Current Understanding of Temperature Stress-Responsive Chloroplast FtsH Metalloproteases
Abstract
:1. Introduction
2. Chloroplast ROS-Mediated Operational Retrograde Signaling
3. Chloroplast FtsH-Dependent Proteostasis Functions in Photoprotection
4. Thylakoid Membrane Ftsh6 and Hsp21 Modules Function in Thermomemory
5. Chloroplast Envelope FtsH11 Mediates Thermotolerance
6. Protein Import-Associated Proteostasis Is Allied with Retrograde Signaling
7. Concluding Remarks
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Acknowledgments
Conflicts of Interest
References
- Fournier-Level, A.; Korte, A.; Cooper, M.D.; Nordborg, M.; Schmitt, J.; Wilczek, A.M. A map of local adaptation in Arabidopsis thaliana. Science 2011, 334, 86–89. [Google Scholar] [CrossRef]
- Hancock, A.M.; Brachi, B.; Faure, N.; Horton, M.W.; Jarymowycz, L.B.; Sperone, F.G.; Toomajian, C.; Roux, F.; Bergelson, J. Adaptation to climate across the Arabidopsis thaliana genome. Science 2011, 334, 83–86. [Google Scholar] [CrossRef] [Green Version]
- Guo, M.; Zhang, X.; Liu, J.; Hou, L.; Liu, H.; Zhao, X. OsProDH negatively regulates thermotolerance in rice by modulating proline metabolism and reactive oxygen species scavenging. Rice (N. Y.) 2020, 13, 61. [Google Scholar] [CrossRef]
- Bokszczanin, K.L.; Solanaceae Pollen Thermotolerance Initial Training Network Consortium; Fragkostefanakis, S. Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance. Front. Plant Sci. 2013, 4, 315. [Google Scholar] [CrossRef]
- Hu, S.; Ding, Y.; Zhu, C. Sensitivity and responses of chloroplasts to heat stress in plants. Front. Plant Sci. 2020, 11, 375. [Google Scholar] [CrossRef] [Green Version]
- Li, Z.; Howell, S.H. Heat stress responses and thermotolerance in maize. Int. J. Mol. Sci. 2021, 22, 948. [Google Scholar] [CrossRef]
- Haynes, C.M.; Petrova, K.; Benedetti, C.; Yang, Y.; Ron, D. ClpP mediates activation of a mitochondrial unfolded protein response in C. elegans. Dev. Cell 2007, 13, 467–480. [Google Scholar] [CrossRef] [Green Version]
- Poveda-Huertes, D.; Matic, S.; Marada, A.; Habernig, L.; Licheva, M.; Myketin, L.; Gilsbach, R.; Tosal-Castano, S.; Papinski, D.; Mulica, P.; et al. An early mtUPR: Redistribution of the nuclear transcription factor Rox1 to mitochondria protects against intramitochondrial proteotoxic aggregates. Mol. Cell 2020, 77, 180–188. [Google Scholar] [CrossRef] [Green Version]
- Baker, M.J.; Tatsuta, T.; Langer, T. Quality control of mitochondrial proteostasis. Cold Spring Harb. Perspect. Biol. 2011, 3, a007559. [Google Scholar] [CrossRef] [Green Version]
- Feller, U.; Anders, I.; Mae, T. Rubiscolytics: Fate of rubisco after its enzymatic function in a cell is terminated. J. Exp. Bot. 2008, 59, 1615–1624. [Google Scholar] [CrossRef] [Green Version]
- Llamas, E.; Pulido, P.; Rodriguez-Concepcion, M. Interference with plastome gene expression and Clp protease activity in arabidopsis triggers a chloroplast unfolded protein response to restore protein homeostasis. PLoS Genet. 2017, 13, e1007022. [Google Scholar] [CrossRef]
- Ramundo, S.; Casero, D.; Muhlhaus, T.; Hemme, D.; Sommer, F.; Crevecoeur, M.; Rahire, M.; Schroda, M.; Rusch, J.; Goodenough, U.; et al. Conditional depletion of the Chlamydomonas Chloroplast ClpP Protease activates nuclear genes involved in autophagy and plastid protein quality control. Plant Cell 2014, 26, 2201–2222. [Google Scholar] [CrossRef] [Green Version]
- Perlaza, K.; Toutkoushian, H.; Boone, M.; Lam, M.; Iwai, M.; Jonikas, M.C.; Walter, P.; Ramundo, S. The Mars1 kinase confers photoprotection through signaling in the chloroplast unfolded protein response. eLife 2019, 8, e49577. [Google Scholar] [CrossRef]
- van Buer, J.; Prescher, A.; Baier, M. Cold-priming of chloroplast ROS signalling is developmentally regulated and is locally controlled at the thylakoid membrane. Sci. Rep. 2019, 9, 3022. [Google Scholar] [CrossRef]
- Majumdar, A.; Kar, R.K. Chloroplast avoidance movement: A novel paradigm of ROS signalling. Photosynth. Res. 2020, 144, 109–121. [Google Scholar] [CrossRef]
- Apel, K.; Hirt, H. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 2004, 55, 373–399. [Google Scholar] [CrossRef] [Green Version]
- Dogra, V.; Rochaix, J.D.; Kim, C. Singlet oxygen-triggered chloroplast-to-nucleus retrograde signalling pathways: An emerging perspective. Plant Cell Environ. 2018, 41, 1727–1738. [Google Scholar] [CrossRef]
- Dogra, V.; Duan, J.; Lee, K.P.; Kim, C. Impaired PSII proteostasis triggers a UPR-like response in the var2 mutant of Arabidopsis. J. Exp. Bot. 2019, 70, 3075–3088. [Google Scholar] [CrossRef]
- Mishra, L.S.; Funk, C. The FtsHi enzymes of Arabidopsis thaliana: Pseudo-proteases with an Important function. Int. J. Mol. Sci. 2021, 22, 5917. [Google Scholar] [CrossRef]
- Wang, L.; Leister, D.; Guan, L.; Zheng, Y.; Schneider, K.; Lehmann, M.; Apel, K.; Kleine, T. The Arabidopsis SAFEGUARD1 suppresses singlet oxygen-induced stress responses by protecting grana margins. Proc. Natl. Acad. Sci. USA 2020, 117, 6918–6927. [Google Scholar] [CrossRef]
- Li, B.; Fang, J.; Singh, R.M.; Zi, H.; Lv, S.; Liu, R.; Dogra, V.; Kim, C. Fatty Acid Desaturase5 Is required to induce autoimmune responses in gigantic chloroplast mutants of arabidopsis. Plant Cell 2020, 32, 3240–3255. [Google Scholar] [CrossRef]
- D’Alessandro, S.; Beaugelin, I.; Havaux, M. Tanned or sunburned: How excessive light triggers plant cell death. Mol. Plant 2020, 13, 1545–1555. [Google Scholar] [CrossRef]
- Dogra, V.; Li, M.; Singh, S.; Li, M.; Kim, C. Oxidative post-translational modification of EXECUTER1 is required for singlet oxygen sensing in plastids. Nat. Commun. 2019, 10, 2834. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Duan, J.; Lee, K.P.; Dogra, V.; Zhang, S.; Liu, K.; Caceres-Moreno, C.; Lv, S.; Xing, W.; Kato, Y.; Sakamoto, W.; et al. Impaired PSII proteostasis promotes retrograde signaling via salicylic acid. Plant Physiol. 2019, 180, 2182–2197. [Google Scholar] [CrossRef]
- Kim, C.; Apel, K. Singlet oxygen-mediated signaling in plants: Moving from flu to wild type reveals an increasing complexity. Photosynth. Res. 2013, 116, 455–464. [Google Scholar] [CrossRef] [Green Version]
- Asada, K. Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol. 2006, 141, 391–396. [Google Scholar] [CrossRef] [Green Version]
- Jiang, J.; Dehesh, K. Plastidial retrograde modulation of light and hormonal signaling: An odyssey. New Phytol. 2021, 230, 931–937. [Google Scholar] [CrossRef]
- Suzuki, N.; Koussevitzky, S.; Mittler, R.; Miller, G. ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ. 2012, 35, 259–270. [Google Scholar] [CrossRef] [PubMed]
- Kim, C. ROS-driven oxidative modification: Its impact on chloroplasts-nucleus communication. Front. Plant Sci. 2019, 10, 1729. [Google Scholar] [CrossRef]
- Havaux, M. beta-Cyclocitral and derivatives: Emerging molecular signals serving multiple biological functions. Plant Physiol. Biochem. 2020, 155, 35–41. [Google Scholar] [CrossRef]
- Chan, K.X.; Phua, S.Y.; Crisp, P.; McQuinn, R.; Pogson, B.J. Learning the languages of the chloroplast: Retrograde signaling and beyond. Annu. Rev. Plant Biol. 2016, 67, 25–53. [Google Scholar] [CrossRef]
- Patel, S.; Latterich, M. The AAA team: Related ATPases with diverse functions. Trends Cell Biol. 1998, 8, 65–71. [Google Scholar] [CrossRef]
- Kedzierska, S. Structure, function and mechanisms of action of ATPases from the AAA superfamily of proteins. Postepy Biochem. 2006, 52, 330–338. [Google Scholar] [PubMed]
- Ogura, T.; Wilkinson, A.J. AAA+ superfamily ATPases: Common structure--diverse function. Genes Cells 2001, 6, 575–597. [Google Scholar] [CrossRef] [PubMed]
- Santos, D.; De Almeida, D.F. Isolation and characterization of a new temperature-sensitive cell division mutant of Escherichia coli K-12. J. Bacteriol. 1975, 124, 1502–1507. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, F.; Qi, Y.; Malnoe, A.; Choquet, Y.; Wollman, F.A.; de Vitry, C. The high light response and redox control of Thylakoid FtsH protease in chlamydomonas reinhardtii. Mol. Plant 2017, 10, 99–114. [Google Scholar] [CrossRef] [Green Version]
- Sakamoto, W.; Zaltsman, A.; Adam, Z.; Takahashi, Y. Coordinated regulation and complex formation of yellow variegated1 and yellow variegated2, chloroplastic FtsH metalloproteases involved in the repair cycle of photosystem II in Arabidopsis thylakoid membranes. Plant Cell 2003, 15, 2843–2855. [Google Scholar] [CrossRef] [Green Version]
- Bec Kova, M.; Yu, J.; Krynicka, V.; Kozlo, A.; Shao, S.; Konik, P.; Komenda, J.; Murray, J.W.; Nixon, P.J. Structure of Psb29/Thf1 and its association with the FtsH protease complex involved in photosystem II repair in cyanobacteria. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2017, 372, 1730. [Google Scholar]
- Mann, N.H.; Novac, N.; Mullineaux, C.W.; Newman, J.; Bailey, S.; Robinson, C. Involvement of an FtsH homologue in the assembly of functional photosystem I in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett. 2000, 479, 72–77. [Google Scholar] [CrossRef] [Green Version]
- Yeo, W.S.; Anokwute, C.; Marcadis, P.; Levitan, M.; Ahmed, M.; Bae, Y.; Kim, K.; Kostrominova, T.; Liu, Q.; Bae, T. A membrane-bound transcription factor is proteolytically regulated by the AAA+ protease FtsH in Staphylococcus aureus. J. Bacteriol. 2020, 202, e00019-20. [Google Scholar] [CrossRef]
- Fuhrer, F.; Langklotz, S.; Narberhaus, F. The C-terminal end of LpxC is required for degradation by the FtsH protease. Mol. Microbiol. 2006, 59, 1025–1036. [Google Scholar] [CrossRef] [PubMed]
- Nguyen, D.; Kelly, K.; Qiu, N.; Misra, R. YejM Controls LpxC Levels by regulating protease activity of the FtsH/YciM complex of Escherichia coli. J. Bacteriol. 2020, 202, e00303-20. [Google Scholar] [CrossRef]
- Schnall, R.; Mannhaupt, G.; Stucka, R.; Tauer, R.; Ehnle, S.; Schwarzlose, C.; Vetter, I.; Feldmann, H. Identification of a set of yeast genes coding for a novel family of putative ATPases with high similarity to constituents of the 26S protease complex. Yeast 1994, 10, 1141–1155. [Google Scholar] [CrossRef] [PubMed]
- Wagner, R.; Aigner, H.; Pruzinska, A.; Jankanpaa, H.J.; Jansson, S.; Funk, C. Fitness analyses of Arabidopsis thaliana mutants depleted of FtsH metalloproteases and characterization of three FtsH6 deletion mutants exposed to high light stress, senescence and chilling. New Phytol. 2011, 191, 449–458. [Google Scholar] [CrossRef]
- Chen, J.; Burke, J.J.; Velten, J.; Xin, Z. FtsH11 protease plays a critical role in Arabidopsis thermotolerance. Plant J. 2006, 48, 73–84. [Google Scholar] [CrossRef]
- Adam, Z.; Aviv-Sharon, E.; Keren-Paz, A.; Naveh, L.; Rozenberg, M.; Savidor, A.; Chen, J. The chloroplast envelope protease FTSH11—Interaction with CPN60 and identification of potential substrates. Front. Plant Sci. 2019, 10, 428. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kato, Y.; Sakamoto, W. FtsH Protease in the thylakoid membrane: Physiological functions and the regulation of protease activity. Front. Plant Sci. 2018, 9, 855. [Google Scholar] [CrossRef] [Green Version]
- Liu, X.; Yu, F.; Rodermel, S. Arabidopsis chloroplast FtsH, var2 and suppressors of var2 leaf variegation: A review. J. Integr. Plant Biol. 2010, 52, 750–761. [Google Scholar] [CrossRef]
- Rodrigues, R.A.; Silva-Filho, M.C.; Cline, K. FtsH2 and FtsH5: Two homologous subunits use different integration mechanisms leading to the same thylakoid multimeric complex. Plant J. 2011, 65, 600–609. [Google Scholar] [CrossRef] [Green Version]
- Wang, L.; Kim, C.; Xu, X.; Piskurewicz, U.; Dogra, V.; Singh, S.; Mahler, H.; Apel, K. Singlet oxygen- and EXECUTER1-mediated signaling is initiated in grana margins and depends on the protease FtsH2. Proc. Natl. Acad. Sci. USA 2016, 113, E3792–3800. [Google Scholar] [CrossRef] [Green Version]
- Nixon, P.J.; Michoux, F.; Yu, J.; Boehm, M.; Komenda, J. Recent advances in understanding the assembly and repair of photosystem II. Ann. Bot-London 2010, 106, 1–16. [Google Scholar] [CrossRef] [Green Version]
- Dreaden, T.M.; Chen, J.; Rexroth, S.; Barry, B.A. N-formylkynurenine as a marker of high light stress in photosynthesis. J. Biol. Chem. 2011, 286, 22632–22641. [Google Scholar] [CrossRef] [Green Version]
- Majeran, W.; Wollman, F.A.; Vallon, O. Evidence for a role of ClpP in the degradation of the chloroplast cytochrome b(6)f complex. Plant Cell 2000, 12, 137–150. [Google Scholar] [CrossRef] [PubMed]
- Halperin, T.; Ostersetzer, O.; Adam, Z. ATP-dependent association between subunits of Clp protease in pea chloroplasts. Planta 2001, 213, 614–619. [Google Scholar] [CrossRef]
- Pulido, P.; Llamas, E.; Llorente, B.; Ventura, S.; Wright, L.P.; Rodriguez-Concepcion, M. Specific Hsp100 chaperones determine the fate of the first enzyme of the plastidial isoprenoid pathway for either refolding or degradation by the stromal clp protease in arabidopsis. PLoS Genet. 2016, 12, e1005824. [Google Scholar] [CrossRef] [PubMed]
- Xiao, Y.; Savchenko, T.; Baidoo, E.E.; Chehab, W.E.; Hayden, D.M.; Tolstikov, V.; Corwin, J.A.; Kliebenstein, D.J.; Keasling, J.D.; Dehesh, K. Retrograde signaling by the plastidial metabolite MEcPP regulates expression of nuclear stress-response genes. Cell 2012, 149, 1525–1535. [Google Scholar] [CrossRef] [Green Version]
- Walley, J.; Xiao, Y.; Wang, J.Z.; Baidoo, E.E.; Keasling, J.D.; Shen, Z.; Briggs, S.P.; Dehesh, K. Plastid-produced interorgannellar stress signal MEcPP potentiates induction of the unfolded protein response in endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 2015, 112, 6212–6217. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Poor, P.; Czekus, Z.; Tari, I.; Ordog, A. The multifaceted roles of plant hormone salicylic acid in endoplasmic reticulum stress and unfolded protein response. Int. J. Mol. Sci. 2019, 20, 5842. [Google Scholar] [CrossRef] [Green Version]
- Zelisko, A.; Garcia-Lorenzo, M.; Jackowski, G.; Jansson, S.; Funk, C. AtFtsH6 is involved in the degradation of the light-harvesting complex II during high-light acclimation and senescence. Proc. Natl. Acad. Sci. USA 2005, 102, 13699–13704. [Google Scholar] [CrossRef] [Green Version]
- Yang, D.H.; Webster, J.; Adam, Z.; Lindahl, M.; Andersson, B. Induction of acclimative proteolysis of the light-harvesting chlorophyll a/b protein of photosystem II in response to elevated light intensities. Plant Physiol. 1998, 118, 827–834. [Google Scholar] [CrossRef] [Green Version]
- Yang, D.H.; Paulsen, H.; Andersson, B. The N-terminal domain of the light-harvesting chlorophyll a/b-binding protein complex (LHCII) is essential for its acclimative proteolysis. FEBS Lett. 2000, 466, 385–388. [Google Scholar] [CrossRef] [Green Version]
- Sedaghatmehr, M.; Mueller-Roeber, B.; Balazadeh, S. The plastid metalloprotease FtsH6 and small heat shock protein HSP21 jointly regulate thermomemory in Arabidopsis. Nat. Commun. 2016, 7, 12439. [Google Scholar] [CrossRef] [Green Version]
- Sedaghatmehr, M.; Thirumalaikumar, V.P.; Kamranfar, I.; Schulz, K.; Mueller-Roeber, B.; Sampathkumar, A.; Balazadeh, S. Autophagy complements metalloprotease FtsH6 in degrading plastid heat shock protein HSP21 during heat stress recovery. J. Exp. Bot. 2021. [Google Scholar] [CrossRef]
- Nishizawa, A.; Yabuta, Y.; Yoshida, E.; Maruta, T.; Yoshimura, K.; Shigeoka, S. Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J. 2006, 48, 535–547. [Google Scholar] [CrossRef] [PubMed]
- Nishad, A.; Nandi, A.K. Recent advances in plant thermomemory. Plant Cell Rep. 2021, 40, 19–27. [Google Scholar] [CrossRef]
- Bernfur, K.; Rutsdottir, G.; Emanuelsson, C. The chloroplast-localized small heat shock protein Hsp21 associates with the thylakoid membranes in heat-stressed plants. Protein Sci. 2017, 26, 1773–1784. [Google Scholar] [CrossRef] [PubMed]
- Chen, J.; Burke, J.J.; Xin, Z. Chlorophyll fluorescence analysis revealed essential roles of FtsH11 protease in regulation of the adaptive responses of photosynthetic systems to high temperature. BMC Plant Biol. 2018, 18, 11. [Google Scholar] [CrossRef] [Green Version]
- Urantowka, A.; Knorpp, C.; Olczak, T.; Kolodziejczak, M.; Janska, H. Plant mitochondria contain at least two i-AAA-like complexes. Plant Mol. Biol. 2005, 59, 239–252. [Google Scholar] [CrossRef]
- Knopf, R.R.; Feder, A.; Mayer, K.; Lin, A.; Rozenberg, M.; Schaller, A.; Adam, Z. Rhomboid proteins in the chloroplast envelope affect the level of allene oxide synthase in Arabidopsis thaliana. Plant J. 2012, 72, 559–571. [Google Scholar] [CrossRef] [PubMed]
- Wagner, R.; von Sydow, L.; Aigner, H.; Netotea, S.; Brugiere, S.; Sjogren, L.; Ferro, M.; Clarke, A.; Funk, C. Deletion of FtsH11 protease has impact on chloroplast structure and function in Arabidopsis thaliana when grown under continuous light. Plant Cell Environ. 2016, 39, 2530–2544. [Google Scholar] [CrossRef]
- Baker, T.A.; Sauer, R.T. ATP-dependent proteases of bacteria: Recognition logic and operating principles. Trends Biochem. Sci. 2006, 31, 647–653. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gerdes, F.; Tatsuta, T.; Langer, T. Mitochondrial AAA proteases—towards a molecular understanding of membrane-bound proteolytic machines. Bba-Bioenergetics 2012, 1823, 49–55. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rainey, R.N.; Glavin, J.D.; Chen, H.W.; French, S.W.; Teitell, M.A.; Koehler, C.M. A new function in translocation for the mitochondrial i-AAA protease Yme1: Import of polynucleotide phosphorylase into the intermembrane space. Mol. Cell Biol. 2006, 26, 8488–8497. [Google Scholar] [CrossRef] [Green Version]
- Chou, M.L.; Fitzpatrick, L.M.; Tu, S.L.; Budziszewski, G.; Potter-Lewis, S.; Akita, M.; Levin, J.Z.; Keegstra, K.; Li, H.M. Tic40, a membrane-anchored co-chaperone homolog in the chloroplast protein translocon. EMBO J. 2003, 22, 2970–2980. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kovacheva, S.; Bedard, J.; Patel, R.; Dudley, P.; Twell, D.; Rios, G.; Koncz, C.; Jarvis, P. In vivo studies on the roles of Tic110, Tic40 and Hsp93 during chloroplast protein import. Plant J. 2005, 41, 412–428. [Google Scholar] [CrossRef] [Green Version]
- Stolz, A.; Hilt, W.; Buchberger, A.; Wolf, D.H. Cdc48: A power machine in protein degradation. Trends Biochem. Sci. 2011, 36, 515–523. [Google Scholar] [CrossRef]
- Dunn, C.D.; Tamura, Y.; Sesaki, H.; Jensen, R.E. Mgr3p and Mgr1p are adaptors for the mitochondrial i-AAA protease complex. Mol. Biol. Cell 2008, 19, 5387–5397. [Google Scholar] [CrossRef] [Green Version]
- Wu, X.; Li, L.; Jiang, H. Mitochondrial inner-membrane protease Yme1 degrades outer-membrane proteins Tom22 and Om45. J. Cell Biol. 2018, 217, 139–149. [Google Scholar] [CrossRef]
- Graef, M.; Seewald, G.; Langer, T. Substrate recognition by AAA+ ATPases: Distinct substrate binding modes in ATP-dependent protease Yme1 of the mitochondrial intermembrane space. Mol. Cell Biol. 2007, 27, 2476–2485. [Google Scholar] [CrossRef] [Green Version]
- Shanmugabalaji, V.; Kessler, F. CHLORAD: Eradicating translocon components from the outer membrane of the chloroplast. Mol. Plant 2019, 12, 467–469. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ling, Q.; Broad, W.; Trosch, R.; Topel, M.; Demiral Sert, T.; Lymperopoulos, P.; Baldwin, A.; Jarvis, R.P. Ubiquitin-dependent chloroplast-associated protein degradation in plants. Science 2019, 363, 836. [Google Scholar] [CrossRef] [PubMed]
- Ling, Q.; Huang, W.; Baldwin, A.; Jarvis, P. Chloroplast biogenesis is regulated by direct action of the ubiquitin-proteasome system. Science 2012, 338, 655–659. [Google Scholar] [CrossRef] [PubMed]
- Ling, Q.; Jarvis, P. Regulation of chloroplast protein import by the ubiquitin e3 ligase sp1 is important for stress tolerance in plants. Curr. Biol. 2015, 25, 2527–2534. [Google Scholar] [CrossRef] [Green Version]
- Wu, G.Z.; Meyer, E.H.; Richter, A.S.; Schuster, M.; Ling, Q.; Schottler, M.A.; Walther, D.; Zoschke, R.; Grimm, B.; Jarvis, R.P.; et al. Control of retrograde signalling by protein import and cytosolic folding stress. Nat. Plants 2019, 5, 525–538. [Google Scholar] [CrossRef]
- Zhao, X.; Huang, J.; Chory, J. GUN1 interacts with MORF2 to regulate plastid RNA editing during retrograde signaling. Proc. Natl. Acad. Sci. USA 2019, 116, 10162–10167. [Google Scholar] [CrossRef] [PubMed] [Green Version]
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Luo, S.; Kim, C. Current Understanding of Temperature Stress-Responsive Chloroplast FtsH Metalloproteases. Int. J. Mol. Sci. 2021, 22, 12106. https://doi.org/10.3390/ijms222212106
Luo S, Kim C. Current Understanding of Temperature Stress-Responsive Chloroplast FtsH Metalloproteases. International Journal of Molecular Sciences. 2021; 22(22):12106. https://doi.org/10.3390/ijms222212106
Chicago/Turabian StyleLuo, Shengji, and Chanhong Kim. 2021. "Current Understanding of Temperature Stress-Responsive Chloroplast FtsH Metalloproteases" International Journal of Molecular Sciences 22, no. 22: 12106. https://doi.org/10.3390/ijms222212106