Vol. 50 No. 4/2003

1245–1256

QUARTERLY

Review

Plant purple acid — genes, structures and biological function.

Mariusz Olczak½, Bronis³awa Morawiecka and Wies³aw W¹torek

Institute of Biochemistry and Molecular Biology, Wroc³aw University, Wroc³aw, Poland Received: 28 August, 2003; revised: 17 November, 2003; accepted: 27 November, 2003

Key words: metallophosphatases, plant purple acid phosphatases

The properties of plant purple acid phosphatases (PAPs), metallophosphoesterases present in some bacteria, plants and animals are reviewed. All members of this group contain a characteristic set of seven amino-acid residues involved in metal li- gation. Animal PAPs contain a binuclear metallic center composed of two irons, whereas in plant PAPs one iron ion is joined by or ion. Among plant PAPs two groups can be distinguished: small PAPs, monomeric proteins with molecular mass around 35 kDa, structurally close to mammalian PAPs, and large PAPs, homodimeric proteins with a single polypeptide of about 55 kDa. Large plant PAPs exhibit two types of structural organization. One type comprises with subunits bound by a disulfide bridge formed by cysteines located in the C-terminal region around position 350. In the second type no cysteines are located in this posi- tion and no disulfide bridges are formed between subunits. Differences in structural organisation are reflected in substrate preferences. Recent data reveal in plants the occurrence of metallophosphoesterases structurally different from small or large PAPs but with metal-ligating sequences characteristic for PAPs and expressing pro- nounced specificity towards phytate or diphosphate nucleosides and inorganic pyrophosphate.

.Financial support was provided by research grant No. 6 P04C 005 23 from the State Committee for Sci- entific Research (KBN, Poland). ½ Corresponding author: Mariusz Olczak, Institute of Biochemistry and Molecular Biology, Wroc³aw Uni- versity, Tamka 2, 51-137 Wroc³aw, Poland; tel.: (48 71) 375 2710; fax: (48 71) 375 2608; e-mail: [email protected] Abbreviations: AP, acid ; At, Arabidopsis thaliana; kbAP, kidney bean ; PAPs, purple acid phosphatases; PEP, phosphoenolpyruvate; pNPP, para-nitrophenyl phosphate; PPD1-5, nucleotide-diphosphate phosphohydrolase 1-5. 1246 M. Olczak and others 2003

Acid phosphatases play a key role in phos- tion and some reactions (Hayman et al., phate acquisition by plants but, except for a 2000; Vogel et al., 2001). In plants a role of few enzymes performing specific metabolic PAPs remains unknown (Vogel et al., 2001). functions, it is difficult to ascribe a precise Two groups of PAPs in plants have been dis- role to the majority of them. Research on tinguished, first — structurally close to mam- plant acid phosphatases has a long history yet malian purple phosphatases, monomeric pro- the available data do not allow to generalize teins with a molecular mass around 35 kDa, on their structure and function. This is a re- and second — composed of homodimeric pro- sult of different aspects considered by re- teins with a polypeptide of about 55 kDa searchers (Duff et al., 1994). Some of them (Schenk et al., 2000). elaborate on physiology, while other on bio- chemistry or molecular biology. There is a very limited number of comprehensive re- SMALL PLANT PURPLE ACID ports on the overall aspects of acid phos- PHOSPHATASES phatases. The most complete data have been published on the largest group of plant Small plant PAPs are known only from their phoshatases known as purple acid cDNA sequences (Vogel et al., 2001), except phosphatases (PAPs) which occur also in mi- for one example — AtACP5, the puri- croorganisms and animals (Schenk et al., fied to homogeneity from Arabidopsis tha- 2000; Oddie et al., 2000; Vogel et al., 2001). liana (Pozo del et al., 1999). AtACP5 is a se- The animal enzymes were purified and char- creted, 35 kDa monomeric enzyme. All five acterized from bovine spleen (Campbell & PAP metal-binding motifs are present in this Zerner, 1973) and pregnant pig uterine fluid protein. Sequence analysis clearly shows that (uteroferrin) (Schlosnagle et al., 1974). In hu- AtCP5 belongs to a group of enzymes closely mans, they were isolated from the spleen related to small purple acid phosphatases (Yam et al., 1971), bones (Allen et al., 1989), known from mammalian tissues (type 5 acid alveolar macrophages (Efstratiadis & Moss, phosphatases), e.g. uteroferrin. The enzyme 1985) and placenta (Ketcham et al., 1989). hydrolyzes pNPP, a standard synthetic phos- The level of these enzymes increases in such phatase substrate; however, nothing is known pathological states as Gaucher disease (Rob- about its substrate specificity towards natural inson & Glew, 1980), hairy cell leukemia phosphoesters. In addition, like mammalian (Yam et al., 1971), osteoclastoma cells (Hay- PAPs, AtACP5 exhibits peroxidase activity. It man et al., 1989) and AIDS (Schindelmeiser et is interesting that AtACP5 production is in- al., 1989). duced during phosphate starvation, a behav- All PAPs are tartrate-resistant and contain a ior established for some large, dimeric PAPs binuclear metal site. The pink/purple color of (Wasaki et al., 1997; 1999, Miller et al., 2001; their concentrated water solution is the result Li et al., 2002). of a charge-transfer transition between "chro- The other known sequences of plant small mophoric" ferric ion and the residue PAPs were identified in Arabidopsis, sweet (Vincent & Averill, 1990). The second "non- potato, soybean and red kidney bean. The pu- chromophoric" metal ion, occupying the binu- tative, mature proteins have approximately clear site, is iron in mammalian PAPs, and 320 amino-acids residues in length and con- zinc or manganese in plant enzymes (Vogel et tain all metal binding motifs (Schenk et al., al., 2001). 2000). The existence of these small PAPs was In mammals, a role of PAPs is ascribed to deduced from genomic analysis and con- iron transport (Buhi et al., 1982), bone resorp- firmed by cloning of cDNA sequences ob- tion (Hayman et al., 1996), antigen presenta- tained from mRNA template isolated from Vol. 50 Plant purple acid phosphatases 1247 plant tissues. The phylogenetic analysis sug- samine and the terminal N-acetylglucosamine gests that small PAPs are closely related to residues; some have additional, terminal their mammalian and bacterial homologs, in galactosyl residues. The glycan pool is highly contrast to large plant PAPs, which are more heterogeneous, which is typical of secreted homologous to the enzymes found in fungi plant enzymes. The three-dimensional struc- and mycobacteria. This may indicate that the ture of this protein is known (Sträer et al., division between small and large PAPs 1995) (Fig. 1). The kbAP dimer is heart- groups was a very early event in phospho- shaped with dimensions of 40 ´ 60 ´ 75 C. evolution. There are two domains in each of its subunits: a smaller N-terminal domain (about 120 resi- dues) and a larger C-terminal domain (about LARGE PLANT PURPLE ACID 210 residues) with [Fe(III)-Zn(II)] metallic PHOSPHATASES center. The subunits are covalently bound by disulfide bridge between cysteines 345 resid- The most comprehensively characterized en- ing in the C-terminal domain. The N-terminal zyme among 55 kDa PAPs was purified from domain is formed by two sandwiched b red kidney bean (Beck et al., 1986). The kid- sheets, each composed of three antiparallel b

Figure 1. 3D-structure of purple acid phosphatase from red kidney bean (kbAP). The protein is a homodimer with disulfide linkage between cysteines located at the C-terminal domains. The figure was made with Swiss-PDB Viewer (Guex & Peitsch, 1997) and rendered in POV-Ray 3.5. ney bean enzyme (kbAP) contains 432 amino- strands. One edge of this sandwich is shielded acid residues per monomer (Klabunde et al., by an additional b strand. Comparison with 1994; Stahl et al., 1994) with five N-glyco- known structures of monomeric mammalian sylation sites, and its sugar moiety comprises PAPs shows that this N-terminal domain is of about 11% of the total molecular mass. All absent in mammalian enzymes (Klabunde et N-glycans have a complex-type xylose-contain- al., 1995). The C-terminal domain contains ing structure, most have fucose residues at- fragments of a and b structures and its core tached to asparagine-bound N-acetylgluco- is composed of two sandwiched mixed b 1248 M. Olczak and others 2003 sheets (Fig. 2). In each sheet the metal-coordi- group. The catalysis is finished by an attack nating motif babab (characteristic for all of a water molecule upon Fe(III) ion, causing metallophosphoesterases) is present. The an inversion of configuration and release of iron ion is coordinated by Tyr167, by the the phosphate group. The enzyme is relatively non-specific, with some preference for ATP (Beck et al., 1986). Cloning and comparative modeling of two 55 kDa PAPs from sweet potato showed high sequentional and structural homology to the red kidney bean enzyme (Durmus et al., 1999b). In one sweet potato PAP form a Fe-Mn binuclear metal center was found (Schenk et al., 2001), in the other — a Fe-Zn center, identical with the kbAP metal center (Durmus et al., 1999a). In the Arabidopsis thaliana genome twenty nine potential PAP genes have been identi- fied (Li et al., 2002). Twenty four putative en- zymes contained a typical for PAPs set of Figure 2. Topology diagram of the kbPAP mono- seven amino-acids residues involved in metal mer. binding. One putative protein lacked four of b-Strands are shown as triangles and a-helices as cir- these seven residues, four others had metal li- cles. Metal-coordinating amino-acid residues are num- gating sequences more similar to those in bered and depicted with one-letter code. Modified from non-PAPs yeast, bacterial or human metallo- Klabunde et al., 1996. phosphoesterases with or phos- phodiesterase activity. This group is e N -atom of His325 and by the carboxylate evolutionarily distinct from typical large and e group of Asp135. The N -atom of His286, the small PAPs and its biochemical and d N -atom of His323 and amide oxygen of enzymatic properties are unknown. Asn201 coordinate the zinc ion. Both metal Out of twenty four PAPs sequences of ions are bridged by carboxylate group of A. thaliana, eighteen cDNAs were synthe- Asp164. sized using the cytosolic, mature mRNA tem- plate. Most of the putative proteins may be In PAP metal-assisted catalysis the SN2-type mechanism is proposed (Klabunde et al., classified as large PAPs (molecular mass of 1996) (Fig. 3). The phosphate group of the approx. 55 kDa per subunit); two of them, substrate interacts with the zinc ion by one of AtPAP7 and AtPAP8, belong to the small the non-estrified oxygen atoms. Other inter- PAPs family. In addition, the splicing vari- actions include His202 and His296. This sub- ants of two sequences (AtPAP10 and strate is attacked by Fe(III) bound hydroxide AtPAP13), truncated at the N-terminus, were ion. As a result, reorientation of phosphate found. It was shown that the transcript level group occurs and a pentacoordinate interme- of AtPAP10, a large PAPs family member, de- diate (transition state) bound to two metal pended on phosphate concentration in the ions and two His residues (202 and 296) is medium. formed. Subsequently, His296 is replaced in Our laboratory has been involved in re- hydrogen bonding at transition state by search on yellow lupin phosphatases for His295. After shift, His296 acts as a general many years. Non-specific acid phosphatase acid by protonation of the leaving alcohol (AP1), with some preference for phos- Vol. 50 Plant purple acid phosphatases 1249 phoenolpyruvate but with low affinity for which suggests, unlike the red kidney bean ATP from yellow lupin seeds belongs to the enzyme, that they are non-covalently bound. large PAPs (Olczak et al., 1997). The enzyme This has recently been confirmed by the anal- is a homodimer, containing 7% carbohydrate ysis of AP1 sequence obtained from its cDNA with a known glycan structure. Although the (Olczak & Watorek, 2003). Unlike kbAP, the majority of sequenced N-glycans belong to the lupin AP1 lacks disulfide bridge-forming paucimannosidic type, characteristic for cysteine residues around position 340–370. A plant vacuolar glycoproteins, 17% of isolated single cysteine in the sequence is localized in structures were found to be of the high-man- position 119. In addition, we have recently nose type. Most of the complex glycans were characterized cDNA for another lupin PAP, both fucosylated and xylosylated; some were AP2, abundant in lupin root (Olczak & either fucosylated or xylosylated (Olczak & Watorek, 2003). This enzyme is structurally Watorek, 1998). During dormancy 50 kDa related to the red kidney bean PAP and subunits of AP1 undergo N-terminal limited contains a cysteine residue in position 372.

Figure 3. Mechanism of phosphomonoesters hydrolysis by PAP. The pentacoordinate transition state is presumed to be stabilized by the metal ions, by His202, and by His296. The release of the alcohol component under inversion of the configuration at the phosphorus is presumably promoted by the protonation by His296. The release of the phosphate group requires attack of the water molecule at Fe(III) in order to start another cycle of catalysis. Reprinted from Klabunde et al., 1996, with permission of Elsevier. proteolytic degradation to 44 kDa (Olczak & We have purified and characterized protein Watorek, 2002). AP1 subunits dissociate dur- and carbohydrate part of a novel metallo- ing SDS electrophoresis in non-reducing con- phosphatase, diphosphate nucleoside-specific ditions (without disulfide bridge reduction), phosphohydrolase (PPD1) (Olczak et al., 1250 M. Olczak and others 2003

2000; Olczak & Watorek, 2000). The enzyme Arabidopsis genome) suggests that the divi- contains a full PAP metal-binding motif. Sur- sion of the PAPs family between "small" (35 prisingly, its overall homology to typical, kDa), mammalian-like PAPs and non-specific large PAPs is less than 27%. The molecular dimeric enzymes with approx. 55 kDa per sub- mass of the PPD1 subunit is 75 kDa, includ- unit ("large" PAPs) may be not complete; ing 4–6% of N-linked sugar oligomers, i.e., it other purple acid phosphoesterases, like the is significantly larger than a typical, large PPD group, unrelated to either "small" or PAP polypeptide (55 kDa). Although we have "large" PAPs have still not been characterized found that the monomer of PPD1 could be en- in details. zymatically active, the native protein is proba- The most representative plant PAPs se- bly a homopolymer composed of noncova- quences are presented in Table 1, comprising lently bound monomers (unpublished data). only enzymes cloned, sequenced and purified PPD1 cleaves pyrophosphate bonds in diphos- from plant material. Analysis of these se- phonucleosides and phosphodiester bonds in synthetic phosphodiesters with a pH opti- mum at 6.25. Its physiological role could be related to regulation of diphosphonucleo- sides or pyrophosphate levels in plant metab- olism. The carbohydrate moiety is composed of twenty four different glycan structures of high-mannose, paucimannosidic or complex type. Among complex type glycans, rare structures with Lewisa epitope were identi- fied. Recent cDNA analysis showed that PPD1 belongs to a new group of plant metallophosphatases (Olczak & Olczak, 2002). Additional genes and transcripts (PPD2-PPD5) were found in yellow lupin tis- sues. To date very little is known about the bi- ological function of this group; however, a strong homology to PPD1, the only purified and characterized member of the PPD family, suggests similar enzymatic properties. The sequence analysis of PPD proteins may indi- cate different localization of the enzymes in the cell. PPD1 is a soluble, secreted protein, PPD2 is predicted to be a membrane enzyme with a high probability of ER localization, and PPD4 is probably located in chloroplasts. For PPD3 and PPD5 only fragments of the se- Figure 4. The phylogenetic tree of plant purple quences are known. Alignment of PPD pro- acid phosphatases (modified from Olczak & teins with small and large plant PAP mem- Watorek, 2003). bers shows that PPD enzymes have an addi- The large plant PAPs are divided into two subfamilies tional, non-homologous sequence at the N-ter- differing in subunit linkage. minus, about 150 amino-acids residues in length. The existence of the PPD group (a few quences allowed to hypothesize that the putative, similar proteins are present in the "large" PAPs composed of two 50–55 kDa sub- Vol. 50 Plant purple acid phosphatases 1251 units can be divided in two subfamilies differ- part of the structures consists of paucima- ing in the degree of homology and the pres- nnosidic xylosylated and fucosylated ence of cysteine residues in positions close to N-glycans. Typically, one large (55 kDa) PAP 120 and around 340–370 (Fig. 4). The first subunit contains 3–5 potential sites of N-gly- subfamily comprises of lupin AP1, phospha- cosylation and approx. 10% sugar content tases from rice and onion, and some putative (Stahl et al., 1994; Olczak & Watorek, 1998); Arabidopsis enzymes. They show 76–68% however, for proteins secreted outside the cell homology to AP1. These enzymes do not have and induced by low phosphate level, the sugar cysteine residues around position 340–370 content may be significantly higher (Miller et and they are unable to form a disulfide bridge al., 2001). between subunits. All of them have a cysteine Most known PAPs are secreted, soluble pro- residue around position 120, which does not teins, except for glycosyl-phoshatidylino- form a linkage between two subunits. For two sitol-anchored phosphatase isolated from members of this subfamily preferences for Spirodela oligorhhiza cell membranes (Morita phosphoenolpyruvate (PEP) are known. The et al., 1998; Nakazato et al., 1999). This is the second subfamily is formed by the majority of only known PAP with experimentally proved known plant PAPs, including the red kidney membrane localization. Although homolo- bean enzyme and PAP izoenzymes isolated gous to other family members, the enzyme from batatas and lupin AP2. This subfamily from Spirodela oligorrhiza has a neutral pH has 59–54% homology to AP1, contains optimum, which is unusual for PAPs, gener- cysteine 370 (sometimes also cysteine 120) ally highly active at pH 5–5.5. The explana- and is able to form a disulfide bridge between tion of this phenomenon is not known. the subunits. Although the data concerning Some enzymes from the PPD group may be substrate specificity of the second large PAP also localized in membranes, and one of subfamily are very limited, ATP seems to be them, PPD2, is assumed to be an ER-mem- the preferential substrate. brane protein, having a non-cleavable trans- The phylogenetic analysis showed that the membrane domain at the N-terminus; how- most distinct from mammalian PAPs are the ever, the enzyme has not been purified from plant high molecular mass lupin PPD en- plant tissue nor its localization was proved ex- zymes (Olczak & Olczak, 2002) and perimentally (Olczak & Olczak, 2002). purified from soybean (Hegeman & Grabau, Recently the sequence of soybean PAP with 2001). Database search for proteins homolo- 82% homology to secretable lupin AP1 en- gous to PPD lupin NDPases/phosphodieste- zyme was published (Liao et al., 2003). The rases proved that these enzymes are unique sequence contains unusual for PAP putative for higher plants, and we found similar puta- mitochondrion targeting transit peptide mo- tive proteins only in Arabidopsis genome (not tif. published). As described earlier, the subunits of large plant PAPs form dimeric structures linked by disulfide bond or only by some non-covalent POSTTRANSLATIONAL interactions. The analysis of the presence and MODIFICATIONS OF PLANT PAPs localization of cysteine around position 120 and/or around position 360, compared to the All known purple acid phosphatases are total number of cysteine residues in known N-glycosylated, which is typical for secreted large PAPs sequences strongly suggests that plant enzymes. Although data concerning de- there are no internal disulfide linkages stabi- tailed structures of attached N-glycans are lizing the subunit structure (Table 1). It is not limited, it seems that in PAPs the prevailing known, why large purple acid phosphatases 1252 M. Olczak and others 2003 form dimeric structures, in contrast to small ters. The same function can be assigned to plant and mammalian PAPs, which are enzy- PAPs localized in vacuoles, taking part in uti- matically active as monomeric proteins. lization of some vacuolar metabolites. The role of phosphate acquisition from glycolytic PEP during low-phosphate stress was pro- FUNCTION OF PLANT PAPs posed by Duff et al. (1994); however, this mechanism requires the transport of PEP Purple plant acid metallophosphatases are into, and pyruvate out of the vacuoles, which abundant in plant tissues. Most PAPs are un- has not been discovered in plant tissues. specific, hydrolyzing a broad spectrum of Some PAPs play an auxiliary role in the utili- phosphate esters, including ATP, PEP, sugar zation of phytate, one of the most important

Table 1. Selected properties of plant purple acid phosphatases

aThe positions of cysteines in non-mature protein containing a signal sequence; bWithout cysteines in signal c d e f g peptide; Olczak & Watorek, 2003; Olczak et al., 1997; Shinano et al., 2001; Beck et al., 1986; Miller et al., 2001; hHegeman & Grabau, 2001; iOlczak et al., 2000; 2001; NA, not applicable. phosphates, mononucleotides and inorganic phosphate storage compounds in plants. Dur- pyrophosphate. Their function is unknown; ing germination, the PAP-phytase isolated from although some biological functions have been soybean cotyledones (Hegeman & Grabau, proposed. First, regulation of some PAPs 2001) efficiently hydrolyses phytate. Homolo- transcripts by phosphate level in the medium gous phytase sequences also have been found in and soil strongly suggests an important role Arabidopsis genome (Li et al., 2002). However, for these enzymes in phosphate acquisition. the majority of plant phytate hydrolyzing activ- Phosphate-regulated PAPs can be secreted ity is probably performed by enzymes unrelated outside the root cells to the extracellular envi- to the PAP family. For example, the cDNA syn- ronment, hydrolyzing various phosphate es- thesized on maize mRNA template encodes 38 Vol. 50 Plant purple acid phosphatases 1253 kDa protein, which is phylogenetically distinct vivo, but it is not an easy task because of the from PAPs (Mougenest et al., 1997). The maize presence of numerous highly homologous enzyme is related to phytate-hydrolyzing PAPs in the same plant tissue. The over- histidine acid phosphatases found in fungi expression of PAPs known only from its DNA (Mitchell et al., 1997). coding sequence, not purified from plant ma- NDPase/diphosphoesterase, PPD1, isolated terial, would be useful in PAPs investigation, from yellow lupin may be involved in regula- for example in substrate specificity analyses, tion of diphosphonucleotide or pyropho- crystallography studies and site-directed mu- sphate level in plant cells (Olczak et al., 2000). tagenesis. Recently, recombinant fully active The peroxidase activity of mammalian and red kidney bean PAP has been overexpressed plant small PAPs (Pozo del et al., 1999) may in insect baculovirus system (Vogel et al., suggest that these enzymes are involved in re- 2002). moval of reactive oxygen compounds in stressed or senescent plant organs. In mam- malian PAPs, the phosphatase and oxygen REFERENCES radical-generating activities are functionally independent as shown by site-directed muta- Allen SH, Nuttleman PR, Ketcham CM, Roberts genesis of a murine recombinant purple acid RM. (1989) Purification and characterization phosphatase (Kaija et al., 2002). of human bone tartrate-resistant acid The two metal ions per each subunit of a phosphatase. J Bone Miner Res.; 4:47–55. PAP molecule and the abundance of these en- Beck JL, McConaghie LA, Summors AC, Arnold zymes in plant tissues may suggest that the WN, de Jersey J, Zerner B. (1986) Proper- proteins take part in iron, zinc and molybde- ties of a purple acid phosphatase from red num transport and storage. kidney bean: a zinc-iron metalloenzyme. Biochim Biophys Acta.; 869: 61–8. Buhi WC, Ducsay CA, Bazer FW, Roberts RM. CONCLUDING REMARKS (1982) Iron transfer between the purple phosphatase uteroferrin and transferrin and For more than 30 years many papers on its possible role in iron metabolism of the fe- plant purple acid phosphates have been pub- tal pig. J Biol Chem.; 257: 1712–3. lished; however, data describing this enzyme Campbell HD, Zerner B. (1973) A low-molecu- family are still fragmentary and many ques- lar-weight acid phosphatase which contains tions remain open: What is the function of iron. Biochem Biophys Res Commun.; 54: non-catalytic N-terminal domains in large 1498–03. PAPs? What is the biological importance of Duff SMG, Sarath G, Plaxton WC. (1994) The the dimeric structure of large PAPs, as con- role of acid phosphatases in plant phospho- trasted with small PAPs, which are functional rus metabolism. Physiol Plant.; 90: 791–800. as monomers? Why do some PAPs contain Durmus A, Eicken C, Sift BK, Kratel A, Kappl two iron ions in a subunit when others have R, Hütermann J, Krebs B. (1999a) The ac- iron and zinc or manganese as a second ion? tive site of purple acid phosphatase from Is the PAPs peroxidase activity biologically sweet potatoes (Ipomoea batatas). Metal con- important for plant tissues? tent and spectroscopic characterization. Eur The combined application of genetic, bio- J Biochem.; 260: 709–16. chemical and immunological methods is nec- Durmus A, Eicken C, Spener F, Krebs B. essary to elucidate these problems. Antibod- (1999b) Cloning and comparative modeling ies to a particular PAP enzyme could be a of two purple acid phosphatase isozymes powerful tool in investigating the enzyme in 1254 M. Olczak and others 2003

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