Photosynth Res DOI 10.1007/s11120-015-0154-5

REVIEW

Organization of chlorophyll biosynthesis and insertion of chlorophyll into the chlorophyll-binding proteins in chloroplasts Peng Wang1 • Bernhard Grimm1

Received: 30 January 2015 / Accepted: 30 April 2015 Ó Springer Science+Business Media Dordrecht 2015

Abstract Oxygenic photosynthesis requires chlorophyll (Chl) for the absorption of light energy, and charge separation in the reaction center of photosystem I and II, to feed electrons into the photosynthetic electron transfer chain. Chl is bound to different Chl-binding proteins assembled in the core complexes of the two photosystems and their peripheral light-harvesting antenna complexes. The structure of the photosynthetic protein complexes has been elucidated, but mechanisms of their biogenesis are in most instances unknown. These processes involve not only the assembly of interacting proteins, but also the functional integration of pigments and other cofactors. As a precondition for the association of Chl with the Chl-binding proteins in both photosystems, the synthesis of the apoproteins is synchronized with Chl biosynthesis. This review aims to summarize the present knowledge on the posttranslational organization of Chl biosynthesis and current attempts to envision the proceedings of the successive synthesis and integration of Chl into Chl-binding proteins in the thylakoid membrane. Potential auxiliary factors, contributing to the control and organization of Chl biosynthesis and the association of Chl with the Chlbinding proteins during their integration into photosynthetic complexes, are discussed in this review. Keywords Tetrapyrrole biosynthesis
Chloroplast biogenesis
Chlorophyll
Photosynthesis
Light-harvesting antenna complex
Chloroplast signal recognition particle & Bernhard Grimm [email protected] 1

Institute of Biology/Plant Physiology, Humboldt-University Berlin, Philippstraße 13, 10115 Berlin, Germany

Introduction Chlorophyll (Chl) biosynthesis is part of the tetrapyrrole metabolism, which also leads to the production of protoheme, siroheme, and phytochromobilin in photosynthetic eukaryotes and, additionally, phycobilins in cyanobacteria and red algae (Mochizuki et al. 2010; Tanaka et al. 2011; Tanaka and Tanaka 2007). Apart from its central role in the supply of essential cofactors and pigments, tetrapyrrole biosynthesis has recently received additional attention due to the proposed contribution of tetrapyrroles to the retrograde signaling between chloroplasts and the nucleus (Woodson and Chory 2008; Chi et al. 2013; Schlicke et al. 2014). Transcriptional and translational regulation meets the need of newly produced components of the tetrapyrrole metabolism in response to long-term developmental and environmental changes. However, research of the mechanisms of posttranslational control in Chl biosynthesis and its subsequent assembly into photosynthetic complexes is still in its infancy, although these processes are also essential for shortterm adjustments of Chl availability to the environmental changes (Czarnecki and Grimm 2012; Komenda et al. 2012; Nickelsen and Rengstl 2013). Unbalanced metabolic activities of tetrapyyrole biosynthesis lead to the accumulation of free Chl, and metabolic intermediates, which may trigger photodynamic damage upon light exposure (Apel and Hirt 2004). Therefore, posttranslational modifications of enzymatic activities, targeting, allocation, and proteolytic degradation of the enzymes in Chl biosynthesis, as well as the spatiotemporal organization of the synchronized supply of Chl and the synthesis of Chl-binding apoproteins deserve closer attention. Apart from posttranslational modifications of proteins involved in Chl biosynthesis, the importance of

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intracellular and suborganellar topology of biochemical pathways turned out to be essential for the regulation of gene expression and the activity of various metabolic reactions, including the biosynthesis of tetrapyrroles, lipids, and isoprenoids (Lunn 2007). Proteins are targeted to the defined intracellular compartments to play their roles in the regulation of metabolism, gene expression, or signal transduction (e.g., Haggie and Verkman 2002; Amato et al. 2011). However, intracellular topology is not only a matter of separating reactions by membranes, but also concerns other subcellular structures. Such structures are often transient and represent the enrichment of a specific set of macromolecules. The benefits of the formation of macromolecular protein complexes within the subcellular compartments are certainly conceivable for metabolism, gene expression, and other functions. Compartmentation and multiprotein complexes allow the concentration of distinct biochemical reactions and a separation of the antagonistic pathways, e.g., the assimilation and dissimilation of organic compounds in spatially separated cellular regions. This review acknowledges the first findings on protein– protein interactions in tetrapyrrole biosynthesis and draws attention to the possibility of the macromolecular protein complex formation for the Chl metabolism and the potential coupling of Chl biosynthesis and Chl utilization. The survey emphasizes the first potential regulatory proteins and auxiliary factors in Chl biosynthesis. These proteins are proposed to be required in the control of the metabolic substrate flow within tetrapyrrole biosynthesis and to bridge Chl metabolism with the assembly of Chl-binding proteins of the photosynthetic complexes.

Organization of tetrapyrrole biosynthesis in chloroplasts Tetrapyrrole biosynthesis is a conserved multi-branched metabolic pathway. Based on the key intermediates and the various end products, the tetrapyrrole biosynthetic pathway is divided into four main sections: synthesis of 5-aminolevulinic acid (ALA), the formation of protoporphyrin IX, the heme-synthesizing iron branch, and the Chlsynthesizing magnesium (Mg) branch. For an additional comprehensive survey of all metabolic steps of tetrapyrrole biosynthesis, including enzymes and metabolic intermediates, we refer to previous reviews, e.g., Tanaka et al. (2011). Although the biosynthesis of tetrapyrrole endproducts Chl and heme has been characterized long time ago, many aspects of the tetrapyrrole metabolism remained to be elucidated, such as the spatiotemporal organization of tetrapyrrole biosynthesis for adequate substrate channeling or the involvement of positive and negative regulators of transcription of genes involved in tetrapyrrole metabolism.

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Metabolic pathways are proposed to be organized in metabolons (Sweetlove and Fernie 2013; Jorgensen et al. 2005; Winkel 2004). By definition, these are multiprotein complexes, in which the assembly of co-operating proteins is coordinated to direct the transfer of metabolic intermediates from one enzyme to the next (metabolite channeling), to achieve high but not excessive local substrate concentrations, to sequester toxic intermediates and to suppress unwanted side reactions. Overall, these complexes ensure the increased efficiency of the metabolism by minimizing the diffusion-limited reaction steps. Although a metabolon for Chl biosynthesis has been proposed already 40 years ago (Shlyk 1971), the lack of suitable technologies in the past has hampered the elucidation of these organizational units. More recently, the initial proteomic analyses of plastid proteins allowed researchers to assign the enzymes of tetrapyrrole biosynthesis to the stroma and/or membrane fraction of chloroplasts (Joyard et al. 2009; Baginsky et al. 2010). The enzymes contributing to tetrapyrrole biosynthesis and their confirmed or hypothetical interactions to other proteins within the pathway are depicted in Fig. 1. The figure includes also certain regulatory and auxiliary factors. The water-soluble or weakly hydrophobic intermediates of tetrapyrrole biosynthesis are metabolites of enzymes that accumulate in the aqueous phase of chloroplasts. When the tetrapyrrole metabolites become more hydrophobic, the enzymatic reactions are performed by membrane-associated proteins (Fig. 1). Following the sequence of metabolic transformations in the tetrapyrrole biosynthetic pathway, protoporphyrinogen oxidase (PPOX) is likely the first enzyme associated with plastid membranes. Interestingly, several enzymes of the Chl-synthesis pathway are coincidently part of subproteomes of the envelope as well as the thylakoid membrane (Ferro et al. 2010). In respect to the significance of subcellular localization of tetrapyrrole biosynthesis, it is worth to mention that distinct portions of the two isoforms of PPOX were identified in the envelope and thylakoid membranes (Watanabe et al. 2001; Matringe et al. 1992). PPOX I was identified in the thylakoid and envelope membrane, whereas PPOX II was found in the envelope membrane. Two isoforms of ferrochelatase (FeCh) participate also in the successive enzymatic step following PPOX and direct protoporphyrin in the heme-synthesizing branch of tetrapyrrole biosynthesis (Chow et al. 1998). FeCh II is the dominant isoform in chloroplasts and FeCh I is proposed to be located also in the same organelle (Suzuki et al. 2002; Masuda et al. 2003b). A distinct plastidal localization of both FeCh isoforms could be reasoned by a diverse contribution of each isoform to heme biosynthesis. Then, it is suggested that both isoforms most likely supply heme to different sets of heme-dependent proteins. FeChI may be in charge of heme

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Heme

Phytochromobilin

FeCH

Inner envelope PPOX

CHLH

GUN4

Fe2+

ATP

ADP CHLI GUN4

CHLH

CHLG cpSRP54

YCF39

GGR LIL

?

DVR Phytyl-PP

FLU

FLU

Chl b

POR

cpSecY/E

CHL27

PPOX

Chl a

GGPP

CHLM

G

BP

BP

CHLD

AT

G

Pi

Mg2+

Glu-tRNA

YidC/ALB3

AA T

SA

R uT Gl

70S Ribosome mRNA

GS

G

Gl uT R

ADP

CPOX ATP

R uT Gl

POR

CHLI

UROS

YCF54

ALAD HMBS

UROD

ALA

Glu-tRNA

Gl uT R

Pi

Heme GSAAT

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CHLD

AT SA

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T AA GS

GSAAT

G

Siroheme

CHL27

TR lu G

R uT Gl

FLU?

YCF54

Glu-tRNA

CHLM

Glu-tRNA

CAO

Thylakoid Lumen

Fig. 1 Model of topological organization of tetrapyrrole biosynthesis and initial links for the successive insertion of Chl into the Chlbinding apoproteins in the thylakoid membrane. With reference to many previous publications on proteomics approaches and different subcellular fractionation studies, a model for the subcellular localization of the enzymes of tetrapyrrole biosynthesis in chloroplasts is proposed. Thereby, the hypothetical topology of the tetrapyrrole biosynthesis pathway in chloroplasts is exemplified with potential enzyme complexes in the stroma and the thylakoid membrane. The enzymes of the early steps of the pathway are mainly found in the stroma. The left part of the scheme illustrates the rate-limiting control step of 5-aminolevulinic acid (ALA) synthesis consisting of glutamyltRNA reductase (GluTR) and glutamate-1-semialdehyde aminotransferase (GSAAT) in light and dark. Thereby, the bulk activity of GluTR in angiosperms can be repressed by thylakoid-bound FLUORESCENT (FLU) in darkness. Regardless from dark repression of ALA, a minor portion of GluTR is proposed to ensure ALA synthesis devoid from light stimulus by binding to the thylakoid membrane via GluTR-binding protein (GBP) and a putative unknown membrane anchor protein. Due to the fragile and photosensitive nature of pyrroles and porphyrins, a loose protein complex of the successive enzymes ALA dehydratase (ALAD), hydroxymethylbilane synthase (HMBS), uroporphyrinogen III synthase (UROS), uroporphyrinogen III decarboxylase (UROD) and coproporphyrinogen III oxidase (CPOX) is envisioned to facilitate a untainted metabolic flow. Protoporphyrinogen IX oxidase (PPOX) is expected to be the first enzymes bound to both envelope and thylakoid membrane. Its enzymatic product, protoporphyrin IX is directed to Mg chelatase (consisting of the three subunits CHLH, CHLD, and CHLI) into the

Chl-synthesizing branch and to ferrochelatase (FeCh). FeCh isoforms are localized in the envelope and thylakoid membrane to provide heme for plastidic and extraplastidic heme-dependent proteins, respectively. Mg chelatase is stimulated by GUN4 and interacts with Mg protoporphyrin methyltransferase (CHLM), which releases the substrate to Mg protoporphyrin monomethylester cyclase, the successive enzyme most likely positioned in close proximity to the preceding enzyme. The cyclase is composed of several subunits, i.e., CHL27 and YCF54. A complex is proposed to be formed containing at least cyclase, POR and FLU. The terpenoid moiety of Chl is reduced by the geranylgeranyl reductase (GGR), which is stabilized in plants by light-harvesting-like protein (LIL3, here indicated by LIL). The final enzymes of the Mg branch pathway are divinyl reductase (DVR) and Chl synthase (CHLG) for Chl a formation and subsequently for Chl b synthesis Chl oxygenase (CAO). In cyanobacteria, CHLG was found in physical contact with the foldase YidC and cpSecY/E (chloroplast Sec translocase), but also with the auxiliary factors HLIP (high light-inducible protein, here also principally indicated by LIL) and YCF39, while indications for these potential protein–protein interactions with the plant homologous LIL proteins in plants are still lacking. At the end of Chl synthesis, the newly characterized Chl-binding complexes may assist in integration of plastid-encoded Chl-binding proteins, such as D1, into the thylakoid membrane and, most likely, in the insertion of Chl into the newly synthesized nascent chains of Chl-binding apoproteins. Additional abbreviations of enzymes, auxiliary factors, and metabolites: GGPP, geranylgeranyl pyrophosphate; Phytyl PP, phytyl pyrophosphate; ALB3, ALBINO3 in higher plants and its homologous protein YidC in bacteria, YCF39, hypothetical open-reading frame

synthesis for cytoplasmic, and more generally, extraplastidal heme-dependent proteins, while FeCh II might be responsible mainly for the heme supply of the plastid-localized proteins requiring heme. Based on crystal structure data of tobacco PPOX II and FeCh, their dimeric protein structures were modeled into a common protein complex (Koch et al. 2004), which ease substrate channeling into the heme pathway and could also contribute to heme synthesis for cytoplasmic heme by directing the protein to the cytoplasmic side of the envelope membranes.

However, heme biosynthesis in plant mitochondria consisting of the last two enzymatic steps, PPOX and FeCh, had been proposed almost 40 years ago (Porra and Lascelles 1968; Little and Jones 1976) and, although further substantial information is still missing, these previous reports can still not be entirely ignored. Besides the predominant plastid-localized heme synthesis, previous studies underscored the mitochondrial translocation of PPOX and FeCh (Chow et al. 1997; Lermontova et al. 1997). But mitochondrial targeting of these two isoforms has been

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challenged by other studies which raised doubts on mitochondrial heme synthesis as only very low FeCh activities in mitochondrial extracts were determined (Suzuki et al. 2002; Masuda et al. 2003b; Lister et al. 2001). The organello translocation experiments of FeCh precursor proteins ended in ambiguous results due to not very distinguished and promiscuous transit peptide sequences of the organellar-localized proteins, which enable uptake into mitochondria and chloroplasts. In conclusion, a clear experimental proof of the precise location of heme synthesis in different subcompartments of plastids and eventually in mitochondria awaits further elucidation (van Lis et al. 2005; Papenbrock et al. 2001; Woodson et al. 2013). Forthcoming studies will hopefully provide adequate and reliable evidence for the topology of the heme-synthesizing pathway in both organelles or exclusively in plastids. Another intriguing question concerns the structural diversity of the C-terminus of the two isoforms of plant FeCh. FeCh II possesses a light-harvesting Chl-binding (LHC) domain at the C-terminus, which may play a regulatory role for heme synthesis in photosynthetic plastids, rather than in heme synthesis for other cellular hemerequiring proteins (Sobotka et al. 2011). Studies on the possible physical interactions between enzymes and regulatory factors of Chl synthesis became an overarching scientific objective to scrutinize the structural complexity of the tetrapyrrole metabolism. These studies are intended to provide the prerequisite for future predictions of the structural organization of the entire metabolic pathway. The first protein–protein interactions of the pathway were indicated between glutamyl-tRNA reductase (GluTR) and glutamate-1-semialdehyde aminotransferase (GSAAT) by a partial chromatographic purification (Jahn et al. 1991). A cofractionation of these two enzymes was plausible, because their interaction would ensure a tight control of the rate-limiting ALA synthesis without the risk of a non-enzymatic transamination reaction (Grimm et al. 1991). Initial modeling merged the dimeric GSAAT (Sundberg et al. 1997) into the V-shaped structure of GluTR (Moser et al. 2001). A GluTR–GSAAT complex was subsequently confirmed at least from E. coli protein extracts and using the two purified recombinant enzymes by co-immune precipitation experiments (Luer et al. 2005). Interactions of both enzymes in plant ALA synthesis were not reported so far. For posttranslational control of the whole pathway, the rate-limiting enzyme GluTR interacts also with the negative regulator FLUORESCENT (FLU) (Meskauskiene et al. 2001) and with the membrane-associated GluTRBINDING PROTEIN (GBP) (Czarnecki et al. 2011). Both interacting proteins, FLU and GBP, assemble GluTR at the thylakoid membrane, most likely at different locations. Via interactions with GluTR, FLU inhibits ALA synthesis in

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response to accumulating protochlorophyllide (PChlide) in the dark (Meskauskiene et al. 2001), while GBP is suggested to preserve a certain quantum of GluTR activity to ensure residual synthesis of ALA molecules needed for heme synthesis, when the majority of ALA synthesis is repressed (Czarnecki et al. 2011). In angiosperms, the light-dependent PChlide reduction to chlorophyllide (Chlide) catalyzed by protochlorophyllide oxidoreductase (POR) is blocked in darkness leading to elevated levels of PChlide. A FLU–protein complex (Kauss et al. 2012) may sense the elevated steady-state levels of PChlide. Thus, at a certain threshold level of PChlide, ALA synthesis will be restricted to a basal activity by inactivation of GluTR through binding to FLU (Richter et al. 2010a). This view is supported by the fact that, GluTR together with POR isoforms and Mg protoporphyrin monomethylester cyclase could be co-immunoprecipated by FLU in darkness (Kauss et al. 2012). The importance of physical interactions is also demonstrated for the substrate-binding subunit CHLH of the Mg chelatase. Mg chelatase consists of three subunits CHLH, CHLI, and CHLD, which are assembled in an active complex in the stoichiometry 1:6:6 (Jensen et al. 1999). CHLH interacts with GENOME UNCOUPLED 4 (GUN4), which binds the substrate and product of the Mg chelatase reaction, protoporphyrin, and Mg protoporphyrin, respectively, and also exerts a stimulatory effect on the enzyme activity (Larkin et al. 2003). GUN4 stimulates Mg chelatase activity by interaction with CHLH at low Mg2? content (Larkin et al. 2003; Verdecia et al. 2005; Davison et al. 2005; Peter and Grimm 2009; Adhikari et al. 2009, 2011). Initial characterization of the huge 148 kDa CHLH subunit began with the dissection of the protein to define domains required for protein–protein interaction and binding of GUN4, CHLI, and CHLD (Adams et al. 2014). CHLH interacts also with the adjacent enzyme, Mg protoporphyrin methyltransferase (CHLM), resulting in a stimulation of the metabolic flow between the two enzymatic reactions (Hinchigeri et al. 1997). Moreover, CHLH was proposed to bind abscisic acid (Shen et al. 2006). This report launched a discussion on the potential ABA receptor function and involvement of Mg chelatase in ABA signaling (Muller and Hansson 2009; Tomiyama et al. 2014; Du et al. 2012). Apart from Mg chelatase, Mg protoporphyrin monomethylester cyclase is another enzyme formed by a protein complex. The enzyme resembles diiron carboxylate proteins, which consist of a catalytic subunit, a scaffolding subunit, and a reductase (Berthold and Stenmark 2003). The AEROBIC CYCLIZATION SYSTEM Fe-CONTAINING subunit (AcsF) (Pinta et al. 2002) is most likely the substrate-binding subunit. Subsequently, AcsF homologs were reported in many organisms, e.g., CHL27,

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XANTHA L, CRD1, ChlAI/CycI (Tottey et al. 2003; Rzeznicka et al. 2005; Moseley et al. 2000; Minamizaki et al. 2008; Peter et al. 2009). Recently, the Ycf54/LCAA (hypothetical chloroplast open-reading frame 54/LOW CHLOROPHYLL ACCUMULATION A) was described as a kind of scaffold protein that is required for Mg protoporphyrin monomethylester cyclase and interacts with CHL27 (Albus et al. 2012; Hollingshead et al. 2012). Another suborganellar localization of Chl-synthesis enzymes was reported for POR. In etiolated tissue, POR was found in the lipid structure of prolamellar bodies of etioplasts (Lutz et al. 1981). Plants possess generally two isoforms. Three POR-encoding genes in Arabidopsis thaliana are an exception. PORA accumulates in etiolated seedlings, while PORB is more continuously expressed. The Arabidopsis PORC gene is light induced. Thus, it is expected, due to the changes of membrane structure during plastid biogenesis, the POR isoforms contribute to different extent to the enzyme activity (Masuda et al. 2003a; Sperling et al. 1998). Ternary complex formation of Pchlide, POR, and NADPH is accepted, however, to which extent oligomerisation of multiple units of the complex exists is still up for debate (Yuan et al. 2012; Gabruk et al. 2015). The yeast two-hybrid and bimolecular fluorescence complementation approaches contribute to experimental evidences for interactions between two proteins. Physical interactions between two enzymes in Chl metabolism are the first hint for the organization of subcellular processes. As a subsequent methodological step in the elucidation of subcellular topology, it is proposed to examine the probability of larger protein complexes. Mass spectrometry analysis of elutes obtained from co-immune precipitation or affinity chromatography as well as analysis of cofractionation of proteins detected in blue native gel electrophoresis, sucrose density gradient ultracentrifugation or size exclusion chromatography allow prediction of proteins assembled in macromolecular complexes. The benefit of an association of proteins in macromolecular complexes ensures an easy metabolic flow among the enzymatic steps and prevents production of harmful side products. Thus, it is expected that the metabolism requires dynamic transient and/or stable interconnection among multiple protein complexes. A good example of a potential protein complex in tetrapyrrole biosynthesis is the proposed interaction among POR, CHL27, and FLU in a united protein assembly, which facilitates also feedback regulation of ALA synthesis (Kauss et al. 2012) (Fig. 1). Assuming that the late enzymatic steps are firstly assembled to prevent accumulation and leakage of photoreactive metabolites, and secondly, coordinated with the successive processes that make use of the tetrapyrrole end products, the attention is directed toward plausible connection of Chl-synthesizing enzymes with the membrane-

bound Chl-binding proteins to ease the delivery of Chl during the biogenesis and assembly of photosynthetic complexes (Haggie and Verkman 2002; Amato et al. 2011; Yang et al. 2011). Elucidation of regulatory mechanisms governing coupling of tetrapyrrole metabolism and assembly of photosynthetic protein complexes represents at present groundbreaking objectives of research on chloroplast biogenesis (Komenda et al. 2012). As introduced in the following chapters for future understanding on biogenesis of photosynthetic membranes, it is expected that these processes require auxiliary factors, which assist in the assembly of the Chl-synthesis enzymes or the Chl-binding proteins in close proximity to the sites of the formation of photosynthetic complexes in the thylakoid membrane. These proteins may either bind Chl or function as a hub for complex formation or an anchor for stable integration of proteins at and in the thylakoid membranes.

Auxiliary factors of the light-harvesting-like (LIL) proteins superfamily and the biogenesis of Chlbinding protein complex in chloroplast In both photosystem I and II, at least two types of Chlbinding proteins can be distinguished in respect to their function, genetic origin, and pigment composition. The first group includes the plastid-encoded Chl a-binding proteins, and among them the core antenna and reaction center proteins D1, D2, CP43, CP47, PsaA, and PsaB, while the second group consists of the nuclear-encoded light-harvesting Chl a/b-binding proteins (LHCPs), which are assembled in peripheral antenna complexes of the two photosystems (Umena et al. 2011; Amunts et al. 2007; Liu et al. 2004). LHCPs belong to the LHC superfamily and are derived from a protein containing a single transmembrane domain, which consists of a hydrophobic consensus sequence of at least 22 amino acid residues, known as the LHC domain. Then, this ancestral protein is evolved by duplication of the coding sequence of the entire protein, by fusion of the transmembrane domain with other gene sequences or deletion events (Green et al. 1991; Jansson 1994). The ancient ancestral LHC peptide domain presumably evolved to function as either a membrane anchor for binding photosynthetic pigments or for mediating protein–protein interactions (Takahashi et al. 2014; Tanaka et al. 2010; Li et al. 2000). The present members of the LHC protein superfamily are distinguished by the presence of one, two, three, or four hydrophobic transmembrane alpha-helix motifs. At least 30 different representatives belong to this protein LHC superfamily (Klimmek et al. 2006). Using the nomenclature as light-harvesting-like proteins (LILs), it is suggested to specify each member with the same abbreviation regardless of their previous

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designations given when these proteins have been described for the first time. Apart from the LHC proteins of photosystem I and II functioning as photosynthetic antenna complexes and the four-helix protein PSBS, at least ten additional representatives belong to the subgroup of LIL proteins, which are characterized by multiple functions and expression profiles (Klimmek et al. 2006; Engelken et al. 2010). One-helix proteins (OHPs) are found among all oxygenic phototrophs and were annotated as HLIP (high light-inducible proteins) or SCPs (small CAB-like proteins) in cyanobacteria (Funk and Vermaas 1999; Engelken et al. 2010; Klimmek et al. 2006; Hernandez-Prieto et al. 2011; Yao et al. 2012; Storm et al. 2008; Yao et al. 2007) and their abbreviations were originally kept in previous reports (Andersson et al. 2003; Garczarek et al. 2003; Jansson et al. 2000). The cyanobacterial HLIPs/SCPs are proposed to be involved in an impressive number of different functions, such as in photoprotection (Wang et al. 2008), in the assembly and repair of photosystem II (Promnares et al. 2006; Vavilin et al. 2007; Yao et al. 2007; Wang et al. 2008; Hernandez-Prieto et al. 2011; Sinha et al. 2012), in regulation of tetrapyrrole biosynthesis (Yao et al. 2012; Xu et al. 2002), and as auxiliary factor facilitating integration of Chl into Chl-binding proteins (Chidgey et al. 2014; Knoppova et al. 2014). More detailed analyses are required to work out the functional mechanism to assign the primary function of OHPs/HLIPs. Initially, it was hypothesized that HLIPs/ SCPs function in the biogenesis and photoprotection of photosynthetic complexes. The more recent studies draw our attention more on OHP action as a scaffold protein, which organizes the assembly of Chl-binding proteins and insertion of Chl into Chl-binding proteins (Chidgey et al. 2014; Knoppova et al. 2014). HLIPs/SCPs were also proposed to interact with Chl-synthesis enzymes and affect metabolic activities in the tetrapyrrole biosynthesis pathway at the rate-limiting step of ALA synthesis (Chidgey et al. 2014). Pull-down experiments with cyanobacterial extracts using Ycf39, a putative assembly factor of photosystem II, as a bait, revealed the connection to Chl synthase (CHLG), the HLIP isoform HliD, the foldase YidC (homolog of ALB3, see below), ribosomal proteins, and the translocase SecY (Knoppova et al. 2014). Chidgey et al. (2014) also described an enzymatically active complex comprising CHLG, HliD, and the other components, such as Ycf39 and YidC. These findings imply a close connection of late steps of Chl synthesis and function of the Ycf39–HliD complex involved in the assembly of Chlbinding proteins. It was proposed that these interactions facilitate the integration of Chl into photosynthetic proteins, at least during cotranslational translocation of the D1 protein (Knoppova et al. 2014).

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OHP/HLIP homologs exist also in higher plants and are also indexed as LIL2 and LIL6 (Klimmek et al. 2006). In comparison to their cyanobacterial homologs very little is known about their function in plants (Heddad and Adamska 2002; Andersson et al. 2003). At present, it is tentatively proposed that the plant OHP homologs may also be involved in similar processes in thylakoid membranes as the HLIPs/SCPs in cyanobacteria. Early light-inducible proteins (ELIPs, LIL1) were reported almost 30 years ago and initially described as a transiently inducible gene family during de-etiolation (Grimm and Kloppstech 1987; Kloppstech 1985). ELIPs turned out to function during different stress conditions, such as high light, low temperature, low oxygen, etc. ELIPs possess three transmembrane helices, similar to LHC proteins. Because evidence for Chl binding to ELIP was reported (Adamska et al. 1999), it was conceivable to suggest the participation of ELIPs in the control of Chl biosynthesis (Tzvetkova-Chevolleau et al. 2007). While the connection of LIL proteins between photosynthetic subunits of both photosystems and Chl biosynthesis has not been directly shown in the past, the physical interactions of LIL3 proteins in plants and HLIPs in cyanobacteria to single proteins have been more recently addressed and ultimately verified the requirement of these LIL proteins either for the functioning of the Chl metabolism or the stability of Chl-binding proteins. Two paralogs of LIL3 exist in Arabidopsis, which belong to the LIL-protein subfamily. These proteins contain two membrane-spanning helices and are found exclusively in photoautotrophic eukaryotes. More recently, the lil3:1/lil3:2 double mutant was shown to be unable to accumulate phytylated Chl (Tanaka et al. 2010). The double mutant contains a low content of geranylgeranyl (GG) reductase (CHLP), which catalyzes the reduction of the GG moiety of Chl. LIL3 and CHLP interact with each other. In addition to the low content of CHLP, the lil3:1/lil3:2 mutant contains also decreased levels of POR (M Rothbart, unpublished results). Additionally, the LIL3-containing fractions of barley etiochloroplasts contain protochlorophyll (Reisinger et al. 2008). These results led to the conclusion that LIL3 action simultaneously contributes to the stability of Chl-synthesis enzyme(s), binds perhaps Chl precursors, and is important for the association of Chl to apoproteins of the two photosystems during the integration process into the thylakoid membrane. Following the hypothesis that LIL3 binds Chl, it could act as a donor synthesized for nascent plastid-encoded Chl a-binding proteins, as well as LHCPs (Takahashi et al. 2014). Consequently, LIL3 might play an important role in the final steps of Chl synthesis, but also for the assembly of Chl into the proteins of the photosystems and their antenna complexes.

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Future intensive studies are required to explore the role of LIL3 for the entire Chl biosynthesis pathway. It will hopefully elucidated, whether LIL3 stabilizes other enzymes of Chl synthesis and facilitates the mutual interdependence between other proteins of the Mg branch, apart from interaction with CHLP (Tanaka et al. 2010). LIL3 accumulates in at least two high molecular weight complexes (Tanaka et al. 2010). These finding suggests that this protein is a component of different protein complexes comprising CHLP and possibly other proteins. It remains to be elucidated whether LIL3 may form a central hub in the thylakoid membrane for transient contact with enzymes of Chl synthesis. Hypothetically, LIL3 function may rely on facilitating a dynamic metabolite channeling, as well as supplying Chl for the assembly with proteins of the photosynthetic complexes. It is not obvious whether LIL3 operates as a monomer, but most likely as an oligomeric unit, as suggested (Takahashi et al. 2014). However, whether and how different enzymes of Chl synthesis may interact with LIL3 at the same time or successively is still entirely elusive. At present, similar binding motifs of enzymes in Chl synthesis and Chl-binding proteins of the two photosystems could not be detected for the contact with LIL3. Further on, it will be attractive to elaborate, whether LIL3 binds Chl and/or its precursors and assists in direct substrate channeling by interim binding between the successive enzymatic steps. This view would favor a dynamic protein complex of LIL3 with proteins in Chl synthesis for optimized catalytic reactions and transfer of the respective product to the adjacent enzyme.

Additional auxiliary factors assisting the assembly of Chl into Chl-binding proteins of photosystems Another group of partners interacting with the enzymes of the Chl metabolism is the family of tetratricopeptide repeat (TPR) domain-containing proteins. A first representative was reported in Synechocystis PCC 6803.The TPR protein Pitt (POR-interacting TPR protein) interacts with the lightdependent POR and was shown to be closely connected to the photosystem II assembly network (Schottkowski et al. 2009). As an integral membrane protein, Pitt may function in the positioning of photosynthetic proteins in the thylakoid membrane, and in anchoring these proteins in the membrane-associated protein complexes. The primary structure of a TPR motif consists of a sequence of 34 amino acid residues and was found to be present in all organisms analyzed so far (Blatch and Lassle 1999; Allan and Ratajczak 2011). One TPR motif is composed of two antiparallel a-helices and the tandem arrangement of 3–16 motifs establishes a cleft for the physical interaction among proteins. These structural properties enable TPR proteins to

form protein complexes (D’Andrea and Regan 2003). Thus, proteins with TPR domains have been found in molecular chaperone complexes, transport complexes, cell cycle, and transcription control complexes. FLU (carrying three TPR motifs) and Ycf3 (hypothetical chloroplast open-reading frame 3 with three TPR motifs) (Naver et al. 2001) belong to the well-known plastid-localized TPR domain-containing proteins. Ycf3 is required in photosystem I assembly (Naver et al. 2001). Thioredoxins (TRX) and NADPH-thioredoxin reductase C (NTRC) belong also to essential regulatory factors assisting in control and organization of Chl biosynthesis and contributing most likely to the assembly and integration of Chl-binding proteins into the thylakoid membrane. These reductants are plastid-localized, interact with several enzymes of Chl biosynthesis (Ikegami et al. 2007; Luo et al. 2012; Richter and Grimm 2013), and affect their stability, activity, and organization of the Chl metabolism during changes in the redox state of chloroplasts (Richter and Grimm 2013). The protein–protein interactions between the enzymes of Chl synthesis and either TRX or NTRC were demonstrated by yeast 2-hybrid and bimolecular fluorescence complementation (BIFC) experiments. Deficiency of NTRC correlates with reduced stability of these enzymes, while reducing conditions in the chloroplasts stimulate these enzymes activities, most likely by opening the inter- and intramolecular disulfide bonds. Furthermore, the three m-type TRXs (TRX m1, m2, and m4) interact with the multiple Chl-binding proteins of photosystem II, including D1, D2, CP47, and LHC subunits, and are specifically involved in the assembly process of the photosystem II complex (Wang et al. 2013). These findings lead to the suggestion that TRX and NTRC have important functions at the interface between Chl biosynthesis and the subsequent incorporation of Chl into Chl-binding proteins of photosystem II.

Coordination of Chl biosynthesis with the cpSRPdependent cotranslational and posttranslational targeting of Chl-binding apoproteins to the thylakoid membrane For the biogenesis of the multi-subunit complexes of photosystem I and II, the Chl-binding proteins have to be transferred from the site of their synthesis, regardless of whether the proteins are derived from nuclear or plastidal genomes, to the thylakoid membranes, where assembly of the pigment–protein complexes takes place (Jarvis and Lopez-Juez 2013). In analogy to the signal recognition particle (SRP) complex in prokaryotes and eukaryotes, a similar SRP (cpSRP) pathway was identified in the chloroplasts of green algae and plants. The cpSRP complex

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performs the cotranslational and posttranslational targeting and integration of Chl-binding apoproteins into the thylakoid membrane (Aldridge et al. 2009; Richter et al. 2010b). The cpSRP54 chloroplast homolog of the evolutionarily conserved SRP54 component is associated with the 70S ribosomes to target cotranslationally the nascent chain of plastid-encoded Chl a-binding proteins to the chloroplast SRP insertase/translocase YidC/ALB3 and secretory translocase cpSecY, which ultimately finalize the insertion of the protein into the thylakoid membrane (Nilsson and van Wijk 2002; Pool 2005; Richter et al. 2010b). The posttranslational transport of nuclear-encoded LHCPs also relies on the cpSRP transport pathway. Surprisingly, the cpSRP system in higher plants lacks the functional SRP RNA moiety, and instead, a chloroplast-specific cpSRP43 subunit functions in the posttranslational targeting of LHCPs (Nussaume 2008; Rosenblad and Samuelsson 2004; Trager et al. 2012; Richter et al. 2008). After import of the precursor LHCPs into plastids and proteolytic cleavage of the transit peptide, mature LHCPs are bound by the heterodimeric cpSRP43–cpSRP54 complex to form a transit complex, which keeps the hydrophobic LHCPs in insertion-competent conformation (Schu¨enemann et al. 1998; Li et al. 1995). The transit complex is targeted to the thylakoid membrane via the interaction with SRP receptor cpFtsY and the chloroplast SRP translocase ALB3, and form the transient insertion complex at the stromal side of the thylakoid membrane (Tu et al. 1999; Moore et al. 2003; Bals et al. 2010; Falk et al. 2010). Ultimately, upon cpSRP54- and cpFtsY-triggered GTP hydrolysis, LHCPs are released from the transient transfer complex to ALB3, which assists the protein folding and insertion into the thylakoid membrane (Hoffman and Franklin 1994; Moore et al. 2000). Meanwhile, the cpSRP43–cpSRP54 complex departs from the thylakoid membrane to stroma for the next targeting processes. While the posttranslational targeting of LHCPs, including their proper folding and stable insertion into the thylakoid membrane, have been intensively explored by in vivo and in vitro studies (Eichacker et al. 1996; Plumley and Schmidt 1995; Kim et al. 1991; Kuttkat et al. 1997; Mu¨ller and Eichacker 1999), very little is known about the spatiotemporal assembly of Chl molecules into the Chlbinding proteins during the thylakoid integration (Nickelsen and Rengstl 2013; Komenda et al. 2012; Richter et al. 2010b; Aldridge et al. 2009; Hoober and Eggink 1999). Mutants lacking components of the cpSRP pathway show a pale-green or albino phenotype and greatly reduced accumulation of pigments (Pilgrim et al. 1998; Amin et al. 1999; Klimyuk et al. 1999; Hutin et al. 2002; Sundberg et al. 1997). These observations were based on the functional deficiency of the cpSRP system, but could be due to

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the direct attenuation of Chl biosynthesis. Because these mutants do not demonstrate photodynamic damage as a result of accumulation of free Chl, a reduced ALA synthesis can be suggested, which points to a possible direct interaction of the cpSRP pathway components with the Chl biosynthesis pathway (Pilgrim et al. 1998; Amin et al. 1999; Klimyuk et al. 1999; Hutin et al. 2002; Sundberg et al. 1997). However, the involvement of cpSRP components and their potential regulatory roles at the early steps of tetrapyrrole biosynthesis remains to be established. It was suggested that cpSRP54 might be involved in the accumulation of carotenoids in higher plants (Yu et al. 2012). Thus, an additional role of cpSRP components seems to be plausible in balancing carotenoid and Chl synthesis.

Conclusion Functional analyses of the biogenesis of protein complexes involved in the synthesis of Chl and Chl-binding proteins for the formation of thylakoid-embedded photosystems have been hampered in the past because of the sophisticated biogenesis mechanisms as well as inadequate methods to explore these processes. However, the low stability of many protein complexes is not only a technical nuisance, but an important hallmark, indicating their transient and highly dynamic nature, when apoproteins are assembled with cofactors and pigments and united into an assembly pathway for the completion of the photosynthetic complexes. Thereby, the protein complex composition can rapidly change when metabolic requirements alter and metabolites are allocated in varying amounts to branched pathways which are located in different subcompartments. In consequence, multiple posttranslational control mechanisms of the participating proteins likely perpetually modify these protein complexes. It is expected that the pioneering work of the Komenda group (Komenda et al. 2012, Chidgey et al. 2014, Knoppova et al. 2014) will be continued and taken up by several research groups to fill the gap of knowledge with regard to the coordination and topology of Chl synthesis and assembly of Chl-binding proteins. The dynamic metabolons for Chl and carotenoids synthesis are tentatively merged into supercomplexes. It is expected that the new proteins, required for protein interactions, such as chaperones, anchor proteins and other regulatory factors for the assembly of protein complexes in defined subcellular compartments, will be identified. It is one of the hypotheses explaining the efficient delivery of Chl to the Chl-binding apoproteins that the final steps of Chl biosynthesis occur in close proximity to the sites of protein synthesis and/or the membrane insertion machinery for Chl-binding proteins. This concept has to be explored in future. However, the

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risk of releasing unbound phototoxic Chls would be minimized, which otherwise might be triggering the formation of reactive oxygen species (Apel and Hirt 2004). The first evidences supporting this hypothesis was provided by Chidgey et al. (2014) and Knoppova et al. (2014) in cyanobacteria. These data supports the view that a protein supercomplex comprising at least CHLG, ribosome subunits, and translocon components, exists at the stromal side of the thylakoid membrane. Such supercomplex would facilitate the integration of newly synthesized Chls into the apoproteins of plastid-encoded Chl a-binding proteins (Sobotka 2014). In comparison to the reported processes in cyanobacteria, the diverse origin of the nuclear and plastidencoded Chl-binding proteins may enhance the complexity of the integration and assembly mechanisms with photosynthetic pigments in eukaryotes. Therefore, it cannot be excluded that other Chl-synthesizing enzymes and other components of the cpSRP43/cpSRP54/cpFtsY machinery are constituents of the protein complex essential for the biogenesis of photosynthetic complexes. With the concept that a transient Chl-binding protein complex exists in the chloroplast, it’s worth to address the question whether special zones exist in chloroplast to support the formation of the Chl-binding protein complex. Recently, a PratA-defined membrane (PDM) in cyanobacteria has been suggested to favor the insertion of Chl into the photosystem II subunits (Rengstl et al. 2011; Schottkowski et al. 2009). The Chl precursors and Chl-synthesis enzymes were found in the PDMs (Rengstl et al. 2011). On the other hand, a discrete region near the pyrenoid in Chlamydomonas has been identified as the ‘‘translation zone’’ (T-zone) that functions as a privileged site for the synthesis of plastid-encoded photosystem II subunits (Nickelsen and Zerges 2013; Schottkowski et al. 2012; Uniacke and Zerges 2007, 2009). The newly synthesized photosystem II subunits will assembly into photosystem II subcomplexes and move by lateral diffusion into the thylakoid lamella (Schottkowski et al. 2012). In this context, the compartmentalization of Chl synthesis and Chl assembly could be envisioned in cyanobacteria and green algae, and even in higher plants. Ultimately, it is worth mentioning that work on these biogenesis processes has just been taken up and the significance of the subcompartmental localization of the tetrapyrrole synthesizing enzymes present in the membranaceous phase or in soluble complexes, has been acknowledged only quite recently. It is expected that the appropriate technologies will facilitate studying of these aspects of tetrapyrrole biosynthesis and photosystems biogenesis. Acknowledgments This work was supported by a grant of the Deutsche Forschungsgemeinschaft given to BG in the framework of

the Priority Program 1710 (Dynamics of Thiol-based Redox Switches in Cellular Physiology). We thank Pawel Brzezowski, Andreas Richter and Boris Hedtke for critically reading the manuscript. No conflict of interest declared.

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