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Starch Biosynthesis, Its Regulation and Biotechnological Approaches to Improve Crop Yields

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Starch Biosynthesis, Its Regulation and Biotechnological Approaches to Improve Crop Yields JBA-06696; No of Pages 20 Biotechnology Advances xxx (2013) xxx–xxx Contents lists available at SciVerse ScienceDirect Biotechnology Advances journal homepage: www.elsevier.com/locate/biotechadv Starch biosynthesis, its regulation and biotechnological approaches to improve crop yields Abdellatif Bahaji a,1, Jun Li a,1, Ángela María Sánchez-López a, Edurne Baroja-Fernández a, Francisco José Muñoz a, Miroslav Ovecka a,b, Goizeder Almagro a, Manuel Montero a, Ignacio Ezquer a, Ed Etxeberria c, Javier Pozueta-Romero a,⁎ a Instituto de Agrobiotecnología (CSIC/UPNA/Gobierno de Navarra), Mutiloako etorbidea z/g, 31192 Mutiloabeti, Nafarroa, Spain b Centre of the Region Haná for Biotechnological and Agricultural Research, Department of Cell Biology, Faculty of Science, Palacky University, Šlechtitelů 11, CZ-783 71 Olomouc, Czech Republic c University of Florida, Institute of Food and Agricultural Sciences, Citrus Research and Education Center, 700 Experiment Station Road, Lake Alfred, FL 33850-2299, USA article info abstract Available online xxxx Structurally composed of the glucose homopolymers amylose and amylopectin, starch is the main storage carbo- hydrate in vascular plants, and is synthesized in the plastids of both photosynthetic and non-photosynthetic cells. Keywords: Its abundance as a naturally occurring organic compound is surpassed only by cellulose, and represents both a ADPglucose cornerstone for human and animal nutrition and a feedstock for many non-food industrial applications including – Calvin Benson cycle production of adhesives, biodegradable materials, and first-generation bioethanol. This review provides an up- Carbohydrate metabolism date on the different proposed pathways of starch biosynthesis occurring in both autotrophic and heterotrophic Genetic engineering organs, and provides emerging information about the networks regulating them and their interactions with the Microbial volatiles fi MIVOISAP environment. Special emphasis is given to recent ndings showing that volatile compounds emitted by microor- Plant–microbe interaction ganisms promote both growth and the accumulation of exceptionally high levels of starch in mono- and dicoty- Endocytosis ledonous plants. We also review how plant biotechnologists have attempted to use basic knowledge on starch Starch futile cycling metabolism for the rational design of genetic engineering traits aimed at increasing starch in annual crop species. Sucrose synthase Finally we present some potential biotechnological strategies for enhancing starch content. © 2013 Elsevier Inc. All rights reserved. Contents 1. Introduction............................................................... 0 2. Proposedstarchbiosyntheticpathways................................................... 0 2.1. Starchbiosynthesisinleaves.................................................... 0 2.1.1. A classic model of starch biosynthesis according to which the starch biosynthetic pathway is linked to the Calvin–Benson cycle by means of plastidialphosphoglucoseisomerase............................................ 0 2.1.2. Models of starch biosynthesis according to which the starch biosynthetic pathway is not linked to the Calvin–Benson cycle by meansofplastidialphosphoglucoseisomerase........................................ 0 2.2. Starchbiosynthesisinheterotrophicorgans............................................. 0 2.2.1. Mechanismsofsucroseunloadinginheterotrophicorgans.................................. 0 2.2.2. Proposed mechanisms of sucrose–starchconversioninheterotrophiccells........................... 0 Abbreviations: ADPG, ADPglucose; AGP, ADPG pyrophosphorylase; AGPP, ADPG pyrophosphatase; A/N-inv, alkaline/neutral invertase; BT1, Brittle 1; F6P, fructose-6-phosphate; G1P, glucose-1-phosphate; G6P, glucose-6-phosphate; GBSS, granule bound starch synthase; GPT, glucose-6-phosphate translocator; GWD, glucan, water dikinase; HvBT1, Hordeum vulgare BT1; MCF, mitochondrial carrier family; MVs, microbial volatiles; NPP, nucleotide pyrophosphatase/phosphodiesterase; MIVOISAP, MIcrobial VOlatiles Induced Starch Accumulation Pro- cess; NTRC, NADP-thioredoxin reductase C; OPPP, oxidative pentose phosphate pathway; Pi, orthophosphate; 3PGA, 3-phosphoglycerate; pHK, plastidial hexokinase; pPGI, plastidial phosphoglucoseisomerase; pPGM, plastidial phosphoglucomutase; PPi, inorganic pyrophosphate; pSP, plastidial starch phosphorylase; RSR1, Rice Starch Regulator1; SuSy, sucrose synthase; SS, starch synthase; T6P, trehalose-6-phosphate; Trx, thioredoxin; UDPG, UDPglucose; UGP, UDPG pyrophosphorylase; WT, wild type; ZmBT1, Zea mays BT1. ⁎ Corresponding author. Tel.: +34 948168009; fax: +34 948232191. E-mail address: [email protected] (J. Pozueta-Romero). 1 These authors contributed equally to this work. 0734-9750/$ – see front matter © 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.biotechadv.2013.06.006 Please cite this article as: Bahaji A, et al, Starch biosynthesis, its regulation and biotechnological approaches to improve crop yields, Biotechnol Adv (2013), http://dx.doi.org/10.1016/j.biotechadv.2013.06.006 2 A. Bahaji et al. / Biotechnology Advances xxx (2013) xxx–xxx 3. Microbialvolatilespromotebothgrowthandaccumulationofexceptionallyhighlevelsofstarchinmono-anddicotyledonousplants........ 0 4. Biotechnologicalapproachesforincreasingstarchcontentinheterotrophicorgans............................... 0 4.1. EnhancementofAGPactivity.................................................... 0 4.2. Increasingsupplyofstarchprecursorstotheamyloplast........................................ 0 4.3. Increasingsupplyofsucrosetoheterotrophiccells.......................................... 0 4.4. Enhancementofsucrosebreakdownwithintheheterotrophiccell................................... 0 4.5. EnhancementofexpressionofstarchsynthaseclassIV......................................... 0 4.6. Blockingstarchbreakdown..................................................... 0 4.7. Alteringtheexpressionofglobalregulators.............................................. 0 4.8. Enhancingtrehalose-6-phosphatecontent.............................................. 0 4.9. Potentialstrategiesforincreasingstarchcontentinheterotrophicorgans................................. 0 4.9.1. Over-expressionofBT1.................................................. 0 4.9.2. BlockingtheactivityofADPGbreakdownenzymes...................................... 0 4.9.3. EctopicexpressionofSuSyintheplastid........................................... 0 4.9.4. Blockingthesynthesisofstorageproteins.......................................... 0 5. Conclusionsandmainchallenges...................................................... 0 Acknowledgments............................................................... 0 References.................................................................. 0 1. Introduction industrial needs and social demands. However, while much is known about starch metabolism, there are still major gaps in our knowledge Starch is the main storage carbohydrate in vascular plants. Its abun- that prevent breeders and biotechnologists from advancing in their at- dance as a naturally occurring compound of living terrestrial biomass is tempts to increase starch content in a predictable way (Chen et al., surpassed only by cellulose, and represents the primary source of calo- 2012). ries in the human diet. Because starch is the principal constituent of In this paper, we first review recent advances in the biochemistry of the harvestable organ of many agronomic plants, its synthesis and accu- starch biosynthesis and its regulation, and provide an update on different mulation also influences crop yields. proposed pathways of starch biosynthesis occurring in both autotrophic Synthesized in the plastids of both photosynthetic and non- and heterotrophic organs. Special emphasis is given to recent findings photosynthetic cells, starch is an insoluble polyglucan produced by showing that volatile compounds emitted by microorganisms promote starch synthase (SS) using ADP-glucose (ADPG) as the sugar donor mol- both growth and the accumulation of exceptionally high levels of starch. ecule. Starch has two major components, amylopectin and amylose, both Finally, we assess the progress in molecular strategies for increasing of which are polymers of α-D-glucose units. Amylose is a linear polymer starch in annual crop species by genetic engineering approaches. of up to several thousand glucose residues, whereas amylopectin is a larger polymer regularly branched with α-1,6-branch points. These 2. Proposed starch biosynthetic pathways two molecules are assembled together to form a semi-crystalline starch granule. The exact proportions of these molecules and the size and Starch is found in the plastids of photosynthetic and non- shape of the granule vary between species and between organs of the photosynthetic tissues. Mature chloroplasts occurring in photosynthet- same plant. The diversity of both composition and physical parameters ically active cells possess the capacity of providing energy (ATP) and of starches from different botanical sources gives rise to their diverse fixed carbon for the synthesis of starch during illumination. By contrast, processing properties and applications in both non-food sectors such as production of long-term storage of starch taking place in amyloplasts of sizing agents in textile and paper industry, adhesive gums, and biode- reserve organs such as tubers, roots and seed endosperms depends gradable materials, and in food industries,
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