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Sucrose and Starch Metabolism

  • Cécile Vriet
  • Anne Edwards
  • Alison M. Smith
  • Trevor L. Wang
Chapter
Part of the Compendium of Plant Genomes book series (CPG)

Abstract

The metabolism of starch and sucrose fuels all aspects of plant growth and development. Over the last decade, significant advances have been made in our understanding of the metabolism of these compounds through the use of model systems, mainly Arabidopsis. Legume species are characterised by their capacity to form symbioses with Rhizobium, a nitrogen-fixing bacterium, leading to up to half the carbon assimilated in photosynthesis being sequestered to their roots. Study of a legume model may therefore increase our knowledge about carbohydrate turnover. We review here the resources available and the contribution that research on Lotus japonicus has made to our knowledge of sucrose breakdown and starch metabolism in relation to plant growth and development processes, especially processes that are legume specific.

Keywords

Starch Granule Starch Content Starch Synthesis Starch Degradation Sucrose Metabolism 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Barratt DH, Derbyshire P, Findlay K, Pike M, Wellner N, Lunn J, Feil R, Simpson C, Maule AJ, Smith AM (2009) Normal growth of Arabidopsis requires cytosolic invertase but not sucrose synthase. Proc Natl Acad Sci USA 106:13124–13129PubMedCrossRefPubMedCentralGoogle Scholar
  2. Caspar T, Huber SC, Somerville C (1985) Alterations in growth, photosynthesis, and respiration in a starchless mutant of Arabidopsis thaliana (L.) deficient in chloroplast phosphoglucomutase activity. Plant Physiol 79:11–17PubMedCrossRefPubMedCentralGoogle Scholar
  3. Craig J, Barratt P, Tatge H, Dejardin A, Handley L, Gardner CD, Barber L, Wang T, Hedley C, Martin C, Smith AM (1999) Mutations at the rug4 locus alter the carbon and nitrogen metabolism of pea plants through an effect on sucrose synthase. Plant J 17:353–362CrossRefGoogle Scholar
  4. Dam S, Laursen BS, Ornfelt JH, Jochimsen B, Staerfeldt HH, Friis C, Nielsen K, Goffard N, Besenbacher S, Krusell L, Sato S, Tabata S, Thøgersen IB, Enghild JJ, Stougaard J (2009) The proteome of seed development in the model legume Lotus japonicus. Plant Physiol 149:1325–1340PubMedCrossRefPubMedCentralGoogle Scholar
  5. Delatte D, 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 281:12050–12059PubMedCrossRefGoogle Scholar
  6. 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) β-AMYLASE4, a noncatalytic protein required for starch breakdown, acts upstream of three active β-amylases in Arabidopsis chloroplasts. Plant Cell 20:1040–1058PubMedCrossRefPubMedCentralGoogle Scholar
  7. Gana JA, Kalengamaliro NE, Cunningham SM, Volenec JJ (1998) Expression of β-amylase from alfalfa taproots. Plant Physiol 118:1495–1505PubMedCrossRefPubMedCentralGoogle Scholar
  8. Glaring MA, Zygadlo A, Thorneycroft D, Schulz A, Smith SM, Blennow A, Baunsgaard L (2007) An extra-plastidial α-glucan, water dikinase from Arabidopsis phosphorylates amylopectin in vitro and is not necessary for transient starch degradation. J Exp Bot 58:3949–3960PubMedCrossRefGoogle Scholar
  9. Gutjahr C, Novero M, Welham T, Wang T, Bonfante P (2011) Root starch accumulation in response to arbuscular mycorrhizal colonization differs among Lotus japonicus starch mutants. Planta 234:639–646PubMedCrossRefGoogle Scholar
  10. Harrison CJ, Hedley CL, Wang TL (1998) Evidence that the rug3 locus of pea (Pisum sativum L.) encodes plastidial phosphoglucomutase confirms that the imported substrate for starch synthesis in pea amyloplasts is glucose-6-phosphate. Plant J 13:753–762CrossRefGoogle Scholar
  11. Hildebrand D, Hymowitz T (1981) Role of β-amylase in starch metabolism during soybean seed development and germination. Physiol Plant 53:429–434CrossRefGoogle Scholar
  12. Horst I, Welham T, Kelly S, Kaneko T, Sato S, Tabata S, Parniske M, Wang TL (2007) TILLING mutants of Lotus japonicus reveal that nitrogen assimilation and fixation can occur in the absence of nodule-enhanced sucrose synthase. Plant Physiol 144:806–820PubMedCrossRefPubMedCentralGoogle Scholar
  13. James MG, Denyer K, Myers AM (2003) Starch synthesis in the cereal endosperm. Curr Opin Plant Biol 6:215–222PubMedCrossRefGoogle Scholar
  14. Kim W-S, Krishnan HB (2010) The lack of beta-amylase activity in soybean cultivar Altona sp 1 is associated with a 1.2 kb deletion in the 5′ region of beta-amylase I gene. Crop Sci 50:1942–1949CrossRefGoogle Scholar
  15. Kötting O, Kossmann J, Zeeman SC, Lloyd JR (2010) Regulation of starch metabolism: the age of enlightenment? Curr Opin Plant Biol 13:321–329PubMedCrossRefGoogle Scholar
  16. Lunn JE, MacRae E (2003) New complexities in the synthesis of sucrose. Curr Opin Plant Biol 6:208–214PubMedCrossRefGoogle Scholar
  17. Oldroyd GED (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11:252–263PubMedCrossRefGoogle Scholar
  18. Monma M, Sugimoto T, Monma M, Kawamura Y, Saio K (1991) Starch breakdown in developing soybean seeds (Glycine max cv. Enrei). Agric Biol Chem 55:67–71CrossRefGoogle Scholar
  19. Reinhold H, Soyk S, Simkova K, Hostettler C, Marafino J, Mainiero S, Vaughan CK, Monroe JD, Zeeman SC (2011) β-Amylase–like proteins function as transcription factors in Arabidopsis, controlling shoot growth and development. Plant Cell 23:1391–1403PubMedCrossRefPubMedCentralGoogle Scholar
  20. Ruzanski C, Smirnova J, Rejzek M, Cockburn D, Pedersen HL, Pike M, Willats WGT, Svensson B, Steup M, Ebenhöh O, Smith AM, Field RA (2013) A bacterial glucanotransferase can replace the complex maltose metabolism required for starch-to-sucrose conversion in leaves at night. J Biol Chem 288:28581–28598PubMedCrossRefPubMedCentralGoogle Scholar
  21. Santelia D, Kötting O, Seung D, Schubert M, Thalmann M, Bischof S, Meekins DA, Lutz A, Patron N, Gentry MS, Allain FH-T, Zeeman SC (2012) The phosphoglucan phosphatase LSF2 (like sex four 2) dephosphorylates starch at the C3-position in Arabidopsis. Plant Cell 23:4096–4111CrossRefGoogle Scholar
  22. Sato S, Nakamura Y, Kaneko T, Asamizu E, Kato T, Nakao M, Sasamoto S, Watanabe A, Ono A, Kawashima K, Fujishiro T, Katoh M, Kohara M, Kishida Y, Minami C, Nakayama S, Nakazaki N, Shimizu Y, Shinpo S, Takahashi C, Wada T, Yamada M, Ohmido N, Hayashi M, Fukui K, Baba T, Nakamichi T, Mori H, Tabata S (2008) Genome structure of the legume, Lotus japonicus. DNA Res 15:227–239 Google Scholar
  23. Smith AM (2012) Starch in the Arabidopsis plant. Starch/Staerke 64:421–434Google Scholar
  24. Smith AM, Zeeman SC, Smith SM (2005) Starch degradation. Annu Rev Plant Biol 56:73–97PubMedCrossRefGoogle Scholar
  25. Sparla F, Costa A, Schiavo FL, Pupillo P, Trost P (2006) Redox regulation of a novel plastid-targeted β-amylase of Arabidopsis thaliana. Plant Physiol 141:840–850PubMedCrossRefPubMedCentralGoogle Scholar
  26. Stitt M, Zeeman SC (2012) Starch turnover: pathways, regulation and role in growth. Curr Opin Plant Biol 15:282–292PubMedCrossRefGoogle Scholar
  27. Streb S, Delatte T, Umhang M, Eicke S, Schorderet M, Reinhardt D, Zeeman SC (2008) Starch granule biosynthesis in Arabidopsis is abolished by removal of all debranching enzymes but restored by the subsequent removal of an endoamylase. Plant Cell 20:3448–3466PubMedCrossRefPubMedCentralGoogle Scholar
  28. Streb S, Zeeman S (2012) Starch metabolism in Arabidopsis. In: The Arabidopsis Book 10:e0160, doi:  10.1199/tab.0160
  29. Streb S, Egli B, Eicke S, Zeeman SC (2009) The debate on the pathway of starch synthesis: a closer look at low-starch mutants lacking plastidial phosphoglucomutase supports the chloroplast-localized pathway. Plant Physiol 151:1769–1772PubMedCrossRefPubMedCentralGoogle Scholar
  30. Sulpice R, Pyl ET, Ishihara H, Trenkamp S, Steinfath M, Witucka-Wall H, Gibon Y, Usadel B, Poree F, Piques MC, Von Korff M, Steinhauser MC, Keurentjes JJB, Guenther M, Hoehne M, Selbig J, Fernie AR, Altmann T, Stitt M (2009) Starch as a major integrator in the regulation of plant growth. Proc Natl Acad Sci U S A 106:10348–10353PubMedCrossRefPubMedCentralGoogle Scholar
  31. Vargas WA, Salerno GL (2010) The Cinderella story of sucrose hydrolysis: alkaline/neutral invertases, from cyanobacteria to unforeseen roles in plant cytosol and organelles. Plant Sci 178:1–8CrossRefGoogle Scholar
  32. Verdier J, Torres-Jerez I, Wang M, Andriankaja A, Allen SN, He J, Tang Y, Murray JD, Udvardi MK (2013) Establishment of the Lotus japonicus Gene Expression Atlas (LjGEA) and its use to explore legume seed maturation. Plant J 74:351–362PubMedCrossRefGoogle Scholar
  33. Vriet C, Welham T, Brachmann A, Pike M, Pike J, Perry J, Parniske M, Sato S, Tabata S, Smith AM, Wang TL (2010) A suite of Lotus japonicus starch mutants reveals both conserved and novel features of starch metabolism. Plant Physiol 154:643–655PubMedCrossRefPubMedCentralGoogle Scholar
  34. Vriet C, Smith AM, Wang TL (2013) Root starch reserves are necessary for vigorous re-growth following cutting back in Lotus japonicus. PLOS ONE (in press)Google Scholar
  35. Wang TL, Bogracheva TY, Hedley CL (1998) Starch: As simple as A, B, C? J Exp Bot 49:481–502CrossRefGoogle Scholar
  36. Welham T, Pike J, Horst I, Flemetakis E, Katinakis P, Kaneko T, Sato S, Tabata S, Perry J, Parniske M, Wang TL (2009) A cytosolic invertase is required for normal growth and cell development in the model legume, Lotus japonicus. J Exp Bot 60:3353–3365PubMedCrossRefPubMedCentralGoogle Scholar
  37. 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) α-amylase is not required for breakdown of transitory starch in Arabidopsis leaves. J Biol Chem 280:9773–9779PubMedCrossRefGoogle Scholar
  38. Zeeman SC, Thorneycroft D, Schupp N, Chapple A, Weck M, Dunstan H, Halidmann P, Bechtold N, Smith AM, Smith SM (2004) Plastidial α-glucan phosphorylase is not required for starch degradation in Arabidopsis leaves but has a role in the tolerance of abiotic stress. Plant Physiol 135:849–858PubMedCrossRefPubMedCentralGoogle Scholar
  39. Zeeman SC, Kossmann J, Smith AM (2010) Starch: its metabolism, evolution, and biotechnological modification in plants. Annu Rev Plant Biol 61:209–234PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Cécile Vriet
    • 1
  • Anne Edwards
    • 2
  • Alison M. Smith
    • 2
  • Trevor L. Wang
    • 2
  1. 1.Laboratoire de Génétique et Biophysique des PlantesAix-Marseille UniversityMarseilleFrance
  2. 2.Metabolic Biology, John Innes CentreNorwich Research ParkColney, NorwichUK

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