Starch Biosynthesis and Degradation in Plants

Abstract

Starch is the main form in which plants store carbon. Its presence and turnover are important for proper plant growth and productivity. The glucose polymers that constitute the semi‐crystalline starch granule are synthesised by the concerted actions of well‐conserved classes of isoforms of starch synthase and starch‐branching enzyme, via a process that also requires the debranching enzyme isoamylase. The degradation of the granule proceeds via different pathways in different types of starch‐storing tissues. The pathway of starch degradation differs between different plant tissues, but has been elucidated in most detail in leaves. The polymer is first phosphorylated to allow access to the insoluble granule by enzymes that cleave bonds between glucose residues. The main product of this degradation is maltose, which is exported into the cytosol before a series of enzymatic steps convert it to sucrose.

Key Concepts

  • Starch is the main carbon store of most plants.
  • It is a glucose polymer that is stored as insoluble granules within plastids.
  • The polymer is composed of two fractions, branched amylopectin and unbranched amylose.
  • It is synthesised by a number of enzymes that control the amount made, as well as the amounts of amylose and amylopectin.
  • Starch is synthesised in leaves during the day and is mobilised at night.
  • The rate of leaf starch degradation at night is closely controlled by mechanisms linked to the circadian clock so that starch is eliminated just before the beginning of day.
  • Leaf starch degradation involves many enzymes that lead to the production of soluble sugars, mainly maltose.
  • Maltose is exported into the cytosol where it is converted to sucrose.
  • Arabidopsis plants in which starch metabolism is impaired grow poorly.
  • Starch synthesised in leaves is often termed transitory starch, while that in storage organs can be termed storage starch. They are different in terms of the structure of the amylose and amylopectin within them.

Keywords: amylase; maltose; starch‐branching enzyme; starch granule; starch synthase

Figure 1. The structure of the starch polymers and the starch granule. Top left: representations of the structures of amylose and amylopectin. The chains in the amylose molecule are 1000 or more glucosyl residues in length. The short chains within the clusters of the amylopectin molecule are typically 12–20 glucosyl residues in length. Top right: adjacent chains within the clusters of the amylopectin molecule form double helices, and these associate together to form crystalline lamellae. The regions between the clusters that contain the branch points do not crystallise, giving rise to alternating crystalline and amorphous lamellae with a periodicity of 9 nm. The layers of the sandwich are parallel with the surface of the granule; in other words, the lamellae form concentric shells within the granule matrix. Bottom: scanning electron micrographs of the inner face of a starch granule from a potato tuber, cracked open and treated with a starch‐degrading enzyme to reveal the growth rings. Each ring consists of tens of the 9 nm repeats shown above. The bar represents 5 µm; the picture on the right is a closer image of part of the picture on the left.
Figure 2. The actions of ADPglucose pyrophosphorylase, starch synthase and starch‐branching enzyme. Starch synthase catalyses the addition of the glucosyl moiety of ADPglucose on to the nonreducing end of a chain via an α1,4 linkage. Starch‐branching enzyme cleaves sections of chains from the nonreducing end and adds them to the side of the same or an adjacent chain via an α1,6 linkage.
Figure 3. The pathway of starch degradation in the endosperm of a germinating cereal seed. The starch granule is attacked by the endoamylase α‐amylase, which releases soluble linear and branched glucans. These are acted on by the debranching enzyme limit dextrinase and the exoamylase β‐amylase to produce maltose. Maltose is then hydrolysed to glucose by an α‐glucosidase (maltase). The glucose is taken up into the growing embryo.
Figure 4. The pathway of starch degradation in an leaf at night. Leaf starch degradation is initiated by phosphorylation of amylopectin via glucan, water dikinases (GWD and PWD). Dephosphorylation of the phosphoglucans by glucan phosphatases (SEX4 and LSF2) presumably occurs concurrently. Debranching of the starch polymers at the granule surface is mainly via isoamylase 3, and linear glucans are metabolised via β‐amylase to yield maltose as the main product, with maltotriose as a more minor product. Possibly, α‐amylase can release branched glucans from the granule surface, which are then debranched via the debranching enzymes isoamylase 3 and limit dextrinase. However, this is at most a minor pathway as indicated by the dashed arrows. Maltose is exported from the chloroplast to the cytosol via the maltose transporter MEX1, and then metabolised via the cytosolic disproportionating enzyme (D‐enzyme; DPE2). DPE2 releases one of the glucosyl moieties of maltose as free glucose and transfers the other to a cytosolic heteroglycan, from which it is released via glucan phosphorylase as hexose phosphate. The maltotriose product of β‐amylase is converted via chloroplastic D‐enzyme (DPE1) to maltopentaose and free glucose. The maltopentaose is a substrate for the further action of β‐amylase, and the glucose is assumed to be transported to the cytosol via a glucose transporter. For convenience, maltotriose and maltopentaose in this figure are represented under the generic term ‘linear glucans’. Hexose phosphates produced in the cytosol from free glucose and the deglucosylation of the heteroglycan are converted to sucrose for export to the nonphotosynthetic parts of the plant.
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References

Baunsgaard L, Lütken H, Mikkelsen R, et al. (2005) A novel isoform of glucan, water dikinase phosphorylates pre‐phosphorylated α‐glucans and is involved in starch degradation in Arabidopsis. Plant Journal 41: 595–605.

Carciofi M, Shaik SS, Jensen SL, et al. (2011) Hyperphosphorylation of cereal starch. Journal of Cereal Science 54: 339–346.

Chia T, Thorneycroft D, Chapple A, et al. (2004) A cytosolic glucosyltransferase is required for conversion of starch to sucrose in Arabidopsis leaves at night. Plant Journal 37: 853–863.

Engelsen SB, Madsen AØ, Blennow A, et al. (2003) The phosphorylation site in double helical amylopectin as investigated by a combined approach using chemical synthesis, crystallography and molecular modeling. FEBS Letters 541: 137–144.

Fettke J, Eckermann N, Poeste S, et al. (2004) The glycan substrate of the cytosolic (Pho 2) phosphorylase isozyme from Pisum sativum L.: identification, linkage analysis and subcellular localization. Plant Journal 39: 933–946.

Fettke J, Eckermann N, Tiessen A, et al. (2005) Identification, subcellular localization and biochemical characterization of water‐soluble heteroglycans (SHG) in leaves of Arabidopsis thaliana L.: distinct SHG reside in the cytosol and in the apoplast. Plant Journal 43: 568–585.

Fettke J, Chia T, Ekermann N, et al. (2006) A transglucosidase necessary for starch degradation and maltose metabolism in leaves at night acts on cytosolic heteroglycans (SHG). Plant Journal 46: 668–684.

Fujita N, Satoh R, Hayashi A, et al. (2011) Starch biosynthesis in rice endosperm requires the presence of either starch synthase I or IIIa. Journal of Experimental Botany 62: 4819–4831.

Fulton DC, Stettler M, Mettler T, et al. (2008) β‐AMYLASE4, a noncatalytic protein required for starch breakdown, acts upstream of three active β‐amylases in Arabidopsis chloroplasts. Plant Cell 20: 1040–1058.

Gentry MS, Dowen RH III, Worby CA, et al. (2007) The phosphatase laforin crosses evolutionary boundaries and links carbohydrate metabolism to neuronal disease. Journal of Cell Biology 178: 477–488.

Gibson K, Park J‐S, Nagai Y, et al. (2011) Exploiting leaf starch synthesis as a transient sink to elevate photosynthesis, plant productivity and yields. Plant Science 181: 275–281.

Graf A and Smith AM (2010) Starch and the clock: the dark side of plant productivity. Trends in Plant Science 16: 169–175.

Graf A, Schlereth A, Stitt M and Smith AM (2010) Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. Proceedings of the National Academy of Sciences of the United States of America 107: 9458–9463.

Hädrich N, Hendriks JHM, Kötting O, et al. (2012) Mutagenesis of cysteine 81 prevents dimerization of the APS1 subunit of ADP‐glucose pyrophosphorylase and alters diurnal starch turnover in Arabidopsis thaliana leaves. The Plant Journal 70: 231–242.

Hejazi M, Fettke J, Kötting O, et al. (2010) The Laforin‐like dual‐specificity phosphatase SEX4 from Arabidopsis hydrolyzes both C6‐and C3‐phosphate esters introduced by starch‐related dikinases and thereby affects phase transition of alpha‐glucans. Plant Physiology 152: 711–722.

Hendriks JHM, Kolbe A, Gibon Y, et al. (2003) ADP‐glucose pyrophosphorylase is activated by posttranslational redox‐modification in response to light and to sugars in leaves of Arabidopsis and other plant species. Plant Physiology 133: 838–849.

Hofvander P, Andersson M, Larsson C‐T, et al. (2004) Field performance and starch characteristics of high‐amylose potatoes obtained by antisense gene targeting of two branching enzymes. Plant Biotechnology Journal 2: 311–320.

Hussain H, Mant A, Seale R, et al. (2003) Three isoforms of isoamylase contribute different catalytic properties for the debranching of potato glucans. Plant Cell 15: 133–149.

James MG, Robertson DS and Myers AM (1995) Characterization of the maize gene sugary1, a determinant of starch composition in kernels. Plant Cell 7: 417–429.

Kubo A, Colleoni C, Dinges JR, et al. (2010) Functions of heteromeric and homomeric isoamylase‐type starch‐debranching enzymes in developing maize endosperm. Plant Physiology 153: 956–969.

Kossmann J and Lloyd J (2000) Understanding and influencing starch biochemistry. Critical Reviews in Plant Sciences 19: 171–226.

Kötting O, Pusch K, Tiessen A, et al. (2005) Identification of a novel enzyme required for starch metabolism in Arabidopsis leaves. The phosphoglucan, water dikinase. Plant Physiology 137: 242–252.

Kötting O, Santelia D, Edner C, et al. (2009) STARCH‐EXCESS4 is a Laforin‐like phosphoglucan phosphatase required for starch degradation in Arabidopsis thaliana. Plant Cell 21: 334–346.

Liu F, Zhao Q, Mano N, et al. (2016) Modification of starch metabolism in transgenic Arabidopsis thaliana increases plant biomass and triples oilseed production. Plant Biotechnology Journal 14: 976–985.

Matsushima R, Maekawa M, Kusano M, et al. (2014) Amyloplast‐localized SUBSTANDARD STARCH GRANULE4 protein influences the size of starch grains in rice endosperm. Plant Physiology 164: 623–636.

Matsushima R, Maekawa M, Kusano M, et al. (2016) Amyloplast membrane protein SUBSTANDARD STARCH GRAIN6 controls starch grain size in rice endosperm. Plant Physiology 170: 1445–1459.

Myers AM, Morell MK, James MG and Ball SG (2000) Recent progress in understanding the biosynthesis of the amylopectin crystal. Plant Physiology 122: 898–997.

Niittylä T, Messerli G, Trevisan M, et al. (2004) A previously unknown maltose transporter essential for starch degradation in leaves. Science 303: 87–89.

Paparelli E, Parlanti S, Gonzali S, et al. (2013) Nightime sugar starvation orchestrates gibbberillin biosynthesis and plant growth in Arabidopsis. Plant Cell 25: 3760–3769.

Peng C, Wang Y, Liu F, et al. (2014) FLOURY ENDOSPERM6 encodes a CBM48 domain‐containing protein involved in compound granule formation and starch synthesis in rice endosperm. The Plant Journal 77: 917–930.

Ritte G, Lloyd JR, Ekermann N, et al. (2002) The starch‐related R1 protein is an α‐glucan, water dikinase. Proceedings of the National Academy of Sciences of the United States of America 99: 7166–7171.

Ritte G, Scharf A, Eckermann N, et al. (2004) Phosphorylation of transitory starch is increased during degradation. Plant Physiology 135: 2068–2077.

Ritte G, Heydenreich M, Mahlow S, et al. (2006) Phosphorylation of C6‐ and C3‐positions of glucosyl residues in starch is catalysed by distinct dikinases. FEBS Letters 580: 4872–4876.

Roldán I, Lucas MM, Devalle D, et al. (2007) The phenotype of soluble starch synthase IV defective mutants in Arabidopsis thaliana suggests a novel function of elongation enzymes in the control of starch granule formation. Plant Journal 49: 492–504.

Santelia D, Kötting O, Seung D, et al. (2011) The phosphoglucan phosphatase Like Sex Four2 dephosphorylates starch at the C3‐position in Arabidopsis. Plant Cell 23: 4096–4111.

Schwall GP, Safford R, Westcott RJ, et al. (2000) Production of very‐high‐amylose potato starch by inhibition of SBE A and B. Nature Biotechnology 18: 551–554.

Smith SM, Fulton DC, Chia T, et al. (2004) Diurnal changes in the transcriptome encoding enzymes of starch metabolism provide evidence for both transcriptional and posttranscriptional regulation of starch metabolism in Arabidopsis leaves. Plant Physiology 136: 2687–2699.

Smith AM, Zeeman SC and Smith SM (2005) Starch degradation. Annual Review of Plant Biology 56: 73–97.

Sonnewald U and Kossmann J (2013) Starches‐from current models to genetic engineering. Plant Biotechnology Journal 11: 223–232.

Streb S and Zeeman SC (2012) Starch metabolism in Arabidopsis. The Arabidopsis Book 10: e0160.

Sulpice R, Pyl E‐T, Ishihara H, et al. (2009) Starch as a major integrator in the regulation of plant growth. Proceedings of the National Academy of Sciences of the United States of America 106: 10348–10353.

Szylowdski N, Ragel P, Raynaud S, et al. (2009) Starch granule initiation in Arabidopsis requires the presence of either class IV or class III starch synthases. Plant Cell 21: 2443–2457.

Takeda Y and Hizukuri S (1981) Studies on starch phosphate. Part 5. Re‐examination of the action of sweet‐potato beta‐amylase on phosphorylated (1‐>4)‐α‐D‐glucan. Carbohydrate Research 89: 174–178.

Tetlow IJ, Wait R, Lu Z, et al. (2004) Protein phosphorylation in amyloplasts regulates starch branching enzyme activity and protein–protein interactions. Plant Cell 16: 694–708.

Toyosawa Y, Kawagoe Y, Matsushima R, et al. (2016) Deficiency of starch synthase IIIa and IVb alters starch granule morphology from polyhedral to spherical in rice endosperm. Plant Physiology 170: 1255–1270.

Waigh TA, Kato KL, Donald AM, et al. (2000) Side‐chain liquid‐crystalline model for starch. Starch/Staerke 52: 450–460.

Yu TS, Kofler H, Häusler RE, et al. (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: 1907–1918.

Zeeman SC, Thorneycroft D, Schupp N, et al. (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 Physiology 135: 849–858.

Further Reading

Arias MC, Pelletier S, Hilliou F, et al. (2014) From dusk till dawn: the Arabidopsis thaliana sugar starving responsive network. Frontiers in Plant Science 5: 482.

Ballicora MA, Iglesias AA and Preiss J (2004) ADP‐glucose pyrophosphorylase: a regulatory enzyme for plant starch synthesis. Photosynthesis Research 79: 1–24.

Blennow A and Engelsen SB (2010) Helix‐breaking news: fighting crystalline starch energy deposits in the cell. Trends in Plant Science 15: 236–240.

Comparot‐Moss S and Denyer K (2009) The evolution of the starch biosynthetic pathway in cereals and other grasses. Journal of Experimental Botany 60: 2481–2492.

Kötting O, Kossmann J, Zeeman SC, et al. (2010) Regulation of starch metabolism: the age of enlightenment? Current Opinion in Plant Biology 13: 321–329.

Li C and Gilbert RG (2016) Progress in controlling starch‐structure by modifying starch‐branching enzymes. Planta 243: 13–22.

Silver D, Kötting O and Moorhead GBG (2014) Phosphoglucan phosphatase function sheds light on starch degradation. Trends in Plant Science 19: 471–478.

Stitt M and Zeeman SC (2012) Starch turnover: pathways, regulation and role in growth. Current Opinion in Plant Biology 15: 282–292.

Tuncel A and Okita TW (2013) Improving starch yield in cereals by over‐expression of ADPglucose pyrophosphorylase: expectations and unanticipated outcomes. Plant Science 211: 52–60.

Zeeman SC, Kossmann J and Smith AM (2010) Starch: its metabolism, evolution, and biotechnological modification in plants. Annual Review of Plant Biology 61: 209–234.

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Lloyd, James R, and Kötting, Oliver(Jul 2016) Starch Biosynthesis and Degradation in Plants. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020124.pub2]