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Journal of Integrative Agriculture  2016, Vol. 15 Issue (9): 1968-1982    DOI: 10.1016/S2095-3119(15)61192-3
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A plastidic ATP/ADP transporter gene, IbAATP, increases starch and amylose contents and alters starch structure in transgenic sweetpotato
WANG Yan-nan, LI Yan, ZHANG Huan, ZHAI Hong, LIU Qing-chang, HE Shao-zhen
College of Agronomy & Biotechnology, China Agricultural University, Beijing 100193, P.R.China
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Abstract      A plastidic adenosine triphosphate (ATP)/adenosine diphosphate (ADP) transporter (AATP) is responsible for importing ATP from the cytosol into plastids. In dicotyledonous plants, increasing ATP supply is a potential way to facilitate anabolic synthesis in heterotrophic plastids. In this study, a gene encoding the AATP protein, named IbAATP, was isolated from sweetpotato (Ipomoea batatas (L.) Lam.). Transcripts of IbAATP were predominantly detected in the storage roots and leaves and were induced by exogenous sucrose and subjected to circadian rhythm. Transient expression of IbAATP in tobacco and onion epidermal cells revealed the plastidic localization of IbAATP. The overexpression of IbAATP in sweetpotato significantly increased the starch and amylose contents and led to enlarged starch granules. The IbAATP-overexpressing plants showed altered fine structure of amylopectin, which contained an increased proportion of chains with a degree of polymerization (DP) of 10–23 and a reduced number of chains with a DP of 5–9 and 24–40. In addition, starch from the transgenic plants exhibited different pasting properties. The transcript levels of starch biosynthetic genes, including IbAGP, IbGBSSI, IbSSI-IV, and IbSBE, were differentially regulated in the transgenic plants. These results revealed the explicit role of IbAATP in the starch biosynthesis of sweetpotato and indicated that this gene has the potential to be used to improve starch content and quality in sweetpotato and other plants.
Keywords:  sweetpotato        IbAATP        starch content and composition        starch granule size        starch structure        pasting properties  
Received: 20 July 2015   Accepted:

This work was supported by the National Natural Science Foundation of China (31371680), the Beijing Food Crops Innovation Consortium Program and the China Agriculture Research System (CARS-11).

Corresponding Authors:  HE Shao-zhen, +86-10-62732559, E-mail:   
About author:  WANG Yan-nan, +86-10-62732559, E-mail:

Cite this article: 

WANG Yan-nan, LI Yan, ZHANG Huan, ZHAI Hong, LIU Qing-chang, HE Shao-zhen. 2016. A plastidic ATP/ADP transporter gene, IbAATP, increases starch and amylose contents and alters starch structure in transgenic sweetpotato. Journal of Integrative Agriculture, 15(9): 1968-1982.

Bae J M, Kwak M S, Noh S A, Oh M J, Kim Y S, Shin J S. 2014. Overexpression of sweetpotato expansin cDNA (IbEXP1) increases seed yield in Arabidopsis. Transgenic Research, 23, 657–667.   

Bläsing O E, Gibon Y, Günther M, Höhne M, Morcuende R, Osuna D, Thimm O, Usadel B, Scheible W R, Stitt M. 2005. Sugar and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. The Plant Cell, 17, 3257–3281.

Blazek J, Copeland L. 2008. Pasting and swelling properties of wheat flour and starch in relation to amylose content. Carbohydrate Polymers, 71, 380–387.  

Bovell-Benjamin A C. 2007. Sweet potato: A review of its past, present, and future role in human nutrition. Advances in Food and Nutrition Research, 52, 1–59.  

Brummell D A, Watson L M, Zhou J, McKenzie M J, Hallett I C, Simmons L, Carpenter M, Timmerman-Vaughan G M. 2015. Overexpression of STARCH BRANCHING ENZYME II increases short-chain branching of amylopectin and alters the physicochemical properties of starch from potato tuber. BMC Biotechnology, 15, 28.  

Buléon A, Gallant D J, Bouchet B, Mouille G, D’Hulst C, Kossmann J, Ball S. 1997. Starches from A to C - Chlamydomonas reinhardtii as a model microbial system to investigate the biosynthesis of the plant amylopectin crystal. Plant Physiology, 115, 949–957. 

Burtardo V M, Fitzgerald M A, Bird A R, Gidley M J, Flanagan B M, Larroque O, Resurreccion A P, Laidlaw H K C, Jobling S A, Morell M K, Rahman S. 2011. Impact of down-regulation of starch branching enzyme IIb in rice by artificial microRNA- and hairpin RNA-mediated RNA silencing. Journal of Experimental Botany, 62, 4927–4941. 

Burton R A, Jenner H, Carrangis L, Fahy B, Fincher G B, Hylton C, Laurie D A, Parker M, Waite D, Wegen S V, Verhoeven T, Denyer K. 2002. Starch granule initiation and growth are altered in barley mutants that lack isoamylase activity. The Plant Journal, 31, 97–112.

Bustos R, Fahy B, Hylton C M, Seale R, Nebane N M, Edwards A, Martin C, Smith A M. 2004. Starch granule initiation is controlled by a heteromultimeric isoamylase in potato tubers. Proceedings of the National Academy of Sciences of the United States of America, 101, 2215–2220.

Emes M J, Neuhaus H E. 1997. Metabolism and transport in non-photosynthetic plastids. Journal of Experimental Botany, 48, 1995–2005.   

FAO. 2009. FAO statistics. [2015-04-24].

Fiore C, Trézéguet V, Saux A L, Roux P, Schwimmer C, Dianoux A C, Noel F, Lauquin G J M, Brandolin G, Vignais P V. 1998. The mitochondrial ADP/ATP carrier: Structural, physiological and pathological aspects. Biochimie, 80, 137–150.  

Frohman M A, Dush M K, Martin G R. 1988. Rapid production of full-length cDNAs from rare transcripts: Amplification using a single gene-specific oligonucleotide primer. Proceedings of the National Academy of Sciences of the United States of America, 85, 8998–9002.   

Fujita N, Yoshida M, Asakura N, Ohdan T, Miyao A, Hirochika H, Nakamura Y. 2006. Function and characterization of starch synthase I using mutants in rice. Plant Physiology, 140, 1070–1084. 

Fujita N, Yoshida M, Kondo T, Saito K, Utsumi Y, Tokunaga T, Nishi A, Satoh H, Park J H, Jane J L, Miyao A, Hirochika H, Nakamura Y. 2007. Characterization of SSIIIa-deficient mutants of rice: The function of SSIIIa and pleiotropic effects by SSIIIa deficiency in the rice endosperm. Plant Physiology, 144, 2009–2023.

Geigenberger P. 2011. Regulation of starch biosynthesis in response to a fluctuating environment. Plant Physiology, 155, 1566–1577.   

Geigenberger P, Stamme C, Tjaden J, Schulz A, Quick P W, Betsche T, Kersting H J, Neuhaus H E. 2001. Tuber physiology and properties of starch from tubers of transgenic potato plants with altered plastidic adenylate transporter activity. Plant Physiology, 125, 1667–1678. 

Green R M, Tingay S, Wang Z Y, Tobin E M. 2002. Circadian rhythms confer a higher level of fitness to Arabidopsis plants. Plant Physiology, 129, 576–584.

Heldt H W. 1969. Adenine nucleotide translocation in spinach chloroplasts. FEBS Letters, 5, 11–14. 

Hillman W S. 1976. Biological rhythms and physiological timing. Annual Review of Plant Biology, 27, 159–179.

Jefferson R A, Kavanagh T A, Bevan M W. 1987. GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. The Embo Journal, 6, 3901–3907.

Jeon J S, Ryoo N, Hahn T R, Walia H, Nakamura Y. 2010. Starch biosynthesis in cereal endosperm. Plant Physiology and Biochemistry, 48, 383–392.

Kimura T, Otani M, Noda T, Ideta O, Shimada T, Saito A. 2001. Absence of amylose in sweet potato [Ipomoea batatas (L.) Lam.] following the introduction of granule-bound starch synthase I cDNA. Plant Cell Reports, 20, 663–666.  

Kitahara K, Hamasuna K, Nozuma K, Otani M, Hamada T, Shimada T, Fujita K, Suganuma T. 2007. Physicochemical properties of amylose-free and high-amylose starches from transgenic sweetpotatoes modified by RNA interference. Carbohydrate Polymers, 69, 233–240.  

Kitahara K, Takahata Y, Otani M, Tanaka M, Katayama K, Yoshinaga M, Fujita K, Suganuma T. 2011. Starch properties of transgenic sweetpotato plants modified by RNA interference of the starch synthase II gene. Journal of Applied Glycoscience, 58, 85–90. 

Koch K E. 1996. Carbohydrate-modulated gene expression in plants. Annual Reviews of Plant Biology, 47, 509–540.  

Leterrier M, Holappa L D, Broglie K E, Beckles D M. 2008. Cloning, characterization and comparative analysis of a starch synthase IV gene in wheat: Functional and evolutionary implications. BMC Plant Biology, 8, 98. 

Linka N, Hurka H, Lang B F, Burger G, Winkler H H, Stamme C, Urbany C, Seil I, Kusch J, Neuhaus H E. 2003. Phylogenetic relationships of non-mitochondrial nucleotide transport proteins in bacteria and eukaryotes. Gene, 306, 27–35.   

Liu D G, He S Z, Zhai H, Wang L J, Zhao Y, Wang B, Li R J, Liu Q C. 2013. Overexpression of IbP5CR enhances salt tolerance in transgenic sweetpotato. Plant Cell, Tissue and Organ Culture, 117, 1–16.  

Liu Q C, Zhai H, Wang Y, Zhang D P. 2001. Efficient plant regeneration from embryogenic suspension cultures of sweetpotato. In Vitro Cellular & Developmental Biology (Plant), 37, 564–567. 

McDonald A M L, Stark J R, Morrison W R, Ellis R P. 1991. The composition of starch granules from developing Barley genotypes. Journal of Cereal Science, 13, 93–112.   

McMaugh S J, Thistleton J L, Anschaw E, Luo J X, Konik-Rose C, Wang H, Huang M, Larroque O, Regina A, Jobling S A, Morell M K, Li Z Y. 2014. Suppression of starch synthase I expression affects the granule morphology and granule size and fine structure of starch in wheat endosperm. Journal of Experimental Botany, 65, 2189–2201. 

Meng K, Chang T J, Liu X, Chen S B, Wang Y Q, Sun A J, Xu H L, Wei X L, Zhu Z. 2005. Cloning and expression pattern of a gene encoding a putative plastidic ATP/ADP transporter from Helianthus tuberosus L. Journal of Integrative Plant Biology, 47, 1123–1132. 

Möhlmann T, Tjaden J, Schwöppe C, Winkler H H, Kampfenkel K, Neuhaus H E. 1998. Occurrence of two plastidic ATP/ADP transporters in Arabidopsis thaliana L. - Molecular characterization and comparative structural analysis of similar ATP/ADP translocators from plastids and Rickettsia prowazekii. European Journal of Biochemistry, 252, 353–359.

Nakamura Y. 2002. Toward a better understanding of the metabolic system for amylopectin biosynthesis in plants: rice endosperm as a model tissue. Plant and Cell Physiology, 43, 718–725.    

Nakamura Y, Yuki K, Park S Y, Ohya T. 1989. Carbohydrate metabolism in the developing endosperm of rice grains. Plant and Cell Physiology, 30, 833–839.

Noda T, Takahata Y, Sato T, Hisamatsu M, Yamada T. 1995. Physicochemical properties of starches extracted from sweet potato roots differing in physiological age. Journal of Agricultural and Food Chemistry, 43, 3016–3020.    

Regierer B, Fernie A R, 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.  

Reiser J, Linka N, Lemke L, Jeblick W, Neuhaus H E. 2004. Molecular physiological analysis of two plastidic ATP/ADP transporters from Arabidopsis. Plant Physiology, 136, 3524–3536.

Roldán I, Wattebled F, Lucas M M, Delvallé D, Planchot V, Jiménez S, Pérez R, Ball S, D’Hulst C, Mérida Á. 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. The Plant Journal, 49, 492–504.

Satoh H, Nishi A, Yamashita K, Takemoto Y, Tanaka Y, Hosaka Y, Sakurai A, Fujita N, Nakamura Y. 2003. Starch-branching enzyme I-deficient mutation specifically affects the structure and properties of starch in rice endosperm. Plant Physiology, 133, 1111–1121. 

Schünemann D, Borchert S, Flügge U I, Heldt H W. 1993. ADP/ATP translocator from pea root plastids-Comparison with translocators from spinach chloroplasts and pea leaf mitochondria. Plant Physiology, 103, 131–137.  

Singh A, Baranwal V, Shankar A, Kanwar P, Ranjan R, Yadav S, Pandey A, Kapoor S, Pandey G K. 2012. Rice phospholipase A superfamily: Organization, phylogenetic and expression analysis during abiotic stresses and development. PLoS ONE, 7, e30947.

Smith A M. 2008. Prospects for increasing starch and sucrose yields for bioethanol production. The Plant Journal, 54, 546–558. 

Smith A M, Denyer K, Martin C. 1997. The synthesis of the starch granule. Annual Reviews of Plant Biology, 48, 67–87.  

Smith A M, Zeeman S C. 2006. Quantification of starch in plant tissues. Nature Protocols, 1, 1342–1345.    

Strasser R, Bondili J S, Schoberer J, Svoboda B, Liebminger E, Glössl J, Altmann F, Steinkellner H, Mach L. 2007. Enzymatic properties and subcellular localization of Arabidopsis β-N-Acetylhexosaminidases. Plant Physiology, 145, 5–16.  

Streb S, Egli B, Eicke S, Zeeman S C. 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 Physiology, 151, 1769–1772.  

Szydlowski N, Ragel P, Raynaud S, Lucas M M, Roldán I, Montero M, Muñoz F J, Ovecka M, Bahaji A, Planchot V, Pozueta-Romero J, D’Hulst C, Mérida Á. 2009. Starch granule initiation in Arabidopsis requires the presence of either class IV or class III starch synthase. The Plant Cell, 21, 2443–2457.

Takahata Y, Tanaka M, Otani M, Katayama K, Kitahara K, Nakayachi O, Nakayama H, Yoshinaga M. 2010. Inhibition of the expression of the starch synthase II gene leads to lower pasting temperature in sweetpotato starch. Plant Cell Reports, 29, 535–543.   

Tanaka M, Takahata Y, Nakayama H, Nakatani M, Tahara M. 2009. Altered carbohydrate metabolism in the storage roots of sweetpotato plants overexpressing the SRF1 gene, which encodes a Dof zinc finger transcription factor. Planta, 230, 737–746.  

Tetlow I J. 2011. Starch biosynthesis in developing seeds. Seed Science Research, 21, 5–32.

Tetlow I J, Morell M K, Emes M J. 2004. Recent developments in understanding the regulation of starch metabolism in higher plants. Journal of Experimental Botany, 55, 2131–2145.

Tjaden J, Möhlmann T, Kampfenkel K, Henrichs G, Neuhaus H E. 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.  

Wang S J, Yeh K W, Tsai C Y. 2001. Regulation of starch granule-bound starch synthase I gene expression by circadian clock and sucrose in the source tissue of sweet potato. Plant Science, 161, 635–644. 

Wang S J, Yeh K W, Tsai C Y. 2004. Circadian control of sweet potato granule-bound starch synthase I gene in Arabidopsis plants. Plant Growth Regulation, 42, 161–168.

Winkler H H, Neuhaus H E. 1999. Non-mitochondrial ATP transport. Trends in Biochemical Sciences, 24, 64–68.    

Yuen C Y L, Leelapon O, Chanvivattana Y, Warakanont J, Narangajavana J. 2009. Molecular characterization of two genes encoding plastidic ATP/ADP transport proteins in cassava. Biologia Plantarum, 53, 37–44.    

Zhao S S, Dufour D, Sánchez T, Ceballos H, Zhang P. 2011. Development of waxy cassava with different biological and physico-chemical characteristics of starches for industrial applications. Biotechnology and Bioengineering, 108, 1925–1935. 

Zhou W Z, Yang J, Hong Y, Liu G L, Zheng J L, Gu Z B, Zhang P. 2015. Impact of amylose content on starch physiochemical properties in transgenic sweet potato. Carbohydrate Polymers, 122, 417–427.
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