Deg/HtrA proteases as components of a network for photosystem II quality control in chloroplasts and cyanobacteria

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Research in Microbiology 160 (2009) 726e732

Deg/HtrA proteases as components of a network for photosystem II quality control in chloroplasts and cyanobacteria Pitter F. Huesgen1, Holger Schuhmann, Iwona Adamska* Department of Plant Physiology and Biochemistry, University of Konstanz, Universita¨tsstrasse 10, D-78457 Konstanz, Germany Received 9 July 2009; accepted 11 August 2009 Available online 2 September 2009

Abstract Organisms that perform oxygenic photosynthesis are subjected to photoinhibition of their photosynthetic function when exposed to excessive illumination. The main target of photoinhibition is the D1 protein in the reaction center of the photosystem II complex. Rapid degradation of photodamaged D1 protein and its replacement by a de novo synthesized functional copy represent an important repair mechanism crucial for cell survival under light stress conditions. This review summarizes the literature on the ATP-independent Deg/HtrA family of serine endopeptidases in cyanobacteria and chloroplasts of higher plants, and discusses their role in D1 protein degradation. We propose that Deg/HtrA proteases are part of a larger network of enzymes that ensure protein quality control, including photosystem II, in plants and cyanobacteria. Ó 2009 Elsevier Masson SAS. All rights reserved. Keywords: Deg/HtrA protease; Chloroplast; Photosystem II; Synechocystis 6803

1. The family of Deg/HtrA proteases: a general overview Deg/HtrA proteases are ATP-independent serine endopeptidases that are found in almost all domains of life, including Bacteria, Archaea and Eukarya. The first member from the Deg/HtrA family was discovered in Escherichia coli and named after the null mutant phenotypes DegP (for degradation of periplasmic proteins) [66] or, alternatively, HtrA (for the high temperature requirement A) [46]. Deg/HtrA proteases belong to the S1B subfamily of the clan PA according to the MEROPS nomenclature [55], and feature a catalytic domain of the trypsin type with His-Asp-Ser as a catalytic triad. Most Deg/HtrA family members contain C-terminally located PDZ domains, which regulate proteolytic activity [25,32,50,70] and are necessary for the formation of functional oligomeric complexes [25,34,59].

* Corresponding author. Tel.: þ49 7531 88 2561; fax: þ49 7531 88 3042. E-mail addresses: [email protected] (P.F. Huesgen), holger. [email protected] (H. Schuhmann), [email protected] (I. Adamska). 1 Present address: Center for Blood Research, University of British Columbia, 2350 Health Sciences Mall, Vancouver, BC, Canada V6T 1Z3. 0923-2508/$ - see front matter Ó 2009 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.resmic.2009.08.005

Deg/HtrA proteases are best studied in E. coli and mammals, where three (DegP/HtrA, DegQ/HhoA and DegS/HhoB) or five (HtrA1-4 and Tysnd1) of these enzymes are present, respectively. Structural studies showed that Deg/HtrA proteases form oligomeric complexes, with a trimer as the basic unit [41,44,70]. DegP/HtrA from E. coli forms a very compact, proteolytically inactive hexameric complex, where two homotrimers are stacked in a face-to-face manner [41]. Activation of DegP/HtrA, either allosterically by interaction of peptides with its PDZ1 domain [42,50] or a shift to higher temperatures [65], triggers an assembly into higher oligomeric structures. In solution, DegP/ HtrA assembles around its substrates into large spherical 12- or 24-mers, composed of 4 or 8 homotrimers, respectively [33,43]. On lipid membranes, E. coli DegP/HtrA forms bowl-shaped structures, independent of the substrate, each with a 4-, 5-, or 6fold symmetry with a trimer as the basic structural unit [61]. Also, human HtrA2/Omi [44] and E. coli DegS/HhoB [70] form homotrimers, but in contrast to E. coli DegP/HtrA, no further oligomerization of the basic trimers into higher order structures has been reported. An intriguing feature of Deg/HtrA proteases is their functional versatility: DegP/HtrA in E. coli has been demonstrated to act as a chaperone or as a protease in a temperature-dependent

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manner, providing quality control of protein folding in the periplasm [9,65,66]. E. coli DegS/HhoB, on the other hand, is a highly specialized enzyme with a single known physiological substrate. DegS/HhoB is activated in response to the accumulation of misfolded proteins in the periplasm, which is a first step in the signal transduction cascade that triggers a stress response in the cytoplasm [13]. Deg/HtrA proteases are involved in responses to various stress conditions. In many bacteria, including E. coli, protease DegP/HtrA is required for survival at elevated temperatures and participates in the response to oxidative stress (reviewed in [9,39,64]), while human HtrA2/Omi [69] and the yeast ortholog Nma111p [14] have been implicated in apoptosis. Human Deg/ HtrA proteases have been shown to play critical roles in severe diseases such as Alzheimer’s disease, age-related macular degeneration and several cancers (reviewed in [69]). Less is known about Deg/HtrA proteases in photosynthetic organisms, including cyanobacteria and higher plants. The aim of this review was to provide a short summary on Deg/HtrA family members in cyanobacteria and their orthologs in chloroplasts of higher plants, with the main focus on their role in photosystem II (PSII) quality control. 2. Deg/HtrA proteases in cyanobacteria All cyanobacteria investigated thus far contain between two and five Deg/HtrA proteases [26]. The only cyanobacterial orthologs studied in some detail are the three family members from Synechocystis sp. PCC 6803 (hereafter Synechocystis 6803), named HtrA (htrA, slr1204), HhoA (hhoA, sll1679) and HhoB (hhoB, sll1427) in analogy to the E. coli enzymes [35]. In contrast to DegP/HhoA and DegQ/HhoA from E. coli that contain two PDZ domains, all three Deg/HtrA proteases from Synechocystis 6803 possess only one [26,39]. Sequence similarity suggested that the HtrA, HhoA and HhoB from Synechocystis 6803 are more closely related to each other than to proteases with the same names present in other organisms [26]. Inference of functions and mechanisms due to the same protease name should therefore be treated with great caution. Proteome analysis found HtrA located in the outer membrane of Synechocystis 6803 [24] and HhoA in the periplasm, both in soluble [16] and in plasma membrane-bound [23] forms. The location of HhoB has not yet been experimentally proven, but this protease is predicted to target to the periplasm [39]. The Deg/HtrA proteases from Synechocystis 6803 have been proposed to be involved in response to light stress [17,62] and to play a role in the maintenance of the extracytoplasmic space, including soluble periplasmic proteins and intrinsic membrane proteins with periplasm-exposed loops, under heat and light stress [7,25]. However, physiological substrates of cyanobacterial Deg/HtrA proteases have not yet been identified. Biochemical characterization of HhoA from Synechocystis 6803 showed that its proteolytic activity increased with temperature and basic pH and was stimulated by the addition of Mgþ2 and Caþ2 [25]. The single PDZ domain of HhoA


played a critical role in regulating protease activity and in the assembly of a homohexameric complex, in contrast to E. coli DegP/HtrA, where these functions were attributed to two PDZ domains [32,34]. Deletion of the PDZ domain strongly reduced, but did not abolish, proteolysis of sterically challenging substrates by Synechocystis 6803 HhoA protease [25]. 3. Deg/HtrA proteases in chloroplasts of higher plants The chloroplasts of green algae and higher plants have evolved from a cyanobacterial ancestor by endocytobiosis and still share many features with modern cyanobacteria, including the photosystem reaction center complexes [49]. Therefore, it is not surprising that the vast majority of proteases found in chloroplasts of green algae and higher plants are also derived from the prokaryotic ancestor [1,28,56]. An initial survey of the genome of Arabidopsis thaliana identified 13 Deg protease-encoding genes [1]. Later studies extended this number to sixteen genes [26,64]. Of these sixteen proteases, four are located in the chloroplasts. Deg1 (At3g27925), Deg5 (At4g18370) and Deg8 (At5g39830) of A. thaliana have been found to be attached to the luminal side of the thylakoid membrane [31,54,60], whereas Deg2 (At2g47940) is attached to the stromal side [20]. Deg1 had been identified as a housekeeping protease in the thylakoid lumen, degrading mistargeted and misfolded proteins in this compartment [8,31]. Plastocyanin and the 33 kDa protein of the oxygen evolving complex were identified as potential luminal substrates in vitro [8]. Size exclusion chromatography indicated that recombinant Deg1 was present in monomeric and homohexameric forms, both proteolytically active [8]. More recent studies revealed that Deg5, which lacks a PDZ domain, and Deg8 form a heterohexameric complex in a 1:1 stoichiometry [67]. Interestingly, recombinant Deg8 alone was proteolytically active, whereas recombinant Deg5 showed no enzymatic activity [67]. Studies on Deg2 demonstrated that this protease is peripherally associated with the non-appressed regions of the thylakoid membrane (e.g., stroma lamellae and grana margins and ends) and accumulates in response to high salt concentration, desiccation and light stress [20]. All three lumenal Deg proteases, Deg1, Deg5 and Deg8, and the stromal-side thylakoid-associated Deg2 were reported to participate in degradation of the photodamaged D1 protein at both sides of the thylakoid membrane [20,37,67,68]. 4. PSII quality control under stress conditions Organisms that perform oxygenic photosynthesis are subjected to inhibition of their photosynthetic functions when exposed to excessive light. This process is referred to as photoinhibition [4]. At ambient temperatures, the major target of photoinhibition is the PSII complex located in the thylakoid membrane and, in particular, its D1 reaction center protein. The D1 protein binds many of the cofactors involved in the primary and secondary electron flow and is therefore prone to irreversible oxidative damage by either reactive oxygen species or highly oxidizing species generated within PSII [4].


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Fig. 1. Schematic representation of the D1 protein and its observed degradation fragments in higher plants. The D1 protein from the PSII reaction center has five transmembrane a-helices (helices A-E) connected by stromal and luminal loops. The fragmentation of photodamaged protein occurs in the stroma-located DE loop and lumen-located AB- and CD-loops generating N-terminal and C-terminal proteolytic fragments of different sizes ([12,26,38], and references within). Experimentally proven fragments generated by Deg1 [37], Deg2 [20] and Deg5/8 [67] are marked by asterisks. Figure modified from [26].

This leads to conformational changes in the structure of the D1 protein [21] followed by its rapid degradation [4,5]. The degradation of photodamaged D1 protein and its replacement by a de novo synthesized functional copy represent an important repair mechanism essential for cell survival under stress conditions [4,12]. Although D1 protein turnover occurs in plants [5] and in cyanobacteria [18], it remains unclear whether the PSII repair mechanism is evolutionarily conserved in both taxonomic groups. Considerable efforts have been directed towards identification of protease(s) responsible for degradation of photodamaged D1 protein [4,12]. Biochemical characterization of the proteolytic process, studies with recombinant proteases and characterization of protease knock-out mutants led to the proposal of several pathways for the degradation of photodamaged D1 protein. A specific degradation of D1 protein by (a) cleavage on the stromal side by Deg2 protease [20], (b) cleavage at the lumenal side by Deg1 protease [37] and the Deg5/Deg8 protease complex [67], and (c) the processive FtsH protease complex [6,40,57], were suggested. In addition, D1 protein is also degraded together with neighboring proteins of the PSII reaction center after formation of intermolecular cross-links [51,53,71]. In the following paragraphs, we briefly discuss evidence for each proteases implicated in D1 turnover in the context of the historically suggested models of D1 degradation. Finally, we propose that degradation of the D1 protein is not a specialized process mediated by a few enzymes, but rather, is the effect of a complex protease network that removes damaged proteins from the thylakoid membrane.

4.1. Degradation of photodamaged D1 protein from PSII reaction center Based on the crystal structure of PSII, the D1 protein in cyanobacteria [74] and higher plants [19] has five transmembrane a-helices (named A to E) connected by cytoplasmic/stromal and lumenal loops (Fig. 1). Early biochemical studies suggested that photodamaged D1 protein is cleaved at distinct sites within soluble loops [4,5], and this is followed by secondary proteolysis of primary cleavage products [45]. 4.1.1. Fragmentation of photodamaged D1 protein by Deg proteases After the genome of A. thaliana was fully sequenced, candidate proteases for these functions were identified and tested in vitro using purified recombinant enzymes. These in vitro studies suggested that the ATP-independent Deg2 serine protease (originally named DegP2) cleaved photodamaged D1 protein selectively in the stroma-exposed DE loop [20], generating N-terminal 23 kDa and C-terminal 10 kDa fragments (Fig. 1). The 23 kDa fragment was removed by secondary proteolysis by the ATP-dependent zinc metalloendopeptidase FtsH1 located within the thylakoid membrane [45]. However, isolated homozygous deg2 knock-out mutants of A. thaliana showed no obvious phenotype and had normal D1 protein turnover under light stress conditions [27] suggesting that participation of this enzyme is not essential in vivo. Recently, A. thaliana deg1 knockdown mutants were shown to be more sensitive to photoinhibition than the wild type. These plants accumulated higher amounts of full-length

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Fig. 2. Schematic summary of published data and historic models for the degradation of photodamaged D1 protein. The yellow oval represents the core complex of PSII, containing either intact (dark green), damaged (white or light gray) or newly synthesized (light green) D1 and D2 proteins. The gray bar represents the thylakoid membrane and small red bars intramolecular covalent cross-links. Proteases implicated in different degradation pathways and corresponding references are shown in black and blue for in vivo evidence in A. thaliana and Synechocystis 6803, respectively, and red and light gray for in vitro experiments with recombinant proteases or protease-enriched extracts from higher plants or cyanobacteria, respectively. Position above or below the membrane indicates a subcellular location in the higher plant stroma/cyanobacterial cytoplasm or in the thylakoid lumen, respectively. Symbol # refers to C. Funk, P.F. Huesgen, I. Adamska, unpublished observations. [For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.]

photodamaged D1 protein and less of its 16 kDa and 5.2 kDa C-terminal degradation products (Fig. 1), thus demonstrating a significant contribution of limited proteolysis in the lumenexposed CD-loop to the degradation of the D1 protein in vivo [37]. The differential abundance of both D1 fragments suggests that the 5.2 kDa fragment might derive from further degradation of the 16 kDa peptide. Similar studies with deg5 and deg8 knock-out mutants and a deg5/deg8 double mutant clearly demonstrated participation of these proteases in D1 protein degradation under high light and high temperature conditions [67,68]. The Deg5/Deg8 protease complex cleaved photodamaged D1 protein within the luminal CD-loop, generating N-terminal 16 kDa and C-terminal 18 kDa proteolytic fragments [67]. Fragmentation of the hydrophobic D1 protein at stromal and luminal sides by Deg proteases, and possibly additional stromal proteases, might be important for efficient degradation of these fragments (transmembrane helices) by, e.g., the FtsH protease complex that can degrade its substrate progressively from either the free N- or C-terminus [30]. Several knock-out mutants have been generated by different research groups to understand the function of Deg/ HtrA proteases in Synechocystis 6803 [7,17,62,64]. A triple mutant, with all three Deg/HtrA proteases deleted, showed degradation of D1 protein in pulse-chase experiments under light stress conditions, and no breakdown/fragmentation products were detected [7]. This suggested that under conditions tested, the participation of Deg/HtrA proteases is not necessary for degradation of photodamaged D1 protein. However, partial purification of a fragment generating

proteolytic activity indicated that, in cyanobacteria as well, a Deg/HtrA protease might cleave photodamaged D1 protein [36]. It remains to be further investigated whether fragmentation of damaged D1 protein, potentially mediated by enzymes other than Deg proteases, is important for its efficient degradation in cyanobacteria as well, or if this reflects refinement of a D1 degradation mechanism during the evolution of higher plants. 4.1.2. Processive degradation of photodamaged D1 protein by the FtsH complex Alternatively, it was suggested that in vivo the FtsH proteases alone can degrade the D1 protein in a processive manner, both in chloroplasts of higher plants and cyanobacteria [52]. Twelve FtsH proteases are encoded by the genome of A. thaliana [1], of which nine were experimentally proven to be chloroplast-located [58]. In chloroplasts, FtsH proteases form a heterohexameric complex of two pairs of redundant gene products, FtsH2/8 and FtsH5/1 (reviewed in [2,3,56]). Involvement of the FtsH complex in D1 protein degradation was implicated by indirect evidence that mutants lacking FtsH2 or FtsH5 are more susceptible to photoinhibition of PSII [6,57]. However, direct evidence of D1 cleavage has only been reported for recombinant FtsH1, which was able to degrade D1 protein fragments, but not the full-length damaged D1 protein [45]. In Synechocystis 6803, only two out of four FtsH proteaseencoding genes could be deleted, while the remaining two appeared to be essential [48]. Synechocystis 6803 mutants with a deletion of the FtsH protease-encoding gene slr0228


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contained stabilized full-length photodamaged D1 protein and did not accumulate D1 protein fragments [63]. Hence, FtsH proteases obviously play an important role in complete removal of the D1 protein, but their importance is clearly not limited to D1 proteolysis. Interestingly, ftsh2 knock-out mutants of A. thaliana accumulated less Deg1 protein, while deg1 knockdown mutants contained less FtsH and Deg2 proteins [37,73]. These results indicate poorly understood cross-regulation of accumulation of different proteolytic systems in the chloroplast, which could also account for the absence of D1 protein fragment accumulation in ftsh2 mutants. 4.2. Degradation of D1 protein cross-links High light intensities or high temperature can also lead to intramolecular covalent cross-linking of the D1 protein to surrounding PSII subunits, such as the reaction center D2 protein, the a-subunit of cytochrome b559 and the antenna chlorophyll-binding protein CP43 [15,22,29,47,51]. Although the molecular mechanism of such cross-linking is unknown, covalent binding of the D1 protein via oxidized amino acids was proposed [47]. The formation of D1 cross-links was observed not only in isolated PSII membranes, thylakoids or intact chloroplasts, but also in intact cells [10,15,29,51]. Earlier biochemical characterization showed that unidentified stromal serine proteases or metalloproteases degraded some of these cross-links [15,51]. Circumstantial evidence indicated that the FtsH protease complex degraded heat-induced D1 protein cross-links in spinach [72]. However, it appears unlikely that the FtsH protease complex alone is able to degrade these cross-linked proteins. It has been shown for E. coli that FtsH degrades target proteins in a processive manner, unfolding the substrate before translocating them into the catalytic chamber [30]. Due to its limited unfoldase activity and limited pore size, FtsH will probably stall at amino acid residues that are cross-linked with neighboring proteins. Our own experiments, on the other hand, indicated that D1 protein cross-links are substrates of the periplasmic HhoA protease in Synechocystis 6803 (C. Funk, P.F. Huesgen and I. Adamska, unpublished). 5. Conclusions A vast body of literature describes numerous biochemical and physiological studies directed towards the identification of the D1-degrading protease(s), with apparently contradicting results (reviewed in [4,5,12,52,71]). The current view that not a single protease, but several enzymes of the FtsH and Deg protease families, cooperatively take care of this essential task [12,27,37,38], reconciles most of the published data in a concise model. We would like to extend this model, and suggest that the role of different enzymes in degradation of the D1 protein should be appreciated from a system biology perspective [11]. Remarkably, recent analyses of mutants of cyanobacterial and chloroplast proteases summarized above have implicated similar sets of enzymes in selective removal

of the photodamaged D1 protein, as in the degradation of D1 cross-links (Fig. 2). The degradation of photodamaged D1 protein, both alone or together with cross-linked neighboring proteins, appears to proceed in a similar manner in cyanobacteria and chloroplasts independently of the source of the damage. Furthermore, other subunits of PSII, including D2, CP43, CP47 and cytochrome b559, also exhibit increased turnover under high intensity light stress ([4,71], and references therein). Turnover of the D1 protein could therefore be the effect of a more general quality control system that monitors the proper fold of thylakoid membrane proteins rather than the result of a D1-specific process. This quality control system may be triggered by various conformational changes that result from oxidative damages or temperature stress. Deg/HtrA and FtsH proteases both contribute to this system, which would most likely include additional factors such as chaperones or other proteases. Such a complex protease network of several cooperating enzymes would be a very robust system that ensures thylakoid membrane protein integrity, including the efficient degradation of damaged D1 protein, which is indispensable for PSII repair and maintenance of photosynthetic functions under stressful environmental conditions. Acknowledgements This work was supported by grants from the Deutsche Forschungsgemeinschaft (AD92/8-2 in the framework of SPP1132 and AD92/8-3 and the Konstanz University (to I.A.)). We apologize to all authors whose original research could not be cited due to space limitations. References [1] Adam, Z., Adamska, I., Nakabayashi, K., Ostersetzer, O., Haussuhl, K., Manuell, A., Zheng, B., Vallon, O., et al. (2001) Chloroplast and mitochondrial proteases in Arabidopsis. A proposed nomenclature. Plant Physiol. 125, 1912e1918. [2] Adam, Z., Rudella, A., van Wijk, K.J. (2006) Recent advances in the study of Clp, FtsH and other proteases located in chloroplasts. Curr. Opin. Plant Biol. 9, 234e240. [3] Adam, Z., Zaltsman, A., Sinvany-Villalobo, G., Sakamoto, W. (2005) FtsH proteases in chloroplasts and cyanobacteria. Physiol. Plant 123, 386e390. [4] Adir, N., Zer, H., Shochat, S., Ohad, I. (2003) Photoinhibition e a historical perspective. Photosynth. Res. 76, 343e370. [5] Andersson, B., Aro, E.-M. (2001) Photodamage and D1 protein turnover in photosystem II. In E.-M. Aro, & B. Andersson (Eds.), Regulation of Photosynthesis (pp. 377e393). Dordrecht: Kluwer. [6] Bailey, S., Thompson, E., Nixon, P.J., Horton, P., Mullineaux, C.W., Robinson, C., Mann, N.H. (2002) A critical role for the Var2 FtsH homologue of Arabidopsis thaliana in the photosystem II repair cycle in vivo. J. Biol. Chem. 277, 2006e2011. [7] Barker, M., de Vries, R., Nield, J., Komenda, J., Nixon, P.J. (2006) The Deg proteases protect Synechocystis sp. PCC 6803 during heat and light stresses but are not essential for removal of damaged D1 protein during the photosystem two repair cycle. J. Biol. Chem. 281, 30347e30355. [8] Chassin, Y., Kapri-Pardes, E., Sinvany, G., Arad, T., Adam, Z. (2002) Expression and characterization of the thylakoid lumen protease DegP1 from Arabidopsis. Plant Physiol. 130, 857e864.

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