Chloroplast Transition Metal Regulation for Efficient Photosynthesis
2020; Elsevier BV; Volume: 25; Issue: 8 Linguagem: Inglês
10.1016/j.tplants.2020.03.003
ISSN1878-4372
AutoresSidsel Birkelund Schmidt, Marion Eisenhut, Anja Schneider,
Tópico(s)Electrocatalysts for Energy Conversion
ResumoThe transition metals Fe, Mn, and Cu have fundamental functions in the photosynthetic machinery but are also involved in undesired oxidative reactions when in excess. Thus, chloroplast transition metal concentrations need tight regulation to maintain efficient photosynthesis.Chloroplast transition metal homeostasis is complex. It involves a sophisticated interplay of specific transport proteins, chaperones and carriers, and protein translocation systems.The availability of full genomic information and organelle-specific protein databases of model plants, such as A. thaliana, allows the identification of chloroplast metal transport candidates. Using this information, the two transport proteins CMT1 and PAM71 were recently discovered to function in tandem for delivery of Mn to the oxygen-evolving complex in PSII. Plants require sunlight, water, CO2, and essential nutrients to drive photosynthesis and fulfill their life cycle. The photosynthetic apparatus resides in chloroplasts and fundamentally relies on transition metals as catalysts and cofactors. Accordingly, chloroplasts are particularly rich in iron (Fe), manganese (Mn), and copper (Cu). Owing to their redox properties, those metals need to be carefully balanced within the cell. However, the regulation of transition metal homeostasis in chloroplasts is poorly understood. With the availability of the arabidopsis genome information and membrane protein databases, a wider catalogue for searching chloroplast metal transporters has considerably advanced the study of transition metal regulation. This review provides an updated overview of the chloroplast transition metal requirements and the transporters involved for efficient photosynthesis in higher plants. Plants require sunlight, water, CO2, and essential nutrients to drive photosynthesis and fulfill their life cycle. The photosynthetic apparatus resides in chloroplasts and fundamentally relies on transition metals as catalysts and cofactors. Accordingly, chloroplasts are particularly rich in iron (Fe), manganese (Mn), and copper (Cu). Owing to their redox properties, those metals need to be carefully balanced within the cell. However, the regulation of transition metal homeostasis in chloroplasts is poorly understood. With the availability of the arabidopsis genome information and membrane protein databases, a wider catalogue for searching chloroplast metal transporters has considerably advanced the study of transition metal regulation. This review provides an updated overview of the chloroplast transition metal requirements and the transporters involved for efficient photosynthesis in higher plants. Chloroplasts harbor three types of membranes: a double (inner and outer) envelope and a thylakoid membrane. The envelope and thylakoid are separated by the stroma compartment. The membranes, and the transporters embedded therein, are selective barriers enabling exchange of ions and metabolites between the cytosol, the stroma, and the thylakoid lumen compartment. Chloroplast functioning and efficient photosynthesis for plant growth rely on the metal cofactor-mediated electron transport chain, in particular the transition metals Fe, Mn, and Cu [1.Merchant S. Trace metal utilization in chloroplasts.in: Wise R. Hoober J.K. The Structure and Function of Plastids. Springer, 2006: 199-218Crossref Google Scholar]. However, as ions, their chemical properties can lead to generation of undesired reactive oxygen species (ROS) [2.Ravet K. Pilon M. Copper and iron homeostasis in plants: the challenges of oxidative stress.Antioxid. Redox Signal. 2013; 19: 919-932Crossref PubMed Scopus (0) Google Scholar], which, together with their different binding affinities to proteins [3.Irving H. Williams R.J.P. Order of stability of metal complexes.Nature. 1948; 162: 746-747Crossref Google Scholar], greatly challenge the use of metals in oxygenic photosynthesis. To avoid harmful generation of ROS, plants chelate metal ions by organic ligands, such as nicotianamine, phenolic compounds, or organic acids (e.g., citrate, malate, ascorbate) [4.Bashir K. et al.Regulating subcellular metal homeostasis: the key to crop improvement.Front. Plant Sci. 2016; 7: 1192Crossref PubMed Scopus (34) Google Scholar]. Thus, the transport, homeostasis, and regulation of the individual transition metals are fundamental to optimizing chloroplast functioning. The chloroplast contains more than 3000 proteins of which about 90 transporters are associated with the chloroplast envelope membranes, controlling the exchange of ions and metabolites [5.Bouchnak I. et al.Unravelling hidden components of the chloroplast envelope proteome: opportunities and limits of better MS sensitivity.Mol. Cell. 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With the availability of arabidopsis (Arabidopsis thaliana) genome information [7.The Arabidopsis Genome Initiative Analysis of the genome sequence of the flowering plant Arabidopsis thaliana.Nature. 2000; 408: 796-815Crossref PubMed Scopus (6236) Google Scholar] and establishment of various total cellular and more specific chloroplast protein membrane databases [8.Schwacke R. et al.ARAMEMNON, a novel database for Arabidopsis integral membrane proteins.Plant Physiol. 2003; 131: 16-26Crossref PubMed Scopus (459) Google Scholar,9.Ferro M. et al.AT_CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins.Mol. Cell. Proteomics. 2010; 9: 1063-1084Crossref PubMed Scopus (316) Google Scholar], a wider catalogue for searching new chloroplast metal transporters is now available. Moving forward, reverse genetic studies combined with targeted proteomics and bioinformatics approaches are likely to identify novel transporters [10.Rolland N. et al.The biosynthetic capacities of the plastids and integration between cytoplasmic and chloroplast processes.Annu. Rev. Genet. 2012; 46: 233-264Crossref PubMed Scopus (64) Google Scholar,11.Ling Q. et al.Ubiquitin-dependent chloroplast-associated protein degradation in plants.Science. 2019; 363eaav4467Crossref PubMed Scopus (17) Google Scholar]. This review provides a comprehensive description of chloroplast transition metal requirements, including an update on identified metal transport proteins for the distribution of Fe, Mn, and Cu within the chloroplast. The dynamics and mechanisms allowing the adaptability of the photosynthetic machinery to constantly changing metal concentrations are discussed. 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The chloroplast metal concentration for Fe, Mn, and Cu is roughly 7 to 10 μg per 109 chloroplasts isolated from arabidopsis mesophyll cells, in a ratio of 5.8:1.0:0.5 (Fe:Mn:Cu) [15.Eisenhut M. et al.The plastid envelope CHLOROPLAST MANGANESE TRANSPORTER1 is essential for manganese homeostasis in Arabidopsis.Mol. Plant. 2018; 11: 955-969Abstract Full Text Full Text PDF PubMed Scopus (11) Google Scholar,16.Zhang B. et al.Inner envelope CHLOROPLAST MANGANESE TRANSPORTER 1 supports manganese homeostasis and phototrophic growth in Arabidopsis.Mol. Plant. 2018; 11: 943-954Abstract Full Text Full Text PDF PubMed Scopus (9) Google Scholar]. Within the chloroplasts, 60 to 80% of Fe, Mn, and Cu is found in thylakoids, reflecting the essential use of these metals in photosynthetic proteins and complexes [12.Terry N. Low G. Leaf chlorophyll content and its relation to the intracellular-localization of iron.J. 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Res. 2019; 139: 337-358Crossref PubMed Scopus (1) Google Scholar], with a total number of 22 Fe atoms, four Mn atoms, and one Cu atom required per photosynthetic electron transport chain (Table 1).Table 1Transition Metal Quota in Proteins of the Photosynthetic Electron Transport ChainMetalChloroplast protein(Gene ID)Ligand/cofactorFunctionProtein Data Bank in EuropeRefsMnPSIIPsbA and PsbC(AtCg00020 and AtCg00280)Mn4CaO5Water oxidationElectron transport3jcu (spinach),5xnm, 5xnl (pea)[103.Wei X. et al.Structure of spinach photosystem II–LHCII supercomplex at 3.2Å resolution.Nature. 2016; 534: 69-74Crossref PubMed Scopus (0) Google Scholar][104.Su X. et al.Structure and assembly mechanism of plant C2S2M2-type PSII-LHCII supercomplex.Science. 2017; 357: 815-820Crossref PubMed Scopus (100) Google Scholar]FePSIIPsbA and PsbD(AtCg0020 and AtCg00270)PsbE and PsbFaHeme bound to PsbE and PsbF constitutes Cyt b556 a and b.(AtCg00580 and AtCg00570)Fe2+hemeElectron transporteFe2+ is involved in electron transport, despite no changes in its oxidation state.Photoprotection5mdx (arabidopsis),3jcu (spinach),5xnm, 5xnl (pea)[105.van Bezouwen L.S. et al.Subunit and chlorophyll organization of the plant photosystem II supercomplex.Nat. Plants. 2017; 3: 17080Crossref PubMed Scopus (44) Google Scholar][103.Wei X. et al.Structure of spinach photosystem II–LHCII supercomplex at 3.2Å resolution.Nature. 2016; 534: 69-74Crossref PubMed Scopus (0) Google Scholar][104.Su X. et al.Structure and assembly mechanism of plant C2S2M2-type PSII-LHCII supercomplex.Science. 2017; 357: 815-820Crossref PubMed Scopus (100) Google Scholar]FeCyt b6/fPetB (AtCg00720)bHeme bound to PetB constitutes Cyt b6.PetA (AtCg00540)cHeme bound to PetA constitutes Cyt f.PetC (At4g03280)d[2Fe–2S] bound to PetC constitutes the Rieske FeS protein.3 × hemeheme[2Fe–2S]Proton translocationElectron transportElectron transport1q90 (Chlamydomonas),4h44 (Nostoc)[106.Stroebel D. et al.An atypical haem in the cytochrome b6f complex.Nature. 2003; 426: 413-418Crossref PubMed Scopus (467) Google Scholar][107.Hasan S.S. et al.Quinone-dependent proton transfer pathways in the photosynthetic cytochrome b6f complex.Proc. Natl. Acad. Sci. U. S. A. 2013; 110: 4297-4302Crossref PubMed Scopus (0) Google Scholar]FePSIPsaA and PsaB(AtCg00350 and AtCg00340)PsaC (AtCg01060)1 × [4Fe–4S]2 × [4Fe–4S]Electron transportElectron transport5zji (maize),2wse (various plants), 5l8r (pea)[108.Pan X. et al.Structure of the maize photosystem I supercomplex with light-harvesting complexes I and II.Science. 2018; 360: 1109-1113Crossref PubMed Scopus (33) Google Scholar][109.Amunts A. et al.Structure determination and improved model of plant photosystem I.J. Biol. Chem. 2010; 285: 3478-3486Crossref PubMed Scopus (0) Google Scholar][110.Mazor Y. et al.Structure of the plant photosystem I supercomplex at 2.6 Å resolution.Nat. Plants. 2017; 3: 17014Crossref PubMed Scopus (0) Google Scholar]FeFdFd1 (At1g10960)Fd2 (At1g60950)Fd3 (At2g27510)Fd4 (At5g10000)[2Fe–2S]Electron transport1pfd (parsley),1gaq (maize)[111.Im S.C. et al.The solution structure of parsley [2Fe–2S]ferredoxin.Eur. J. Biochem. 1998; 258: 465-477Crossref PubMed Google Scholar][112.Kurisu G. et al.Structure of the electron transfer complex between ferredoxin and ferredoxin-NADP+ reductase.Nat. Struct. Biol. 2001; 8: 117-121Crossref PubMed Scopus (0) Google Scholar]CuPCPete1 (At1g76100)Pete2 (At1g20340)Cu+/Cu2+Electron transport9pcy (bean)[113.Moore J.M. et al.High-resolution solution structure of reduced French bean plastocyanin and comparison with the crystal structure of poplar plastocyanin.J. Mol. Biol. 1991; 221: 533-555Crossref PubMed Scopus (0) Google Scholar]a Heme bound to PsbE and PsbF constitutes Cyt b556 a and b.b Heme bound to PetB constitutes Cyt b6.c Heme bound to PetA constitutes Cyt f.d [2Fe–2S] bound to PetC constitutes the Rieske FeS protein.e Fe2+ is involved in electron transport, despite no changes in its oxidation state. Open table in a new tab Fe is the prominent transition metal for protein complexes in the photosynthetic electron chain (Table 1). It is present as Fe2+ ligated to PsbA and PsbD in photosystem II (PSII), in heme proteins of PSII and cytochrome b6/f (Cyt b6/f), and in Fe–Sulfur [Fe–S] clusters of Cyt b6/f, photosystem I (PSI), and ferredoxin (Fd) (Figure 1, Key Figure, and Table 1). Biomass and seed yields in arabidopsis can be significantly increased through improved photosynthesis by overexpression of the Rieske [2Fe–2S] protein (PetC) [18.Simkin A.J. et al.Overexpression of the RieskeFeS protein increases electron transport rates and biomass yield.Plant Physiol. 2017; 175: 134-145Crossref PubMed Scopus (0) Google Scholar], implying that Fe availability is not a bottleneck [18.Simkin A.J. et al.Overexpression of the RieskeFeS protein increases electron transport rates and biomass yield.Plant Physiol. 2017; 175: 134-145Crossref PubMed Scopus (0) Google Scholar]. [Fe–S] clusters have an essential role in linear electron transport but also serve as redox cofactor of the NADH dehydrogenase-like complex (NDH) in cyclic electron flow around PSI [19.Laughlin T.G. et al.Structure of the complex I-like molecule NDH of oxygenic photosynthesis.Nature. 2019; 566: 411-414Crossref PubMed Scopus (23) Google Scholar], a mechanism to balance the levels of ATP and NADPH necessary for efficient photosynthesis. Fe also plays an essential auxiliary function as di-Fe cofactor in the enzyme plastid terminal oxidase (PTOX) [20.Nawrocki W.J. et al.The plastid terminal oxidase: its elusive function points to multiple contributions to plastid physiology.Annu. Rev. Plant Biol. 2015; 66: 49-74Crossref PubMed Scopus (0) Google Scholar,21.Krieger-Liszkay A. Feilke K. The dual role of the plastid terminal oxidase PTOX: between a protective and a pro-oxidant function.Front. Plant Sci. 2015; 6: 1147PubMed Google Scholar], which is localized to the nonappressed regions of the thylakoids. PTOX protects the plastoquinone pool from overreduction by reducing the number of electrons available for photosynthetic reactions, specifically under abiotic stress [20.Nawrocki W.J. et al.The plastid terminal oxidase: its elusive function points to multiple contributions to plastid physiology.Annu. Rev. Plant Biol. 2015; 66: 49-74Crossref PubMed Scopus (0) Google Scholar,21.Krieger-Liszkay A. Feilke K. The dual role of the plastid terminal oxidase PTOX: between a protective and a pro-oxidant function.Front. Plant Sci. 2015; 6: 1147PubMed Google Scholar]. In addition to the crucial role in photosynthesis, Fe is also involved as cofactor in many stroma and envelope localized processes. In these compartments, Fe-containing superoxide dismutase (FeSOD) [22.Pilon M. et al.The biogenesis and physiological function of chloroplast superoxide dismutases.Biochim. Biophys. Acta. 2011; 1807: 989-998Crossref PubMed Scopus (0) Google Scholar] catalyzes the dismutation of harmful superoxide radicals (O2-) into hydrogen peroxide (H2O2), which is further decomposed by heme-containing ascorbate peroxidases (APX) to produce H2O and O2 [23.Wada K. et al.Crystal structure of chloroplastic ascorbate peroxidase from tobacco plants and structural insights into its instability.J. Biochem. 2003; 134: 239-244Crossref PubMed Scopus (34) Google Scholar]. Moreover, [Fe–S] clusters occur as cofactors of enzymes involved in chlorophyll metabolism, including chlorophyll a oxygenase (CAO), pheophorbide a oxygenase (PAO), 7-hydroxymethyl chlorophyll a reductase (HCAR) (for review, see [24.Lu Y. Assembly and transfer of iron–sulfur clusters in the plastid.Front. 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Mn is essential for light-driven oxidation of H2O to extract the electrons needed in the photosynthetic electron chain and to release protons to generate the universal energy unit adenosine triphosphate (ATP). As a byproduct, O2 is produced. For this purpose, four Mn ions constitute the catalytic center in the Mn4CaO5 cluster of the oxygen-evolving complex in PSII (Table 1 and Figure 1). In accordance with the Kok cycle [28.Kok B. et al.Cooperation of charges in photosynthetic O2 evolution-I. A linear four step mechanism.Photochem. Photobiol. 1970; 11: 457-475Crossref PubMed Google Scholar], the Mn ions cycle through different oxidation states (Mn3+, Mn4+), the so-called S states, driven by the successive absorption of photons to extract electrons from H2O [29.Shen J.-R. The structure of photosystem II and the mechanism of water oxidation in photosynthesis.Annu. Rev. Plant Biol. 2015; 66: 23-48Crossref PubMed Scopus (243) Google Scholar]. PSII activity is therefore highly sensitive to Mn deficiency [30.Schmidt S.B. et al.Photosystem II functionality in barley responds dynamically to changes in leaf manganese status.Front. Plant Sci. 2016; 7: 1-12Crossref PubMed Scopus (10) Google Scholar]. Moreover, a binuclear Mn2+ center is involved in recognition of the thylakoid-associated phosphatase 38 (TAP38) and phosphorylated light-harvesting chlorophyll a/b binding protein 1 (Lhcb1) during state transition; a mechanism allowing plants to regulate energy distribution between PSI and PSII [31.Pribil M. et al.Role of plastid protein phosphatase TAP38 in LHCII dephosphorylation and thylakoid electron flow.PLoS Biol. 2010; 8e1000288Crossref PubMed Scopus (189) Google Scholar,32.Wei X. et al.Structural mechanism underlying the specific recognition between the Arabidopsis state-transition phosphatase TAP38/PPH1 and phosphorylated light-harvesting complex protein Lhcb1.Plant Cell. 2015; 27: 1113-1127Crossref PubMed Scopus (14) Google Scholar]. In the chloroplast stroma, enzymes of amino acid biosynthetic pathways are activated by Mn2+. The imidazoleglycerol-phosphate dehydratase (IGPD) is a key enzyme in histidine biosynthesis [33.Ingle, R.A. (2011) Histidine biosynthesis. Arabidopsis Book 9, e0141Google Scholar, 34.Bisson C. et al.Crystal structures reveal that the reaction mechanism of imidazoleglycerol-phosphate dehydratase is controlled by switching Mn(II) coordination.Structure. 2015; 23: 1236-1245Abstract Full Text Full Text PDF PubMed Google Scholar, 35.Rawson S. et al.Elucidating the structural basis for differing enzyme inhibitor potency by cryo-EM.Proc. Natl. Acad. Sci. U. S. A. 2018; 115: 1795-1800Crossref PubMed Scopus (13) Google Scholar]. The shikimate pathway of aromatic amino acid biosynthesis involves the Mn2+-dependent 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase (DAHP) enzyme [36.Entus R. et al.Redox regulation of Arabidopsis 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase.Plant Physiol. 2002; 129: 1866-1871Crossref PubMed Scopus (0) Google Scholar]. 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However, the PC1 isoform accumulates at lower levels than PC2, which is more sensitive to Cu availability at the protein level [38.Abdel-Ghany S.E. Contribution of plastocyanin isoforms to photosynthesis and copper homeostasis in Arabidopsis thaliana grown at different copper regimes.Planta. 2009; 229: 767-779Crossref PubMed Scopus (0) Google Scholar,39.Pesaresi P. et al.Mutants, overexpressors, and interactors of Arabidopsis plastocyanin isoforms: revised roles of plastocyanin in photosynthetic electron flow and thylakoid redox state.Mol. Plant. 2009; 2: 236-248Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar]. Another abundant Cu enzyme, polyphenol oxidase (PPO), contains two Cu2+/Cu+ ions per monomer. In the thylakoid lumen of spinach (Spinacia oleracea), the enzyme is thought to function in defense against biotic attacks [40.Aguirre G. Pilon M. Copper delivery to chloroplast proteins and its regulation.Front. 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Fe and Mn deficiency cause interveinal chlorosis, which appears as a sharp distinction between veins and chlorotic areas of the youngest leaves [48.Briat J.-F. et al.Iron nutrition, biomass production, and plant product quality.Trends Plant Sci. 2015; 20: 33-40Abstract Full Text Full Text PDF PubMed Scopus (168) Google Scholar,49.Schmidt S.B. et al.Ancient barley landraces adapted to marginal soils demonstrate exceptional tolerance to manganese limitation.Ann. Bot. 2019; 123: 831-843Crossref PubMed Scopus (1) Google Scholar]. At the cellular level, transition metal deficiency conditions often trigger disorganization of the chloroplast and its thylakoid membrane system. For instance, arabidopsis permease in chloroplasts 1 (pic1) mutants are unable to import Fe into chloroplasts, and their chloroplast number and size are reduced. Chloroplast development was found to be distorted with inchoate or even absent thylakoids [50.Duy D. et al.PIC1, an ancient permease in Arabidopsis chloroplasts, mediates iron transport.Plant Cell. 2007; 19: 986-1006Crossref PubMed Scopus (170) Google Scholar]. Likewise, in Mn-deficient chloroplasts of arabidopsis chloroplast Mn transporter 1 (cmt1) mutants, chloroplast development was abnormal and thylakoids appeared disorganized, with either hypo- or hyper-stacked grana lamellae [15.Eisenhut M. et al.The plastid envelope CHLOROPLAST MANGANESE TRANSPORTER1 is essential for manganese homeostasis in Arabidopsis.Mol. Plant. 2018; 11: 955-969Abstract Full Text Full Text PDF PubMed Scopus (11) Google Scholar,16.Zhang B. et al.Inner envelope CHLOROPLAST MANGANESE TRANSPORTER 1 supports manganese homeostasis and phototrophic growth in Arabidopsis.Mol. Plant. 2018; 11: 943-954Abstract Full Text Full Text PDF PubMed Scopus (9) Google Scholar]. Clearly, Fe and Mn deficiencies directly affect the biogenesis of photosynthetic membrane complexes. At the molecular level, genes associated with photosynthesis and tetrapyrrole metabolism are extensively downregulated under Fe deficiency [51.Rodríguez-Celma J. et al.The transcriptional response of Arabidopsis leaves to Fe deficiency.Front. Plant Sci. 2013; 4: 276Crossref PubMed Scopus (55) Google Scholar]. Accordingly, impairment of chlorophyll biosynthesis is the most prominent sign of Fe deficiency. Decreased mRNA levels are also reflected in reduced protein levels of abundant Fe proteins, such as Fd (especially Fd2), proteins of the Cyt b6/f complex, and enzymes of the S assimilation pathway [52.Hantzis L.J. et al.A program for iron economy during deficiency targets specific Fe proteins.Plant Physiol. 2018; 176: 596-610Crossref PubMed Scopus (16) Google Scholar]. Reduced accumulation of proteins of the [Fe–S] cluster assembly system, S mobilization A and B (SufA and SufB), presumably avoids the risk of forming incomplete [Fe–S] clusters, which are likely to accelerate the formation of the highly reactive hydroxyl radical in the Fenton reaction [52.Hantzis L.J. et al.A program for iron economy during deficiency targets specific Fe proteins.Plant Physiol. 2018; 176: 596-610Crossref PubMed Scopus (16) Google Scholar]. For the apoprotein SufA, the lack of Fe as cofactor may cause protein instability rather than decreased mRNA levels [52.Hantzis L.J. et al.A program for iron economy during deficiency targets specific Fe proteins.Plant Physiol. 2018; 176: 596-610Crossref PubMed Scopus (16) Google Scholar]. Disrupting the transfer of [Fe–S] clusters to their target proteins, such as Fd, triggers leaf Fe-deficiency responses and, interestingly, results in overaccumulation of Fe in the chloroplast [53.Zandalinas S.I. et al.Expression of a dominant-negative AtNEET-H89C protein disrupts iron-sulfur metabolism and iron homeostasis in Arabidopsis.Plant J. 2020; 101: 1152-1169Crossref PubMed Scopus (1) Google Scholar]. In the absence of Mn, the PSII supercomplexes are less stable [54.Schneider A. et al.The evolutionarily conserved protein PHOTOSYNTHESIS AFFECTED MUTANT71 is required for efficient manganese uptake at the thylakoid membrane in Arabidopsis.Plant Cell. 2016; 28: 892-910PubMed Google Scholar,55.Schmidt S.B. et al.Metal binding in photosystem II super- and subcomplexes from barley thylakoids.Plant Physiol. 2015; 168: 1490-1502Crossref PubMed Google Scholar]. A conceptual model explains the main events of Mn deficiency in PSII with Mn deficiency leading to reduced Mn binding in PSII complexes, which causes disintegration of PSII supercomplexes [56.Schmidt S.B. et al.Manganese deficiency in plants: the impact on photosystem II.Trends Plant Sci. 2016; 21: 622-632Abstract Full Text Full Text PDF PubMed Scopus (42) Google Scholar]. Consequently, the PSII core is increasingly affected by oxidative damage, which lowers PSII yield and eventually CO2 assimilation and biomass production [30.Schmidt S.B. et al.Photosystem II functionality in barley responds dynamically to changes in leaf manganese status.Front. Plant Sci. 2016; 7: 1-12Crossref PubMed Scopus (10) Google Scholar,54.Schneider A. et al.The evolutionarily conserved protein PHOTOSYNTHESIS AFFECTED MUTANT71 is required for efficient manganese uptake at the thylakoid membrane in Arabidopsis.Plant Cell. 2016; 28: 892-910PubMed Google Scholar]. To prevent those detrimental effects, plants are able to mobilize s
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