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J. Appl. Glycosci., 60, 21‒27 (2013) doi:10.5458/jag.jag.JAG-2012_016 ©2013 The Japanese Society of Applied Glycoscience Special Issue: Metabolism, Structure and Properties Review Variation of Storage Polysaccharides in Phototrophic (Received October 24, 2012; Accepted December 3, 2012) (J-STAGE Advance Published Date: January 25, 2013) Eiji Suzuki1,＊ and Ryuichiro Suzuki1 1Department of Biological Production, Faculty of Bioresource Sciences, Akita Prefectural University (241‒438 Kaidobata-Nishi, Nakano, Shimoshinjo, Akita 010‒0195, Japan)

Abstract: Phototrophic eukaryotes were established by the engulfment of oxygenic phototrophic prokary- otes () by a heterotrophic host. This process, called primary endosymbiosis, gave rise to the taxon , which comprises green , rhodophytes and . Further rounds of endosymbiotic events produced a variety of phototrophic organisms, which could accumulate α-1,4-/α-1,6- (including starch) or β-1,3-/β-1,6-glucans. In this article, we review the recent progress in the study of the intracellular localization and molecular forms of storage , especially starch, among the known and related organisms.

Key words: Archaeplastida, cyanobacteria, endosymbiosis, semi-, starch

Starch is produced and stored in of tissues characteristics of these polysaccharides, especially starch-like ( in leaves and amyloplasts in seeds and tubers). α-glucans in representative organisms from each lineage, as It is widely accepted that the organelle was derived from an revealed by recent studies are discussed. independent organism, which was closely related to the extant cyanobacteria, through an event known as endosym- The form of storage polysaccharide and the site of its biosis.1) During the course of evolution of photosynthetic accumulation in various phototrophic organisms. organisms, the “primary” endosymbiosis gave rise to plastids 1. Cyanobacteria. in green plants (including land plants and green ), red In the bacterial domain, photosynthetic organisms are algae and glaucophytes,2) which are collectively designated distributed in 6 phyla, but the members of only 1 phylum, as Archaeplastida.3,4) Moreover, some green and cyanobacteria, are capable of oxygenic , were thought to be subjected to secondary endosymbiosis, which can be achieved by the operation of 2 distinct types where they were engulfed by heterotrophic eukaryotes, of reaction centers (type II/quinone type, and type resulting in their diversification into euglenophytes and I/FeS type).10) All the other photosynthetic have , which acquired plastids from green only 1 type of reaction center (either quinone- or algae, and stramenopiles, , cryptophytes, and FeS-type) and carry out anoxygenic (non-oxygen-evolving) (dinoflagellates and apicomplexans), which photosynthesis, which is confined to the bacterial domain.10) acquired plastids from a red alga.2,5) These organisms have Cyanobacteria are thus regarded as the progenitors of all plastids enveloped by 3 or 4 membranes, which are the relics photosynthetic eukaryotes. of multiple rounds of previous endosymbiotic events.6) In the cyanobacterial cells, photosynthetic carbon assimi- Furthermore, some of these organisms subsequently lost lation and accumulation of storage polysaccharide takes their ability to perform photosynthesis, while they retained place in the cytoplasmic compartment (Fig. 1). While most plant-like genes (Trypanosoma related to euglenophytes)7) species of cyanobacteria produce soluble , several or even the remnants of plastids ( unicellular, diazotrophic (nitrogen-fixing) species synthe- related to dinoflagellates).8,9) The complex evolutionary size insoluble α-glucan, which is closely analogous to histories of these organisms are reflected in the diversity of amylopectin found in cereal plants.11‒14) The latter polysac- their metabolism. The molecular form of storage polysac- charide was termed as semi-amylopectin, based on its lower charides (α- or β-glucans) and their intracellular localization content of long glucan chains, as compared to that of vary greatly depending on the lineage of the organism. In amylopectin.11) A few cyanobacterial species even contain this mini-review, the variation in the forms of storage polysac- in addition to semi-amylopectin.12,14) In the organisms charide among photosynthetic organisms is summarized. The containing semi-amylopectin (plus amylose), the starch granules have been observed as electron-transparent particles ＊Corresponding author (Tel. +81‒18‒872‒1653, Fax. +81‒18‒872‒1681, in the cells.15‒17) The occurrence of a starch-like substance in E-mail: [email protected]). photosynthetic prokaryotes is highly intriguing in the light Abbreviations: AGPase, ADP- pyrophosphorylase; DP, degree of of evolution of starch metabolism.13,18,19) polymerization; FACE, fluorophore-assisted carbohydrate electrophoresis; GBSS, granule-bound starch synthase; ISA, isoamylase; SS, starch synthase. 22 J. Appl. Glycosci., Vol. 60, No. 1 (2013)

α α α α α α α α α α α α β β β β β β

Fig. 1. Intracellular localization and the molecular form of storage polysaccharide in various phototrophic organisms. Tabular (upper) and schematic (lower) representations are indicated together to assist comprehension of the variety of polysaccharide species and localization. Upper panel: Green plants consist of chlorophytes () and land plants, and are shaded in green, while rhodophytes (red algae) are shaded in red. Organisms whose plastids are derived from a red alga (cryptophytes, dinoflagellates, stramenopiles, and haptophytes) or green algae (euglenophytes and chlorarachniophytes) are indicated as “red” or “green,” respectively. As the storage carbohydrates, α-glucans (comprising α-1,4 glucan chains with branches at α-1,6 linkages) or β-glucans (including β-1,3 glucans with branches at β-1,6 linkages or β-1,6 glucans with branches at β-1,3 linkages) are shaded in green or yellow, respectively. Lower panel: Green and yellow ovals represent α-1,4 (α-1,6) and β-1,3 (β-1,6) glucans, respectively. Oval lines indicate lipid membranes. For cyanobacteria (Gram-negative bacteria), plasma membrane and outer membrane are shown. For eukaryotic algae, plasma membrane, envelope membranes, periplastidal endoplasmic reticulum membranes, and glucan storage vesicle or vacuole membrane are shown. Nucleus, mitochondria, , other organelles, membranes, and pyrenoid within the plastids are not shown for simplicity. Red and green lines indicate that the plastids were derived from rhodophyte and chlorophyte algae through secondary endosymbiosis, respectively. For dinoflagellates and euglenophytes, it remains to be elucidated whether the intermediate membrane of the triple plastid envelope was derived from or host.

2. Archaeplastida: organisms derived by primary endosym- several granules of starch were distributed in the stroma biosis. between the thylakoid membranes.26) Ostreococcus tauri is In many cases (if not all), accumulation of storage polysac- an ancient green alga belonging to Prasinophyceae and is the charide in various algae appears to be associated, structurally smallest free-living eukaryote.27) The organism has only 1 and hence metabolically, with the distinct protein body in the , apparently lacks pyrenoids and retains a single plastid, the pyrenoid,20,21) which is primarily composed of starch granule at the chloroplast center.28) During plastid ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) division, the starch granule constricts in the middle and then protein.22,23) In a model green alga reinhardtii, partitions into 2 plastids that belong to the daughter cells.28) starch was observed as “the sheath” around the pyrenoid.20) Unlike in green plants, the storage polysaccharide in red Distribution of starch granules within the chloroplast of algae and glaucophytes is accumulated in the (Fig. green algae may also differ depending on the growth 1). The storage polysaccharide in the red algae is referred to conditions. For example, starch granules were dispersed in as floridean starch, because the color of the iodine complex the stroma of the chloroplast in Chlorella kessleri strain 11h is not blue, but varies from deep violet to brown.29,30) As grown with an elevated CO2 concentration (3%), while described below in detail, recent studies have shown that the starch accumulated around the developed pyrenoid in the polysaccharide species in red algae are diverse, ranging from 31‒35) organism exposed to a lower CO2 concentration (0.04%, or glycogen to semi-amylopectin with or without amylose. In 24) air-level). During the exposure to low CO2 concentration, a unicellular red alga Porphyridium cruentum, starch granules relative amylose content increased from 9‒14% to 28%.25) A lacking a bounding membrane were distributed throughout study with Chloromonas lacking pyrenoids showed that the cytosol, while the pyrenoid was located at the center of Suzuki et al.: Starch in Various Phototrophic Organisms 23 the chloroplast.20) In another unicellular red alga, Rhodoso- In euglenophytes, chlorarachniophytes, stramenopiles and rus marinus, the pyrenoid was found to be bounded by haptophytes, the storage polysaccharide is β-1,3-glucan (with peripheral thylakoid and chloroplast envelope membranes, or without β-1,6 branching linkages), which is localized in protruding into the cytosol, and was surrounded by starch vacuoles. The storage polysaccharide in euglenophytes is an granules.36) In the latter case, although starch granules and unbranched β-1,3-glucan called paramylon,50) which forms the pyrenoid seem to be physically associated, they are highly crystalline, fibrillar granules bounded by a membrane separated by multiple membranes. in the cytosol (Fig. 1).51‒54) It is not clear whether the membrane Glaucophytes are a small group of freshwater microalgae surrounding the paramylon granule constitutes an organelle, retaining apparently ancient traits in their cellular structure, that is comparable to the vacuole. A study with 2 species of such as a peptidoglycan layer around the chloroplast (termed Chlorarachnion showed that β-1,3-glucan, with an approxi- as “cyanelle”), and a carboxysome (also called central body) mate degree of polymerization (DP) of 23 was accumulated at the center of the cyanelle, both reminiscent of those in a vacuole (Fig. 1), which encapsulated the pyrenoid observed in extant cyanobacteria.37,38) In the cells of a model protruding from the chloroplast.55) While there appeared to be a Cyanophora paradoxa, starch granules were close association between the stored carbohydrate and the observed in the cytosol, apart from the central body in the pyrenoid in Chlorarachnion, they were separated by 5 cyanelles.37,38) membranes (the vacuole membrane and 4 layers of the chloro- As in cyanobacteria, storage-polysaccharide is biosynthe- plast envelope).55) sized in green plants by the ADP-glucose pathway, which Stramenopiles (meaning hollow hairs attached to 1 of the operates in the plastids,39) while the UDP-glucose pathway is 2 flagella) or (meaning 2 differently shaped functional in the cytosol of red algae and glaucophytes.40‒42) flagella) are the most flourishing phototrophic eukaryotes on However, in both of the green and the red lineages, the this planet,56) and include , , and other pathway of starch (α-glucan) biosynthesis is composed of phototrophic and non-phototrophic microorganisms.3,4) Water- derived from the endosymbiont, as well as from the soluble β-D-glucan in brown algal macrophytes (Laminaria host.43) Only in the green plants, it is postulated that the and related species) is called laminaran (or laminarin57)), which biosynthetic pathway for starch was transiently established was shown to comprise β-1,3-linked chains with occasional in the cytosol and subsequently rewired into the plastids.12,19) β-1,6-linked branches.58,59) Laminaran exhibited DP of approxi- Although the accumulation of starch in the stroma of plastids mately 25, and a substantial proportion of the molecules is regarded as a common trait, it is rather exceptional among contained a mannitol moiety at their reducing end through β-1,1 photosynthetic organisms exclusive to green plants (Fig. 1). linkage.58‒61) The storage polysaccharide in diatoms and haptophytes is 3. Organisms with secondary plastids. chrysolaminaran (originally termed as chrysolaminarin62)), Among organisms with secondary plastids, starch-like despite a distant phylogenetic relationship between the 2 α-glucans have been found in cryptophytes and alveolates algal groups. The chrysolaminaran of diatoms consists of (dinoflagellates and Apicomplexa protozoa), whose plastids β-1,3-linked glucan chains with the presence of β-1,6-linked are of red algal origin. chains,58) or branching at C-2 and C-6 positions and DP In cryptophytes, starch granules accumulate in the periplas- values of 24‒80.63,64) The storage glucan of the , tidal (also spelled as periplastidial) compartment (correspond- Phaeocystis globosa was reported to consist of about 20 ing to the cytosol of the red algal endosymbiont) between 2 glucose residues, linked mainly by β-1,3-glucosidic bonds, inner and 2 outer envelope membranes of the chloroplast with branching at C-6 positions.65) In contrast, studies with 2 (Fig. 1).44) Some of the starch granules are closely associated other haptophyte species showed that chrysolaminaran with the pyrenoid protruding into the periplastidal compart- comprised primarily β-1,6-linked glucan with a smaller ment, even though starch and the pyrenoid are separated by proportion of β-1,3-linkages and had a mean DP of 106 2 inner envelope membranes.44,45) Cryptophytes and chlorarach- (Emiliania huxleyi) or 203 (Pleurochrysis haptonemofera).66,67) niophytes are known to retain a degenerated nucleus of the As described above, the molecular structure of laminaran and eukaryotic endosymbiont, termed as nucleomorph46,47) in the chrysolaminaran seems to be quite diverse and may differ periplastidal compartment and are therefore intriguing models depending on the source organisms. In addition, although it has for investigating the mechanism of secondary endosymbiosis. been reported (in studies with a limited number of species) that The predicted outcome of secondary endosymbiosis would chrysolaminaran is stored in vacuoles in diatoms68,69) and be that the plastids should be surrounded by 4 membranes. haptophytes70,71) (Fig. 1), extensive examination of the intracel- Therefore, how or why dinoflagellates (as well as eugleno- lular distribution of these β-glucans remains to be carried out. phytes) have plastids bounded by 3 membranes, while apicom- plexans, relatives of dinoflagellates, have plastids bounded by 4 Variation in the properties of α-glucans in phototrophic membranes remains unresolved.5,6,21) Following secondary microorganisms. endosymbiosis, starch metabolism appears to be further Through the examination of 26 species of cyanobacteria, relocated in dinoflagellates and apicomplexans. In a hetero- Nakamura et al.11) found that a few species accumulated a trophic dinoflagellate Crypthecodinium cohnii and an distinct α-glucan (named as semi-amylopectin) instead of apicomplexan parasite Toxoplasma gondii, starch granules glycogen. The relative amount of long chains (DP ≥ 37) of have been shown to be accumulated in the cytosol (Fig. 1).48) α-1,4-glucan in semi-amylopectin was 2‒6% (depending on Starch granules in cryptophytes and alveolates are synthe- the species), which was an amount intermediate to that of sized by the UDP-glucose pathway, which originated from amylopectin in rice endosperm (6.7%) and glycogen in red algae.45,48,49) cyanobacteria (< 1%).11,14) The most abundant α-1,4-glucan 24 J. Appl. Glycosci., Vol. 60, No. 1 (2013) chains in semi-amylopectin were found to have DP of 11‒12, STA3 (soluble starch synthase III, SS III),76,77) STA6 (small which was similar to that of cereal amylopectin, while those subunit of AGPase),78) STA7 (isoamylase, ISA),79) STA8 (a in glycogen of cyanobacteria were in the range of DP polypeptide in multimeric ISA complex)80) and STA11 6‒8.11,14) The molecular mass of semi-amylopectin was much (α-1,4-glucanotransferase).81) Starch from the wild type and greater than that of glycogen and virtually indistinguishable sta2 mutant of Chlamydomonas displayed the A-type from that of amylopectin.11,12,14) The water-insoluble polysac- allomorph (Table 1): starch in sta3 and sta8 mutants exhibit- charide preparations purified from 3 strains of cyanobacteria ed B-type: and starch in sta2/sta3 double mutant showed exhibited thermal properties and crystallinity with A-type C-type diffraction pattern, a mixture of A- and B-type.80,82) diffraction pattern (Table 1).14) Gel filtration analysis after The ability of starch production was completely or partially debranching treatment indicated the presence of B2 chains in lost in sta7 and sta8 mutants, respectively, and substituted semi-amylopectin: evidence supporting that the polysaccha- by the accumulation of phytoglycogen.79,80) Analysis of ride has tandem-cluster structure.14) Furthermore, one of these purified starch granules from several green algae, including strains, Cyanobacterium sp. CLg1 had amylose in addition to Chlorella vulgaris, Scenedesmus basilensis and Chlamydo- semi-amylopectin.12,14) Based on these properties, we propose monas sp., showed that all the starch preparations consisted that semi-amylopectin with or without amylose in cyanobac- of amylopectin and amylose and displayed A-type diffrac- teria should be called as “cyanobacterial starch.” tion pattern.83) The A-type pattern of the starch granules The chain length profile essential to distinguish remained unchanged whether the Chlorella vulgaris cells semi-amylopectin from glycogen can be determined by the were grown at 20, 30°C or 40°C.84) Examination of the fluorophore-assisted carbohydrate electrophoresis (FACE) genome sequence of a prasinophyte Ostreococcus taurii method.72) Since the method is applicable for the analysis of indicated the presence of multiple forms of enzymes for either purified polysaccharide granules or crude methanol each step of starch metabolism, including AGPase, SS, extracts of the cells,73) it is suitable for examination of a branching and ISA.28) The metabolism of starch in small amount of material as well as a large number of green plants is therefore virtually complete in the very early samples simultaneously. stage of their evolution. The starch of O. taurii showed the The unicellular green alga Chlamydomonas reinhardtii B-type allomorph (Table 1).28) served as a model system to study of the mechanism of Recent studies with unicellular red algae demonstrated a starch metabolism. Mutants with defects or alterations in considerable variability in the physicochemical property of starch metabolism were characterized, and the genetic loci the storage α-glucans in these organisms. Among species encoding the responsible enzymes were identified, including belonging to the most ancient , Cyanidium STA1 (large subunit of ADP-glucose pyrophosphorylase, caldarium and produced glycogen, AGPase),74) STA2 (granule-bound starch synthase I, GBSSI),75) while the model rhodophyte Cyanidioschyzon merolae

Table 1. Property of α-glucans in cyanobacteria, microalgae and related organisms. Organism Type of α-glucan Allomorph a Reference Cyanobacteria Synechococcus elongatus PCC 7942b Glycogen n/a c 11), 14), 86) Cyanobacterium sp. NBRC 102756 Semi-amylopectin A-type 11), 14) Cyanobacterium sp. CLg1 Semi-amylopectin + amylose A-type 12), 14) Cyanothece sp. ATCC 51142 Semi-amylopectin A-type 12), 14) Chlorophytes (green algae) Ostreococcus tauri Amylopectin + amylose B-type 28) Chlorella vulgaris Amylopectin + amylose A-type 83) Chlamydomonas reinhardtii Amylopectin + amylose A-type 82) Rhodophytes (red algae) Cyanidium caldarium Glycogen n/a c 33) Galdieria sulphuraria Glycogen n/a c 34) Cyanidioschyzon merolae Semi-amylopectin A-type 35) Rhodosorus marinus Semi-amylopectin + amylose weak A-type 34) Porphyridium purupureum Semi-amylopectin + amylose A-type 33) Porphyridium sordidum Semi-amylopectin + amylose weak A-type 34) Rhodella violacea Semi-amylopectin + amylose B-type 34) Gracilariopsis lemaneiformis Semi-amylopectin C-type 32) Glaucophyte Cyanophora paradoxa Amylopectin + amylose B-type 42) Cryptophyte Guillardia theta Amylopectin + amylose A-type 45) Dinoflagellate Crypthecodinium cohnii Amylopectin + amylose A-type 49) Apicomplexa Toxoplasma gondii Amylopectin B-type 48) a X-ray diffraction pattern. b Shown as a representative of most cyanobacterial species. c Not applicable. Suzuki et al.: Starch in Various Phototrophic Organisms 25 synthesized semi-amylopectin and lacked amylose (Table otes. J. Eukaryot. Microbiol., 59, 429‒493 (2012). 1).33‒35) Four other species of Porphyridiales, Rhodosorus 5 ) P.J. Keeling: The endosymbiotic origin, diversification and fate of plastids. Phil. Trans. R. Soc. B, 365, 729‒748 (2010) marinus, Porphyridium purpureum, P. sordidum and Rhodel- 6 ) K. Ishida: Protein targeting into plastids: a key to understanding 33,34) la violacea contained semi-amylopectin plus amylose. The the symbiogenetic acquisitions of plastids. J. Plant Res., 118, floridean starch of R. violacea displayed B-type allomorph, 237‒245 (2005). whereas that of the other unicellular species showed A-type 7 ) V. Hannaert, E. Saavedra, F. Duffieux, J.P. Szikora, D.J. Rigden, diffraction pattern, with varying degrees of crystallinity P.A. Michels and F.R. Opperdoes: Plant-like traits associated with 33‒35) metabolism of Trypanosoma parasites. Proc. Natl. Acad. Sci. (Table 1). These observations are in contrast to the USA, 100, 1067‒1071 (2003). findings of an earlier study, in which A-type floridean starch 8 ) L. Lim and G.I. McFadden: The evolution, metabolism and was not reported to be found.85) It has been reported that a functions of the . Phil. Trans. R. Soc. B, 365, 749-763 red algal macrophyte, Gracilariopsis lemaneiformis, has (2010). floridean starch which consists of semi-amylopectin (inferred 9 ) S. Sato: The apicomplexan plastid and its evolution. Cell. Mol. Life Sci., 68, 1285‒1296 (2011). from the chain length profile), lacks amylose, and shows 10 ) M.F. Hohmann-Marriott and R.E. Blankenship: Evolution of C-type diffraction pattern (Table 1).32) It should be noted that photosynthesis. Annu. Rev. Plant Biol., 62, 515‒548 (2011). semi-amylopectin from any rhodophyte species so far 11) Y. Nakamura, J. Takahashi, A. Sakurai, Y. Inaba, E. Suzuki, S. examined by gel filtration invariably has demonstrated high Nihei, S. Fujiwara, M. Tsuzuki, H. Miyashita, H. Ikemoto, M. Kawachi, H. Sekiguchi and N. Kurano: Some cyanobacteria molecular mass, comparable to that of amylopectin in green synthesize semi-amylopectin type α-polyglucans instead of 33‒35) plants. glycogen. Plant Cell Physiol., 46, 539‒545 (2005). α-glucan-type storage polysaccharides have been charac- 12 ) P. Deschamps, C. Colleoni, Y. Nakamura, E. Suzuki, J.-L. Putaux, terized in 4 representative organisms, 1 from each of the 4 A. Buléon, S. Haebel, G. Ritte, M. Steup, L.I. Falcón, D. Moreira, distinct taxa. A glaucophyte Cyanophora paradoxa produc- W. Löffelhardt, J.N. Raj, C. Plancke, C. d’Hulst, D. Dauvillée and S. Ball: Metabolic symbiosis and the birth of the Plant Kingdom. es starch, which showes high amylose content (ranging from Mol. Biol. Evol., 25, 536‒548 (2008). 30% to 60% depending on the growth conditions) and B-type 13 ) C. Colleoni and E. 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