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Polyamines interaction with thylakoid proteins during stress
Journal of Photochemistry and Photobiology B: Biology 104 (2011) 314–319
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Journal of Photochemistry and Photobiology B: Biology journal homepage: www.elsevier.com/locate/jphotobiol
Short Review
Polyamines interaction with thylakoid proteins during stress S. Hamdani, H. Yaakoubi, R. Carpentier ⇑ Groupe de Recherche en Biologie Végétale, Département de Chimie-Biologie, Université du Québec à Trois-Rivières, C. P. 500, Trois-Rivières (Québec), Canada G9A 5H7
a r t i c l e
i n f o
Article history: Available online 4 March 2011 Keywords: Abiotic stress Electrostatic interaction Extrinsic proteins Photosystem II Polyamines
a b s t r a c t The involvement of polyamines in plant responses to abiotic stresses is well investigated, while there has been few reports on the specific mode of action of polyamines on the photosynthetic apparatus. The objective of this review is thus to examine the mode of interaction of polyamines with proteins of photosystem II core and LHCII, including methylamine (monoamine) as a simplified model to better understand the mode of action of polyamines. Spectroscopic methods used to determine the binding mode of amines with PSII proteins showed that amines such as spermine, putrescine and methylamine interact with protein (H-bonding) through polypeptide C@O, CAN and NAH groups with major perturbations of protein secondary structure as the concentration of amines was raised. High concentration of amines added to PSII-enriched submembrane fractions causes a significant loss of PSII activity. However, at lower concentration, polyamines, especially spermine, improve the photosynthetic functions under stress. We concluded from this review that besides the conjugation of polyamines with LHC polypeptides, polyamines are likely to interact with extrinsic proteins and the hydrophilic part of intrinsic proteins of PSII by electrostatic interaction. This could stabilize the conformation of proteins under various stresses. However, at high concentration of polyamines a strong inhibition of PSII activity is observed. Ó 2011 Elsevier B.V. All rights reserved.
Contents 1. 2. 3. 4. 4.
5. 6. 7.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Polyamine metabolism and photosynthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Polyamines and stress responses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Interaction sites of PAs with PSII proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Extrinsic proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Interaction sites of PAs with PSII proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Extrinsic proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. D1 and D2 proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3. LHCII antenna complex . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Interaction mode of PAs with PSII proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Abbreviations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction Higher plants photosystem II (PSII) is a membrane bound protein complex composed of chlorophyll and carotenoid pigments
⇑ Corresponding author. Tel.: +1 819 376 5011; fax: +1 819 376 5057. E-mail address: [email protected] (R. Carpentier). 1011-1344/$ - see front matter Ó 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.jphotobiol.2011.02.007
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that harvest light energy to be transferred to a reaction center where charge separation takes place. This charge separation initiates the electron transport responsible for plastoquinone reduction and water oxidation with the concurrent oxygen evolution. PSII contains multiple intrinsic and extrinsic proteins. Amongst them, the extrinsic polypeptides of the luminal side with apparent masses of 17, 23 and 33 kDa are involved in maintaining the tetranuclear manganese cluster and cofactors such as Ca2+ and Cl in an
S. Hamdani et al. / Journal of Photochemistry and Photobiology B: Biology 104 (2011) 314–319
Fig. 1. Structure of endogenous polyamines.
active oxygen-evolving complex (OEC) [1]. At this site, water oxidation is performed through the so-called S-state cycle. The heterodimeric core of PSII is formed by the intrinsic proteins D1 and D2, which cross the thylakoid membrane and bind the redox-active cofactors involved in electron transfer [2]. Both subunits have been revealed to interact with the oxygen evolving site and participate in the stabilization of electron transfer reactions [3]. Polyamines (PAs) are small ubiquitous nitrogenous compounds. They are formed by aliphatic hydrocarbons substituted with two or more amino groups. Several studies have reported the interaction of PAs with proteins of PSII [4–6]. However, whereas the influence of PAs on the structural organization and functional activity of thylakoid membranes was examined in general, there is little information available regarding the site of action of PAs in PSII and about the binding modes by which PAs may affect this photosystem. PAs occur in a free form as cations at physiological pH or conjugated [7–9]. Their polycationic nature is one of the main properties believed to mediate their biological activity. In fact, membrane properties, proteins structure, and enzyme activities were shown to be strongly influenced by the interaction of PAs positive charges with the negative charges of macromolecules [8,10,11]. The purpose of this review is to summarize the available observations that indicate the electrostatic interaction of PAs or their conjugation with proteins of PSII may confer some stability of their conformational structure and function under various stresses. However, at high concentration of PAs a strong inhibition of PSII activity is observed. 2. Polyamine metabolism and photosynthesis The common PAs are putrescine (PUT), spermidine (SPD) and spermine (SPM) (Fig. 1). The pathways of biosynthesis of PAs have been established in plants. Two pathways lead to PUT formation. In the first one, PUT (diamine) is synthesized by the decarboxylation of arginine by arginine decarboxylase (ADC) for the synthesis of agmatine and then PUT. The other pathway involves the decarboxylation of ornithine by the enzyme ornithine decarboxylase (ODC). PUT is converted into SPD (triamine), and then into SPM (tetraamine) by successive addition of aminopropyl groups from decarboxylated S-adenosylmethionine. The aminopropyl groups are generated from S-adenosylmethionine (SAM) by SAM decarboxylase (SAMDC). The transfer of the aminopropyl groups is catalyzed by SPD and SPM synthase, respectively [12–15]. Some of the genes involved in PA biosynthesis are found in the chloroplast [16], showing their possible relation with photosynthetic processes. The induction or inhibition of PAs biosynthesis is regulated by light and correlated with the ATP levels [17,18]. As example, ODC activity increases under illumination. In contrast, in dark-adapted materials the reduced ATP level decreases protein biosynthesis, which especially reduces ODC activity [17]. Thus light may have an important function in PAs biosynthesis.
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The PAs transport across cell membranes (uptake and efflux) constitutes an important mean of regulating the intracellular PAs content [19]. The specific mechanism of this transport remains unclear. However, from cell culture studies, it was suggested that the entry of PAs into the cells is driven by the transmembrane electrical gradient, with a possible antiport mechanism between external and internal PAs [20]. Such mechanism could also intervene for the translocation of polyamines across the chloroplasts membranes. In plant cells, PA content depends not only on their biosynthesis and transport but also on their degradation and conjugation reactions. PAs are oxidatively deaminated in reactions catalyzed by amine oxidases, in particular diamine oxidases (DAO), a copper containing enzyme, and flavin-containing PA oxidases (PAO). DAOs display high affinity for PUT, while PAOs oxidize secondary amine groups from SPD and SPM. On the other hand, PAs may occur as conjugates to small molecules like phenolic acids and also to various macromolecules such as DNA, RNA and proteins. This interaction can modulate the cell function of these compounds [21–23]. In chloroplasts, the conjugation of PAs is catalyzed by an enzyme named transglutaminase (TGase) [24]. This enzyme catalyses the incorporation of PAs into thylakoid and stromal proteins such as the light harvesting complex (LHC) and the large subunit of Rubisco [25–28]. The TGase activity is up-regulated by Ca2+ and light [29].
3. Polyamines and stress responses The physiological significance of PA accumulation and their regulatory function in plant cells have attracted considerable attention [30]. PAs are involved in various physiological events such as cell division, DNA replication, development, and senescence. Moreover, it has been suggested that PAs are associated with plant responses under stress conditions [30–32,14,33–35]. Indeed, it has been observed that plants significantly accumulate PAs under environmental stresses. This accumulation constitutes a mechanism that may confer adaptive and protective functions under abiotic stresses [8,30–32]. Hence, the increase of endogenous PAs content was suggested to reverse the damaging effects and enhance the tolerance of plants to various stresses [36–38]. Stress-tolerant plants generally have a large capacity to enhance PA biosynthesis in response to abiotic stresses compare to intolerant plants. For example, ozone-tolerant tobacco and wild type of Arabidopsis thaliana enhanced PA accumulation in their tissues, while, the sensitive species did not increase the PA content [39,40]. Also, the enhancement of the endogenous PAs level through transgenic approaches increased the tolerance of sensitive plants [41,42]. It is now well accepted that the ability of plants to control stress is correlated to their ability to synthesize PAs [39,40, 43,44]. The expression of several genes involved in PA biosynthesis (ADC2, SPMS, SAMDC2) is up-regulated in the presence of one or more abiotic stresses [12,45]. The activity of ADC, a major PA biosynthetic enzyme, increased under stress conditions, leading to enhancement of PA levels [8,46,47]. These adaptation mechanisms are also pertinent to the photosynthetic apparatus. In fact, variation of thylakoid-associated PAs have been observed during plant response to various external stresses such as salinity, UV-B radiation, ozone, heavy metal, water stress, or chilling [12,32,39,43,48–50]. It was also observed that high CO2 concentrations increased the thylakoid bound PUT [51]. However, UV-B radiations increased the thylakoid-associated SPM [32]. Some reports have shown that PUT, exogenously added during salt stress, enhances the level of the photochemical efficiency of PSII [52]. Moreover, the application of PAs during stress induced senescence, prevented chlorophyll loss, and preserved the thylakoid membranes structure [53,54].
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ing between the exposed negative charges of proteins and the positive charges of PAs. This can lead to conformational changes of the proteases that reduce their catalytic action [66]. As a consequence, PAs can maintain the stability of D1 and D2 proteins of PSII and retard their apparent degradation during stress conditions.
4.3. LHCII antenna complex
Fig. 2. Amine concentration leading to 50% inhibition of oxygen yield and Fv/Fm in PSII submembrane fractions after addition of SPM, PUT or MET. Results obtained from Refs. [4,5,69].
4. Interaction sites of PAs with PSII proteins 4.1. Extrinsic proteins The involvement of PAs in stress resistance and their association with thylakoid membranes and the light reactions of photosynthesis indicate that PAs are likely to interact directly with photosystems. SPM at relatively low concentration was reported to enhance or restore the loss of photochemical activity both in vivo and in vitro [55,56]. However, some other studies have shown that exogenous PAs added to isolated PSII submembrane fractions are able to interact with the luminal side of PSII, which leads to the loss of photosynthetic activity at high concentration of PAs (>1 mM) [4,5]. It was reported that exogenously added PAs can penetrate to the luminal side of thylakoid membranes [57]. Thus, PAs can interact with hydrophilic portions of proteins and the extrinsic polypeptides of the OEC. This interaction releases the extrinsic proteins of PSII leading to the loss of PSII activity [4,58]. Removal of the two extrinsic polypeptides of 17 and 23 kDa decreases the affinity of Ca2+ and Cl for the OEC [59]. Also, the release of the other extrinsic polypeptide of 33 kDa is responsible for the loss of the Mn cluster and consequently the oxygen-evolving activity is abolished [60]. The loss of the three extrinsic polypeptides after addition of high concentrations of PAs disorganizes the OEC and abolish the electron supply for the reduction of the quinone acceptors of PSII [4]. In comparison with PAs, methylamine (MET), a non biogenic monoamine, used as a simplified model to better understand the action of PAs, induces the same inhibition in oxygen evolution at high MET concentration [61]. In fact, Fig. 2 shows that 50% inhibition of both oxygen yield and Fv/Fm was reached at around 2.5 mM SPM, 5 mM PUT and 10 mM MET. This result can be explained by the strength of the positive charges of PAs which exerts an electrostatic interaction with PSII proteins. This interaction is proportional in part to the number of positive charges of PAs (Fig. 1). So, the relative inhibition in decreasing order is SPM > PUT > MET. 4.2. D1 and D2 proteins Several reports have shown that drought and osmotic stresses induce a decrease of the PSII major proteins D1 and D2 and the transcripts of their corresponding genes psbA, psbD. Exogenous application of SPD alleviates the decrease of proteins transcripts and retards the loss of D1 and D2 under these conditions [62,63]. The protective action of SPD in PSII can be explained by a role of PAs in the modulation of synthesis and turnover of these proteins [64,65]. A proposed mode of action of PAs consists in a direct bind-
Variation of PAs levels in chloroplasts can modify the organization of thylakoid membranes. The stromal side of the transmembrane LHCII proteins is negatively charged. This property allows their electrostatic interaction with positive charges [67]. Further, some amount of PUT, SPD and SPM can be found conjugated to LHCII [26,29]. It was reported that SPM is the most efficiently conjugated PA to isolated LHCII [29,68]. Some abiotic stresses such as low temperature reduce thylakoid-bound PAs and affect the LHCII proteins and the transcripts of their corresponding gene. Exogenously added PAs may alleviate the decrease of these proteins during stress [30,32,62]. The response of the photosynthetic apparatus to stress conditions is affected by the changes occurring in the pattern of LHCII-associated PUT and SPM which was shown to adjust the size of LHCII [18,31,32]. The decrease of the PUT/SPM ratio leads to an increase in the LHCII size. This structural modification of thylakoid membranes may enhance the energy dissipation and reduce the photochemical activity. However, the increase in the PUT/SPM ratio observed at high-CO2 concentrations decreases the LHCII size and augments the photosynthetic yield [51]. The relation between increased PUT level in thylakoids and the LHCII antenna size suggests that thylakoid-bound PAs exert a regulatory role in the adaptation processes of the photosynthetic apparatus [39].
5. Interaction mode of PAs with PSII proteins Little attention has been focused on the exact binding mode of PAs and their effects on the structure and dynamics of PSII proteins. The Fourier transformed infrared difference spectroscopy (FTIR) provided evidence regarding the binding mode and the effects of PAs complexation on the proteins secondary structure of isolated PSII submembrane fractions and of whole thylakoid membranes. FTIR results showed that, at low concentration, the electrostatic interaction of PAs with PSII proteins displays no major perturbation of proteins secondary structure. However, at high concentration of PAs major alterations of the proteins of PSII secondary structure occurs as positive charge increases. In fact, the major secondary structural changes were reported upon SPD and SPM complexation with proteins of PSII [5,6]. The structural modifications included a reduction of a-helices and an increased proportion of b-sheet and random coil structures. This further interaction of PUT, SPD and SPM with proteins of PSII (H-bonding) occurs through the polypeptides C@O, CAN and NAH groups [5,6,69]. The interaction of MET with proteins of PSII was less investigated. Our previous work [69] using MET as a simplified model to better understand the binding mode of PAs displayed that MET interaction occurs primarily with the extrinsic proteins of PSII through the polypeptides C@O, CAN and NAH groups. This interaction with the extrinsic polypeptides associated with the OEC must be responsible for the strong inhibition of PSII activity. A comparison of MET with biogenic PAs revealed that modification of proteins secondary structure is more pronounced when the positive charges of PAs increases. However, at high concentration (15 mM), MET has shown stronger effects on the protein secondary structure than biogenic PAs (Table 1). Because of its small size, MET
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S. Hamdani et al. / Journal of Photochemistry and Photobiology B: Biology 104 (2011) 314–319 Table 1 Secondary structure determination of proteins in PSII submembrane fractions in the presence of methylamine (MET), putrescine (PUT) or spermine (SPM). Amide I (cm
1
)
Conformation
% of conformation METa (mM)
a-Helix
1654–1660 1614–1637 1638–1648 1670–1678 1680–1691 a b c
b-Sheet Random Turn b-antiparallel
PUTb (mM)
SPMc (mM)
0
15
0
20
0
20
50 10 19 17 4
35 16 27 12 10
51 11 19 14 5
49 15 19 12 5
47 11 16 19 7
35 20 17 19 9
Data from [63]. Data from [5]. Data from [6].
A
B
Normal Condition
Photoinhibition PUT
SPM
Fig. 3. A proposed model of interaction of polyamines with PSII proteins under photoinhibition conditions.
may also have access to more inner parts of extrinsic proteins of PSII, while diamines and PAs probably bind onto surface [69]. 6. Conclusions From previous investigations, it can be deduced that PAs play an important role in plant development and in the protection of the photosynthetic apparatus. We have discussed the implication of PAs on the functionality of thylakoid membranes and the target sites of PAs on PSII proteins. The involvement of PAs in restoring the photochemical activity operates in a positive charge dependent manner. Indeed, SPM restores more effectively the loss of chlorophyll content, electron transport and energy transfer between PSII and PSI than SPD and PUT [55,56]. However, PUT was shown with more affinity towards LHCII antenna than the other PAs. In comparison with inorganic cations (K+ and Mg2+), SPM and SPD showed a stronger effect on restoring the photochemical efficiency [55,70]. Also, PUT is more effective to increase the oxygen evolution rates than K+, but not than Mg2+ [57]. These results displayed the existence of several factors involved in the interaction between these cations and their site of action including the number of positive charges and the specificity of the binding mode. Besides the conjugation of PAs with LHC polypeptides, the mechanism of their action probably involves direct binding of PAs to the extrinsic proteins and the hydrophilic portions of intrinsic polypeptides of PSII through electrostatic interaction related to their polycationic nature (Fig. 3). This electrostatic interaction
could provide some stability to the conformation of proteins against various stresses and consequently help in maintaining the photosynthetic activity. However, at high concentration of PAs this protection is reversed into modification of proteins secondary structure due to strong interaction with the polypeptides C@O, CAN and NAH groups leading to the inhibition of photosynthetic processes. Validation of this model with other complexes of the thylakoid membrane, such as the cytochrome b/f complex and ATPsynthase, should be the subject of future work. 7. Abbreviations ADC Chl DAO LHC MET ODC OEC PA PAO PSII PUT SPD SPM
arginine decarboxylase chlorophyll diamine oxidases light harvesting complex methylamine ornithine decarboxylase oxygen-evolving complex polyamine PA oxidase photosystem II putrescine spermidine spermine
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Kasinathan, A. Wingler, Effect of reduced arginine decarboxylase activity on salt tolerance and on polyamine formation during salt stress in Arabidopsis thaliana, Physiol. Plant. 121 (2004) 101–107. [41] S.S. Gill, N. Tuteja, Polyamines and abiotic stress tolerance in plants, Plant Signal Behav. 5 (2010) 26–33. [42] P. Roy, K. Niyogi1, D.N. SenGupta, B. Ghosh, Spermidine treatment to rice seedlings recovers salinity stress-induced damage of plasma membrane and PM-bound H+-ATPase in salt-tolerant and salt-sensitive rice cultivars, Plant Sci. 168 (2005) 583–591. [43] S. Mapelli, I.M. Brambilla, N.L. Radyukina, Y.V. Ivanov, A.V. Kartashov, R. Reggiani, V.V. Kuznetsov, Free and bound polyamines changes in different plants as a consequence of UV-B light irradiation, Gen. Appl. Plant Physiol. 34 (2008) 55–66. [44] J.H. Liu, H. Kitashiba, J. Wang, Y. Ban, T. Moriguchi, Polyamines and their ability to provide environmental stress tolerance to plants, Plant Biotechnol. 24 (2007) 117–126. [45] S. Soyka, A.G. Heyer, Arabidopsis knockout mutation of ADC2 gene reveals inducibility by osmotic stress, FEBS Lett. 458 (1999) 219–223. [46] J.H. Liu, K. Nada, C. Honda, H. Kitashiba, X.P. Wen, X.M. Pang, T. Moriguchi, Polyamine biosynthesis of apple callus under salt stress: importance of the arginine decarboxylase pathway in stress response, J. Exp. Bot. 57 (2006) 2589–2599. [47] S. Jantaro, P. Mäenpää, P. Mulo, A. Incharoensakdi, Content and biosynthesis of polyamines in salt and osmotically stressed cells of Synechocystis sp. PCC 680, FEMS Microbiol. Lett. 228 (2003) 129–135. [48] G. Demetriou, C. Neonaki, E. Navakoudis, K. Kotzabasis, Salt stress impact on the molecular structure and function of the photosynthetic apparatus: the protective role of polyamines, Biochim. Biophys. Acta 1767 (2007) 272– 280. [49] M.D. Groppa, M.P. Benavides, Polyamines and abiotic stress: recent advances, Amino Acids 34 (2008) 35–45. [50] A. Kaumar, T. Altabella, M.A. Taylor, A.F. Tiburcio, Recent advances in polyamine research, Trends Plant Sci. 2 (1997) 124–130. [51] K. Logothetis, S. Dakanali, N. Ioannidis, K. Kotzabasis, The impact of high CO2 concentrations on the structure and function of the photosynthetic apparatus and the role of polyamines, J. Plant Physiol. 161 (2004) 715–724. [52] R.H. Zhang, J. Li, S.R. Guo, T. Tezuka, Effects of exogenous putrescine on gasexchange characteristics and chlorophyll fluorescence of NaCl-stressed cucumber seedlings, Photosynth. Res. 100 (2009) 155–162. [53] R.B. Popovic, D.J. Kyle, A.S. Cohen, S. Zalik, Stabilization of thylakoid membranes by spermine during stress induced senescence of barley leaf discs, Plant Physiol. 64 (1979) 721–726. [54] A.S. Cohen, R.B. Popovic, S. Zalik, Effects of polyamines on chlorophyll and protein content, photochemical activity, and chloroplast ultrastructure of barley leaf discs during senescence, Plant Physiol. 64 (1979) 717–720. [55] N.E. Ioannidis, K. 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Contents lists available at ScienceDirect
Journal of Photochemistry and Photobiology B: Biology journal homepage: www.elsevier.com/locate/jphotobiol
Short Review
Polyamines interaction with thylakoid proteins during stress S. Hamdani, H. Yaakoubi, R. Carpentier ⇑ Groupe de Recherche en Biologie Végétale, Département de Chimie-Biologie, Université du Québec à Trois-Rivières, C. P. 500, Trois-Rivières (Québec), Canada G9A 5H7
a r t i c l e
i n f o
Article history: Available online 4 March 2011 Keywords: Abiotic stress Electrostatic interaction Extrinsic proteins Photosystem II Polyamines
a b s t r a c t The involvement of polyamines in plant responses to abiotic stresses is well investigated, while there has been few reports on the specific mode of action of polyamines on the photosynthetic apparatus. The objective of this review is thus to examine the mode of interaction of polyamines with proteins of photosystem II core and LHCII, including methylamine (monoamine) as a simplified model to better understand the mode of action of polyamines. Spectroscopic methods used to determine the binding mode of amines with PSII proteins showed that amines such as spermine, putrescine and methylamine interact with protein (H-bonding) through polypeptide C@O, CAN and NAH groups with major perturbations of protein secondary structure as the concentration of amines was raised. High concentration of amines added to PSII-enriched submembrane fractions causes a significant loss of PSII activity. However, at lower concentration, polyamines, especially spermine, improve the photosynthetic functions under stress. We concluded from this review that besides the conjugation of polyamines with LHC polypeptides, polyamines are likely to interact with extrinsic proteins and the hydrophilic part of intrinsic proteins of PSII by electrostatic interaction. This could stabilize the conformation of proteins under various stresses. However, at high concentration of polyamines a strong inhibition of PSII activity is observed. Ó 2011 Elsevier B.V. All rights reserved.
Contents 1. 2. 3. 4. 4.
5. 6. 7.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Polyamine metabolism and photosynthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Polyamines and stress responses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Interaction sites of PAs with PSII proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Extrinsic proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Interaction sites of PAs with PSII proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Extrinsic proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. D1 and D2 proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3. LHCII antenna complex . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Interaction mode of PAs with PSII proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Abbreviations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction Higher plants photosystem II (PSII) is a membrane bound protein complex composed of chlorophyll and carotenoid pigments
⇑ Corresponding author. Tel.: +1 819 376 5011; fax: +1 819 376 5057. E-mail address: [email protected] (R. Carpentier). 1011-1344/$ - see front matter Ó 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.jphotobiol.2011.02.007
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that harvest light energy to be transferred to a reaction center where charge separation takes place. This charge separation initiates the electron transport responsible for plastoquinone reduction and water oxidation with the concurrent oxygen evolution. PSII contains multiple intrinsic and extrinsic proteins. Amongst them, the extrinsic polypeptides of the luminal side with apparent masses of 17, 23 and 33 kDa are involved in maintaining the tetranuclear manganese cluster and cofactors such as Ca2+ and Cl in an
S. Hamdani et al. / Journal of Photochemistry and Photobiology B: Biology 104 (2011) 314–319
Fig. 1. Structure of endogenous polyamines.
active oxygen-evolving complex (OEC) [1]. At this site, water oxidation is performed through the so-called S-state cycle. The heterodimeric core of PSII is formed by the intrinsic proteins D1 and D2, which cross the thylakoid membrane and bind the redox-active cofactors involved in electron transfer [2]. Both subunits have been revealed to interact with the oxygen evolving site and participate in the stabilization of electron transfer reactions [3]. Polyamines (PAs) are small ubiquitous nitrogenous compounds. They are formed by aliphatic hydrocarbons substituted with two or more amino groups. Several studies have reported the interaction of PAs with proteins of PSII [4–6]. However, whereas the influence of PAs on the structural organization and functional activity of thylakoid membranes was examined in general, there is little information available regarding the site of action of PAs in PSII and about the binding modes by which PAs may affect this photosystem. PAs occur in a free form as cations at physiological pH or conjugated [7–9]. Their polycationic nature is one of the main properties believed to mediate their biological activity. In fact, membrane properties, proteins structure, and enzyme activities were shown to be strongly influenced by the interaction of PAs positive charges with the negative charges of macromolecules [8,10,11]. The purpose of this review is to summarize the available observations that indicate the electrostatic interaction of PAs or their conjugation with proteins of PSII may confer some stability of their conformational structure and function under various stresses. However, at high concentration of PAs a strong inhibition of PSII activity is observed. 2. Polyamine metabolism and photosynthesis The common PAs are putrescine (PUT), spermidine (SPD) and spermine (SPM) (Fig. 1). The pathways of biosynthesis of PAs have been established in plants. Two pathways lead to PUT formation. In the first one, PUT (diamine) is synthesized by the decarboxylation of arginine by arginine decarboxylase (ADC) for the synthesis of agmatine and then PUT. The other pathway involves the decarboxylation of ornithine by the enzyme ornithine decarboxylase (ODC). PUT is converted into SPD (triamine), and then into SPM (tetraamine) by successive addition of aminopropyl groups from decarboxylated S-adenosylmethionine. The aminopropyl groups are generated from S-adenosylmethionine (SAM) by SAM decarboxylase (SAMDC). The transfer of the aminopropyl groups is catalyzed by SPD and SPM synthase, respectively [12–15]. Some of the genes involved in PA biosynthesis are found in the chloroplast [16], showing their possible relation with photosynthetic processes. The induction or inhibition of PAs biosynthesis is regulated by light and correlated with the ATP levels [17,18]. As example, ODC activity increases under illumination. In contrast, in dark-adapted materials the reduced ATP level decreases protein biosynthesis, which especially reduces ODC activity [17]. Thus light may have an important function in PAs biosynthesis.
315
The PAs transport across cell membranes (uptake and efflux) constitutes an important mean of regulating the intracellular PAs content [19]. The specific mechanism of this transport remains unclear. However, from cell culture studies, it was suggested that the entry of PAs into the cells is driven by the transmembrane electrical gradient, with a possible antiport mechanism between external and internal PAs [20]. Such mechanism could also intervene for the translocation of polyamines across the chloroplasts membranes. In plant cells, PA content depends not only on their biosynthesis and transport but also on their degradation and conjugation reactions. PAs are oxidatively deaminated in reactions catalyzed by amine oxidases, in particular diamine oxidases (DAO), a copper containing enzyme, and flavin-containing PA oxidases (PAO). DAOs display high affinity for PUT, while PAOs oxidize secondary amine groups from SPD and SPM. On the other hand, PAs may occur as conjugates to small molecules like phenolic acids and also to various macromolecules such as DNA, RNA and proteins. This interaction can modulate the cell function of these compounds [21–23]. In chloroplasts, the conjugation of PAs is catalyzed by an enzyme named transglutaminase (TGase) [24]. This enzyme catalyses the incorporation of PAs into thylakoid and stromal proteins such as the light harvesting complex (LHC) and the large subunit of Rubisco [25–28]. The TGase activity is up-regulated by Ca2+ and light [29].
3. Polyamines and stress responses The physiological significance of PA accumulation and their regulatory function in plant cells have attracted considerable attention [30]. PAs are involved in various physiological events such as cell division, DNA replication, development, and senescence. Moreover, it has been suggested that PAs are associated with plant responses under stress conditions [30–32,14,33–35]. Indeed, it has been observed that plants significantly accumulate PAs under environmental stresses. This accumulation constitutes a mechanism that may confer adaptive and protective functions under abiotic stresses [8,30–32]. Hence, the increase of endogenous PAs content was suggested to reverse the damaging effects and enhance the tolerance of plants to various stresses [36–38]. Stress-tolerant plants generally have a large capacity to enhance PA biosynthesis in response to abiotic stresses compare to intolerant plants. For example, ozone-tolerant tobacco and wild type of Arabidopsis thaliana enhanced PA accumulation in their tissues, while, the sensitive species did not increase the PA content [39,40]. Also, the enhancement of the endogenous PAs level through transgenic approaches increased the tolerance of sensitive plants [41,42]. It is now well accepted that the ability of plants to control stress is correlated to their ability to synthesize PAs [39,40, 43,44]. The expression of several genes involved in PA biosynthesis (ADC2, SPMS, SAMDC2) is up-regulated in the presence of one or more abiotic stresses [12,45]. The activity of ADC, a major PA biosynthetic enzyme, increased under stress conditions, leading to enhancement of PA levels [8,46,47]. These adaptation mechanisms are also pertinent to the photosynthetic apparatus. In fact, variation of thylakoid-associated PAs have been observed during plant response to various external stresses such as salinity, UV-B radiation, ozone, heavy metal, water stress, or chilling [12,32,39,43,48–50]. It was also observed that high CO2 concentrations increased the thylakoid bound PUT [51]. However, UV-B radiations increased the thylakoid-associated SPM [32]. Some reports have shown that PUT, exogenously added during salt stress, enhances the level of the photochemical efficiency of PSII [52]. Moreover, the application of PAs during stress induced senescence, prevented chlorophyll loss, and preserved the thylakoid membranes structure [53,54].
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ing between the exposed negative charges of proteins and the positive charges of PAs. This can lead to conformational changes of the proteases that reduce their catalytic action [66]. As a consequence, PAs can maintain the stability of D1 and D2 proteins of PSII and retard their apparent degradation during stress conditions.
4.3. LHCII antenna complex
Fig. 2. Amine concentration leading to 50% inhibition of oxygen yield and Fv/Fm in PSII submembrane fractions after addition of SPM, PUT or MET. Results obtained from Refs. [4,5,69].
4. Interaction sites of PAs with PSII proteins 4.1. Extrinsic proteins The involvement of PAs in stress resistance and their association with thylakoid membranes and the light reactions of photosynthesis indicate that PAs are likely to interact directly with photosystems. SPM at relatively low concentration was reported to enhance or restore the loss of photochemical activity both in vivo and in vitro [55,56]. However, some other studies have shown that exogenous PAs added to isolated PSII submembrane fractions are able to interact with the luminal side of PSII, which leads to the loss of photosynthetic activity at high concentration of PAs (>1 mM) [4,5]. It was reported that exogenously added PAs can penetrate to the luminal side of thylakoid membranes [57]. Thus, PAs can interact with hydrophilic portions of proteins and the extrinsic polypeptides of the OEC. This interaction releases the extrinsic proteins of PSII leading to the loss of PSII activity [4,58]. Removal of the two extrinsic polypeptides of 17 and 23 kDa decreases the affinity of Ca2+ and Cl for the OEC [59]. Also, the release of the other extrinsic polypeptide of 33 kDa is responsible for the loss of the Mn cluster and consequently the oxygen-evolving activity is abolished [60]. The loss of the three extrinsic polypeptides after addition of high concentrations of PAs disorganizes the OEC and abolish the electron supply for the reduction of the quinone acceptors of PSII [4]. In comparison with PAs, methylamine (MET), a non biogenic monoamine, used as a simplified model to better understand the action of PAs, induces the same inhibition in oxygen evolution at high MET concentration [61]. In fact, Fig. 2 shows that 50% inhibition of both oxygen yield and Fv/Fm was reached at around 2.5 mM SPM, 5 mM PUT and 10 mM MET. This result can be explained by the strength of the positive charges of PAs which exerts an electrostatic interaction with PSII proteins. This interaction is proportional in part to the number of positive charges of PAs (Fig. 1). So, the relative inhibition in decreasing order is SPM > PUT > MET. 4.2. D1 and D2 proteins Several reports have shown that drought and osmotic stresses induce a decrease of the PSII major proteins D1 and D2 and the transcripts of their corresponding genes psbA, psbD. Exogenous application of SPD alleviates the decrease of proteins transcripts and retards the loss of D1 and D2 under these conditions [62,63]. The protective action of SPD in PSII can be explained by a role of PAs in the modulation of synthesis and turnover of these proteins [64,65]. A proposed mode of action of PAs consists in a direct bind-
Variation of PAs levels in chloroplasts can modify the organization of thylakoid membranes. The stromal side of the transmembrane LHCII proteins is negatively charged. This property allows their electrostatic interaction with positive charges [67]. Further, some amount of PUT, SPD and SPM can be found conjugated to LHCII [26,29]. It was reported that SPM is the most efficiently conjugated PA to isolated LHCII [29,68]. Some abiotic stresses such as low temperature reduce thylakoid-bound PAs and affect the LHCII proteins and the transcripts of their corresponding gene. Exogenously added PAs may alleviate the decrease of these proteins during stress [30,32,62]. The response of the photosynthetic apparatus to stress conditions is affected by the changes occurring in the pattern of LHCII-associated PUT and SPM which was shown to adjust the size of LHCII [18,31,32]. The decrease of the PUT/SPM ratio leads to an increase in the LHCII size. This structural modification of thylakoid membranes may enhance the energy dissipation and reduce the photochemical activity. However, the increase in the PUT/SPM ratio observed at high-CO2 concentrations decreases the LHCII size and augments the photosynthetic yield [51]. The relation between increased PUT level in thylakoids and the LHCII antenna size suggests that thylakoid-bound PAs exert a regulatory role in the adaptation processes of the photosynthetic apparatus [39].
5. Interaction mode of PAs with PSII proteins Little attention has been focused on the exact binding mode of PAs and their effects on the structure and dynamics of PSII proteins. The Fourier transformed infrared difference spectroscopy (FTIR) provided evidence regarding the binding mode and the effects of PAs complexation on the proteins secondary structure of isolated PSII submembrane fractions and of whole thylakoid membranes. FTIR results showed that, at low concentration, the electrostatic interaction of PAs with PSII proteins displays no major perturbation of proteins secondary structure. However, at high concentration of PAs major alterations of the proteins of PSII secondary structure occurs as positive charge increases. In fact, the major secondary structural changes were reported upon SPD and SPM complexation with proteins of PSII [5,6]. The structural modifications included a reduction of a-helices and an increased proportion of b-sheet and random coil structures. This further interaction of PUT, SPD and SPM with proteins of PSII (H-bonding) occurs through the polypeptides C@O, CAN and NAH groups [5,6,69]. The interaction of MET with proteins of PSII was less investigated. Our previous work [69] using MET as a simplified model to better understand the binding mode of PAs displayed that MET interaction occurs primarily with the extrinsic proteins of PSII through the polypeptides C@O, CAN and NAH groups. This interaction with the extrinsic polypeptides associated with the OEC must be responsible for the strong inhibition of PSII activity. A comparison of MET with biogenic PAs revealed that modification of proteins secondary structure is more pronounced when the positive charges of PAs increases. However, at high concentration (15 mM), MET has shown stronger effects on the protein secondary structure than biogenic PAs (Table 1). Because of its small size, MET
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S. Hamdani et al. / Journal of Photochemistry and Photobiology B: Biology 104 (2011) 314–319 Table 1 Secondary structure determination of proteins in PSII submembrane fractions in the presence of methylamine (MET), putrescine (PUT) or spermine (SPM). Amide I (cm
1
)
Conformation
% of conformation METa (mM)
a-Helix
1654–1660 1614–1637 1638–1648 1670–1678 1680–1691 a b c
b-Sheet Random Turn b-antiparallel
PUTb (mM)
SPMc (mM)
0
15
0
20
0
20
50 10 19 17 4
35 16 27 12 10
51 11 19 14 5
49 15 19 12 5
47 11 16 19 7
35 20 17 19 9
Data from [63]. Data from [5]. Data from [6].
A
B
Normal Condition
Photoinhibition PUT
SPM
Fig. 3. A proposed model of interaction of polyamines with PSII proteins under photoinhibition conditions.
may also have access to more inner parts of extrinsic proteins of PSII, while diamines and PAs probably bind onto surface [69]. 6. Conclusions From previous investigations, it can be deduced that PAs play an important role in plant development and in the protection of the photosynthetic apparatus. We have discussed the implication of PAs on the functionality of thylakoid membranes and the target sites of PAs on PSII proteins. The involvement of PAs in restoring the photochemical activity operates in a positive charge dependent manner. Indeed, SPM restores more effectively the loss of chlorophyll content, electron transport and energy transfer between PSII and PSI than SPD and PUT [55,56]. However, PUT was shown with more affinity towards LHCII antenna than the other PAs. In comparison with inorganic cations (K+ and Mg2+), SPM and SPD showed a stronger effect on restoring the photochemical efficiency [55,70]. Also, PUT is more effective to increase the oxygen evolution rates than K+, but not than Mg2+ [57]. These results displayed the existence of several factors involved in the interaction between these cations and their site of action including the number of positive charges and the specificity of the binding mode. Besides the conjugation of PAs with LHC polypeptides, the mechanism of their action probably involves direct binding of PAs to the extrinsic proteins and the hydrophilic portions of intrinsic polypeptides of PSII through electrostatic interaction related to their polycationic nature (Fig. 3). This electrostatic interaction
could provide some stability to the conformation of proteins against various stresses and consequently help in maintaining the photosynthetic activity. However, at high concentration of PAs this protection is reversed into modification of proteins secondary structure due to strong interaction with the polypeptides C@O, CAN and NAH groups leading to the inhibition of photosynthetic processes. Validation of this model with other complexes of the thylakoid membrane, such as the cytochrome b/f complex and ATPsynthase, should be the subject of future work. 7. Abbreviations ADC Chl DAO LHC MET ODC OEC PA PAO PSII PUT SPD SPM
arginine decarboxylase chlorophyll diamine oxidases light harvesting complex methylamine ornithine decarboxylase oxygen-evolving complex polyamine PA oxidase photosystem II putrescine spermidine spermine
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