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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
REVIEW

Transporters in starch synthesis

Thomas Martin A B and Frank Ludewig C D
+ Author Affiliations
- Author Affiliations

A School of Biomedical, Biomolecular and Chemical Sciences, University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.

B School of Plant Biology, M310 Biochemistry and Molecular Biology, University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.

C Botanical Institute, University of Cologne, Gyrhofstr. 15, 50 931 Cologne, Germany.

D Corresponding author. Email: frank.ludewig@uni-koeln.de

Functional Plant Biology 34(6) 474-479 https://doi.org/10.1071/FP06280
Submitted: 1 November 2006  Accepted: 12 January 2007   Published: 1 June 2007

Abstract

Starch is synthesised and stored in plastids. In autotrophic tissues, the carbon skeletons and energy required for starch synthesis are directly available from photosynthesis. However, plastids of heterotrophic tissues require the metabolites for starch synthesis to be imported. Depending on plant species and tissue type, import is facilitated by several different plastid inner envelope metabolite transporters. Commonly, glucose-6-phosphate/phosphate translocators and adenylate translocators are used, but in the cereal endosperm, the role is carried out by ADP glucose transporters (Brittle1, BT1). This review predominantly focuses on transporters of the plastid inner envelope membrane. Their roles are discussed within an overview of starch synthesis. We also examine additional functions of these transporters according to our current knowledge.


References


Ball SG, Morell MK (2003) From bacterial glycogen to starch: understanding the biogenesis of the plant starch granule. Annual Review of Plant Biology 54, 207–233.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ball SG, van de Wal M, Visser RGF (1998) Progress in understanding the biosynthesis of amylose. Trends in Plant Science 3, 462–467.
Crossref | GoogleScholarGoogle Scholar | open url image1

Batz O, Scheibe R, Neuhaus HE (1992) Transport processes and corresponding changes in metabolite levels in relation to starch synthesis in barley (Hordeum vulgare L.) etioplasts. Plant Physiology 100, 184–190.
PubMed |
open url image1

Beckles DM, Smith AM, ap Rees T (2001) A cytosolic ADP-glucose pyrophosphorylase is a feature of graminaceous endosperms, but not of other starch-storing organs. Plant Physiology 125, 818–827.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Birkenhead K, Walker D, Foyer C (1982) The intracellular distribution of adenylate kinase in the leaves of spinach, wheat and barley. Planta 156, 171–175.
Crossref | GoogleScholarGoogle Scholar | open url image1

Boldt R, Zrenner R (2003) Purine and pyrimidine biosynthesis in higher plants. Physiologia Plantarum 117, 297–304.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cao HP, Sullivan TD, Boyer CD, Shannon JC (1995) Bt1, a structural gene for the major 39–44 kDa amyloplast membrane polypeptides. Physiologia Plantarum 95, 176–186.
Crossref | GoogleScholarGoogle Scholar | open url image1

Carrari F, Coll-Garcia D, Schauer N, Lytovchenko A, Palacios-Rojas N, Balbo I, Rosso M, Fernie AR (2005) Deficiency of a plastidial adenylate kinase in Arabidopsis results in elevated photosynthetic amino acid biosynthesis and enhanced growth. Plant Physiology 137, 70–82.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Delvalle D, Dumez S, Wattlebled F, Roldan , Planchot V, Berbezy P , et al. (2005) Soluble starch synthase I: a major determinant for the synthesis of amylopectin in Arabidopsis thaliana leaves. The Plant Journal 43, 398–412.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Denyer K, Dunlap F, Thorbjornsen T, Keeling P, Smith AM (1996) The major form of ADP-glucose pyrophosphorylase in maize endosperm is extra-plastidial. Plant Physiology 112, 779–785.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Eicks M, Maurino V, Knappe S, Flügge UI, Fischer K (2002) The plastidic pentose phosphate translocator represents a link between the cytosolic and the plastidic pentose phosphate pathways in plants. Plant Physiology 128, 512–522.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Emes MJ, Neuhaus HE (1997) Metabolism and transport in non-photosynthetic plastids. Journal of Experimental Botany 48, 1995–2005. open url image1

Entwistle G, ap Rees T (1990) Lack of fructose-1,6-bisphosphatase in a range of higher plants that store starch. The Biochemical Journal 271, 467–472.
PubMed |
open url image1

Fiore C, Trezeguet V, Le Saux A, Roux P, Schwimmer C, Dianoux AC , et al. (1998) The mitochondrial ADP/ATP carrier: structural, physiological and pathological aspects. Biochimie 80, 137–150.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Fischer K, Weber A (2002) Transport of carbon in non-green plastids. Trends in Plant Science 7, 345–351.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Fischer K, Kammerer B, Gutensohn M, Arbinger B, Weber A, Häusler RE, Flügge UI (1997) A new class of plastidic phosphate translocators: a putative link between primary and secondary metabolism by the phosphoenolpyruvate/phosphate antiporter. The Plant Cell 9, 453–462.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Flügge UI (1992) Reaction-mechanism and asymmetric orientation of the reconstituted chloroplast phosphate translocator. Biochimica et Biophysica Acta 1110, 112–118.
Crossref | PubMed |
open url image1

Flügge UI (1999) Phosphate translocators in plastids. Annual Review of Plant Physiology and Plant Molecular Biology 50, 27–45.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Flügge UI, Fischer K, Gross A, Sebald W, Lottspeich F, Eckerskorn C (1989) The triose phosphate-3-phosphoglycerate phosphate translocator from spinach chloroplasts – nucleotide-sequence of a full-length cDNA clone and import of the in vitro synthesized precursor protein into chloroplasts. EMBO Journal 8, 39–46.
PubMed |
open url image1

Flügge UI, Häusler RE, Ludewig F, Fischer K (2003) Functional genomics of phosphate antiport systems of plastids. Physiologia Plantarum 118, 475–482.
Crossref | GoogleScholarGoogle Scholar | open url image1

Geiger DR, Servaites JC, Fuchs MA (2000) Role of starch in carbon translocation and partitioning at the plant level. Australian Journal of Plant Physiology 27, 571–582. open url image1

Haferkamp I, Schmitz-Esser S, Wagner M, Neigel N, Horn M, Neuhaus HE (2006) Tapping the nucleotide pool of the host: novel nucleotide carrier proteins of Protochlamydia amoebophila. Molecular Microbiology 60, 1534–1545.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Heldt HW (1969) Adenine nucleotide translocation in spinach chloroplasts. FEBS Letters 5, 11–14.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hill LM, Smith AM (1991) Evidence that glucose-6-phosphate is imported as the substrate for starch synthesis by the plastids of developing pea embryos. Planta 185, 91–96. open url image1

James MG, Denyer K, Myers AM (2003) Starch synthesis in the cereal endosperm. Current Opinion in Plant Biology 6, 215–222.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kammerer B, Fischer K, Hilpert B, Schubert S, Gutensohn M, Weber A, Flügge UI (1998) Molecular characterization of a carbon transporter in plastids from heterotrophic tissues: the glucose 6-phosphate phosphate antiporter. The Plant Cell 10, 105–117.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kampfenkel K, Möhlmann T, Batz O, van Montagu M, Inze D, Neuhaus HE (1995) Molecular characterization of an Arabidopsis thaliana cDAN-encoding a novel putative adenylate translocator of higher plants. FEBS Letters 374, 351–355.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kang F, Rawsthorne S (1994) Starch and fatty-acid synthesis in plastids from developing embryos of oilseed rape (Brassica napus L). The Plant Journal 6, 795–805.
Crossref | GoogleScholarGoogle Scholar | open url image1

Klingenberg M (1989) Molecular aspects of the adenine-nucleotide carrier from mitochondria. Archives of Biochemistry and Biophysics 270, 1–14.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Knappe S, Flügge UI, Fischer K (2003) Analysis of the plastidic phosphate translocator gene family in Arabidopsis and identification of new phosphate translocator-homologous transporters, classified by their putative substrate-binding site. Plant Physiology 131, 1178–1190.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kofler H, Häusler RE, Schulz B, Gröner F, Flügge UI, Weber A (2000) Molecular characterisation of a new mutant allele of the plastid phosphoglucomutase in Arabidopsis, and complementation of the mutant with the wild-type cDNA. Molecular and General Genetics 263, 978–986.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kosegarten H, Mengel K (1994) Evidence for a glucose 1-phosphate translocator in storage tissue amyloplasts of potato (Solanum tuberosum) suspension-cultured cells. Physiologia Plantarum 91, 111–120.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kuipers AGJ, Jacobsen E, Visser RGF (1994) Formation and deposition of amylose in the potato-tuber starch granule are affected by the reduction of granule-bound starch synthase gene expression. The Plant Cell 6, 43–52.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Leroch M, Kirchberger S, Haferkamp I, Wahl M, Neuhaus HE, Tjaden J (2005) Identification and characterization of a novel plastidic adenine nucleotide uniporter from Solanum tuberosum. Journal of Biological Chemistry 280, 17 992–18 000.
Crossref | GoogleScholarGoogle Scholar | open url image1

Linka N, Hurka H, Lang BF, Burger G, Winkler HH, Stamme C , et al. (2003) Phylogenetic relationships of non-mitochondrial nucleotide transport proteins in bacteria and eukaryotes. Gene 306, 27–35.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Millar AH, Heazlewood JL (2003) Genomic and proteomic analysis of mitochondrial carrier proteins in Arabidopsis. Plant Physiology 131, 443–453.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Möhlmann T, Batz O, Maass U, Neuhaus HE (1995) Analysis of carbohydrate transport across the envelope of isolated cauliflower-bud amyloplasts. The Biochemical Journal 307, 521–526.
PubMed |
open url image1

Möhlmann T, Tjaden J, Henrichs G, Quick WP, Häusler R, Neuhaus HE (1997) ADP-glucose drives starch synthesis in isolated maize endosperm amyloplasts: characterization of starch synthesis and transport properties across the amyloplast envelope. The Biochemical Journal 324, 503–509.
PubMed |
open url image1

Möhlmann T, Tjaden J, Schwoppe C, Winkler HH, Kampfenkel K, Neuhaus HE (1998) Occurrence of two plastidic ATP/ADP transporters in Arabidopsis thaliana L. – molecular characterisation and comparative structural analysis of similar ATP/ADP translocators from plastids and Rickettsia prowazekii. European Journal of Biochemistry 252, 353–359.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Morita MT, Tasaka M (2004) Gravity sensing and signaling. Current Opinion in Plant Biology 7, 712–718.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Naeem M, Tetlow IJ, Emes MJ (1997) Starch synthesis in amyloplasts purified from developing potato tubers. The Plant Journal 11, 1095–1103.
Crossref | GoogleScholarGoogle Scholar | open url image1

Neuhaus HE, Maass U (1996) Unidirectional transport of orthophosphate across the envelope of isolated cauliflower-bud amyloplasts. Planta 198, 542–548.
Crossref | GoogleScholarGoogle Scholar | open url image1

Neuhaus HE, Henrichs G, Scheibe R (1993) Characterization of glucose-6-phosphate incorporation into starch by isolated intact cauliflower-bud plastids. Plant Physiology 101, 573–578.
PubMed |
open url image1

Niewiadomski P, Knappe S, Geimer S, Fischer K, Schulz B, Unte US , et al. (2005) The arabidopsis plastidic glucose 6-phosphate/phosphate translocator GPT1 is essential for pollen maturation and embryo sac development. The Plant Cell 17, 760–775.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Niittylä T, Messerli G, Trevisan M, Chen J, Smith AM, Zeeman SC (2004) A previously unknown maltose transporter essential for starch degradation in leaves. Science 303, 87–89.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Patron NJ, Greber B, Fahy BF, Laurie DA, Parker ML, Denyer K (2004) The lys5 mutations of barley reveal the nature and importance of plastidial ADP-Glc transporters for starch synthesis in cereal endosperm. Plant Physiology 135, 2088–2097.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Perbal G, Driss-Ecole D (2003) Mechanotransduction in gravisensing cells. Trends in Plant Science 8, 498–504.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Rawsthorne S (2002) Carbon flux and fatty acid synthesis in plants. Progress in Lipid Research 41, 182–196.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Regierer B, Fernie AR, Springer F, Perez-Melis A, Leisse A, Koehl K, Willmitzer L, Geigenberger P, Kossmann J (2002) Starch content and yield increase as a result of altering adenylate pools in transgenic plants. Nature Biotechnology 20, 1256–1260.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Reiser J, Linka N, Lemke L, Jeblick W, Neuhaus HE (2004) Molecular physiological analysis of the two plastidic ATP/ADP transporters from Arabidopsis. Plant Physiology 136, 3524–3536.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Saraste M, Walker JE (1982) Internal sequence repeats and the path of polypeptide in mitochondrial ADP/ATP translocase. FEBS Letters 144, 250–254.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Schott K, Borchert S, Müller Röber B, Heldt HW (1995) Transport of inorganic-phosphate and C-3-sugar and C-6-sugar phosphates across the envelope membranes of potato-tuber amyloplasts. Planta 196, 647–652.
Crossref | GoogleScholarGoogle Scholar | open url image1

Schulz B, Frommer WB, Flügge UI, Hummel S, Fischer K, Willmitzer L (1993) Expression of the triose phosphate translocator gene from potato is light-dependent and restricted to green tissues. Molecular and General Genetics 238, 357–361.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Schünemann D, Borchert S, Flügge UI, Heldt HW (1993) ADP/ATP translocator from pea root plastids – comparison with translocators from spinach-chloroplasts and pea leaf mitochondria. Plant Physiology 103, 131–137.
PubMed |
open url image1

Schünemann D, Schott K, Borchert S, Heldt HW (1996) Evidence for the expression of the triosephosphate translocator gene in green and non-green tissues of tomato and potato. Plant Molecular Biology 31, 101–111.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Shannon JC, Pien FM, Liu KC (1996) Nucleotides and nucleotide sugars in developing maize endosperms – synthesis of ADP-glucose in brittle-1. Plant Physiology 110, 835–843.
PubMed |
open url image1

Shannon JC, Pien FM, Cao HP, Liu KC (1998) Brittle-1, an adenylate translocator, facilitates transfer of extraplastidial synthesized ADP-glucose into amyloplasts of maize endosperms. Plant Physiology 117, 1235–1252.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Smith AM (2001) The biosynthesis of starch granules. Biomacromolecules 2, 335–341.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Smith AM, Denyer K, Martin C (1997) The synthesis of the starch granule. Annual Review of Plant Physiology and Plant Molecular Biology 48, 67–87.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Strotmann H, Berger S (1969) Adenine nucleotide translocation across the membrane of isolated acetabularia chloroplats. Biochemical and Biophysical Research Communications 35, 20–26.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tauberger E, Fernie AR, Emmermann M, Renz A, Kossman J, Willmitzer L, Trethewey RN (2000) Antisense inhibition of plastidial phosphoglucomutase provides compelling evidence that potato tuber amyloplasts import carbon from the cytosol in the form of glucose-6-phosphate. Plant Journal 23, 43–53.
Crossref | PubMed |
open url image1

Tetlow IJ, Blissett KJ, Emes MJ (1994) Starch synthesis and carbohydrate oxidation in amyloplasts from developing wheat endosperm. Planta 194, 454–460.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tetlow IJ, Davies EJ, Vardy KA, Bowsher CG, Burrell MM, Emes MJ (2003) Subcellular localization of ADPglucose pyrophosphorylase in developing wheat endosperm and analysis of the properties of a plastidial isoform. Journal of Experimental Botany 54, 715–725.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tjaden J, Möhlmann T, Kampfenkel K, Henrichs G, Neuhaus HE (1998) Altered plastidic ATP/ADP-transporter activity influences potato (Solanum tuberosum L.) tuber morphology, yield and composition of tuber starch. The Plant Journal 16, 531–540.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tjaden J, Haferkamp I, Boxma B, Tielens AGM, Huynen M, Hackstein JHP (2004) A divergent ADP/ATP carrier in the hydrogenosomes of Trichomonas gallinae argues for an independent origin of these organelles. Molecular Microbiology 51, 1439–1446.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Visser RGF, Somhorst I, Kuipers GJ, Ruys NJ, Feenstra WJ, Jacobsen E (1991) Inhibition of the expression of the gene for granule-bound starch synthase in potato by antisense constructs. Molecular and General Genetics 225, 289–296.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Weber A, Servaites JC, Geiger DR, Kofler H, Hille D, Gröner F, Hebbeker U, Flügge UI (2000) Identification, purification, and molecular cloning of a putative plastidic glucose translocator. The Plant Cell 12, 787–801.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Winkler HH, Neuhaus HE (1999) Non-mitochondrial ATP transport. Trends in Biochemical Sciences 24, 64–68.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wischmann B, Nielsen TH, Möller BL (1999) In vitro biosynthesis of phosphorylated starch in intact potato amyloplasts. Plant Physiology 119, 455–462.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yu TS, Lue WL, Wang SM, Chen JC (2000) Mutation of Arabidopsis plastid phosphoglucose isomerase affects leaf starch synthesis and floral initiation. Plant Physiology 123, 319–325.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zeeman SC, Delatte T, Messerli G, Umhang M, Stettler M , et al. (2007) Starch breakdown: recent discoveries suggest distinct pathways and novel mechanisms. Functional Plant Biology 34, 465–473.
Crossref | GoogleScholarGoogle Scholar | open url image1

Zrenner R, Stitt M, Sonnewald U, Boldt R (2006) Pyrimidine and purine biosynthesis and degradation in plants. Annual Review of Plant Biology 57, 805–836.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1