Abstract
During starch metabolism, the phosphorylation of glucosyl residues of starch, to be more precise of amylopectin, is a repeatedly observed process. This phosphorylation is mediated by dikinases, the glucan, water dikinase (GWD) and the phosphoglucan, water dikinase (PWD). The starch-related dikinases utilize ATP as dual phosphate donor transferring the terminal γ-phosphate group to water and the β-phosphate group selectively to either C6 position or C3 position of a glucosyl residue within amylopectin. By the collaborative action of both enzymes, the initiation of a transition of α-glucans from highly ordered, water-insoluble state to a less order state is realized and thus the initial process of starch degradation. Consequently, mutants lacking either GWD or PWD reveal a starch excess phenotype as well as growth retardation. In this review, we focus on the increased knowledge collected over the last years related to enzymatic properties, the precise definition of the substrates, the physiological implications, and discuss ongoing questions.
Similar content being viewed by others
Abbreviations
- AMY:
-
α-Amylase
- BAM, BMY:
-
β-Amylase
- BE:
-
Starch branching enzyme
- CBM:
-
Carbohydrate-binding module
- CLD:
-
Chain length distribution
- DBE:
-
Starch debranching enzyme
- G3P:
-
Glucose-3 phosphate
- G6P:
-
Glucose-6 phosphate
- GWD:
-
Glucan, water dikinase
- ISA:
-
Iso-amylase
- LDA:
-
Limit dextrinase
- LSF:
-
Starch-related phosphatase Like-Sex-Four
- MDcryst :
-
Crystalline maltodextrin
- PHS:
-
Glucan phosphorylase
- PWD:
-
Phosphoglucan, water dikinase
- SBD:
-
Starch-binding domain
- SEM:
-
Scanning electron microscopy
- sex1 :
-
Starch excess1 mutant
- SEX4:
-
Starch-related phosphatase 4
- SS:
-
Starch synthase
References
Buleon A, Colonna P, Planchot V, Ball S (1998) Starch granules: structure and biosynthesis. Int J Biol Macromol 23(2):85–112. doi:10.1016/S0141-8130(98)00040-3
Imberty A, Chanzy H, Perez S, Buleon A, Tran V (1988) The double-helical nature of the crystalline part of a-starch. J Mol Biol 201(2):365–378. doi:10.1016/0022-2836(88)90144-1
Imberty A, Perez S (1988) A revisit to the three-dimensional structure of b-type starch. Biopolymers 27(8):1205–1221. doi:10.1002/bip.360270803
Deschamps P, Colleoni C, Nakamura Y, Suzuki E, Putaux JL, Buleon A, Haebel S, Ritte G, Steup M, Falcon LI, Moreira D, Loffelhardt W, Raj JN, Plancke C, d’Hulst C, Dauvillee D, Ball S (2008) Metabolic symbiosis and the birth of the plant kingdom. Mol Biol Evol 25(3):536–548. doi:10.1093/molbev/msm280
Ball S (2012) Evolution of the starch pathway. In: Tetlow IJ (ed) Starch: Origins, structure and metabolism, vol 5., Essential reviews in experimental biologyThe Society for Experimental Biology, London, pp 29–54
Smith AM, Stitt M (2007) Coordination of carbon supply and plant growth. Plant Cell Environ 30(9):1126–1149. doi:10.1111/j.1365-3040.2007.01708.x
Geigenberger P (2011) Regulation of starch biosynthesis in response to a fluctuating environment. Plant Physiol 155(4):1566–1577. doi:10.1104/pp.110.170399
Yu HT, Xu SB, Zheng CH, Wang T (2012) Comparative proteomic study reveals the involvement of diurnal cycle in cell division, enlargement, and starch accumulation in developing endosperm of Oryza sativa. J Proteom Res 11(1):359–371. doi:10.1021/pr200779p
Yan D, Duermeyer L, Leoveanu C, Nambara E (2014) The functions of the endosperm during seed germination. Plant Cell Physiol 55(9):1521–1533. doi:10.1093/pcp/pcu089
Viola R, Pelloux J, van der Ploeg A, Gillespie v, Marquis N, Roberts AG, Hancock RD (2007) Symplastic connection is required for bud outgrowth following dormancy in potato (Solanum tuberosum L.) tubers. Plant Cell Environ 30(8):973–983. doi:10.1111/j.1365-3040.2007.01692.x
Sonnewald S, Sonnewald U (2014) Regulation of potato tuber sprouting. Planta 239(1):27–38. doi:10.1007/s00425-013-1968-z
Dominguez F, Cejudo FJ (2014) Programmed cell death (pcd): an essential process of cereal seed development and germination. Front Plant Sci 5:366. doi:10.3389/fpls.2014.00366
Pfister B, Zeeman SC (2016) Formation of starch in plant cells. Cell Mol Life Sci. doi:10.1007/s00018-016-2250-x
Yu TS, Zeeman SC, Thorneycroft D, Fulton DC, Dunstan H, Lue WL, Hegemann B, Tung SY, Umemoto T, Chapple A, Tsai DL, Wang SM, Smith AM, Chen J, Smith SM (2005) Alpha-amylase is not required for breakdown of transitory starch in Arabidopsis leaves. J Biol Chem 280(11):9773–9779. doi:10.1074/jbc.M413638200
Fulton DC, Stettler M, Mettler T, Vaughan CK, Li J, Francisco P, Gil M, Reinhold H, Eicke S, Messerli G, Dorken G, Halliday K, Smith AM, Smith SM, Zeeman SC (2008) Beta-amylase4, a noncatalytic protein required for starch breakdown, acts upstream of three active beta-amylases in Arabidopsis chloroplasts. Plant Cell 20(4):1040–1058. doi:10.1105/tpc.107.056507
Zeeman SC, Umemoto T, Lue WL, Au-Yeung P, Martin C, Smith AM, Chen J (1998) A mutant of Arabidopsis lacking a chloroplastic isoamylase accumulates both starch and phytoglycogen. Plant Cell 10(10):1699–1712. doi:10.1105/tpc.10.10.1699
Zeeman SC, Northrop F, Smith AM, Rees T (1998) A starch-accumulating mutant of Arabidopsis thaliana deficient in a chloroplastic starch-hydrolysing enzyme. Plant J 15(3):357–365. doi:10.1046/j.1365-313X.1998.00213.x
Delatte T, Umhang M, Trevisan M, Eicke S, Thorneycroft D, Smith SM, Zeeman SC (2006) Evidence for distinct mechanisms of starch granule breakdown in plants. J Biol Chem 281(17):12050–12059. doi:10.1074/jbc.M513661200
Kaplan F, Guy CL (2005) RNA interference of arabidopsis beta-amylase8 prevents maltose accumulation upon cold shock and increases sensitivity of PSII photochemical efficiency to freezing stress. Plant J 44(5):730–743. doi:10.1111/j.1365-313X.2005.02565.x
Streb S, Zeeman SC (2012) Starch metabolism in Arabidopsis. Arabidopsis Book 10:e0160. doi:10.1199/tab.0160
Seung D, Thalmann M, Sparla F, Abou Hachem M, Lee SK, Issakidis-Bourguet E, Svensson B, Zeeman SC, Santelia D (2013) Arabidopsis thaliana AMY3 is a unique redox-regulated chloroplastic alpha-amylase. J Biol Chem 288(47):33620–33633. doi:10.1074/jbc.M113.514794
Zeeman SC, Thorneycroft D, Schupp N, Chapple A, Weck M, Dunstan H, Haldimann P, Bechtold N, Smith AM, Smith SM (2004) Plastidial alpha-glucan phosphorylase is not required for starch degradation in Arabidopsis leaves but has a role in the tolerance of abiotic stress. Plant Physiol 135(2):849–858. doi:10.1104/pp.103.032631
Malinova I, Mahlow S, Alseekh S, Orawetz T, Fernie AR, Baumann O, Steup M, Fettke J (2014) Double knockout mutants of Arabidopsis grown under normal conditions reveal that the plastidial phosphorylase isozyme participates in transitory starch metabolism. Plant Physiol 164(2):907–921. doi:10.1104/pp.113.227843
Scheidig A, Frohlich A, Schulze S, Lloyd JR, Kossmann J (2002) Downregulation of a chloroplast-targeted beta-amylase leads to a starch-excess phenotype in leaves. Plant J 30(5):581–591. doi:10.1046/j.1365-313X.2002.01317.x
Edner C, Li J, Albrecht T, Mahlow S, Hejazi M, Hussain H, Kaplan F, Guy C, Smith SM, Steup M, Ritte G (2007) Glucan, water dikinase activity stimulates breakdown of starch granules by plastidial beta-amylases. Plant Physiol 145(1):17–28. doi:10.1104/pp.107.104224
Mahlow S, Hejazi M, Kuhnert F, Garz A, Brust H, Baumann O, Fettke J (2014) Phosphorylation of transitory starch by alpha-glucan, water dikinase during starch turnover affects the surface properties and morphology of starch granules. New Phytol 203(2):495–507. doi:10.1111/nph.12801
Lloyd JR, Kossmann J, Ritte G (2005) Leaf starch degradation comes out of the shadows. Trends Plant Sci 10(3):130–137. doi:10.1016/j.tplants.2005.01.001
Lorberth R, Ritte G, Willmitzer L, Kossmann J (1998) Inhibition of a starch-granule-bound protein leads to modified starch and repression of cold sweetening. Nat Biotechnol 16(5):473–477. doi:10.1038/nbt0598-473
Hizukuri S, Tabata S, Nikuni Z (1970) Studies on starch phosphate.1. Estimation of glucose-6-phosphate residues in starch and presence of other bound phosphate(s). Starke 22(10):338. doi:10.1002/Star.19700221004
Tabata S, Hizukuri S (1971) Starch phosphate. Part 2. Isolation of glucose 3-phosphate and maltose phosphate by acid hydrolysis of potato starch. Starke 23(8):267. doi:10.1002/Star.19710230803
Hoover R (2001) Composition, molecular structure, and physicochemical properties of tuber and root starches: a review. Carbohyd Polym 45(3):253–267. doi:10.1016/S0144-8617(00)00260-5
Jane J, Kasemsuwan T, Chen JF, Juliano BO (1996) Phosphorus in rice and other starches. Cereal Foods World 41(11):827–832
Ritte G, Heydenreich M, Mahlow S, Haebel S, Kotting O, Steup M (2006) Phosphorylation of C6- and C3-positions of glucosyl residues in starch is catalysed by distinct dikinases. FEBS Lett 580(20):4872–4876. doi:10.1016/j.febslet.2006.07.085
Ritte G, Scharf A, Eckermann N, Haebel S, Steup M (2004) Phosphorylation of transitory starch is increased during degradation. Plant Physiol 135(4):2068–2077. doi:10.1104/pp.104.041301
Ral JP, Colleoni C, Wattebled F, Dauvillee D, Nempont C, Deschamps P, Li Z, Morell MK, Chibbar R, Purton S, d’Hulst C, Ball SG (2006) Circadian clock regulation of starch metabolism establishes gbssi as a major contributor to amylopectin synthesis in Chlamydomonas reinhardtii. Plant Physiol 142(1):305–317. doi:10.1104/pp.106.081885
Ritte G, Lloyd JR, Eckermann N, Rottmann A, Kossmann J, Steup M (2002) The starch-related R1 protein is an alpha-glucan, water dikinase. Proc Natl Acad Sci USA 99(10):7166–7171. doi:10.1073/pnas.062053099
Yu TS, Kofler H, Hausler RE, Hille D, Flugge UI, Zeeman SC, Smith AM, Kossmann J, Lloyd J, Ritte G, Steup M, Lue WL, Chen J, Weber A (2001) The Arabidopsis sex1 mutant is defective in the R1 protein, a general regulator of starch degradation in plants, and not in the chloroplast hexose transporter. Plant Cell 13(8):1907–1918. doi:10.1105/TPC.010091
Caspar T, Lin TP, Kakefuda G, Benbow L, Preiss J, Somerville C (1991) Mutants of Arabidopsis with altered regulation of starch degradation. Plant Physiol 95(4):1181–1188. doi:10.1104/pp.95.4.1181
Baunsgaard L, Lutken H, Mikkelsen R, Glaring MA, Pham TT, Blennow A (2005) A novel isoform of glucan, water dikinase phosphorylates pre-phosphorylated alpha-glucans and is involved in starch degradation in Arabidopsis. Plant J 41(4):595–605. doi:10.1111/j.1365-313X.2004.02322.x
Kotting O, Pusch K, Tiessen A, Geigenberger P, Steup M, Ritte G (2005) Identification of a novel enzyme required for starch metabolism in Arabidopsis leaves. The phosphoglucan, water dikinase. Plant Physiol 137(1):242–252. doi:10.1104/pp.104.055954
Glaring MA, Zygadlo A, Thorneycroft D, Schulz A, Smith SM, Blennow A, Baunsgaard L (2007) An extra-plastidial alpha-glucan, water dikinase from Arabidopsis phosphorylates amylopectin in vitro and is not necessary for transient starch degradation. J Exp Bot 58(14):3949–3960. doi:10.1093/jxb/erm249
Fettke J, Eckermann N, Kotting O, Ritte G, Steup M (2006) Novel starch-related enzymes and carbohydrates. Cell Mol Biol 52:OL883–OL904. doi:10.1170/102
Mikkelsen R, Blennow A (2005) Functional domain organization of the potato alpha-glucan, water dikinase (GWD): evidence for separate site catalysis as revealed by limited proteolysis and deletion mutants. Biochem J 385(Pt 2):355–361. doi:10.1042/BJ20041119
Attwood PV, Piggott MJ, Zu XL, Besant PG (2007) Focus on phosphohistidine. Amino Acids 32(1):145–156. doi:10.1007/s00726-006-0443-6
Christiansen C, Abou Hachem M, Janecek S, Vikso-Nielsen A, Blennow A, Svensson B (2009) The carbohydrate-binding module family 20–diversity, structure, and function. FEBS J 276(18):5006–5029. doi:10.1111/j.1742-4658.2009.07221.x
Mikkelsen R, Suszkiewicz K, Blennow A (2006) A novel type carbohydrate-binding module identified in alpha-glucan, water dikinases is specific for regulated plastidial starch metabolism. Biochemistry 45(14):4674–4682. doi:10.1021/bi051712a
Glaring MA, Baumann MJ, Abou Hachem M, Nakai H, Nakai N, Santelia D, Sigurskjold BW, Zeeman SC, Blennow A, Svensson B (2011) Starch-binding domains in the CBM45 family–low-affinity domains from glucan, water dikinase and alpha-amylase involved in plastidial starch metabolism. FEBS J 278(7):1175–1185. doi:10.1111/j.1742-4658.2011.08043.x
Ritte G, Lorberth R, Steup M (2000) Reversible binding of the starch-related R1 protein to the surface of transitory starch granules. Plant J 21(4):387–391. doi:10.1046/j.1365-313x.2000.00683.x
Haebel S, Hejazi M, Frohberg C, Heydenreich M, Ritte G (2008) Mass spectrometric quantification of the relative amounts of C6 and C3 position phosphorylated glucosyl residues in starch. Anal Biochem 379(1):73–79. doi:10.1016/j.ab.2008.04.002
Hejazi M, Fettke J, Haebel S, Edner C, Paris O, Frohberg C, Steup M, Ritte G (2008) Glucan, water dikinase phosphorylates crystalline maltodextrins and thereby initiates solubilization. Plant J 55(2):323–334. doi:10.1111/j.0960-7412.2008.03513.x
Hejazi M, Fettke J, Paris O, Steup M (2009) The two plastidial starch-related dikinases sequentially phosphorylate glucosyl residues at the surface of both the a- and b-type allomorphs of crystallized maltodextrins but the mode of action differs. Plant Physiol 150(2):962–976. doi:10.1104/pp.109.138750
Fettke J, Hejazi M, Smirnova J, Hochel E, Stage M, Steup M (2009) Eukaryotic starch degradation: integration of plastidial and cytosolic pathways. J Exp Bot 60(10):2907–2922. doi:10.1093/jxb/erp054
Blennow A, Engelsen SB (2010) Helix-breaking news: fighting crystalline starch energy deposits in the cell. Trends Plant Sci 15(4):236–240. doi:10.1016/j.tplants.2010.01.009
Zeeman SC, Smith SM, Smith AM (2007) The diurnal metabolism of leaf starch. Biochem J 401(1):13–28. doi:10.1042/BJ20061393
Orzechowski S (2008) Starch metabolism in leaves. Acta Biochim Pol 55(3):435–445
Hejazi M, Fettke J, Steup M (2012) Starch phosphorylation and dephosphorylation: The consecutive action of starch-related dikinases and phosphatases. In: Tetlow IJ (ed) Starch: Origins, structure and metabolism, vol 5. SEB Publishing, London, pp 279–310
Emanuelle S, Brewer MK, Meekins DA, Gentry MS (2016) Unique carbohydrate binding platforms employed by the glucan phosphatases. Cell Mol Life Sci. doi:10.1007/s00018-016-2249-3
Roldan I, Wattebled F, Mercedes Lucas M, Delvalle D, Planchot V, Jimenez S, Perez R, Ball S, D’Hulst C, Merida A (2007) The phenotype of soluble starch synthase IV defective mutants of Arabidopsis thaliana suggests a novel function of elongation enzymes in the control of starch granule formation. Plant J 49(3):492–504. doi:10.1111/j.1365-313X.2006.02968.x
Crumpton-Taylor M, Grandison S, Png KM, Bushby AJ, Smith AM (2012) Control of starch granule numbers in Arabidopsis chloroplasts. Plant Physiol 158(2):905–916. doi:10.1104/pp.111.186957
Gibon Y, Blasing OE, Palacios-Rojas N, Pankovic D, Hendriks JH, Fisahn J, Hohne M, Gunther M, Stitt M (2004) Adjustment of diurnal starch turnover to short days: depletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADP-glucose pyrophosphorylase in the following light period. Plant J 39(6):847–862. doi:10.1111/j.1365-313X.2004.02173.x
Skeffington AW, Graf A, Duxbury Z, Gruissem W, Smith AM (2014) Glucan, water dikinase exerts little control over starch degradation in Arabidopsis leaves at night. Plant Physiol 165(2):866–879. doi:10.1104/pp.114.237016
Delvalle D, Dumez S, Wattebled F, Roldan I, Planchot V, Berbezy P, Colonna P, Vyas D, Chatterjee M, Ball S, Merida A, D’Hulst C (2005) Soluble starch synthase I: a major determinant for the synthesis of amylopectin in Arabidopsis thaliana leaves. Plant J 43(3):398–412. doi:10.1111/j.1365-313X.2005.02462.x
Hejazi M, Mahlow S, Fettke J (2014) The glucan phosphorylation mediated by alpha-glucan, water dikinase (GWD) is also essential in the light phase for a functional transitory starch turn-over. Plant Signal Behav 9(7):e28892. doi:10.4161/psb.28892
Vikso-Nielsen A, Blennow A, Jorgensen K, Kristensen KH, Jensen A, Moller BL (2001) Structural, physicochemical, and pasting properties of starches from potato plants with repressed R1-gene. Biomacromolecules 2(3):836–843. doi:10.1021/bm0155165
Kozlov SS, Blennow A, Krivandin AV, Yuryev VP (2007) Structural and thermodynamic properties of starches extracted from GBSS and GWD suppressed potato lines. Int J Biol Macromol 40(5):449–460. doi:10.1016/j.ijbiomac.2006.11.001
Mikkelsen R, Mutenda KE, Mant A, Schurmann P, Blennow A (2005) Alpha-glucan, water dikinase (GWD): a plastidic enzyme with redox-regulated and coordinated catalytic activity and binding affinity. Proc Natl Acad Sci USA 102(5):1785–1790. doi:10.1073/pnas.0406674102
Orzechowski S, Grabowska A, Sitnicka D, Siminska J, Felus M, Dudkiewicz M, Fudali S, Sobczak M (2013) Analysis of the expression, subcellular and tissue localisation of phosphoglucan, water dikinase (PWD/GWD3) in Solanum tuberosum L.: a bioinformatics approach for the comparative analysis of two alpha-glucan, water dikinases (GWDs) from Solanum tuberosum L. Acta Physiol Plant 35(2):483–500. doi:10.1007/s11738-012-1091-y
Carpenter MA, Joyce NI, Genet RA, Cooper RD, Murray SR, Noble AD, Butler RC, Timmerman-Vaughan GM (2015) Starch phosphorylation in potato tubers is influenced by allelic variation in the genes encoding glucan water dikinase, starch branching enzymes I andII, and starch synthase III. Front Plant Sci 6:143. doi:10.3389/fpls.2015.00143
Hejazi M, Steup M, Fettke J (2012) The plastidial glucan, water dikinase (GWD) catalyses multiple phosphotransfer reactions. FEBS J 279(11):1953–1966. doi:10.1111/j.1742-4658.2012.08576.x
Carciofi M, Shaif SS, Jensen SL, Blennow A, Svensson JT, Vincze E, Hebelstrup KH (2011) Hyperphosphorylation of cereal starch. J Cereal Sci 54(3):339–346. doi:10.1016/j.jcs.2011.06.013
Weise SE, Aung K, Jarou ZJ, Mehrshahi P, Li Z, Hardy AC, Carr DJ, Sharkey TD (2012) Engineering starch accumulation by manipulation of phosphate metabolism of starch. Plant Biotechnol J 10(5):545–554. doi:10.1111/j.1467-7652.2012.00684.x
Ral JP, Bowerman AF, Li Z, Sirault X, Furbank R, Pritchard JR, Bloemsma M, Cavanagh CR, Howitt CA, Morell MK (2012) Down-regulation of glucan, water-dikinase activity in wheat endosperm increases vegetative biomass and yield. Plant Biotechnol J 10(7):871–882. doi:10.1111/j.1467-7652.2012.00711.x
Hirose T, Aoki N, Harada Y, Okamura M, Hashida Y, Ohsugi R, Akio M, Hirochika H, Terao T (2013) Disruption of a rice gene for alpha-glucan water dikinase, OsGWD1, leads to hyperaccumulation of starch in leaves but exhibits limited effects on growth. Front Plant Sci 4:147. doi:10.3389/fpls.2013.00147
Ohlrogge J, Allen D, Berguson B, Dellapenna D, Shachar-Hill Y, Stymne S (2009) Driving on biomass. Science 324(5930):1019–1020. doi:10.1126/science.1171740
Bowerman AF, Newberry M, Dielen AS, Whan A, Larroque O, Pritchard J, Gubler F, Howitt CA, Pogson BJ, Morell MK, Ral JP (2016) Suppression of glucan, water dikinase in the endosperm alters wheat grain properties, germination and coleoptile growth. Plant Biotechnol J 14(1):398–408. doi:10.1111/pbi.12394
Derelle E, Ferraz C, Rombauts S, Rouze P, Worden AZ, Robbens S, Partensky F, Degroeve S, Echeynie S, Cooke R, Saeys Y, Wuyts J, Jabbari K, Bowler C, Panaud O, Piegu B, Ball SG, Ral JP, Bouget FY, Piganeau G, De Baets B, Picard A, Delseny M, Demaille J, Van de Peer Y, Moreau H (2006) Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci USA 103(31):11647–11652. doi:10.1073/pnas.0604795103
Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud PF, Lindquist EA, Kamisugi Y, Tanahashi T, Sakakibara K, Fujita T, Oishi K, Shin IT, Kuroki Y, Toyoda A, Suzuki Y, Hashimoto S, Yamaguchi K, Sugano S, Kohara Y, Fujiyama A, Anterola A, Aoki S, Ashton N, Barbazuk WB, Barker E, Bennetzen JL, Blankenship R, Cho SH, Dutcher SK, Estelle M, Fawcett JA, Gundlach H, Hanada K, Heyl A, Hicks KA, Hughes J, Lohr M, Mayer K, Melkozernov A, Murata T, Nelson DR, Pils B, Prigge M, Reiss B, Renner T, Rombauts S, Rushton PJ, Sanderfoot A, Schween G, Shiu SH, Stueber K, Theodoulou FL, Tu H, Van de Peer Y, Verrier PJ, Waters E, Wood A, Yang L, Cove D, Cuming AC, Hasebe M, Lucas S, Mishler BD, Reski R, Grigoriev IV, Quatrano RS, Boore JL (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319(5859):64–69. doi:10.1126/science.1150646
Szydlowski N, Ragel P, Hennen-Bierwagen TA, Planchot V, Myers AM, Merida A, d’Hulst C, Wattebled F (2011) Integrated functions among multiple starch synthases determine both amylopectin chain length and branch linkage location in Arabidopsis leaf starch. J Exp Bot 62(13):4547–4559. doi:10.1093/jxb/err172
Beel B, Prager K, Spexard M, Sasso S, Weiss D, Muller N, Heinnickel M, Dewez D, Ikoma D, Grossman AR, Kottke T, Mittag M (2012) A flavin binding cryptochrome photoreceptor responds to both blue and red light in Chlamydomonas reinhardtii. Plant Cell 24(7):2992–3008. doi:10.1105/tpc.112.098947
Acknowledgments
This work was supported by the Deutsche Forschungsgemeinschaft (DFG Grant FE 1030/1-1). The authors are grateful to Irina Malinova for help during preparation of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Mahlow, S., Orzechowski, S. & Fettke, J. Starch phosphorylation: insights and perspectives. Cell. Mol. Life Sci. 73, 2753–2764 (2016). https://doi.org/10.1007/s00018-016-2248-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00018-016-2248-4