and roles of photosystem Ⅱ assembly,stability,and repair factors in Arabidopsis.Front Plant Sci,7:168
Michoux F,Takasaka K,Boehm M,et al(2012).Crystal structure of the Psb27 assembly factor at 1.6?:implications for binding to photosystem Ⅱ.Photosynth Res,110(3):169-175
Muranaka LS,Rütgers M,Bujaldon S,et al(2016).TEF30interacts with photosystem Ⅱ monomers and is involved in the repair of photodamaged photosystem Ⅱ in Chlamydomonas reinhardtii.Plant Physiol,170(2):821-840
Nath K,Poudyal RS,Eom JS,et al(2013).Loss-of-function of OsSTN8 suppresses the photosystem Ⅱ core protein phosphorylation and interferes with the photosystem Ⅱrepair mechanism in rice(Oryza sativa).Plant J,76(4):675-686
Nickelsen J,Rengstl B(2013).Photosystem Ⅱ assembly:from cyanobacteria to plants.Annu Rev Plant Biol,64:609-635
Park S,Khamai P,Garcia-Cerdan JG,et al(2007).REP27,a tetratricopeptide repeat nuclear-encoded and chloroplast-localized protein,functions in D1/32-kD reaction center protein turnover and photosystem Ⅱ repair from photodamage.Plant Physiol,143(4):1547-1560
Pl?chinger M,Schwenkert S,Sydow LV,et al(2016).Functional update of the auxiliary proteins PsbW,PsbY,HCF136,PsbN,TerC and ALB3 in maintenance and assembly of PSⅡ.Front Plant Sci,7:423
Plücken H,Müller B,Grohmann D,et al(2002).The HCF136protein is essential for assembly of the photosystem Ⅱ reaction center in Arabidopsis thaliana.FEBS Lett,532(1):85-90
Pospí?il P(2012).Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem Ⅱ.Biochim Biophys Acta,1817(1):218-231
Pribil M,Pesaresi P,Hertle A,et al(2010).Role of plastid protein phosphatase TAP38 in LHCⅡ dephosphorylation and thylakoid electron flow.PLoS Biol,8(1):e1000288
Roose JL,Pakrasi HB(2008).The Psb27 protein facilitates manganese cluster assembly in photosystem Ⅱ.J Biol Chem,283(7):4044-4050
Samol I,Shapiguzov A,Ingelsson B,et al(2012).Identification of a photosystem Ⅱ phosphatase involved in light acclimation in Arabidopsis.Plant Cell,24(6):2596-2609
Sch?nberg A,Baginsky S(2012).Signal integration by chloroplast phosphorylation networks:an update.Front Plant Sci,3:256
Schottkowski M,Gkalympoudis S,Tzekova N,et al(2009).Interaction of the periplasmic PratA factor and the PsbA(D1)protein during biogenesis of photosystem Ⅱ in Synechocystis sp.PCC 6803.J Biol Chem,284(3):1813-1819
Shapiguzov A,Ingelsson B,Samol I,et al(2010).The PPH1phosphatase is specifically involved in LHCⅡ dephosphorylation and state transitions in Arabidopsis.Proc Natl Acad Sci USA,107(10):4782-4787
Shi LX,Hall M,Funk C,et al(2012).Photosystem Ⅱ,a growing complex:updates on newly discovered components and low molecular mass proteins.Biochim Biophys Acta,1817(1):13-25
Silva P,Thompson E,Bailey S,et al(2003).FtsH is involved in the early stages of repair of photosystem Ⅱ in Synechocystis sp PCC 6803.Plant Cell,15(9):2152-2164
Snellenburg JJ,Wlodarczyk LM,Dekker JP,et al(2017).Amodel for the 77K excited state dynamics in Chlamydomonas reinhardtii in state 1 and state 2.Biochim Biophys Acta Bioenerg,1858(1):64-72
Sun X,Min O,Guo JK,et al(2010).The thylakoid protease Deg1 is involved in photosystem-Ⅱ assembly in Arabidopsis thaliana.Plant J,62(2):240-249
Sun X,Peng L,Guo J,et al(2007).Formation of DEG5 and DEG8 complexes and their involvement in the degradation of photodamaged photosystem Ⅱ reaction center D1protein in Arabidopsis.Plant Cell,19(4):1347-1361
Tikkanen M,Mekala NR,Aro EM(2014).Photosystem Ⅱphotoinhibition-repair cycle protects photosystem I from irreversible damage.Biochim Biophys Acta,1837(1):210-215
Tyystj?rvi E,Aro EM(1996).The rate constant of photoinhibition,measured in lincomycin-treated leaves,is directly proportional to light intensity.Proc Natl Acad Sci USA,93(5):2213-2218
Walter B,Hristou A,Nowaczyk MM,et al(2015).In vitro reconstitution of co-translational D1 insertion reveals a role of the cpSec-Alb3 translocase and Vipp1 in photosystem Ⅱ biogenesis.Biochem J,468(2):315-324
Wei L,Guo J,Ouyang M,et al(2010).LPA19,a Psb27 homolog in Arabidopsis thaliana,facilitates D1 protein precursor processing during PSⅡ biogenesis.J Biol Chem,285(28):21391-21398
Yang Y,Guo R,Gaffney K,et al(2018).Folding-degradation relationship of a membrane protein mediated by the universally conserved ATP-dependent protease FtsH.J Am Chem Soc,140(13):4656-4665
Zhang S,Frankel LK,Bricker TM(2010).The Sll0606 protein is required for photosystem Ⅱ assembly/stability in the cyanobacterium Synechocystis sp.PCC 6803.J Biol Chem,285(42):32047-32054
Berne N,Fabryova T,Bistaz F,et al(2018).The peculiar NPQregulation in the stramenopile Phaeomonas sp.challenges the xanthophyll cycle dogma.Biochim Biophys Acta Bioenerg,1859(7):491-500
Bhuiyan NH,Friso G,Poliakov A,et al(2015).MET1 is a thylakoid-associated TPR protein involved in photosystem Ⅱ supercomplex formation and repair in Arabidopsis.Plant Cell,27(1):262-285
Boehm M,Yu J,Reisinger V,et al(2012).Subunit composition of CP43-less photosystem Ⅱ complexes of Synechocystis sp.PCC 6803:implications for the assembly and repair of photosystem Ⅱ.Philos Trans R Soc Lond B Biol Sci,367(1608):3444-3454
Bonardi V,Pesaresi P,Becker T,et al(2005).Photosystem Ⅱ core phosphorylation and photosynthetic acclimation require two different protein kinases.Nature,437(7062):1179-1182
Chen H,Zhang D,Guo J,et al(2006).A Psb27 homologue in Arabidopsis thaliana is required for efficient repair of photodamaged photosystem Ⅱ.Plant Mol Biol,61(4-5):567-575
Cormann KU,M?ller M,Nowaczyk MM(2016).Critical assessment of protein cross-linking and molecular docking:An updated model for the interaction between photosystem Ⅱ and Psb27.Front Plant Sci,7:157
Horton P,Ruban AV,Rees D,et al(1991).Control of the light-harvesting function of chloroplast membranes by aggregation of the LHCⅡ chlorophyll-protein complex.FEBS Lett,292(1-2):1-4
Huesgen PF,Schuhmann H,Adamska I(2006).Photodamaged D1 protein is degraded in Arabidopsis mutants lacking the Deg2 protease.FEBS Lett,580(30):6929-6932
Jeong J,Baek K,Kirst H,et al(2017).Loss of CpSRP54function leads to a truncated light-harvesting antenna size in Chlamydomonas reinhardtii.Biochim Biophys Acta Bioenerg,1858(1):45-55
Karamoko M,Cline S,Redding K,et al(2011).Lumen Thiol Oxidoreductase1,a disulfide bond-forming catalyst,is required for the assembly of photosystem Ⅱ in Arabidopsis.Plant Cell,23(12):4462-4475
Karim S,Aronsson H(2014).The puzzle of chloroplast vesicle transport-involvement of GTPases.Front Plant Sci,5:472
Kato Y,Sakamoto W(2009).Protein quality control in chloroplasts:a current model of D1 protein degradation in the photosystem Ⅱ repair cycle.J Biochem,146(4):463-469
Knopf RR,Adam Z(2018).Lumenal exposed regions of the D1 protein of PSⅡ are long enough to be degraded by the chloroplast Deg1 protease.Sci Rep,8(1):5230
Koivuniemi A,Aro EM,Andersson B(1995).Degradation of the D1-and D2-proteins of photosystem Ⅱ in higher plants is regulated by reversible phosphorylation.Biochemistry,34(49):16022-16029
Komenda J,KuvikováS,Granvogl B,et al(2007).Cleavage after residue Ala352 in the C-terminal extension is an early step in the maturation of the D1 subunit of photosystem Ⅱ in Synechocystis PCC 6803.Biochim Biophys Acta,1767(6):829-837
Komenda J,LupínkováL,KopeckyJ(2002).Absence of the psbH gene product destabilizes photosystem Ⅱ complex and bicarbonate binding on its acceptor side in Synechocystis PCC 6803.Eur J Biochem,269(2):610-619
Komenda J,Nickelsen J,Tichy M,et al(2008).The cyanobacterial homologue of HCF136/YCF48 is a component of an early photosystem Ⅱ assembly complex and is important for both the efficient assembly and repair of photosystem Ⅱ in Synechocystis sp.PCC 6803.J Biol Chem,283(33):22390-22399
Krishna N,Roshan Sharma P,Joon-Seob E,et al(2013).Lossof-function of osstn8 suppresses the photosystem Ⅱ core protein phosphorylation and interferes with the photosystem Ⅱ repair mechanism in rice(Oryza sativa).Plant J,76(4):675-686
Lindahl M,Spetea C,Hundal T,et al(2000).The thylakoid FtsH protease plays a role in the light-induced turnover of the photosystem Ⅱ D1 protein.Plant Cell,12(3):419-431
Liu H,Huang RY,Chen J,et al(2011b).Psb27,a transiently associated protein,binds to the chlorophyll binding protein CP43 in photosystem Ⅱ assembly intermediates.Proc Natl Acad Sci USA,108(45):18536-18541
Liu H,Roose JL,Cameron JC,et al(2011a).A genetically tagged Psb27 protein allows purification of two consecutive photosystem Ⅱ(PSⅡ)assembly intermediates in Synechocystis 6803,a cyanobacterium.J Biol Chem,286(28):24865-24871
Lu Y(2016).Identification and roles of photosystem Ⅱ assembly,stability,and repair factors in Arabidopsis.Front Plant Sci,7:168
Michoux F,Takasaka K,Boehm M,et al(2012).Crystal structure of the Psb27 assembly factor at 1.6?:implications for binding to photosystem Ⅱ.Photosynth Res,110(3):169-175
Muranaka LS,Rütgers M,Bujaldon S,et al(2016).TEF30interacts with photosystem Ⅱ monomers and is involved in the repair of photodamaged photosystem Ⅱ in Chlamydomonas reinhardtii.Plant Physiol,170(2):821-840
Nath K,Poudyal RS,Eom JS,et al(2013).Loss-of-function of OsSTN8 suppresses the photosystem Ⅱ core protein phosphorylation and interferes with the photosystem Ⅱrepair mechanism in rice(Oryza sativa).Plant J,76(4):675-686
Nickelsen J,Rengstl B(2013).Photosystem Ⅱ assembly:from cyanobacteria to plants.Annu Rev Plant Biol,64:609-635
Park S,Khamai P,Garcia-Cerdan JG,et al(2007).REP27,a tetratricopeptide repeat nuclear-encoded and chloroplast-localized protein,functions in D1/32-kD reaction center protein turnover and photosystem Ⅱ repair from photodamage.Plant Physiol,143(4):1547-1560
Pl?chinger M,Schwenkert S,Sydow LV,et al(2016).Functional update of the auxiliary proteins PsbW,PsbY,HCF136,PsbN,TerC and ALB3 in maintenance and assembly of PSⅡ.Front Plant Sci,7:423
Plücken H,Müller B,Grohmann D,et al(2002).The HCF136protein is essential for assembly of the photosystem Ⅱ reaction center in Arabidopsis thaliana.FEBS Lett,532(1):85-90
Pospí?il P(2012).Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem Ⅱ.Biochim Biophys Acta,1817(1):218-231
Pribil M,Pesaresi P,Hertle A,et al(2010).Role of plastid protein phosphatase TAP38 in LHCⅡ dephosphorylation and thylakoid electron flow.PLoS Biol,8(1):e1000288
Roose JL,Pakrasi HB(2008).The Psb27 protein facilitates manganese cluster assembly in photosystem Ⅱ.J Biol Chem,283(7):4044-4050
Samol I,Shapiguzov A,Ingelsson B,et al(2012).Identification of a photosystem Ⅱ phosphatase involved in light acclimation in Arabidopsis.Plant Cell,24(6):2596-2609
Sch?nberg A,Baginsky S(2012).Signal integration by chloroplast phosphorylation networks:an update.Front Plant Sci,3:256
Schottkowski M,Gkalympoudis S,Tzekova N,et al(2009).Interaction of the periplasmic PratA factor and the PsbA(D1)protein during biogenesis of photosystem Ⅱ in Synechocystis sp.PCC 6803.J Biol Chem,284(3):1813-1819
Shapiguzov A,Ingelsson B,Samol I,et al(2010).The PPH1phosphatase is specifically involved in LHCⅡ dephosphorylation and state transitions in Arabidopsis.Proc Natl Acad Sci USA,107(10):4782-4787
Shi LX,Hall M,Funk C,et al(2012).Photosystem Ⅱ,a growing complex:updates on newly discovered components and low molecular mass proteins.Biochim Biophys Acta,1817(1):13-25
Silva P,Thompson E,Bailey S,et al(2003).FtsH is involved in the early stages of repair of photosystem Ⅱ in Synechocystis sp PCC 6803.Plant Cell,15(9):2152-2164
Snellenburg JJ,Wlodarczyk LM,Dekker JP,et al(2017).Amodel for the 77K excited state dynamics in Chlamydomonas reinhardtii in state 1 and state 2.Biochim Biophys Acta Bioenerg,1858(1):64-72
Sun X,Min O,Guo JK,et al(2010).The thylakoid protease Deg1 is involved in photosystem-Ⅱ assembly in Arabidopsis thaliana.Plant J,62(2):240-249
Sun X,Peng L,Guo J,et al(2007).Formation of DEG5 and DEG8 complexes and their involvement in the degradation of photodamaged photosystem Ⅱ reaction center D1protein in Arabidopsis.Plant Cell,19(4):1347-1361
Tikkanen M,Mekala NR,Aro EM(2014).Photosystem Ⅱphotoinhibition-repair cycle protects photosystem I from irreversible damage.Biochim Biophys Acta,1837(1):210-215
Tyystj?rvi E,Aro EM(1996).The rate constant of photoinhibition,measured in lincomycin-treated leaves,is directly proportional to light intensity.Proc Natl Acad Sci USA,93(5):2213-2218
Walter B,Hristou A,Nowaczyk MM,et al(2015).In vitro reconstitution of co-translational D1 insertion reveals a role of the cpSec-Alb3 translocase and Vipp1 in photosystem Ⅱ biogenesis.Biochem J,468(2):315-324
Wei L,Guo J,Ouyang M,et al(2010).LPA19,a Psb27 homolog in Arabidopsis thaliana,facilitates D1 protein precursor processing during PSⅡ biogenesis.J Biol Chem,285(28):21391-21398
Yang Y,Guo R,Gaffney K,et al(2018).Folding-degradation relationship of a membrane protein mediated by the universally conserved ATP-dependent protease FtsH.J Am Chem Soc,140(13):4656-4665
Zhang S,Frankel LK,Bricker TM(2010).The Sll0606 protein is required for photosystem Ⅱ assembly/stability in the cyanobacterium Synechocystis sp.PCC 6803.J Biol Chem,285(42):32047-32054