植物叶绿体蛋白质周转的研究进展及潜在应用
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摘要
叶绿体的正常周转是维持胁迫条件下植物光合作用和代谢反应高效进行的必要条件。对叶绿体维持平衡的生理和分子机制的理解是控制植物叶绿体质量的基础,这涉及两个重要的生理过程:叶绿体蛋白质的导入和降解。叶绿体蛋白质的有序导入和受损伤叶绿体及其组分的及时降解在调节植物环境适应性中起着关键作用。本文首先综述了叶绿体蛋白质的导入机制,随后介绍了叶绿体蛋白质的多种降解途径,并对通过调控叶绿体质量提高作物环境适应性的策略进行了概述和展望。
The normal chloroplast turnover is necessary for keeping efficient operation of photosynthesis and metabolic reactions under stress condition. The understanding of the physiological and molecular mechanisms of the maintenance of chloroplasts homeostasis is the basis for controlling chloroplast quality in plants, which involves two important physiological processes: the import and degradation of chloroplast proteins. The orderly import of chloroplast proteins and the timely degradation of damaged chloroplast and its components play a key role in the regulation of plant environmental acclimation. This paper firstly reviews the mechanism of chloroplast proteins import, then, multiple degradation pathways of chloroplast proteins were introduced and, finally,the strategies for improving environmental adaptability of crops through chloroplast quality control were summarized and prospected.
The normal chloroplast turnover is necessary for keeping efficient operation of photosynthesis and metabolic reactions under stress condition. The understanding of the physiological and molecular mechanisms of the maintenance of chloroplasts homeostasis is the basis for controlling chloroplast quality in plants, which involves two important physiological processes: the import and degradation of chloroplast proteins. The orderly import of chloroplast proteins and the timely degradation of damaged chloroplast and its components play a key role in the regulation of plant environmental acclimation. This paper firstly reviews the mechanism of chloroplast proteins import, then, multiple degradation pathways of chloroplast proteins were introduced and, finally,the strategies for improving environmental adaptability of crops through chloroplast quality control were summarized and prospected.
引文
Albinlak AM,Baglieri J,Robinson C(2012).Targeting of lumenal proteins across the thylakoid membrane.J Exp Bot,63(4):1689-1698
Andrès C,Agne B,Kessler F(2010).The TOC complex:preprotein gateway to the chloroplast.BBA-Mol Cell Res,1803(6):715-723
Bédard J,Tr?sch R,Wu F,et al(2017).Suppressors of the chloroplast protein import mutant tic40 reveal a genetic link between protein import and thylakoid biogenesis.Plant Cell,29(7):1726-1747
Bionda T,Gross LE,Becker T,et al(2016).Eukaryotic Hsp70chaperones in the intermembrane space of chloroplasts.Planta,243(3):733-747
Carrión CA,Costa ML,Martínez DE,et al(2013).In vivo inhibition of cysteine proteases provides evidence for the involvement of‘senescence-associated vacuoles’in chloroplast protein degradation during dark-induced senescence of tobacco leaves.J Exp Bot,64(16):4967-4980
Cederholm SN,B?ckman HG,Pesaresi P,et al(2009).Deletion of an organellar peptidasome PreP affects early development in Arabidopsis thaliana.Plant Mol Biol,71:497-508
Chang JS,Chen LJ,Yeh YH,et al(2017).Chloroplast preproteins bind to the dimer interface of the Toc159 receptor during import.Plant Physiol,173(4):2148-2162
Chen LJ,Li HM(2017).Stable megadalton TOC-TIC supercomplexes as major mediators of protein import into chloroplasts.Plant J,92(2):178-188
de Jesus MPRH,Nielsen AZ,Mellor SB,et al(2017).Tat proteins as novel thylakoid membrane anchors organize a biosynthetic pathway in chloroplasts and increase product yield 5-fold.Metab Eng,44:108-116
de Souza A,Wang JZ,Dehesh K(2017).Retrograde signals:integrators of interorganellar communication and orchestrators of plant development.Annu Rev Plant Biol,68:85-108
Evans IM,Rus AM,Belanger EM,et al(2010).Dismantling of Arabidopsis thaliana mesophyll cell chloroplasts during natural leaf senescence.Plant Biol,12(1):1-12
Flores-Pérezú,Jarvis P(2013).Molecular chaperone involvement in chloroplast protein import.BBA-Mol Cell Res,1833(2):332-340
Ishida H,Yoshimoto K(2008).Chloroplasts are partially mobilized to the vacuole by autophagy.Autophagy,4(7):961-962
Izumi M,Ishida H,Nakamura S,et al(2017).Entire photodamaged chloroplasts are transported to the central vacuole by autophagy.Plant Cell,29(2):377-394
Izumi M,Wada S,Makino A,et al(2010).The autophagic degradation of chloroplasts via Rubisco-containing bodies is specifically linked to leaf carbon status but not nitrogen status in Arabidopsis.Plant Physiol,154(3):1196-1209
Jeong J,Baek K,Yu J,et al(2017).Deletion of the chloroplast LTD protein impedes LHCI import and PSI-LHCI assembly in Chlamydomonas reinhardtii.J Exp Bot,69(5):1147-1158
Kato Y,Murakami S,Yamamoto Y,et al(2004).The DNA-binding protease,CND41,and the degradation of ribulose-1,5-bisphosphate carboxylase/oxygenase in senescent leaves of tobacco.Planta,220(1):97-104
Kim DH,Park MJ,Gwon GH,et al(2014).An ankyrin repeat domain of AKR2 drives chloroplast targeting through coincident binding of two chloroplast lipids.Dev Cell,30(5):598-609
Kim J,Kimber MS,Nishimura K,et al(2015).Structures,functions,and interactions of ClpT1 and ClpT2 in the Clp protease system of Arabidopsis chloroplasts.Plant Cell,27(5):1477-1496
K?hler D,Montandon C,Hause G,et al(2015).Characterization of chloroplast protein import without Tic56,a component of the 1-MDa TIC translocon at the inner envelope membrane of chloroplasts.Plant Physiol,167(3):972-990
Kong SG,Okajima K(2016).Diverse photoreceptors and light responses in plants.J Plant Res,129(2):111-114
Lee DW,Jung C,Hwang I(2013).Cytosolic events involved in chloroplast protein targeting.BBA-Mol Cell Res,1833(2):245-252
Lee DW,Lee J,Hwang I(2017).Sorting of nuclear-encoded chloroplast membrane proteins.Curr Opin Plant Biol,40:1-7
Li HM,Teng YS(2013).Transit peptide design and plastid import regulation.Trends Plant Sci,18(7):360-366
Ling Q,Huang W,Baldwin A,et al(2012).Chloroplast biogenesis is regulated by direct action of the ubiquitin-proteasome system.Science,338(6107):655-659
Ling Q,Jarvis P(2015).Regulation of chloroplast protein import by the ubiquitin E3 ligase SP1 is important for stress tolerance in plants.Curr Biol,25(19):2527-2534
Michaeli S,Honig A,Levanony H,et al(2014).Arabidopsis ATG8-INTERACTING PROTEIN1 is involved in autophagy-dependent vesicular trafficking of plastid proteins to the vacuole.Plant Cell,26(10):4084-4101
Nakai M(2015).The TIC complex uncovered:the alternative view on the molecular mechanism of protein translocation across the inner envelope membrane of chloroplasts.BBA-Bioenergetics,1847(9):957-967
Nishimura K,Kato Y,Sakamoto W(2017).Essentials of proteolytic machineries in chloroplasts.Mol Plant,10(1):4-19
Otegui MS,Noh YS,Martínez DE,et al(2005).Senescence-associated vacuoles with intense proteolytic activity develop in leaves of Arabidopsis and soybean.Plant J,41(6):831-844
Paila YD,Richardson LGL,Schnell DJ(2015).New insights into the mechanism of chloroplast protein import and its integration with protein quality control,organelle biogenesis and development.J Mol Biol,427(5):1038-1060
Petroutsos D,Tokutsu R,Maruyama S,et al(2016).A bluelight photoreceptor mediates the feedback regulation of photosynthesis.Nature,537(7621):563-566
Rudolf M,Machettira AB,Gro?LE,et al(2013).In vivo function of Tic22,a protein import component of the intermembrane space of chloroplasts.Mol Plant,6(3):817-829
Sade N,Umnajkitikorn K,Wilhelmi MMR,et al(2017).Delaying chloroplast turnover increases water-deficit stress tolerance through the enhancement of nitrogen assimilation in rice.J Exp Bot,69(4):867-878
Sjuts I,Soll J,B?lter B(2017).Import of soluble proteins into chloroplasts and potential regulatory mechanisms.Front Plant Sci,8:168
Springer A,Kang CH,Rustgi S,et al(2016).Programmed chloroplast destruction during leaf senescence involves13-lipoxygenase(13-LOX).Proc Nati Acad Sci USA,113(12):3383-3388
Vercruyssen L,Tognetti VB,Gonzalez N,et al(2015).GROWTH REGULATING FACTOR5 stimulates Arabidopsis chloroplast division,photosynthesis,and leaf longevity.Plant Physiol,167(3):817-832
Vermeulen SJ,Campbell BM,Ingram JSI(2012).Climate change and food systems.Annu Rev Env Resour,37:195-222
Wada S,Ishida H,Izumi M,et al(2009).Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves.Plant Physiol,149(2):885-893
Wagner R,von Sydow L,Aigner H,et al(2016).Deletion of FtsH11 protease has impact on chloroplast structure and function in Arabidopsis thaliana when grown under continuous light.Plant Cell Environ,39(11):2530-2544
Wang P,Hendron RW,Kelly S(2017).Transcriptional control of photosynthetic capacity:conservation and divergence from Arabidopsis to rice.New Phytol,216(1):32-45
Wang S,Blumwald E(2014).Stress-induced chloroplast degradation in Arabidopsis is regulated via a process independent of autophagy and senescence-associated vacuoles.Plant Cell,26(12):4875-4888
Woodson JD,Joens MS,Sinson AB,et al(2015).Ubiquitin facilitates a quality-control pathway that removes damaged chloroplasts.Science,350(6259):450-454
Xu XM,Chi W,Zhang LX(2016).Recent advances in plastid retrograde signaling.Plant Physiol J,52(11):1618-1626(in Chinese with English abstract)[徐秀美,迟伟,张立新(2016).质体反向信号研究进展.植物生理学报,52(11):1618-1626]
You QY,He ZH(2016).Research advances on ubiquitin-26Sproteasome-mediated plant immunity.Plant Physiol J,52(6):771-781(in Chinese with English abstract)[游全远,何祖华(2016).泛素-26S蛋白酶体系统参与调控植物免疫研究进展.植物生理学报,52(6):771-781]
Zhao P,Cui R,Xu P,et al(2017).ATHB17 enhances stress tolerance by coordinating photosynthesis associated nuclear gene and ATSIG5 expression in response to abiotic stress.Sci Rep,7:45492
Zufferey M,Montandon C,Douet V,et al(2017).The novel chloroplast outer membrane kinase KOC1 is a required component of the plastid protein import machinery.J Biol Chem,292(17):6952-6964
Andrès C,Agne B,Kessler F(2010).The TOC complex:preprotein gateway to the chloroplast.BBA-Mol Cell Res,1803(6):715-723
Bédard J,Tr?sch R,Wu F,et al(2017).Suppressors of the chloroplast protein import mutant tic40 reveal a genetic link between protein import and thylakoid biogenesis.Plant Cell,29(7):1726-1747
Bionda T,Gross LE,Becker T,et al(2016).Eukaryotic Hsp70chaperones in the intermembrane space of chloroplasts.Planta,243(3):733-747
Carrión CA,Costa ML,Martínez DE,et al(2013).In vivo inhibition of cysteine proteases provides evidence for the involvement of‘senescence-associated vacuoles’in chloroplast protein degradation during dark-induced senescence of tobacco leaves.J Exp Bot,64(16):4967-4980
Cederholm SN,B?ckman HG,Pesaresi P,et al(2009).Deletion of an organellar peptidasome PreP affects early development in Arabidopsis thaliana.Plant Mol Biol,71:497-508
Chang JS,Chen LJ,Yeh YH,et al(2017).Chloroplast preproteins bind to the dimer interface of the Toc159 receptor during import.Plant Physiol,173(4):2148-2162
Chen LJ,Li HM(2017).Stable megadalton TOC-TIC supercomplexes as major mediators of protein import into chloroplasts.Plant J,92(2):178-188
de Jesus MPRH,Nielsen AZ,Mellor SB,et al(2017).Tat proteins as novel thylakoid membrane anchors organize a biosynthetic pathway in chloroplasts and increase product yield 5-fold.Metab Eng,44:108-116
de Souza A,Wang JZ,Dehesh K(2017).Retrograde signals:integrators of interorganellar communication and orchestrators of plant development.Annu Rev Plant Biol,68:85-108
Evans IM,Rus AM,Belanger EM,et al(2010).Dismantling of Arabidopsis thaliana mesophyll cell chloroplasts during natural leaf senescence.Plant Biol,12(1):1-12
Flores-Pérezú,Jarvis P(2013).Molecular chaperone involvement in chloroplast protein import.BBA-Mol Cell Res,1833(2):332-340
Ishida H,Yoshimoto K(2008).Chloroplasts are partially mobilized to the vacuole by autophagy.Autophagy,4(7):961-962
Izumi M,Ishida H,Nakamura S,et al(2017).Entire photodamaged chloroplasts are transported to the central vacuole by autophagy.Plant Cell,29(2):377-394
Izumi M,Wada S,Makino A,et al(2010).The autophagic degradation of chloroplasts via Rubisco-containing bodies is specifically linked to leaf carbon status but not nitrogen status in Arabidopsis.Plant Physiol,154(3):1196-1209
Jeong J,Baek K,Yu J,et al(2017).Deletion of the chloroplast LTD protein impedes LHCI import and PSI-LHCI assembly in Chlamydomonas reinhardtii.J Exp Bot,69(5):1147-1158
Kato Y,Murakami S,Yamamoto Y,et al(2004).The DNA-binding protease,CND41,and the degradation of ribulose-1,5-bisphosphate carboxylase/oxygenase in senescent leaves of tobacco.Planta,220(1):97-104
Kim DH,Park MJ,Gwon GH,et al(2014).An ankyrin repeat domain of AKR2 drives chloroplast targeting through coincident binding of two chloroplast lipids.Dev Cell,30(5):598-609
Kim J,Kimber MS,Nishimura K,et al(2015).Structures,functions,and interactions of ClpT1 and ClpT2 in the Clp protease system of Arabidopsis chloroplasts.Plant Cell,27(5):1477-1496
K?hler D,Montandon C,Hause G,et al(2015).Characterization of chloroplast protein import without Tic56,a component of the 1-MDa TIC translocon at the inner envelope membrane of chloroplasts.Plant Physiol,167(3):972-990
Kong SG,Okajima K(2016).Diverse photoreceptors and light responses in plants.J Plant Res,129(2):111-114
Lee DW,Jung C,Hwang I(2013).Cytosolic events involved in chloroplast protein targeting.BBA-Mol Cell Res,1833(2):245-252
Lee DW,Lee J,Hwang I(2017).Sorting of nuclear-encoded chloroplast membrane proteins.Curr Opin Plant Biol,40:1-7
Li HM,Teng YS(2013).Transit peptide design and plastid import regulation.Trends Plant Sci,18(7):360-366
Ling Q,Huang W,Baldwin A,et al(2012).Chloroplast biogenesis is regulated by direct action of the ubiquitin-proteasome system.Science,338(6107):655-659
Ling Q,Jarvis P(2015).Regulation of chloroplast protein import by the ubiquitin E3 ligase SP1 is important for stress tolerance in plants.Curr Biol,25(19):2527-2534
Michaeli S,Honig A,Levanony H,et al(2014).Arabidopsis ATG8-INTERACTING PROTEIN1 is involved in autophagy-dependent vesicular trafficking of plastid proteins to the vacuole.Plant Cell,26(10):4084-4101
Nakai M(2015).The TIC complex uncovered:the alternative view on the molecular mechanism of protein translocation across the inner envelope membrane of chloroplasts.BBA-Bioenergetics,1847(9):957-967
Nishimura K,Kato Y,Sakamoto W(2017).Essentials of proteolytic machineries in chloroplasts.Mol Plant,10(1):4-19
Otegui MS,Noh YS,Martínez DE,et al(2005).Senescence-associated vacuoles with intense proteolytic activity develop in leaves of Arabidopsis and soybean.Plant J,41(6):831-844
Paila YD,Richardson LGL,Schnell DJ(2015).New insights into the mechanism of chloroplast protein import and its integration with protein quality control,organelle biogenesis and development.J Mol Biol,427(5):1038-1060
Petroutsos D,Tokutsu R,Maruyama S,et al(2016).A bluelight photoreceptor mediates the feedback regulation of photosynthesis.Nature,537(7621):563-566
Rudolf M,Machettira AB,Gro?LE,et al(2013).In vivo function of Tic22,a protein import component of the intermembrane space of chloroplasts.Mol Plant,6(3):817-829
Sade N,Umnajkitikorn K,Wilhelmi MMR,et al(2017).Delaying chloroplast turnover increases water-deficit stress tolerance through the enhancement of nitrogen assimilation in rice.J Exp Bot,69(4):867-878
Sjuts I,Soll J,B?lter B(2017).Import of soluble proteins into chloroplasts and potential regulatory mechanisms.Front Plant Sci,8:168
Springer A,Kang CH,Rustgi S,et al(2016).Programmed chloroplast destruction during leaf senescence involves13-lipoxygenase(13-LOX).Proc Nati Acad Sci USA,113(12):3383-3388
Vercruyssen L,Tognetti VB,Gonzalez N,et al(2015).GROWTH REGULATING FACTOR5 stimulates Arabidopsis chloroplast division,photosynthesis,and leaf longevity.Plant Physiol,167(3):817-832
Vermeulen SJ,Campbell BM,Ingram JSI(2012).Climate change and food systems.Annu Rev Env Resour,37:195-222
Wada S,Ishida H,Izumi M,et al(2009).Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves.Plant Physiol,149(2):885-893
Wagner R,von Sydow L,Aigner H,et al(2016).Deletion of FtsH11 protease has impact on chloroplast structure and function in Arabidopsis thaliana when grown under continuous light.Plant Cell Environ,39(11):2530-2544
Wang P,Hendron RW,Kelly S(2017).Transcriptional control of photosynthetic capacity:conservation and divergence from Arabidopsis to rice.New Phytol,216(1):32-45
Wang S,Blumwald E(2014).Stress-induced chloroplast degradation in Arabidopsis is regulated via a process independent of autophagy and senescence-associated vacuoles.Plant Cell,26(12):4875-4888
Woodson JD,Joens MS,Sinson AB,et al(2015).Ubiquitin facilitates a quality-control pathway that removes damaged chloroplasts.Science,350(6259):450-454
Xu XM,Chi W,Zhang LX(2016).Recent advances in plastid retrograde signaling.Plant Physiol J,52(11):1618-1626(in Chinese with English abstract)[徐秀美,迟伟,张立新(2016).质体反向信号研究进展.植物生理学报,52(11):1618-1626]
You QY,He ZH(2016).Research advances on ubiquitin-26Sproteasome-mediated plant immunity.Plant Physiol J,52(6):771-781(in Chinese with English abstract)[游全远,何祖华(2016).泛素-26S蛋白酶体系统参与调控植物免疫研究进展.植物生理学报,52(6):771-781]
Zhao P,Cui R,Xu P,et al(2017).ATHB17 enhances stress tolerance by coordinating photosynthesis associated nuclear gene and ATSIG5 expression in response to abiotic stress.Sci Rep,7:45492
Zufferey M,Montandon C,Douet V,et al(2017).The novel chloroplast outer membrane kinase KOC1 is a required component of the plastid protein import machinery.J Biol Chem,292(17):6952-6964
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