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Formation of Elongated Starch Granules in High-Amylose Maize

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Formation of Elongated Starch Granules in High-Amylose Maize Genetics, Development and Cell Biology Genetics, Development and Cell Biology Publications 4-2010 Formation of elongated starch granules in high- amylose maize Hongxin Jiang Iowa State University Harry T. Horner Iowa State University, [email protected] Tracey M. Pepper Iowa State University Michael Blanco United States Department of Agriculture Mark Campbell Truman State University SeFoe nelloxtw pa thige fors aaddndition addal aitutionhorsal works at: http://lib.dr.iastate.edu/gdcb_las_pubs Part of the Agronomy and Crop Sciences Commons, Food Biotechnology Commons, and the Plant Breeding and Genetics Commons The ompc lete bibliographic information for this item can be found at http://lib.dr.iastate.edu/ gdcb_las_pubs/41. For information on how to cite this item, please visit http://lib.dr.iastate.edu/ howtocite.html. This Article is brought to you for free and open access by the Genetics, Development and Cell Biology at Iowa State University Digital Repository. It has been accepted for inclusion in Genetics, Development and Cell Biology Publications by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. Formation of elongated starch granules in high-amylose maize Abstract GEMS-0067 maize starch contains up to 32% elongated starch granules, much higher than amylose-extender (ae) single-mutant maize starch (∼7%) and normal (non-mutant) maize starch (0%). These elongated granules are highly resistant to enzymatic hydrolysis at 95–100 °C, which function as resistant starch. The structure and formation of these elongated starch granules, however, were not known. In this study, light, confocal laser-scanning, scanning electron, and transmission electron microscopy were used to reveal the structure and formation of these elongated starch granules. The transmission electron micrographs showed fusion through amylose interaction between adjacent small granules in the amyloplast at the early stage of granule development. A mechanistic model for the formation of elongated starch granules is proposed. Keywords High-amylose maize starch, Amylose-extender mutant, Resistant starch, Starch structure, Long-chain double- helical crystallite, Elongated starch granule, Starch granule formation Disciplines Agronomy and Crop Sciences | Food Biotechnology | Plant Breeding and Genetics Comments This article is from Carbohydrate Polymers 80 (2010); 533, doi: 10.1016/j.carbpol.2009.12.016. Rights Works produced by employees of the U.S. Government as part of their official duties are not copyrighted within the U.S. The onc tent of this document is not copyrighted. Authors Hongxin Jiang, Harry T. Horner, Tracey M. Pepper, Michael Blanco, Mark Campbell, and Jay-Lin Jane This article is available at Iowa State University Digital Repository: http://lib.dr.iastate.edu/gdcb_las_pubs/41 Carbohydrate Polymers 80 (2010) 533–538 Contents lists available at ScienceDirect Carbohydrate Polymers journal homepage: www.elsevier.com/locate/carbpol Formation of elongated starch granules in high-amylose maize Hongxin Jiang a, Harry T. Horner b, Tracey M. Pepper b, Michael Blanco c, Mark Campbell d, Jay-lin Jane a,* a Department of Food Science and Human Nutrition, Iowa State University, Ames, IA 50011, USA b Department of Genetics, Development and Cell Biology & Microscopy and NanoImaging Facility, Iowa State University, Ames, IA 50011, USA c USDA-ARS/Plant Introduction Research Unit, Ames, IA 50011, USA d Truman State University, Kirksville, MO 63501, USA article info abstract Article history: GEMS-0067 maize starch contains up to 32% elongated starch granules, much higher than amylose- Received 14 November 2009 extender (ae) single-mutant maize starch (7%) and normal (non-mutant) maize starch (0%). These elon- Received in revised form 10 December 2009 gated granules are highly resistant to enzymatic hydrolysis at 95–100 °C, which function as resistant Accepted 11 December 2009 starch. The structure and formation of these elongated starch granules, however, were not known. In this Available online 16 December 2009 study, light, confocal laser-scanning, scanning electron, and transmission electron microscopy were used to reveal the structure and formation of these elongated starch granules. The transmission electron Keywords: micrographs showed fusion through amylose interaction between adjacent small granules in the amylo- High-amylose maize starch plast at the early stage of granule development. A mechanistic model for the formation of elongated Amylose-extender mutant Resistant starch starch granules is proposed. Starch structure Ó 2009 Elsevier Ltd. All rights reserved. Long-chain double-helical crystallite Elongated starch granule Starch granule formation 1. Introduction Burn, & Mathers, 2009; Van Munster, Tangerman, & Nagengast, 1994). Starch exists widely in seeds, roots, tubers, and fruits as an energy Normal maize starch contains less than 1% RS (AOAC, 2003), reserve of plants (Robyt, 1998). Because starch is a renewable, whereas starch of maize ae single-mutant has 15% RS (Li, Jiang, economical, and environmentally friendly biopolymer, it is widely Campbell, Blanco, & Jane, 2008). A recently developed GEMS- used in food and non-food applications, such as a thickener, binder, 0067 high-amylose maize starch, through the USDA-ARS Germ- film, and foam (Richardson, Jeffcoat, & Shi, 2000). There has been an plasm Enhancement of Maize (GEM) Project, contains up to increased interest in producing resistant starch (RS) from high-amy- 43.2% RS (Li et al., 2008). The GEMS-0067 is an inbred line of maize lose maize starch. RS is a portion of starch that cannot be hydrolyzed homozygous mutant of ae gene and a high-amylose modifier by human digestive enzymes and functions as a prebiotic for bacte- (HAM) gene (Campbell, Jane, Pollak, Blanco, & O’Brien, 2007). rial fermentation in the large intestine (Englyst & Cummings, 1985; Normal maize starch is composed of 30% primarily linear Englyst & Macfarlane, 1986). RS from high-amylose maize starch has amylose and 70% highly-branched amylopectin, which are orga- been reported to provide many health benefits. When RS is used to nized in granules with a semi-crystalline structure of double heli- replace rapidly digestible starch in food, it lowers the glycemic and ces. Amylose is a polysaccharide of essentially (1?4)-linked a-D- insulin responses and reduces the risk for developing type II diabe- glucopyranose, and exists in an amorphous state within the normal tes, obesity, and cardiovascular disease (Behall, Scholfield, & Hall- maize starch granule. Amylopectin molecules consist of (a1?6) frisch, 2006a; Behall, Scholfield, Hallfrisch, & Liljeberg-Elmstaahl, linked branch-chains of (1?4) a-D-glucopyranose, which contrib- 2006b; Robertson, Bickerton, Dennis, Vidal, & Frayn, 2005; Robert- ute to the crystallinity of starch (French, 1984; Jane, Xu, Radosavlj- son, Currie, Morgan, Jewell, & Frayn, 2003; Zhang, Wang, Zhang, & evic, & Seib, 1992; Kasemsuwan & Jane, 1994). The GEMS-0067 Yang, 2007). RS lowers calories of foods (Behall & Howe, 1996) and starch consists of 85% amylose, much greater than normal maize enhances lipid oxidation (Higgins et al., 2004), which reduce body starch (30%) and starches of maize ae single-mutant (50–70%) (Li, fat and impact body composition (Pawlak, Kushner, & Ludwig, Blanco, & Jane, 2007; Li et al., 2008). 2004). Fermentation of RS in the colon promotes a healthy colon Normal maize starch has starch granules with spherical and and reduces the risk of colon cancer (Dronamraju, Coxhead, Kelly, angular shapes, whereas high-amylose maize (ae single-mutant) starch consists of 7% elongated granules (Jiang, Campbell, Blanco, * Corresponding author. Tel.: +1 515 294 9892; fax: +1 515 294 8181. & Jane, 2009; Perera, Lu, Sell, & Jane, 2001). The GEMS-0067 starch E-mail address: [email protected] (J.-l. Jane). consists of up to 32% elongated starch granules (Jiang et al., 2010). 0144-8617/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.carbpol.2009.12.016 534 H. Jiang et al. / Carbohydrate Polymers 80 (2010) 533–538 The elongated starch granules and the outer layer of the spherical using a transmission electron microscope (JEOL 2100, www.jeol.- starch granules are highly resistant to enzymatic hydrolysis and re- com), and images were captured using a high-resolution digital main in the RS residue that consists of partially hydrolyzed amylose camera (U-1000, www.gatan.com). with molecular weights of DP 411–675 (Jiang et al., 2010). It is of great interest to understand how the elongated starch granules are 3. Results and discussion formed during kernel development and the RS formation in the high-amylose maize starch. In this study, we used different micro- 3.1. Morphology of GEMS-0067 starch granules scopic approaches to reveal the internal structures and the forma- tion of elongated starch granules during kernel development. GEMS-0067 starch consisted of mainly spherical and elongated Combining these results with the chemical structures of the starch starch granules (Fig. 1) as reported by Jiang et al. (Jiang et al., crystallites reported previously (Jiang et al., 2010), we propose a 2010). The elongated starch granules displayed shapes including mechanism of the development of elongated granules. rods, filaments, and triangles (Fig. 1). It has been shown that maize ae-mutant starches contain elongated granules (Boyer, Daniels, & 2. Materials and methods Shannon, 1976; Mercier, Charbonniere, Gallant, & Guilbot,
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