gradually decreasing starch branching enzyme expression is … · 2017/11/13 · one sentence...

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Short Title: 1

SBEs and heterogeneous starch granules in rice 2

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Corresponding Author: 4

Cunxu Wei, Qiaoquan Liu 5

Jiangsu Key Laboratory of Crop Genetics and Physiology, Yangzhou University, Yangzhou 6

225009, China 7

E-mail: [email protected] (C.W.), [email protected] (Q.L.) 8

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Long Title: 10

Gradually decreasing starch branching enzyme expression is responsible for 11

the formation of heterogeneous starch granules 12

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Authors: 14

Juan Wang, Pan Hu, Lingshang Lin, Zichun Chen, Qiaoquan Liu*, and Cunxu Wei* 15

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Author Affiliations: 17

Key Laboratory of Crop Genetics and Physiology of Jiangsu Province / Key Laboratory of 18

Plant Functional Genomics of the Ministry of Education, Yangzhou University, Yangzhou 19

225009, China 20

Co-Innovation Center for Modern Production Technology of Grain Crops of Jiangsu Province 21

/ Joint International Research Laboratory of Agriculture & Agri-Product Safety of the 22

Ministry of Education, Yangzhou University, Yangzhou 225009, China 23

*Address correspondence to [email protected] (C.W.), [email protected] (Q.L.) 24

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One sentence summary: 26

The gradually decreasing starch branching enzymes are responsible for the formation of four 27

heterogeneous starch granules distributed regionally from inside to outside in high-amylose 28

rice endosperm. 29

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Plant Physiology Preview. Published on November 13, 2017, as DOI:10.1104/pp.17.01013

Copyright 2017 by the American Society of Plant Biologists

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Footnotes 31

Authors’ contributions: 32

J.W. and C.W. conceived the project; J.W., Q.L., and C.W. planned and designed the research; 33

J.W. performed the experiments with contributions of P.H., S.L., and Z.C.; J.W. and C.W. 34

analyzed the data; J.W., Q.L., and C.W. wrote the article. 35

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Funding information: 37

This work was supported by grants from the National Natural Science Foundation of China 38

(31270221), the Natural Science Foundation of Jiangsu Province (BK20160457), the China 39

Postdoctoral Science Foundation (2016590509), the Qing Lan Project of Jiangsu Province, 40

and the Priority Academic Program Development of Jiangsu Higher Education Institutions. 41

42

Corresponding author email: 43

[email protected] 44

45

The author responsible for distribution of materials integral to the findings presented in this 46

article in accordance with the policy described in the instructions for Authors 47

(www.plantphysiol.org) is: Cunxu Wei ([email protected]).48



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Abstract 49

Rice endosperm is mainly occupied by homogeneous polygonal starch from inside to outside. 50

However, morphologically different (heterogeneous) starches have been identified in some 51

rice mutants. How these heterogeneous starches form remains unknown. A high-amylose rice 52

line (TRS) generated through the antisense inhibition of starch branching synthase (SBE) I 53

and IIb contains four heterogeneous starches: polygonal, aggregate, elongated, and hollow 54

starch; these starches are regionally distributed in the endosperm from inside to outside. Here, 55

we investigated the relationship between SBE dosage and morphological architecture of 56

heterogeneous starches in TRS endosperm from the view of molecular structure of starch. 57

Results indicated that their molecular structures take a regular changes, including gradually 58

increasing true amylose content but decreasing amylopectin content and gradually increasing 59

ratio of amylopectin long chain but decreasing ratio of amylopectin short chain. 60

Granule-bound starch synthase I (GBSSI) amounts in the four heterogeneous starches were 61

not significant different from each other, but SBEI, SBEIIa and SBEIIb showed gradually 62

decreasing trend. Further immunostaining analysis revealed that the gradually decreasing 63

SBEs acting on the formation of the four heterogeneous granules was mainly due to the 64

spatial distribution of the three SBEs in the endosperm. It was suggested that the decreased 65

amylopectin in starch might remove steric hindrance and provide extra space for abundant 66

amylose accumulation when GBSSI amount was not elevated. Furthermore, extra amylose 67

coupled with altered amylopectin structure possibly led to morphological changes in 68

heterogeneous granules. 69

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71

Introduction 72

Starch granules are composed of two glucan polymers: linear amylose and frequently 73

branched amylopectin. Most cereal starches have an amylose content of approximately 15-25% 74

(Jobling, 2004). Granule-bound starch synthase I (GBSSI) is reported to contribute to the 75

polymerization of amylose and tends to be buried in the starch granule in order to function 76

(Denyer et al., 2001). Amylopectin is the main component of starch, accounting for 75-85%, 77

and is composed of clustered short-to-intermediate-length glucan chains. Amylopectin is 78

synthesized by the combined action of several isoforms, including starch synthases (SSs), 79

starch branching synthases (SBEs), and debranching enzymes (DBEs) (Nakamura, 2002; 80

Davis et al., 2003; Tetlow, 2006). In addition, starch phosphorylase 1 (Pho1) has also been 81

reported to play a role in starch synthesis, although its precise role remains elusive (Yu et al., 82

2001; Satoh et al., 2008). 83

Starches from different botanical sources have different granule morphology and shape. 84

Sometimes, even in a single seed, the starch morphology can be diverse. Rice seeds are 85

mainly occupied by compound starch, consisting of several polygonal granules with a sharp 86

edge in each amyloplast, except that the central region of endosperm is more densely packed 87

than that of the peripheral region. By separating the starch granules located in different 88

regions of the rice endosperm, it has been shown that the granules have not only similar 89

appearance but also the same molecular structure (Kubo et al., 2008; Cai et al., 2014). 90

However, when diverse ranges of genes are mutated, distinct effects on granule morphology 91

in a seed are detected. For example, once the soluble starch synthase OsSSIIIa/Flo5, which is 92



5

responsible for the extension of relatively long chains of both amylopectin B2 and B3 to B4 93

(Gao et al., 1998; Jane et al., 1999; Fujita et al., 2006), is eliminated from the genome, a 94

phenotype of loosely packed central portions exhibiting a floury white-core endosperm is 95

detected. The granules located in this region are smaller than those of the parental control and 96

exhibit round morphology with no sharp edges, while the peripheral region in ssIIIa/flo5 97

contains normal compound starch (Ryoo et al., 2007). A similar phenotype was identified in 98

previously reported knockouts of BT1, RSR1, and FLO4, which encode an ADP-glucose 99

transporter, APETALA2/ethylene-responsive element binding protein family transcription 100

factor, and pyruvate orthophosphate dikinase (PPDK), respectively (Kang et al., 2005; Fu and 101

Xue, 2010; Li et al., 2017). Recently, Zhang et al. (2016) reported that a mutation in a gene of 102

unknown function, FLO7, cause an interestingly converse phenotypic variation with a 103

normally developed core but aberrant periphery. Overall, the spatially distributed phenotypes 104

of morphologically different starch granules in these mutants suggest the essential role of 105

these genes in starch development of crops. Furthermore, in wild-type varieties, the starch 106

granules located in the different regions in one seed may have different formation and 107

regulation mechanisms, despite these granules displaying uniform appearance and parallel 108

molecular structures from inside to outside of the endosperm (Cai et al., 2014). However, why 109

this occurs still remains unknown. 110

In high-amylose crops, the spatially distributed phenotype of starch granules in one seed 111

is also recognized. In the maize amylose extender (ae) mutant, in which the amylose content 112

is increased to approximately 60% from 30% (Li et al., 2008), the granules range from blue in 113

color, through to a range of biphasic forms containing both blue- and pink-stained regions, to 114



6

completely pink in color, from the outer to the inner of endosperm when stained with KI/I2 115

(Liu et al., 2013). High-resolution topographical atomic force microscope images of the 116

growth rings and Raman microscopy reveal that differently stained granules have different 117

molecular structures (Wellner et al., 2011; Liu et al., 2013). A transgenic resistant starch rice 118

line (TRS) has been developed by the antisense RNA inhibition of both SBEI and SBEIIb of 119

the indica rice cultivar Teqinq (TQ) in our laboratory. In contrast to TQ, which has 120

approximately 25% amylose content, the amylose content in TRS reaches approximately 60% 121

(Wei et al., 2010; Zhu et al., 2012). In situ observation of whole sections of mature seeds 122

shows that TRS contains four heterogeneous starch granules, including polygonal, aggregate, 123

elongated, and hollow granule, that are regionally distributed in a single seed from inside to 124

outside of the endosperm (Cai et al., 2014). The TRS polygonal granule has polygonal 125

morphology and forms into compound starch as do normal varieties (Wei et al., 2010; Cai et 126

al., 2014). The aggregate consists of some subgranules, similar to compound starch to some 127

extent, but encircled by a thick band, causing these subgranules to pack together during 128

separation. TRS elongated granules are composed of several spherical granules arranged in 129

line. TRS hollow granules resemble aggregate granules in shape, but there are no granules 130

located in the interior. A series of investigations have indicated that these heterogeneous 131

starch granules contain different structures, thermal properties and digestive properties (Cai et 132

al., 2014; Man et al., 2014; Huang et al., 2016). The above previous reports are focused on 133

mature seeds, and mainly investigate the properties of heterogeneous starch granules and their 134

spatial distribution in endosperm. However, from the points of endosperm development and 135

starch synthesis, how these heterogeneous granules are formed, why they exist exclusively in 136



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some regions of endosperm, and the changes of their molecular structures all remain 137

unknown. 138

Herein, we analyzed in detail the molecular structures of four TRS heterogeneous starch 139

granules and the relationship of their molecular structures with starch synthesis-related 140

enzymes. The results indicated that gradually increasing amylose content in four TRS 141

heterogeneous granules was due to decreased amylopectin synthesis and enhanced amylose 142

synthesis but that their GBSSI amounts were not significantly different from those of the 143

control. The granule-associated proteins of four heterogeneous starch granules and 144

immunostaining analysis of developing rice kernels both indicated that the gradually 145

decreasing dosages of SBEI, SBEIIa, and SBEIIb were responsible for the differences in 146

molecular structure and morphological architecture of the granules. The questions of why the 147

amylose content of the four TRS heterogeneous starches from polygonal to hollow granules 148

showed gradually increasing trends when there were similar GBSSI amounts and why three 149

SBEs displayed a regional distribution in a single TRS seed are discussed. 150

151

Results 152

Dynamic deposition of four heterogeneous starch granules in developing endosperm 153

Similar to the deposition mode of normal rice starch, the accumulation pattern of starch 154

in TRS endosperm first began in the core and then spread to the outer region of the endosperm 155

(Fig. 1). At 4 days after flowering (DAF), the whole TRS endosperm was observed to be 156

dominated by compound starch granules (Fig. 1, a‒d). With the continual outspread of 157

endosperm cells, morphologically different granules gradually appeared in these newly 158 https://plantphysiol.orgDownloaded on February 26, 2021. - Published by

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generated endosperms. At 7 DAF, aggregate and elongated granules were detected in regions 159

II and III of the endosperm, respectively (Fig. 1, g and h). After this stage, the peripheral 160

subaleurone layer (region IV) began to be filled with hollow granules (Fig. 1l). By this phase, 161

four heterogeneous starch granules had formed that were regionally distributed in the four 162

regions, and then the differentially located endosperms in each seed were gradually filled with 163

corresponding granules (Fig. 1, m‒p) until maturity. 164

Changes in amylose and amylopectin contents in developing endosperm 165

Amylose and amylopectin synthesis were not significantly different between TQ and 166

TRS at 4 DAF (Fig. 2; Supplemental Fig. S1), a stage only compound starch granules were 167

detected (Fig. 1, a‒d). Afterward, due to the genesis of heterogeneous starch granules (Fig. 1, 168

g, h, and j‒l), their starch accumulations became different. Amylose synthesis showed a nearly 169

identical increasing trend in the two materials, but its accumulation in TRS was more than 170

that of control after 4 DAF, and this gap between them became larger along with endosperm 171

development (Fig. 2; Supplemental Fig. S1). Ultimately, the amylose content in TRS seed was 172

approximately 40% higher than that of control. However, the GBSSI amount and activity was 173

almost the same as that of TQ (Fig. 3, A, B, and D; Supplemental Fig. S2, A and C). On the 174

contrary, amylopectin deposition in TRS was continually lower than that of TQ after 4 DAF, 175

and the deposition modes were significantly different between the two materials. TRS showed 176

a moderate accumulation from 7 DAF to 10 DAF in contrast to the control, which showed a 177

faster rate during this stage. In the following stage, amylopectin synthesis was extremely low 178

in TRS, but a mild amylopectin increase in TQ was detected (Fig. 2). Ultimately, the 179

amylopectin content per seed in TRS decreased by approximately 70%, which was 180 https://plantphysiol.orgDownloaded on February 26, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.


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responsible for the markedly reduced starch content and seed weight. Overall, the increased 181

amylose content in TRS flour or starch was attributed to two factors, amylose increases and 182

amylopectin decreases, and the latter contributed more to it. 183

Pleiotropic effects of SBEI and SBEIIb down-regulation on other starch 184

biosynthesis-related enzymes 185

The results from quantitative real-time PCR (Fig. 3A), immunoblotting assays (Fig. 3B; 186

Supplemental Fig. S2A), and native PAGE/activity staining (Fig. 3C; Supplemental Fig. S2B) 187

of starch synthesis-related enzymes indicated that the antisense inhibition of SBEI and SBEIIb 188

in TRS not only resulted in the largely decreased expression of SBEI and SBEIIb themselves 189

but also caused the significantly reduced expression of SBEIIa. This might be due to the 190

sequence similarity between SBEIIa and SBEIIb, allowing the antisense inhibition designed 191

for SBEIIb to also play a role in SBEIIa repression. Therefore, in TRS, a series of changes 192

including amylose increases and the occurrence of heterogeneous starch granules were a 193

result of three SBE isoform deficiencies instead of deficiencies in only SBEI and SBEIIb. It 194

has been reported that SBE isoforms are responsible for the branching of amylopectin, and 195

their reduction may be expected to reduce the overall rate of amylopectin synthesis (Fig. 2; 196

Supplemental Fig. S1) through a decrease in the number of available non-reducing termini of 197

glucan chains available for SSs (Liu et al., 2012a). Further dynamic expression analysis of the 198

three SBEs indicated that the SBEs were gradually inhibited along with endosperm 199

development in TRS, while in TQ, it showed an increased protein level until 10 DAF but then 200

a decreasing trend (Fig. 4A; Supplemental Fig. S3A). This suggested that there might be 201

regular SBE amounts acting on the formation of TRS heterogeneous granules based on the 202 https://plantphysiol.orgDownloaded on February 26, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.


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spatial and temporal development characteristics of the granules (Fig. 1). 203

SSI activity in TRS was approximately 50% lower than that in TQ (Fig. 3C; 204

Supplemental Fig. S2B), although SSI mRNA levels and protein amounts were not 205

significantly different between TQ and TRS (Fig. 3, A and B; Supplemental Fig. S2A). A 206

reduction in SSI activity was demonstrated previously in sbe2b-related mutants, including the 207

sbe2b single mutant, ae mutant (Nishi et al., 2001) and ss1L/be2b and ss3a/be2b double 208

mutant (Abe et al., 2014; Asai et al., 2014). For other starch biosynthesis-related enzymes, 209

including SSIIa, SSIIIa, isoamylase1 (ISA1), ISA2, pullulanase (PUL) and Pho1, their mRNA 210

levels, soluble protein amounts, and activity were not significantly different between these 211

two materials (Fig. 3, A‒C; Supplemental Fig. S2, A and B). 212

Molecular structure of four heterogeneous starch granules in TRS 213

The total amylose increase and amylopectin decrease in TRS starch or flour was the 214

averaged results derived from the four heterogeneous starch granules. Through isolation and 215

purification of heterogeneous starch granules from TRS kernels at 25 DAF, gel-permeation 216

chromatography (GPC) profiles of isoamylase-debranched starches indicated that these 217

starches had different molecular weight distributions (Fig. 5, A‒F, Table 1). The 218

innermost-situated polygonal granule contained the least amylose proportion (30.3-30.7%). 219

Aggregate and elongated starch granules located in the middle region of TRS endosperm 220

accounted for 41.0-42.7% and 67.0-67.2% of the amylose content, respectively. The 221

outermost-enriched hollow granule had the highest amylose percentage (77.4-78.6%) (Table 222

1). The GPC profiles of isoamylase-debranched amylopectins indicated that amylopectin 223

extra-long chains in the polygonal, aggregate, elongated, and hollow TRS heterogeneous 224 https://plantphysiol.orgDownloaded on February 26, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.


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starch granules accounted for 4.2%, 2.7%, 4.6%, and 2.5%, respectively, which were not more 225

than that of the control, 7.2% (Fig. 5, A‒F; Table 1). The true amylose content in TRS 226

polygonal, aggregate, elongated, and hollow starch was 26.1-26.5%, 38.3-40.0%, 62.4-64.5%, 227

and 74.9-76.7%, respectively (Table 1). The above results indicated that the enriched amylose 228

content in TRS heterogeneous starches was true amylose instead of amylopectin extra-long 229

chains. However, their GBSSI amounts were not significantly different from those of wild 230

type (Fig. 6). 231

The fine structure of amylopectin measured using fluorophore-assisted capillary 232

electrophoresis (FACE) indicated that the chain length of amylopectin in TRS heterogeneous 233

starches also presented a regular distribution (Fig. 5, G and H; Table 2). From polygonal to 234

hollow starch granules, the results showed a moderately gradual reduction in the short-chain 235

proportion of DP 6-12 and DP 13-24 and a significantly gradual increase in the proportion of 236

DP ≥ 37. The proportion of DP 25-36 in the four starch granules was almost maintained at the 237

same state but displayed a slightly elevated trend in contrast to that of the TQ counterpart. The 238

averaged chain length of the four heterogeneous granules was longer than that of the control. 239

Taken together, the structural analysis indicated that in TRS endosperm, from the inside 240

to outside, the four morphologically different starch granules contained gradually enriched 241

amylose and decreased amylopectin contents. At the same time, their amylopectin structures 242

changed greatly, with increasing amounts of long chains but decreasing amounts of short 243

chains. In contrast to TQ, the molecular structures of the four heterogeneous starch granules 244

in TRS greatly changed, except the polygonal ones, which were not significantly different 245

from that of TQ. 246



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Dynamic deposition of amylopectin biosynthetic enzymes in the granules 247

The regular alterations of molecular structures in four TRS heterogeneous starch 248

granules were reminiscent of the effects of different SBEIIb dosages on molecular structures. 249

Butardo et al. (2011) reported that amylose content and amylopectin long chains (DP ≥ 36) 250

were promoted more markedly but amylopectin short chains decreased more significantly in 251

transgenic lines with more pronounced decrease of SBEIIb. Tanaka et al. (2004) further 252

detected that SBEIIb dosage was positively related to amylopectin short chains and negatively 253

related to amylopectin long chains. Therefore, the question about whether the different 254

molecular structures in TRS heterogeneous starch granules originated from the different 255

dosages of the three SBE isoforms was raised. In addition, the fact that SBEs were gradually 256

inhibited along with endosperm development in TRS supported this idea again (Fig. 4A; 257

Supplemental Fig. S3A). 258

A series of biochemical evidence has shown that SBEs are prone to forming a great 259

variety of multisubunit complexes with SSs, DBEs and Pho1 in the soluble fraction of 260

amyloplasts in order to function (Hennen-Bierwagen et al., 2008, 2009; Crofts et al., 2015). 261

This fact, coupled with the complexity of starch development, makes it difficult to quantity 262

SBEs that directly act on starch formation in TRS heterogeneous granules. Therefore, we 263

skipped the possible interactions between starch biosynthetic enzymes in the stromal fraction, 264

because no matter how the interactions changed among those enzyme proteins in the soluble 265

fractions, those proteins were stably buried into the granule during starch development (Fig. 266

4B; Supplemental Fig. S3B). Regarding the dynamic deposition mode of starch during 267

development process in the control, the fast seed-filling stage occurred from 4 DAF to 10 268 https://plantphysiol.orgDownloaded on February 26, 2021. - Published by



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DAF, moderate accumulation occurred from 10 DAF to 15 DAF, and then a relatively low 269

accumulation occurred until maturity along with the dehydration process (Fig. 2). The three 270

SBEs bound with the granule also behaved consistently in TQ: a fast rate occurred from 4 271

DAF to 10 DAF, a mild rate occurred from 10 DAF to 15 DAF, and then a relatively low rate 272

occurred until maturity (Fig. 4B). In TRS, the three SBEs still exhibited an accumulating 273

trend in the granule-bound fraction before 10 DAF, although their abundance continuously 274

decreased in the soluble fraction (Fig. 4A). Following this stage, the SBEs seemed to be 275

maintained at a stable level in the granule due to the markedly repressive effect in the soluble 276

part (Fig. 4; Supplemental Fig. S3). 277

A similar deposition mode was also detected for SSI and SSIIa in these two materials, 278

whereas Pho1 only displayed an accumulating trend in TRS. Regardless of whether these 279

soluble enzyme proteins were fixed completely into the granule, these proteins had a dynamic 280

deposition or maintained a sustainable level in the granules throughout starch development. 281

This finding suggests that granule-bound enzymes are a valuable indicator of enzymes acting 282

on the formation of starch granules. Importantly, the dynamic accumulation of these enzymes 283

in the granule made it possible to quantify the six enzymes acting on starch synthesis in the 284

four heterogeneous starches, as these heterogeneous granules were capable of being well 285

separated and were used for the dosage analysis of starch biosynthetic enzymes. 286

Allocations of granule-bound enzymes among four heterogeneous starch granules 287

How the six amylopectin biosynthetic enzymes were distributed into the four 288

heterogeneous granules was examined (Fig. 6). The abundance of three SBE isoforms in the 289

four heterogeneous starches was obviously less than that of TQ, and they showed a gradually 290 https://plantphysiol.orgDownloaded on February 26, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.


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decreasing trend from polygonal to hollow starch granules. In addition, the distribution of SSI 291

in the four types of granules also showed a similar tendency, which was consistent with their 292

gradually decreasing ratio of amylopectin short chains (Fig. 5, G and H; Table 2). SSIIa 293

maintained almost the same level in the four heterogeneous granules. In contrast to the other 294

three granules, which revealed a thick band of Pho1, only a faint band existed in the 295

innermost polygonal starch (Fig. 6A). 296

Regional distribution of three SBE isoforms in developing endosperm 297

To further demonstrate the different dosages of three SBE isoforms on four TRS 298

heterogeneous starches, an immunofluorescence analysis was conducted on the developing 299

endosperm at 10 DAF, the stage that the four heterogeneous starch granules had formed (Fig. 300

1). The results revealed that SBEI, SBEIIa and SBEIIb were broadly associated with all 301

granules in TQ (Fig. 7, A, C, and E). At the outermost region of endosperm, the residual 302

stroma with bright SBE signals in the amylopalst was discovered (Fig. 7, A4, C4, and E4). 303

This was due to that the amyloplast located in this region developed more slowly and were 304

less densely packed than those of the inner regions, resulting in that they were not completely 305

filled with starch granules. However, in TRS, it seemed that the fluorescence signals of SBEI, 306

SBEIIa and SBEIIb were mainly distributed in the grain center, the region that polygonal 307

granules locate (Fig. 7, B1, D1, and F1), and the outline of granule morphology could be 308

easily drawn by the fluorescence signals, as it could in the control. However, weak and diffuse 309

signals were barely detected in the other three regions when these regions were magnified 310

(Fig. 7, B2‒B4, D2‒D4, and F2‒F4), and these dots became less and less frequent when more 311

and more closer to the peripheral region of the endosperm. Overall, these fluorescence signals 312 https://plantphysiol.orgDownloaded on February 26, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.


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of the three SBEs exhibited a spatial distribution throughout the whole TRS endosperm and a 313

gradual reduction from the inside to the outside of the endosperm, which indicated that the 314

gradually decreasing SBE dosages acting on the formation of heterogeneous starches were 315

mainly due to the regional distribution of SBEI, SBEIIa, and SBEIIb in the rice endosperm. 316

317

Discussion 318

Expanded physical space resulting from reduced amylopectin synthesis may be a key 319

factor for the large enrichment of amylose 320

An amylose increase can be achieved by enhancing the expression levels of GBSSI. For 321

example, elevated level of GBSSI by introduction of Waxya into a japonica waxy mutant leads 322

to amylose increase (approximately 25%) in contrast with that of the japonica Waxyb cultivar 323

(approximately 20%) (Itoh et al., 2003). However, when further overexpressing GBSSI in 324

normal cereal crops that usually contain approximately 25-30% amylose content, no or little 325

amylose promotion is detected (Flipse et al., 1996; Itoh et al, 2003; Sestili et al., 2012), which 326

means that the Waxy-dosage effect is restricted within a range and that GBSSI is not always 327

the key factor to promote amylose content. Flipse et al. (1996) suggested that, except GBSSI, 328

the amylose content of starch potentially correlates with the availability of ADP-glucose and 329

the limited physical space available within the matrix of amylopectin. However, even though 330

overexpressing the BRITTLE1 (Bt1) gene in an up-regulated AGPase background generating 331

a rice line with enhanced ADP-glucose synthesis and import into amyloplasts, only a limited 332

carbon flow into starch was observed (Cakir et al., 2016). Therefore, substrate amount is not 333

the rate-limiting step for increasing amylose. Starch is synthesized as discrete semicrystalline 334 https://plantphysiol.orgDownloaded on February 26, 2021. - Published by



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granules having a layered organization with alternating semicrystalline and amorphous 335

growth rings (Gallant et al., 1997). The semicrystalline ring consists of the lamellar structure 336

of alternating crystalline and amorphous regions. Amylopectin branch-chains form double 337

helices and are packed laterally to form crystalline lamellae. The large portion of amylose 338

resides in amorphous growth rings, and some amylose molecules also accumulate in 339

crystalline and amorphous lamellae (Blazek and Gilbert, 2011). During starch granule 340

formation, the amylopectin is synthesized firstly and forms the architecture of granule, and 341

then GBSSI is bound into granule and synthesizes the amylose molecules. When amylopectin 342

synthesis is reduced, the steric hindrance for amylose accumulation in crystalline and 343

amorphous lamellae is partly vanquished, inferring that the expanded physical space due to 344

the reduced amylopectin content might be a key factor for amylose increase. 345

In TRS, amylose content per grain increased by 40% (Fig. 2; Supplemental Fig. S1) 346

although GBSSI amounts and activity were not significantly different between TQ and TRS 347

(Fig. 3, A, B, and D; Supplemental Fig. S2, A and C). Cakir et al. (2016) reported that when 348

enriched ADP-glucose supply was provided, starch content could be elevated limitedly (about 349

10%) in the condition of that activity of starch synthase kept unchanged. This indicated that 350

starch content could be elevated even though the amounts and activity of starch synthase 351

including GBSSI was not increased, only that a limited amount of starch increase was 352

detected. Therefore, such an abundant amylose increase in TRS is mainly attributed to 353

amylopectin decrease. Amylopectin synthesis per grain in TRS decreased by 70%, resulting in 354

abundant soluble substrate (Supplemental Fig. S4) and enlarged physical space. From 355

polygonal to hollow starch granules, three SBEs showed a gradually decreasing trend, 356



17

indicating that their amylopectin synthesis was gradually decreased. This meant that more and 357

more space was released for amylose synthesis and accumulation in lamellae from TRS 358

polygonal to hollow starch granules, even though GBSSI contents were not increased (Fig. 6). 359

In barley, when three SBEs were simultaneously reduced by more than 70% compared to that 360

of the control, amylopectin synthesis is completely inhibited, and pure amylose is derived 361

(Carciofi et al., 2012). 362

The SSIIIa mutation seems to demonstrate the abovementioned opinion again. The 363

SSIIIa mutation in the japonica background (ssIIIa/Waxyb) causes an increase of GBSSI and 364

inhibits amylopectin synthesis, resulting in a 1.3-fold increase in amylose (Fujita et al., 2007). 365

When this mutation is created in the indica background (ss3a/Waxya), a higher increase in 366

GBSSI and amylose in contrast to that of japonica is detected as expected, but the GBSSI 367

content is not significantly different from the GBSSI content in indica itself (SS3a/Waxya) 368

(Crofts et al., 2012; Zhou et al., 2016). This is possibly due to that the reduced amylopectin in 369

ss3a/Waxya provides more space for amylose synthesis. 370

Gradual reduction of three SBEs is responsible for granule morphology 371

Starch is consisted of approximately 75% ~ 85% amylopectin and 15% ~ 25% amylose 372

(Gallant et al., 1997). It has been proposed that structure and arrangement of amylopectin 373

molecules are crucial for the shape and morphology based on the blocklet model of starch 374

granule architecture. For example, wheat, triticale and barley contain large, disk-shaped 375

A-granules and small, spherical B-granules. Ao and Jane (2007) suggested that more long 376

chains but fewer short chains of amylopectin in A-granules are more parallel aligned in the 377

disk shape, while more short chains but fewer long chains in B-granules are available in the 378 https://plantphysiol.orgDownloaded on February 26, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.


18

cone shape. It seems that amylose has no effect on the starch morphology. For example, both 379

waxy, japonica and indica rice exhibit compound starch granules, although their amylose 380

contents are different from each other. However, this does not mean that amylose content has 381

no effect on the phenotype of starch granules when amylose occupies the major proportion 382

instead of amylopectin. It has been found that the elongated granules in high-amylose maize, 383

ae, originate from two adjacent simple starch granules by amylose interaction, forming 384

anti-parallel double helices between them (Jiang et al., 2010). The high accumulation of 385

amylose in crystalline lamellae disorders the packing of lamellar structure and destroys the 386

granule layered organization (Blazek and Gilbert, 2011). The very high amylose in wheat and 387

barley starches alters starch morphology from disk-shaped to sickle-shaped granules with a 388

significant loss of birefringence (Regina et al., 2006, 2010; Carciofi et al., 2012; Slade et al., 389

2012). 390

In TRS, the ratio of amylose and amylopectin content and fine structure of amylopectin 391

take great changes. Therefore, the morphology of heterogeneous granules must be a result of 392

these combined factors. TRS polygonal granules could be completely maintained in a 393

compound morphology due to the similarity of contents and molecular structures of amylose 394

and amylopectin with those of the control (Fig. 5; Tables 1 and 2), although three SBEs 395

exhibited 28%, 51%, and 51% levels relative to that of TQ (Fig. 6B). These amounts of three 396

SBEs that existed in the TRS polygonal starches were considered transition points: when there 397

was more than these values, the starch morphology could be maintained in a state similar to 398

that of wild type; but when there was less, amylopectin content and molecular structure would 399

substantially change and amylose accordingly accumulated in crystalline lamellae, leading to 400



19

that the morphological heterogeneity would become more discrepant from that of the wild 401

type. For example, in TRS hollow starch, the SBEs were seriously inhibited (Fig. 6), leading 402

to that the amylopectin content decreased from 76.3% to 22.6%, amylopectin branch-chain 403

length increased from 22.8 DP to 37.6 DP, and the ratio of short to long branch-chains of 404

amylopectin decreased from 3.1 to 0.4 compared with TQ polygonal starch. The decreased 405

amylopectin accordingly increased the true amylose content from about 17% to 75% (Tables, 406

1 and 2). The above molecular structure changes of amylopectin and the accumulation of 407

amylose destroyed the granule structure with no birefringence and lamellae (Man et al., 2014), 408

and changed the morphology from compound starch with polygonal subgranules to hollow 409

starch without inner subgranules. Furthermore, we analyzed the relationship between the 410

amount of SBEI, SBEIIa and SBE IIb in starch granule and the content and molecular 411

structure of amylose and amylopectin (Table 3). The amount of SBEs in granules, especially 412

SBEIIa and SBEIIb, was significantly and positively correlated with amylopectin content and 413

its branching degree, extra long chain and short branch-chain, and negatively correlated with 414

amylopectin branch-chain length and amylose content. 415

Taken together, the present study indicated that the gradual reduction of SBEs, from TRS 416

polygonal to hollow granules, accordingly decreased the amylopectin synthesis and changed 417

its molecular structure, leading to the change of lamellar structure and more accumulation of 418

amylose in lamellae. The different changes in content and molecular structure of amylose and 419

amylopectin in starch granules resulted in four heterogeneous granules. 420

Why do regional distributions of three SBEs exist in a single seed in TRS? 421

An interesting question raised by this research was why regional distributions of three 422 https://plantphysiol.orgDownloaded on February 26, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.


20

SBEs existed in a single seed. At first thought, the glutelin Gt1 (GluA-2) promoter utilized in 423

TRS transgenic plants might be responsible for the regional distribution of the three SBEs, as 424

the activity of this promoter is stronger in the outer portion but much weaker in the inner part 425

of the endosperm (Qu et al., 2008). This resulted in the three SBE isoforms being more 426

severely inhibited in the outer portion of the endosperm but less inhibited in the inner region. 427

In addition, the mRNA of GluA-2 gene started to accumulate during the early stages of 428

endosperm development, peaking at approximately 10 DAF (Crofts et al., 2005; Kawakatsu et 429

al., 2008), inferring that the GT1 promoter functions during the early stages of endosperm 430

development but subsequently shows an increasing trend. In the TRS endosperm development 431

process, the inhibition effect of the three SBEs was gradually enhanced (Fig. 4A). It seemed 432

that the inhibition effect in TRS was consistent with the function of the GT1 promoter. 433

However, spatial heterogeneity that existed in the rice ae mutant partly ruled out this 434

possibility (Supplemental Fig. S5). Based on the whole sections of mature ae seeds, we found 435

that three types of starch granules were detected from inside to outside of the endosperm in a 436

single seed, ranging from the innermost compound starch granule consisting of several 437

polygonal granules (Supplemental Fig. S5G), through to the small granules composed of only 438

two or three subgranules (Supplemental Fig. S5, A‒C), to aggregate granules similar to 439

compound granules but encircled by a thick pink band (Supplemental Fig. S5, D‒F). The 440

significant regional distribution of heterogeneous starch granules is also reported in maize ae 441

mutant (Liu et al., 2013). This indicated that different dosage requirements of SBEIIb for the 442

granule formation of different regions in a single rice seed indeed existed and might also exist 443

for SBEI and SBEIIa. 444



21

Granule-bound amylopectin biosynthetic enzymes are an important indicator of enzyme 445

action on amylopectin molecular structure 446

Increasing amounts of evidence have demonstrated that different compositions of 447

amylopectin biosynthetic enzymes exhibit significant effects on the molecular structure and 448

morphological architecture of starch granules. These enzyme proteins are prone to forming 449

varieties of complexes in the soluble amyloplast fraction instead of operating individually. 450

This phenomenon is especially true for the SSs and SBEs, which then purportedly attach to 451

the surface of the starch granule to play a role in amylopectin synthesis (Grimaud et al., 2008; 452

Hennen-Bierwagen et al., 2008; Liu et al., 2009). When the complex fails to become the 453

granule-bound component or the composition of the complex changes, the molecular structure 454

and starch morphology concurrently change. An allelic variant of the sugray-2 (su2) mutation, 455

expressing a catalytically inactive form of SSIIa in maize, enables the trimeric assembly of 456

SSI, SSIIa and SBEIIb in the stroma of amyloplasts as in wild type but causes the inability of 457

the complex to become a granule-bound component. Altered molecular structure and granule 458

morphology are observed in su2 starch granules, providing a clue to the role of granule-bound 459

amylopectin biosynthetic enzymes in the structural organization of starch granules (Liu et al., 460

2012a). Two maize amylose extender mutations lead to the absence of SBEIIb in ae- (ae1.1) 461

and a catalytically inactive form of SBEIIb in ae1.2, respectively. The different mutation 462

patterns cause different granule-bound protein compositions, even though the primary cause 463

of the mutation, the loss of SBEIIb activity, is the same (Liu et al., 2009; 2012b). A novel 464

protein complex formed in the stroma that includes SBEI, SBEIIa, Pho1, SSI, and SSIIa 465

effectively becomes localized to starch granules in ae- (Liu et al., 2009). In ae1.2, the internal 466



22

granule-bound components consist of SSI, SSIIa, SBEI, SBEIIa, and null SBEIIb. Starch of 467

ae1.2 has much lower apparent amylose and fewer intermediate-length glucan chains (degree 468

of polymerization 16–20) than does ae- and has altered granule morphology that is distinctly 469

different from that of both the ae- mutant and wild type (Liu et al., 2012b). Only seven 470

amylopectin biosynthetic enzymes, including SSI, SSIIa, SSIIIa, SBEI, SBEIIa, SBEIIb, and 471

Pho1, are capable of binding to the starch granule in wild type and various mutants, although 472

there are more than seven enzyme proteins responsible for amylopectin formation (Grimaud 473

et al., 2008). 474

The abovementioned literatures show that the granule-bound amylopectin biosynthetic 475

enzymes can be used as an important indicator of enzyme action on the formation of 476

amylopectin molecular structure (Grimaud et al., 2008; Liu et al., 2009, 2012a, 2012b). In the 477

present study, we investigated the allocations of granule-bound amylopectin biosynthetic 478

enzymes among TRS four heterogeneous granules to disclose their amylopectin difference 479

(Fig. 6). From polygonal to aggregate, elongated and hollow granules, the amount of SBEI, 480

SBEIIa and SBE IIb gradually decreased, agreeing with that the branching degree of 481

amylopectin decreased and branch-chain length increased gradually (Nishi et al., 2001; 482

Butardo et al., 2011; Tables, 1 and 2). The different amounts of SBEI, SBEIIa and SBEIIb 483

distributed in the four heterogeneous starch granules caused different binding amounts of SSI. 484

It has been reported that SSI plays a critical role in generating chains of DP 8-12 from chains 485

of DP 6-7 that emerge from the branch points of amylopectin, carried out by SBE (Fujita et al., 486

2006). This finding greatly helped to elucidate the gradually decreasing ratio of DP 6-12 in 487

the four TRS heterogeneous starch granules (Fig. 5, G and H; Table 2). However, for SSIIa, 488



23

no difference was detected, although it has been suggested that SSIIa preferentially elongates 489

DP 6-11 to DP 13-28 (Nakamura et al., 2005). This may be because SSIIa traffics others 490

enzymes into the granule, leading this enzyme can be unbiasedly bound to the granule (Liu et 491

al., 2012a). However, we failed to detect SSIIIa in the granule-bound fraction both in TQ and 492

TRS (data not shown). For Pho1, it has been reported that it produces short-chained MOS and 493

the resulting MOS is able to primer amylose synthesis (Kitamura et al., 1982; Satoh et al., 494

2008). Pho1 exhibited a granule-bound fraction in TRS (Fig. 6), whereas it was absent in the 495

control. We reasonably inferred that the granule-bound Pho1 in TRS might facilitate the MOS 496

synthesis, making it more convenient and efficient for the granule-bound GBSSI to synthesize 497

amylose. However, the Pho1 amounts in aggregate, elongated and hollow starches were not 498

significantly different from each other. This might be still due to the expanded physical space, 499

not the Pho1, responsible for the different amylose accumulation in TRS four heterogeneous 500

starch granules. 501

502

Conclusion 503

This study revealed that TRS heterogeneous starch granules contained gradually 504

enriched amylose and decreased amylopectin. This result was mainly due to the gradually 505

decreasing SBEI, SBEIIa and SBEIIb, which might release more space for amylose synthesis 506

by reducing amylopectin synthesis and/or the branching degree. Along with the altered 507

amounts of three SBEs acting on the formation of four heterogeneous granules, other proteins 508

also effected changes, including SSI and Pho1. In addition, there was not always a linear 509

relationship between SBE dosage and granule morphology. Only when three SBEs decreased 510



24

to a transition level did the granule morphology substantially change, and the more decreases 511

that occurred, the more alterations there were. The reasons causing the spatial distribution of 512

the three SBEs in rice endosperm could be due to two possibilities: (1) the endosperm-specific 513

promoter GT1 used in TRS transgenic plants plays a weak role in the inner region but a strong 514

role in outer region of the rice endosperm; and (2) different dosage requirements of SBEI, 515

SBEIIa and SBEIIb for starch development exist in different regions of the rice endosperm. 516

517

Materials and Methods 518

Plant materials 519

The indica rice cultivar Te-qing (TQ) and its transgenic resistant starch rice line (TRS) 520

were used in this study. TRS were generated by the antisense RNA inhibition of both SBEI 521

and SBEIIb in the background of TQ (Zhu et al., 2012). The ae mutant rice was obtained from 522

japonica rice Zhonghua 11. They were cultivated in a closed transgenic experiment field of 523

Yangzhou University, Yangzhou, China. Kernels were harvested at different days after 524

flowering, and developing endosperms were carefully dissected from kernels and stored at ‒525

70 °C. All the results showed in this manuscript were from two or three biological replicates 526

in the same year, and most experiments were repeated two years in 2015 and 2016. 527

Kernel sections for light microscopy 528

The developing kernels were permeated and embedded in LR White resin after being 529

fixed and dehydration, and sectioned transversely at the midregion of kernel using an ultrathin 530

microtome (EM UC7) following the method of Zhao et al. (2016). The semi-thin sections 531



25

were stained with safranine and I2/KI and subsequently observed using a light microscope. 532

Amylose, amylopectin, and soluble sugar contents in developing kernels 533

The contents of amylose and amylopectin in developing kernels were determined using 534

the Megazyme Amylose/Amylopectin Assay Kit. The analysis was performed according to 535

the manufacturer’s instructions. The soluble sugar was extracted from developing kernels with 536

80% ethanol, and determined using the colorimetric method of anthrone-H2SO4. 537

Starch isolation and the purification of TRS heterogeneous starch granules 538

The isolation of TQ and TRS total starch and the purification of TRS heterogeneous 539

starch granules from developing kernels at 25 DAF were performed as described in detail by 540

Man et al. (2014). 541

Starch components and molecular structure 542

Amylopectin was isolated and purified from starch granules using n-butanol as described 543

by Li et al. (2008). Starch and amylopectin were debranched using isoamylase, and their 544

molecular weight distributions were analyzed using a PL-GPC 220 chromatograph with three 545

columns (PL110-6100, 6300, 6526) and a differential refractive index detector following the 546

methods of Man et al. (2014). The chain length distribution of amylopectin was determined 547

using FACE following the methods of Lin et al. (2016). 548

RNA isolation and real-time RT PCR 549

Endosperm RNA was extracted using an RNAprep pure Plant Kit (Tiangen). One 550

microgram of total RNA was reverse-transcribed. The primers and detailed procedures used in 551



26

the analysis were derived from the methods of Ohdan et al. (2005). 552

Native PAGE/activity staining 553

Endosperm samples from 8 kernels harvested at 10 DAF were homogenized on ice in 554

corresponding extraction buffer consisting of 50 mM HEPES NaOH (pH 7.4), 2 mM MgCl2, 555

and 12.5% (v/v) glycerol. The homogenate was centrifuged to obtain the supernatant for 556

further enzyme activity assays. The enzyme assays and activity staining were performed as 557

described previously (Nishi et al., 2001). The experiments were conducted in two successive 558

years, and two biological replicates were performed in every year. 559

Determination of GBSSI activity 560

The GBSSI activity in developing endosperm was performed following the method of 561

Zhang et al (2010). For the GBSSI activity in isolated starch, starch was prepared essentially 562

according to Hunt et al. (2010), and the GBSSI activity was determined as described by Fujita 563

et al. (2001). The GBSSI activity was evaluated by the amount of liberated ADP from per min 564

per mg fresh endosperm or starch. 565

Preparation of protein extracts 566

The soluble and granule-bound protein extractions from developing endosperms were 567

performed using a modified version of the methods described by Butardo et al. (2011). The 568

soluble fraction was obtained by suspending endosperms from 10 kernels at 4, 7, 10, 15 and 569

25 DAF in 500 μL of buffer (pH 7.4, 50 mM Tris-HCl, 0.25 M sucrose, 2.0 mM EDTA, 2 mM 570

DTT, and 1 mM PMSF). After centrifuging, the supernatant was collected. The resulting 571

pellet was washed with extraction buffer six times to completely remove the residual soluble 572 https://plantphysiol.orgDownloaded on February 26, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.


27

protein and then dispersed in the gelatinized buffer, which consisted of 50 mM Tris-HCl and 573

10% SDS. This gelatinized mixture was heated under constant stirring in a boiling water bath 574

in order to release the granule-bound protein. The two fractions containing the soluble 575

fraction and the granule-bound fraction were precipitated in acetone overnight, and each 576

precipitated protein fraction was resuspended in gelatin buffer. The experiments were 577

conducted in two successive years, and two biological replicates were performed in every 578

year. 579

Western blot 580

Proteins were transferred to polyvinylidene difluoride (PVDF) membranes after 581

SDS-PAGE. The blots proceeded directly to the blocking step and then were exposed to 582

antibodies. Bound antibodies were probed by goat anti-rabbit immunoglobulins conjugated to 583

horseradish peroxidase. Detection was carried out using ECL detection reagents, and imaging 584

was performed by a chemiluminescence analyzer. Antibodies against GBSSI, SBEI, SBEIIb, 585

SSI and Pho1 were described previously (Liu et al., 2014). Anti-SBEIIa, anti-SSIIa and 586

anti-SSIIIa were produced against the synthetic peptides CVTEGVIKDADEPTV, 587

LLSGRDDDTPASRN and CTKDRDGISKKSGGD, respectively. 588

Immunofluorescence analysis 589

Kernels at 10 DAF were fixed in 4% paraformaldehyde (PFA) solution and 0.1 M 590

phosphate buffer saline (PBS, pH 7.4) containing 4% PFA for at least 4 h. After washing and 591

dehydration, the kernels were embedded into paraffin. Slides with samples attached were 592

wiped clean of any residual paraffin. After immersing the slide in wash buffer I (0.1 M PBS, 593



28

pH 7.4, 1% Triton-X100) for 1 h at room temperature, the slide was transferred to the 594

blocking buffer (0.1 M PBS, pH 7.4, 1‰ Tween-20, 1 mM EDTA, 5% BSA) at 37 °C for 1 h. 595

One hundred microliters of blocking buffer and the appropriate diluted concentration of 596

antibodies were added to each slide, after which the slide was covered with parafilm and then 597

incubated overnight at 4 °C. The slide was washed with washing buffer II (0.1 M PBS, pH 7.4, 598

1‰ Triton-X100) three times for 15 min each and was immersed in blocking buffer again as 599

previously described. Afterward, 100 μL of blocking buffer containing fluorescent secondary 600

antibodies was added to each slide, after which the slide was incubated in a humidified and 601

dark atmosphere at 37 °C for 60 min. The slide was washed again with washing buffer II in 602

the dark. Finally, nuclei were counterstained with 4,6-diamidinophenylindole (DAPI), and the 603

signals were observed using a fluorescence microscope. Two biological replicates were 604

conducted. 605

Statistical Analysis 606

For statistical analysis, one-way ANOVA with Tukey’s test, Pearson’s bivariate 607

correlations, and Student’s t test were evaluated using the SPSS 16.0 Statistical Software 608

Program. 609

610

Acknowledgements 611

We are grateful to Prof. Xiuling Cai (Institute of Plant Physiology & Ecology, Chinese 612

Academy of Sciences) and Prof. Xiangbai Dong (Institute of Botany, Chinese Academy of 613

Sciences) for kindly providing the antibodies of starch biosynthesis-related enzymes. This 614



29

work was supported by grants from the National Natural Science Foundation of China 615

(31270221), the Natural Science Foundation of Jiangsu Province (BK20160457), the China 616

Postdoctoral Science Foundation (2016590509), the Qing Lan Project of Jiangsu Province, 617

and the Priority Academic Program Development of Jiangsu Higher Education Institutions. 618

619



30

Tables 620

Table 1 The carbohydrate composition of starch and purified amylopectin from developing TQ and TRS kernels at 25 DAF in 2015 and 2016 621

2016

2015

Peak 1 (%) Peak 2 (%) Peak 3 (%) TAC (%) Peak 1/Peak 2 Peak 3 (%) TAC (%)

TQ Starch 57.3±1.4f 19.0±0.1b 23.7±1.3a 16.5±1.8a 3.01±0.09d 25.5±0.1a 18.2±0.1a

Amylopectin 57.6±1.7F 18.7±0.4B 7.2±0.6D* ‒ 3.07±0.16D 7.3±0.1E* ‒

TRS Starch 24.8±0.5c 23.8±0.7cd 51.4±1.2d 48.5±1.0d 1.04±0.01b 58.9±0.8d 56.6±0.8d

Amylopectin 24.0±0.1C 24.6±1.3D 2.9±0.2AD* ‒ 0.98±0.06B 2.3±0.1B* ‒

TRS-polygonal Starch 44.7±1.0e 24.9±1.7d 30.3±0.7b 26.1±0.8b 1.80±0.16c 30.7±0.2b 26.5±0.2b

Amylopectin 43.9±0.5E 25.8±0.3D 4.2±0.1BC* ‒ 1.70±0.01C 4.2±0.1D* ‒

TRS-aggregate Starch 29.5±1.8d 29.5±0.7e 41.0±2.5c 38.3±2.6c 1.00±0.03b 42.7±0.1c 40.0±0.2c

Amylopectin 31.6±1.3D 27.3±1.2D 2.7±0.1A* ‒ 1.16±0.01B 2.6±0.1C* ‒

TRS-elongated Starch 11.4±0.1b 21.6±1.1bc 67.0±1.0e 62.4±1.7e 0.53±0.03a 67.2±1.2e 64.5±1.3e

Amylopectin 11.6±0.2B 21.4±0.7C 4.6±0.8C* ‒ 0.54±0.01A 2.7±0.1C* ‒

TRS-hollow Starch 7.5±1.1a 15.1±0.3a 77.4±0.8f 74.9±1.1f 0.50±0.08a 78.6±0.9f 76.7±1.0f

Amylopectin 6.7±0.6A 15.9±0.3A 2.5±0.3A* ‒ 0.42±0.03A 1.9±0.1A* ‒

Values are means ± SD from two biological replicates. Values in the same column with different lowercase letters for starch and capital letters for 622

amylopectin are significantly different (P < 0.05) as determined by one-way ANOVA and Tukey’s test. 623

Peak 1, Peak 2, and Peak 3 are the amylopectin short branch-chain, amylopectin long branch-chain, and amylose, respectively. Peak 1/Peak 3 is 624

the area ratio of Peak 1 and Peak 2. Asterisks represent the amount of extra long chain of amylopectin. TAC (true amylose content) = amylose 625

content (Peak 3 of starch) ‒ extra long chains (Peak 3 of amylopectin). 626 https://plantphysiol.orgDownloaded on February 26, 2021. - Published by



31

Table 2 Chain length distribution of amylopectin from developing TQ and TRS kernels at 25 DAF in 2016 627

DP 6-12 (%) DP 13-24 (%) DP 25-36 (%) DP≥37 (%) Average chain length (DP)

TQ 22.0±0.8d 50.4±0.3e 11.3±0.4a 16.4±0.1a 22.8±0.1a

TRS 13.1±0.3bc 41.3±0.5c 14.1±0.1b 31.6±0.3d 31.2±0.2d

TRS-polygonal 15.2±0.1c 45.0±0.1d 14.0±0.1b 25.8±0.1b 28.1±0.1b

TRS-aggregate 13.2±0.2bc 44.4±0.2d 13.5±0.1b 28.8±0.2c 29.8±0.2c

TRS-elongated 12.2±1.3b 39.2±0.6b 14.3±0.5b 34.3±1.3e 32.9±0.7e

TRS-hollow 9.6±0.2a 32.3±0.6a 15.4±0.1c 42.7±0.8f 37.6±0.4f

Values are means ± SD from two biological replicates. Values in the same column with different lowercase letters are significantly different (P < 628

0.05) as determined by one-way ANOVA and Tukey’s test. 629

630



32

Table 3 Correlation coefficients between molecular composition and SBE protein amount in TQ and TRS total and heterogeneous starches 631

AP content AP-SBC AP-LBC AP-SBC/LBC AP-ABCL AP-ELC AC TAC

SBEI 0.741 0.856* ‒0.181 0.959** ‒0.865* 0.965** ‒0.741 ‒0.775

SBEIIa 0.918** 0.956** 0.178 0.955** ‒0.951** 0.883* ‒0.918** ‒0.930**

SBEIIb 0.867* 0.952** ‒0.023 0.997** ‒0.937** 0.973** ‒0.867* ‒0.893*

*, significant at P < 0.05; **, significant at P < 0.01. 632

AP: amylopectin; SBC: short branch-chain; LBC: long branch-chain; ABCL: average branch-chain length; ELC: extra long chain; AC: amylose 633

content; TAC=true amylose content (AC ‒ ELC). 634

635



33

Figure legends 636

Figure 1. Dynamic deposition of four heterogeneous starch granules in TRS developing 637

kernel in 2016. The whole sections with 2 μm thickness are sectioned transversely at the 638

midregion of developing kernel, and stained with safranine and I2/KI. The endosperm after 7 639

DAF is divided into four regions of I, II, III, and IV from the inner to outer. The four squared 640

areas in whole section from the inner to outer are successively magnified, showing that the 641

polygonal, aggregate, elongated, and hollow granules are gradually deposited regionally in the 642

endosperm from the inner to outer. Scale bar = 1 mm for the whole section and 10 μm for the 643

magnified photograph. 644

Figure 2. Changes of amylose, amylopectin, and starch contents in developing kernels in 645

2016. The contents are standardized by one seed. Values are means ± SD from three biological 646

replicates. Asterisks highlight significant differences in amylose, amylopectin, and starch 647

contents between TQ and TRS by Student’s t test (* P < 0.05; ** P < 0.01; *** P < 0.001). 648

Figure 3. Pleiotrophic effects of SBEI and SBEIIb down-regulation on other starch 649

biosynthesis-related enzymes in developing endosperm at 10 DAF in 2016. (A) RT-PCR 650

analysis of starch biosynthesis-related enzyme genes. The actin gene is used as a reference for 651

comparative quantitation. Values are means ± SD from three biological replicates each with 652

technical triplicates. Asterisks highlight significant differences in starch synthesis-related 653

enzymes between TQ and TRS by Student’s t test (*** P < 0.001). (B) Immunoblotting of 654

starch biosynthesis-related enzymes. Anti-HSP82 antibody is used as a loading control. (C) 655

Native PAGE/activity staining of SBEs, SSs, Pho, and DBEs. (D) GBSSI activities of starch 656

granules isolated from TQ and TRS endosperm. Values are means ± SD from three biological 657

replicates. 658

Figure 4. Dynamic expression and deposition of amylopectin synthesis-related enzymes in 659

soluble fraction (A) and granule-associated fraction (B) of developing kernel in 2016. The 660

amount of soluble protein is standardized by HSP82 and granule-bound fraction is 661

standardized by one seed. 662



34

Figure 5. Starch components and amylopectin molecular structure of TQ and TRS developing 663

kernels at 25 DAF in 2016. (A-F) GPC profiles of isoamylase-debranched starch (solid lines) 664

and purified amylopectin (dotted lines). Peak 1 and Peak 2 consist of short and long 665

branch-chains of amylopectin, respectively. Peak 3 is a mixture of amylose and amylopectin 666

extra-long chains. (G) Chain-length distribution of amylopectin by FACE. (H) The difference 667

in amylopectin chain lengths between TQ and TRS starches. 668

Figure 6. Distribution (A) and relative protein amount (B) of granule-bound proteins in 669

starch granules from TQ and TRS developing kernels at 25 DAF in 2016. (A) The protein 670

amount is standardized by milligrams of starch. TRS-p, a, e, and h represents the polygonal, 671

aggregate, elongated, and hollow starch granules from TRS, respectively. (B) The relative 672

protein amount is the proportion of protein amount in TRS to that of the protein amount in TQ. 673

Values are means ± SD from three biological replicates. Values for the same protein indicated 674

by different lowercase letters are significantly different (P < 0.05) as determined by one-way 675

ANOVA and Tukey’s test. 676

Figure 7. Immunostaining analysis of three SBEs in developing kernel at 10 DAF in 2016. 677

The SBEI, SBEIIa, and SBEIIb are broadly associated to all the granules in TQ (A, C, E), 678

while their fluorescence signals display a gradually decreased trend in endosperm from the 679

inner to outer in TRS (B, D, F). Scale bar = 1 mm for (A‒F), and 10 μm for (A1‒F4). 680

681

Supplemental Data 682

The following supplemental materials are available. 683

Supplemental Figure S1. Changes of amylose, amylopectin, and starch contents in 684

developing kernels in 2015. 685

Supplemental Figure S2. Pleiotrophic effects of SBEI and SBEIIb down-regulation on other 686

starch biosynthesis-related enzymes in developing endosperm in 2015. 687



35

Supplemental Figure S3. Dynamic expression and deposition of amylopectin 688

synthesis-related enzymes in soluble fraction and granule-associated fraction of developing 689

kernel in 2015. 690

Supplemental Figure S4. Soluble sugar content in developing kernel of TQ and TRS in 691

2016. 692

Supplemental Figure S5. Regional distribution of three heterogeneous starch granules in 693

mature seed of rice ae mutant from japonica rice Zhonghua 11. 694

695

696

Supplemental Figure S1. Changes of amylose, amylopectin, and starch contents in 697

developing kernels in 2015. The contents are standardized by one seed. Values are means ± 698

SD from two biological replicates. Asterisks highlight significant differences in amylose, 699

amylopectin, and starch contents between TQ and TRS by Student’s t test (* P < 0.05; ** P < 700

0.01; *** P < 0.001). 701

Supplemental Figure S2. Pleiotrophic effects of SBEI and SBEIIb down-regulation on other 702

starch biosynthesis-related enzymes in developing endosperm in 2015. (A) Immunoblotting of 703

starch biosynthesis-related enzymes from endosperm at 10 DAF. Anti-HSP82 antibody is used 704

as a loading control. (B) Native PAGE/activity staining of SBEs, SSs, Pho, and DBEs from 705

endosperm at 10 DAF. (C) GBSSI activities of TQ and TRS developing endosperm from 5 to 706

15 DAF. Values are means ± SD from three biological replicates. 707

Supplemental Figure S3. Dynamic expression and deposition of amylopectin 708

synthesis-related enzymes in soluble fraction (A) and granule-associated fraction (B) of 709

developing kernel in 2015. The amount of soluble protein is standardized by HSP82 and 710

granule-bound fraction is standardized by one seed. 711

Supplemental Figure S4. Soluble sugar content in developing kernel of TQ and TRS in 712

2016. 713 https://plantphysiol.orgDownloaded on February 26, 2021. - Published by



36

Supplemental Figure S5. Regional distribution of three heterogeneous starch granules in 714

mature seed of rice ae mutant from japonica rice Zhonghua 11. Region I, II, and III is 715

occupied by compound starch granules (G), small granules (A, B, C), and aggregate granules 716

(D, E, F), respectively. Scale bar = 1 mm for whole section, and 10 μm for (A‒G). 717

718



37

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Parsed CitationsAbe N, Asai H, Yago H, Oitome NF, Itoh R, Crofts N, Nakamura Y, Fujita N (2014) Relationships between starch synthase I and branchingenzyme isozymes determined using double mutant rice lines. BMC Plant Biol 14: 80

Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Ao Z, Jane JL (2007) Characterization and modeling of the A- and B-granule starches of wheat, triticale, and barley. Carbohyd Polym 67:46-55


Asai H, Abe N, Matsushima R, Crofts N, Oitome NF, Nakamura Y, Fujita N (2014) Deficiencies in both starch synthase IIIa and branchingenzyme IIb lead to a significant increase in amylose in SSIIa-inactive japonica rice seeds. J Exp Bot 65: 5497-5507


Blazek J, Gilbert EP (2011) Application of small-angle X-ray and neutron scattering techniques to the characterisation of starchstructre: A review. Carbohyd Polym 85: 281-293


Butardo VM, Fitzgerald MA, Bird AR, Gidley MJ, Flanagan BM, Larroque O, Resurreccion AP, Laidlaw HKC, Jobling SA, Morell MK,Rahman S (2011) Impact of down-regulation of starch branching enzyme IIb in rice by artificial microRNA- and hairpin RNA-mediatedRNA silencing. J Exp Bot 62: 4927-4941


Cai C, Huang J, Zhao L, Liu Q, Zhang C, Wei C (2014) Heterogeneous structure and spatial distribution in endosperm of high-amyloserice starch granules with different morphologies. J Agric Food Chem 62: 10143-10152


Cakir B, Shiraishi S, Tuncel A, Matsusaka H, Satoh R, Singh S, Crofts N, Hosaka Y, Fujita N, Hwang SK, Satoh H, Okita TW (2016)Analysis of the rice ADP-glucose transporter (OsBT1) indicates the presence of regulatory processes in the amyloplast stroma thatcontrol ADP-glucose flux into starch. Plant Physiol 170: 1271-1283


Carciofi M, Blennow A, Jensen SL, Shaik SS, Henriksen A, Buléon A, Holm PB, Hebelstrup KH (2012) Concerted suppression of allstarch branching enzyme genes in barley produces amylose-only starch granules. BMC Plant Biol 12: 223


Crofts AJ, Washida H, Okita TW, Satoh M, Ogawa M, Kumamaru T, Satoh H (2005) The role of mRNA and protein sorting in seed storageprotein synthesis, transport, and deposition. Biochem Cell Biol 83: 728-737


Crofts N, Abe K, Aihara S, Itoh R, Nakamura Y, Itoh K., Fujita N (2012) Lack of starch synthase IIIa and high expression of granule-boundstarch synthase I synergistically increase the apparent amylose content in rice endosperm. Plant Sci 193-194: 62-69


Crofts N, Abe N, Oitome NF, Matsushima R, Hayashi M, Tetlow IJ, Emes MJ, Nakamura Y, Fujita N (2015) Amylopectin biosyntheticenzymes from developing rice seed form enzymatically active protein complexes. J Exp Bot 66: 4469-4482


Davis JP, Supatcharee N, Khandelwal RL, Chibbar RN (2003) Synthesis of novel starches in planta: opportunities and challenges.Starch 55: 107-120

Pubmed: Author and TitleCrossRef: Author and Title


http://www.ncbi.nlm.nih.gov/pubmed?term=Abe N%2C Asai H%2C Yago H%2C Oitome NF%2C Itoh R%2C Crofts N%2C Nakamura Y%2C Fujita N %282014%29 Relationships between starch synthase I and branching enzyme isozymes determined using double mutant rice lines%2E BMC Plant Biol 14%3A 80&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Abe N, Asai H, Yago H, Oitome NF, Itoh R, Crofts N, Nakamura Y, Fujita N (2014) Relationships between starch synthase I and branching enzyme isozymes determined using double mutant rice lines. BMC Plant Biol 14: 80

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http://search.crossref.org/?page=1&rows=2&q=Asai H, Abe N, Matsushima R, Crofts N, Oitome NF, Nakamura Y, Fujita N (2014) Deficiencies in both starch synthase IIIa and branching enzyme IIb lead to a significant increase in amylose in SSIIa-inactive japonica rice seeds. J Exp Bot 65: 5497-5507

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Asai&hl=en&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=Butardo VM%2C Fitzgerald MA%2C Bird AR%2C Gidley MJ%2C Flanagan BM%2C Larroque O%2C Resurreccion AP%2C Laidlaw HKC%2C Jobling SA%2C Morell MK%2C Rahman S %282011%29 Impact of down%2Dregulation of starch branching enzyme IIb in rice by artificial microRNA%2D and hairpin RNA%2Dmediated RNA silencing%2E J Exp Bot 62%3A 4927%2D4941&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Butardo VM, Fitzgerald MA, Bird AR, Gidley MJ, Flanagan BM, Larroque O, Resurreccion AP, Laidlaw HKC, Jobling SA, Morell MK, Rahman S (2011) Impact of down-regulation of starch branching enzyme IIb in rice by artificial microRNA- and hairpin RNA-mediated RNA silencing. J Exp Bot 62: 4927-4941

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http://www.ncbi.nlm.nih.gov/pubmed?term=Cai C%2C Huang J%2C Zhao L%2C Liu Q%2C Zhang C%2C Wei C %282014%29 Heterogeneous structure and spatial distribution in endosperm of high%2Damylose rice starch granules with different morphologies%2E J Agric Food Chem 62%3A 10143%2D10152&dopt=abstract

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http://scholar.google.com/scholar?as_q=Heterogeneous structure and spatial distribution in endosperm of high-amylose rice starch granules with different morphologies&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Cai&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Cakir B%2C Shiraishi S%2C Tuncel A%2C Matsusaka H%2C Satoh R%2C Singh S%2C Crofts N%2C Hosaka Y%2C Fujita N%2C Hwang SK%2C Satoh H%2C Okita TW %282016%29 Analysis of the rice ADP%2Dglucose transporter %28OsBT1%29 indicates the presence of regulatory processes in the amyloplast stroma that control ADP%2Dglucose flux into starch%2E Plant Physiol 170%3A 1271%2D1283&dopt=abstract

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http://scholar.google.com/scholar?as_q=Analysis of the rice ADP-glucose transporter (OsBT1) indicates the presence of regulatory processes in the amyloplast stroma that control ADP-glucose flux into starch&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Analysis of the rice ADP-glucose transporter (OsBT1) indicates the presence of regulatory processes in the amyloplast stroma that control ADP-glucose flux into starch&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Cakir&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Carciofi M%2C Blennow A%2C Jensen SL%2C Shaik SS%2C Henriksen A%2C Bul�on A%2C Holm PB%2C Hebelstrup KH %282012%29 Concerted suppression of all starch branching enzyme genes in barley produces amylose%2Donly starch granules%2E BMC Plant Biol 12%3A 223&dopt=abstract

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http://scholar.google.com/scholar?as_q=Concerted suppression of all starch branching enzyme genes in barley produces amylose-only starch granules.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Carciofi&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Crofts AJ%2C Washida H%2C Okita TW%2C Satoh M%2C Ogawa M%2C Kumamaru T%2C Satoh H %282005%29 The role of mRNA and protein sorting in seed storage protein synthesis%2C transport%2C and deposition%2E Biochem Cell Biol 83%3A 728%2D737&dopt=abstract

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http://scholar.google.com/scholar?as_q=The role of mRNA and protein sorting in seed storage protein synthesis, transport, and deposition&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Crofts&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Crofts N%2C Abe K%2C Aihara S%2C Itoh R%2C Nakamura Y%2C Itoh K%2E%2C Fujita N %282012%29 Lack of starch synthase IIIa and high expression of granule%2Dbound starch synthase I synergistically increase the apparent amylose content in rice endosperm%2E Plant Sci 193%2D194%3A 62%2D69&dopt=abstract

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http://scholar.google.com/scholar?as_q=Lack of starch synthase IIIa and high expression of granule-bound starch synthase I synergistically increase the apparent amylose content in rice endosperm&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Crofts&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Crofts N%2C Abe N%2C Oitome NF%2C Matsushima R%2C Hayashi M%2C Tetlow IJ%2C Emes MJ%2C Nakamura Y%2C Fujita N %282015%29 Amylopectin biosynthetic enzymes from developing rice seed form enzymatically active protein complexes%2E J Exp Bot 66%3A 4469%2D4482&dopt=abstract

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http://scholar.google.com/scholar?as_q=Amylopectin biosynthetic enzymes from developing rice seed form enzymatically active protein complexes&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Crofts&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

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Denyer K, Johnson P, Zeeman S, Smith AM (2001) The control of amylose synthesis. J Plant Physiol 158: 479-487Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Flipse E, Keetels CJAM, Jacobsen E, Visser RGF (1996) The dosage effect of the wildtype GBSS allele is linear for GBSS activity butnot for amylose content: absence of amylose has a distinct influence on the physico-chemical properties of starch. Theor Appl Genet92: 121-127


Fu FF, Xue HW (2010) Coexpression analysis identifies rice starch regulator1, a rice AP2/EREBP family transcription factor, as a novelrice starch biosynthesis regulator. Plant Physiol 154: 927-938


Fujita N, Hasegawa H, Taira T (2001) The isolation and characterization of a waxy mutant of diploid wheat (Triticum monococcum L.).Plant Sci 160: 595-602


Fujita N, Yoshida M, Asakura N, Ohdan T, Miyao A, Hirochika H, Nakamura Y (2006) Function and characterization of starch synthase Iusing mutants in rice. Plant Physiol 140: 1070-1084


Fujita N, Yoshida M, Kondo T, Saito K, Utsumi Y, Tokunaga T, Nishi A, Satoh H, Park JH, Jane JL, 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 riceendosperm. Plant Physiol 144: 2009-2023


Gallant DJ, Bouchet B, Baldwin PM (1997) Microscopy of starch: evidence of a new level of granule organization. Carbohyd Polym 32:177-191


Gao M, Wanat J, Stinard PS, James MG, Myers AM (1998) Characterization of dull1, a maize gene coding for a novel starch synthase.Plant Cell 10: 399-412


Grimaud F, Rogniaux H, James MG, Myers AM, Planchot V (2008) Proteome and phosphoproteome analysis of starch granule-associated proteins from normal maize and mutants affected in starch biosynthesis. J Exp Bot 59: 3395-3406


Hennen-Bierwagen TA, Lin Q, Grimaud F, Planchot V, Keeling PL, James MG, Myers AM (2009) Proteins from multiple metabolicpathways associate with starch biosynthetic enzymes in high molecular weight complexes: a model for regulation of carbon allocationin maize amyloplasts. Plant Physiol 149: 1541-1559


Hennen-Bierwagen TA, Liu F, Marsh RS, Kim S, Gan Q, Tetlow IJ, Emes MJ, James MG, Myers AM (2008) Starch biosynthetic enzymesfrom developing maize endosperm associate in multisubunit complexes. Plant Physiol 146: 1892-1908


Huang J, Lin L , Wang J, Wang Z, Liu Q, Wei C (2016) In vitro digestion properties of heterogeneous starch granules from high-amyloserice. Food Hydrocolloid 54: 10-22



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http://scholar.google.com/scholar?as_q=Synthesis of novel starches in planta: opportunities and challenges&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=Denyer K%2C Johnson P%2C Zeeman S%2C Smith AM %282001%29 The control of amylose synthesis%2E J Plant Physiol 158%3A 479%2D487&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Denyer K, Johnson P, Zeeman S, Smith AM (2001) The control of amylose synthesis. J Plant Physiol 158: 479-487

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Denyer&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The control of amylose synthesis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The control of amylose synthesis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Denyer&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Flipse E%2C Keetels CJAM%2C Jacobsen E%2C Visser RGF %281996%29 The dosage effect of the wildtype GBSS allele is linear for GBSS activity but not for amylose content%3A absence of amylose has a distinct influence on the physico%2Dchemical properties of starch%2E Theor Appl Genet 92%3A 121%2D127&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Flipse E, Keetels CJAM, Jacobsen E, Visser RGF (1996) The dosage effect of the wildtype GBSS allele is linear for GBSS activity but not for amylose content: absence of amylose has a distinct influence on the physico-chemical properties of starch. Theor Appl Genet 92: 121-127

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Flipse&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The dosage effect of the wildtype GBSS allele is linear for GBSS activity but not for amylose content: absence of amylose has a distinct influence on the physico-chemical properties of starch&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The dosage effect of the wildtype GBSS allele is linear for GBSS activity but not for amylose content: absence of amylose has a distinct influence on the physico-chemical properties of starch&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Flipse&as_ylo=1996&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Fu FF%2C Xue HW %282010%29 Coexpression analysis identifies rice starch regulator1%2C a rice AP2%2FEREBP family transcription factor%2C as a novel rice starch biosynthesis regulator%2E Plant Physiol 154%3A 927%2D938&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Fu FF, Xue HW (2010) Coexpression analysis identifies rice starch regulator1, a rice AP2/EREBP family transcription factor, as a novel rice starch biosynthesis regulator. Plant Physiol 154: 927-938

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Fu&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Fu&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Fujita N%2C Hasegawa H%2C Taira T %282001%29 The isolation and characterization of a waxy mutant of diploid wheat %28Triticum monococcum L%2E%29%2E Plant Sci 160%3A 595%2D602&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Fujita N, Hasegawa H, Taira T (2001) The isolation and characterization of a waxy mutant of diploid wheat (Triticum monococcum L.). Plant Sci 160: 595-602

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Fujita&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The isolation and characterization of a waxy mutant of diploid wheat (Triticum monococcum L&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The isolation and characterization of a waxy mutant of diploid wheat (Triticum monococcum L&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Fujita&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Fujita N%2C Yoshida M%2C Asakura N%2C Ohdan T%2C Miyao A%2C Hirochika H%2C Nakamura Y %282006%29 Function and characterization of starch synthase I using mutants in rice%2E Plant Physiol 140%3A 1070%2D1084&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=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 Physiol 140: 1070-1084


http://scholar.google.com/scholar?as_q=Function and characterization of starch synthase I using mutants in rice&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Function and characterization of starch synthase I using mutants in rice&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Fujita&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Fujita N%2C Yoshida M%2C Kondo T%2C Saito K%2C Utsumi Y%2C Tokunaga T%2C Nishi A%2C Satoh H%2C Park JH%2C Jane JL%2C Miyao A%2C Hirochika H%2C Nakamura Y %282007%29 Characterization of SSIIIa%2Ddeficient mutants of rice%3A the function of SSIIIa and pleiotropic effects by SSIIIa deficiency in the rice endosperm%2E Plant Physiol 144%3A 2009%2D2023&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Fujita N, Yoshida M, Kondo T, Saito K, Utsumi Y, Tokunaga T, Nishi A, Satoh H, Park JH, Jane JL, 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 Physiol 144: 2009-2023


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http://scholar.google.com/scholar?as_q=Characterization of SSIIIa-deficient mutants of rice: the function of SSIIIa and pleiotropic effects by SSIIIa deficiency in the rice endosperm&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Fujita&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

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http://search.crossref.org/?page=1&rows=2&q=Gallant DJ, Bouchet B, Baldwin PM (1997) Microscopy of starch: evidence of a new level of granule organization. Carbohyd Polym 32: 177-191

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Gallant&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Microscopy of starch: evidence of a new level of granule organization&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Microscopy of starch: evidence of a new level of granule organization&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Gallant&as_ylo=1997&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Gao M%2C Wanat J%2C Stinard PS%2C James MG%2C Myers AM %281998%29 Characterization of dull1%2C a maize gene coding for a novel starch synthase%2E Plant Cell 10%3A 399%2D412&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Gao M, Wanat J, Stinard PS, James MG, Myers AM (1998) Characterization of dull1, a maize gene coding for a novel starch synthase. Plant Cell 10: 399-412

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Gao&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Gao&as_ylo=1998&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Grimaud F%2C Rogniaux H%2C James MG%2C Myers AM%2C Planchot V %282008%29 Proteome and phosphoproteome analysis of starch granule%2Dassociated proteins from normal maize and mutants affected in starch biosynthesis%2E J Exp Bot 59%3A 3395%2D3406&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Grimaud F, Rogniaux H, James MG, Myers AM, Planchot V (2008) Proteome and phosphoproteome analysis of starch granule-associated proteins from normal maize and mutants affected in starch biosynthesis. J Exp Bot 59: 3395-3406

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Grimaud&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Proteome and phosphoproteome analysis of starch granule-associated proteins from normal maize and mutants affected in starch biosynthesis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Proteome and phosphoproteome analysis of starch granule-associated proteins from normal maize and mutants affected in starch biosynthesis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Grimaud&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=Proteins from multiple metabolic pathways associate with starch biosynthetic enzymes in high molecular weight complexes: a model for regulation of carbon allocation in maize amyloplasts&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Hennen-Bierwagen&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=Starch biosynthetic enzymes from developing maize endosperm associate in multisubunit complexes&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Hennen-Bierwagen&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Huang J%2C Lin L %2C Wang J%2C Wang Z%2C Liu Q%2C Wei C %282016%29 In vitro digestion properties of heterogeneous starch granules from high%2Damylose rice%2E Food Hydrocolloid 54%3A 10%2D22&dopt=abstract

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Hunt HV, Denyer K, Packman LC, Jones MK, Howe CJ (2010) Molecular basis of the waxy endosperm starch phenotype in broomcornmillet (Panicum miliaceum L.). Mol Biol Evol 27: 1478-1494


Itoh K, Ozaki H, Okada K, Hori H, Takeda Y, Mitsui T (2003) Introduction of Wx transgene into rice wx mutants leads to both high- andlow-amylose rice. Plant Cell Physiol 44: 473-480


Jane JL, Chen YY, Lee LF, McPherson AE, Wong KS, Radosavljevic M, Kasemsuwan T (1999) Effects of amylopectin branch chainlength and amylose content on the gelatinization and pasting properties of starch. Cereal Chem 76: 629-637


Jiang H, Horner HT, Pepper TM, Blanco M, Campbell M, Jane JL (2010) Formation of elongated starch granules in high-amylose maize.Carbohyd Polym 80: 533-538


Jobling S (2004) Improving starch for food and industrial applications. Curr Opin Plant Biol 7: 210-218Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Kang HG, Park S, Matsuoka M, An G (2005) White-core endosperm floury endosperm-4 in rice is generated by knockout mutations inthe C4-type pyruvate orthophosphate dikinase gene (OsPPDKB). Plant J 42: 901-911


Kawakatsu T, Yamamoto MP, Hirose S, Yano M, Takaiwa F (2008) Characterization of a new rice glutelin gene GluD-1 expressed in thestarchy endosperm. J Exp Bot 59: 4233-4245


Kitamura S, Yunokawa H, Mitsuie S, and Kuge T (1982) Study on polysaccharides by the fluorescence method. II. Micro-Brownianmotion and conformational change of amylase in aqueous solution. Polym J 14: 93–99


Kubo A, Yuguchi Y, Takemasa M, Suzuki S, Satoh H, Kitamura S (2008) The use of micro-beam X-ray diffraction for the characterizationof starch crystal structure in rice mutant kernels of waxy, amylose extender, and sugary1. J Cereal Sci 48: 92-97


Li L, Jiang H, Campbell M, Blanco M, Jane JL (2008) Characterization of maize amylose-extender (ae) mutant starches. Part I:Relationship between resistant starch contents and molecular structures. Carbohyd Polym 74: 396-404


Li S, Wei X, Ren Y, Qiu J, Jiao G, Guo X, Tang S, Wan J, Hu P (2017) OsBT1 encodes an ADP-glucose transporter involved in starchsynthesis and compound granule formation in rice endosperm. Sci Rep-UK 7: 40124


Lin L, Cai C, Gibert RG, Li E, Wang J, Wei C (2016) Relationships between amylopectin molecular structures and functional propertiesof different-sized fractions of normal and high-amylose maize starches. Food Hydrocolloid 52: 359-368


Liu D, Parker Ml, Wellner N, Kirby AR, Cross K, Morris VJ, Cheng F (2013) Structural variability between starch granules in wild typeand in ae high-amylose mutant maize kernels. Carbohyd Polym 97: 458-468

Pubmed: Author and TitleCrossRef: Author and Title


http://www.ncbi.nlm.nih.gov/pubmed?term=Hunt HV%2C Denyer K%2C Packman LC%2C Jones MK%2C Howe CJ %282010%29 Molecular basis of the waxy endosperm starch phenotype in broomcorn millet %28Panicum miliaceum L%2E%29%2E Mol Biol Evol 27%3A 1478%2D1494&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Hunt HV, Denyer K, Packman LC, Jones MK, Howe CJ (2010) Molecular basis of the waxy endosperm starch phenotype in broomcorn millet (Panicum miliaceum L.). Mol Biol Evol 27: 1478-1494

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http://search.crossref.org/?page=1&rows=2&q=Itoh K, Ozaki H, Okada K, Hori H, Takeda Y, Mitsui T (2003) Introduction of Wx transgene into rice wx mutants leads to both high- and low-amylose rice. Plant Cell Physiol 44: 473-480

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Itoh&hl=en&c2coff=1

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http://search.crossref.org/?page=1&rows=2&q=Jane JL, Chen YY, Lee LF, McPherson AE, Wong KS, Radosavljevic M, Kasemsuwan T (1999) Effects of amylopectin branch chain length and amylose content on the gelatinization and pasting properties of starch. Cereal Chem 76: 629-637

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Jane&hl=en&c2coff=1

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http://search.crossref.org/?page=1&rows=2&q=Jiang H, Horner HT, Pepper TM, Blanco M, Campbell M, Jane JL (2010) Formation of elongated starch granules in high-amylose maize. Carbohyd Polym 80: 533-538

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http://www.ncbi.nlm.nih.gov/pubmed?term=Jobling S %282004%29 Improving starch for food and industrial applications%2E Curr Opin Plant Biol 7%3A 210%2D218&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Jobling S (2004) Improving starch for food and industrial applications. Curr Opin Plant Biol 7: 210-218

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http://www.ncbi.nlm.nih.gov/pubmed?term=Kang HG%2C Park S%2C Matsuoka M%2C An G %282005%29 White%2Dcore endosperm floury endosperm%2D4 in rice is generated by knockout mutations in the C4%2Dtype pyruvate orthophosphate dikinase gene %28OsPPDKB%29%2E Plant J 42%3A 901%2D911&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kang HG, Park S, Matsuoka M, An G (2005) White-core endosperm floury endosperm-4 in rice is generated by knockout mutations in the C4-type pyruvate orthophosphate dikinase gene (OsPPDKB). Plant J 42: 901-911

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kang&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=White-core endosperm floury endosperm-4 in rice is generated by knockout mutations in the C4-type pyruvate orthophosphate dikinase gene (OsPPDKB)&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=White-core endosperm floury endosperm-4 in rice is generated by knockout mutations in the C4-type pyruvate orthophosphate dikinase gene (OsPPDKB)&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kang&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kawakatsu T%2C Yamamoto MP%2C Hirose S%2C Yano M%2C Takaiwa F %282008%29 Characterization of a new rice glutelin gene GluD%2D1 expressed in the starchy endosperm%2E J Exp Bot 59%3A 4233%2D4245&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kawakatsu T, Yamamoto MP, Hirose S, Yano M, Takaiwa F (2008) Characterization of a new rice glutelin gene GluD-1 expressed in the starchy endosperm. J Exp Bot 59: 4233-4245

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http://scholar.google.com/scholar?as_q=Characterization of a new rice glutelin gene GluD-1 expressed in the starchy endosperm&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kawakatsu&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

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http://search.crossref.org/?page=1&rows=2&q=Kitamura S, Yunokawa H, Mitsuie S, and Kuge T (1982) Study on polysaccharides by the ?uorescence method. II. Micro-Brownian motion and conformational change of amylase in aqueous solution. Polym J 14: 93?99

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http://www.ncbi.nlm.nih.gov/pubmed?term=Kubo A%2C Yuguchi Y%2C Takemasa M%2C Suzuki S%2C Satoh H%2C Kitamura S %282008%29 The use of micro%2Dbeam X%2Dray diffraction for the characterization of starch crystal structure in rice mutant kernels of waxy%2C amylose extender%2C and sugary1%2E J Cereal Sci 48%3A 92%2D97&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kubo A, Yuguchi Y, Takemasa M, Suzuki S, Satoh H, Kitamura S (2008) The use of micro-beam X-ray diffraction for the characterization of starch crystal structure in rice mutant kernels of waxy, amylose extender, and sugary1. J Cereal Sci 48: 92-97

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http://search.crossref.org/?page=1&rows=2&q=Li L, Jiang H, Campbell M, Blanco M, Jane JL (2008) Characterization of maize amylose-extender (ae) mutant starches. Part I: Relationship between resistant starch contents and molecular structures. Carbohyd Polym 74: 396-404

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http://scholar.google.com/scholar?as_q=Characterization of maize amylose-extender (ae) mutant starches&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Li&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=OsBT1 encodes an ADP-glucose transporter involved in starch synthesis and compound granule formation in rice endosperm.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Li&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Lin L%2C Cai C%2C Gibert RG%2C Li E%2C Wang J%2C Wei C %282016%29 Relationships between amylopectin molecular structures and functional properties of different%2Dsized fractions of normal and high%2Damylose maize starches%2E Food Hydrocolloid 52%3A 359%2D368&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Lin L, Cai C, Gibert RG, Li E, Wang J, Wei C (2016) Relationships between amylopectin molecular structures and functional properties of different-sized fractions of normal and high-amylose maize starches. Food Hydrocolloid 52: 359-368

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Lin&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Relationships between amylopectin molecular structures and functional properties of different-sized fractions of normal and high-amylose maize starches&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Relationships between amylopectin molecular structures and functional properties of different-sized fractions of normal and high-amylose maize starches&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lin&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Liu D%2C Parker Ml%2C Wellner N%2C Kirby AR%2C Cross K%2C Morris VJ%2C Cheng F %282013%29 Structural variability between starch granules in wild type and in ae high%2Damylose mutant maize kernels%2E Carbohyd Polym 97%3A 458%2D468&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Liu D, Parker Ml, Wellner N, Kirby AR, Cross K, Morris VJ, Cheng F (2013) Structural variability between starch granules in wild type and in ae high-amylose mutant maize kernels. Carbohyd Polym 97: 458-468


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http://scholar.google.com/scholar?as_q=Structural variability between starch granules in wild type and in ae high-amylose mutant maize kernels&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Liu&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Liu D%2C Wang W%2C Cai X %282014%29 Modulation of amylose content by structure%2Dbased modification of OsGBSS1 activity in rice %28Oryza sativa L%2E%29%2E Plant Biotechnol J 12%3A 1297%2D1307&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Liu F%2C Ahmed Z%2C Lee EA%2C Donner E%2C Liu Q%2C Ahmed R%2C Morell MK%2C Emes MJ%2C Tetlow IJ %282012a%29 Allelic variants of the amylose extender mutation of maize demonstrate phenotypic variation in starch structure resulting from modified protein%2Dprotein interactions%2E J Exp Bot 63%3A 1167%2D1183&dopt=abstract

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http://scholar.google.com/scholar?as_q=Allelic variants of the amylose extender mutation of maize demonstrate phenotypic variation in starch structure resulting from modified protein-protein interactions&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Liu&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Liu F%2C Makhmoudova A%2C Lee EA%2C Wait R%2C Emes MJ%2C Tetlow IJ %282009%29 The amylose extender mutant of maize conditions novel protein%2Dprotein interactions between starch biosynthetic enzymes in amyloplasts%2E J Exp Bot 60%3A 4423%2D4440&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Liu F%2C Romanova N%2C Lee EA%2C Ahmed R%2C Evans M%2C Gilbert EP%2C Morell MK%2C Emes MJ%2C Tetlow IJ %282012b%29 Glucan affinity of starch synthase IIa determines binding of starch synthase I and starch%2Dbranching enzyme IIb to starch granules%2E Biochem J 448%3A 373%2D387&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Regina A%2C Bird A%2C Topping D%2C Bowden S%2C Freeman J%2C Barsby T%2C Kosar%2DHashemi B%2C Li Z%2C Rahman S%2C Morell M %282006%29 High%2Damylose wheat generated by RNA interference improves indices of large%2Dbowel health in rats%2E P Natl Acad Sci USA 103%3A 3546%2D3551&dopt=abstract

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Satoh H, Shibahara K, Tokunaga T, Nishi A, Tasaki M, Hwang SK, Okita TW, Kaneko N, Fujita N, Yoshida M, Hosaka Y, Sato A, Utsumi Y,Ohdan T, Nakamura Y (2008) Mutation of the plastidial α-glucan phosphorylase gene in rice affects the synthesis and structure ofstarch in the endosperm. Plant Cell 20: 1833-1849


Sestili F, Botticella E, Proietti G, Janni M, D’Ovidio R., Lafiandra D (2012) Amylose content is not affected by overexpression of the Wx-B1 gene in durum wheat. Plant Breed 131: 700-706


Slade AJ, McGuire C, Loeffler D, Mullenberg J, Skinner W, Fazio G, Holm A, Brandt KM, Steine MN, Goodstal JF, Knauf VC (2012)Development of high amylose wheat through TILLING. BMC Plant Biol, 12: 69


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http://www.ncbi.nlm.nih.gov/pubmed?term=Satoh H%2C Shibahara K%2C Tokunaga T%2C Nishi A%2C Tasaki M%2C Hwang SK%2C Okita TW%2C Kaneko N%2C Fujita N%2C Yoshida M%2C Hosaka Y%2C Sato A%2C Utsumi Y%2C Ohdan T%2C Nakamura Y %282008%29 Mutation of the plastidial α%2Dglucan phosphorylase gene in rice affects the synthesis and structure of starch in the endosperm%2E Plant Cell 20%3A 1833%2D1849&dopt=abstract

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http://scholar.google.com/scholar?as_q=Mutation of the plastidial �?±-glucan phosphorylase gene in rice affects the synthesis and structure of starch in the endosperm&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Mutation of the plastidial �?±-glucan phosphorylase gene in rice affects the synthesis and structure of starch in the endosperm&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Satoh&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Sestili F%2C Botticella E%2C Proietti G%2C Janni M%2C D�??Ovidio R%2E%2C Lafiandra D %282012%29 Amylose content is not affected by overexpression of the Wx%2DB1 gene in durum wheat%2E Plant Breed 131%3A 700%2D706&dopt=abstract

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http://scholar.google.com/scholar?as_q=Amylose content is not affected by overexpression of the Wx-B1 gene in durum wheat&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Amylose content is not affected by overexpression of the Wx-B1 gene in durum wheat&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Sestili&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Slade AJ%2C McGuire C%2C Loeffler D%2C Mullenberg J%2C Skinner W%2C Fazio G%2C Holm A%2C Brandt KM%2C Steine MN%2C Goodstal JF%2C Knauf VC %282012%29 Development of high amylose wheat through TILLING%2E BMC Plant Biol%2C 12%3A 69&dopt=abstract

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12849Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Zhu L, Gu M, Meng X, Cheung SCK, Yu H, Huang J, Sun Y, Shi Y, Liu Q (2012). High-amylose rice improves indices of animal health innormal and diabetic rats. Plant Biotechnol J 10: 353-362



http://www.ncbi.nlm.nih.gov/pubmed?term=Zhou H%2C Wang L%2C Liu G%2C Meng X%2C Jing Y%2C Shu X%2C Kong X%2C Sun J%2C Yu H%2C Smith SM%2C Wu D%2C Li J %282016%29 Critical roles of soluble starch synthase SSIIIa and granule%2Dbound starch synthase Waxy in synthesizing resistant starch in rice%2E Proc Natl Acad Sci USA 113%3A 12844%2D12849&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhou H, Wang L, Liu G, Meng X, Jing Y, Shu X, Kong X, Sun J, Yu H, Smith SM, Wu D, Li J (2016) Critical roles of soluble starch synthase SSIIIa and granule-bound starch synthase Waxy in synthesizing resistant starch in rice. Proc Natl Acad Sci USA 113: 12844-12849

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http://scholar.google.com/scholar?as_q=Critical roles of soluble starch synthase SSIIIa and granule-bound starch synthase Waxy in synthesizing resistant starch in rice&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhou&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhu L%2C Gu M%2C Meng X%2C Cheung SCK%2C Yu H%2C Huang J%2C Sun Y%2C Shi Y%2C Liu Q %282012%29%2E High%2Damylose rice improves indices of animal health in normal and diabetic rats%2E Plant Biotechnol J 10%3A 353%2D362&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhu L, Gu M, Meng X, Cheung SCK, Yu H, Huang J, Sun Y, Shi Y, Liu Q (2012). High-amylose rice improves indices of animal health in normal and diabetic rats. Plant Biotechnol J 10: 353-362

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Zhu&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=High-amylose rice improves indices of animal health in normal and diabetic rats&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=High-amylose rice improves indices of animal health in normal and diabetic rats&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhu&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1


gradually decreasing starch branching enzyme expression is … · 2017/11/13 · one sentence...

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