1 running title: characterization of maize rea1 mutant 2dec 08, 2015 · rea1 is an aaa-atpase that...

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Running title: Characterization of Maize rea1 mutant 1

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To whom all the correspondence should be sent: 4

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Rentao Song 6

Address: Shanghai Key Laboratory of Bio-Energy Crops, School of Life 7

Sciences, Shanghai University, 333 Nanchen Road, Shanghai 200444, China 8

Telephone: 86-21-66135182 9

E-mail: [email protected] 10

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Research Area: Genes, Development and Evolution 13

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Plant Physiology Preview. Published on December 8, 2015, as DOI:10.1104/pp.15.01722

Copyright 2015 by the American Society of Plant Biologists

https://plantphysiol.orgDownloaded on March 12, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.

https://plantphysiol.org

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Title: Maize rea1 mutant stimulates ribosome use efficiency and triggers 35

distinct transcriptional and translational responses 36

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Weiwei Qi 1ab, Jie Zhu 1a, Qiao Wu 1a, Qun Wang a, Xia Li a, Dongsheng Yao a, 38

Ying Jin a, Gang Wang ab, Guifeng Wang ab, and Rentao Song 2ab 39

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1 These authors contributed equally to this study 41

2 Address for correspondence to [email protected] 42

a Shanghai Key Laboratory of Bio-Energy Crops, School of Life Sciences, 43

Shanghai University, Shanghai 200444, China 44

b Coordinated Crop Biology Research Center (CBRC), Beijing 100193, China 45

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Summary: 48

Impaired ribosome biogenesis enhances ribosome use efficiency, triggers 49

distinct transcriptional and translational cellular responses, and affects cell 50

growth and proliferation. 51

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This work was supported by the Major Research plan of the National Natural 68

Sciences Foundation of China (91335208 and 31425019), and the Ministry of 69

Science and Technology of China (2014CB138204). 70

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The author responsible for distribution of materials integral to the findings 73

presented in this article in accordance with the policy described in the 74

Instructions for Authors (www.plantphysiol.org) is: 75

[email protected]. 76

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Maize rea1 mutant stimulates ribosome use efficiency and 98

triggers distinct transcriptional and translational responses 99

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Abstract 101

Ribosome biogenesis is a fundamental cellular process in all cells. Impaired 102

ribosome biogenesis causes developmental defects; however, its molecular 103

and cellular basis is not fully understood. We cloned a gene responsible for a 104

maize small seed mutant dek*, and found it encodes Ribosome export 105

associated 1 (ZmRea1). Rea1 is an AAA-ATPase that controls 60S ribosome 106

export from the nucleus to the cytoplasm after ribosome maturation. dek* is a 107

weak mutant allele with decreased Rea1 function. In dek* cells, mature 60S 108

ribosome subunits are reduced in the nucleus and cytoplasm, but the 109

proportion of actively translating polyribosomes in cytosol is significantly 110

increased. Reduced phosphorylation of eIF2α and the increased eEF1α level 111

indicate an enhancement of general translational efficiency in dek* cells. The 112

mutation also triggers dramatic changes in differentially transcribed genes 113

(DTGs) and differentially translated RNAs (DTRs). Discrepancy was observed 114

between DTGs and DTRs, indicating distinct cellular responses at transcription 115

and translation levels to the stress of defective ribosome processing. DNA 116

replication and nucleosome assembly related gene expression are selectively 117

suppressed at translational level, resulting in inhibited cell growth and 118

proliferation in dek* cells. This study provides insight into cellular responses 119

due to impaired ribosome biogenesis. 120

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Introduction 131

Ribosomes are organelles that translate genetic information into proteins. A 132

great percentage of total RNA transcription is devoted to ribosomal RNA 133

synthesis, and a great part of RNA polymerase Ⅱ transcription and mRNA 134

splicing are devoted to synthesis of ribosomal proteins (Warner, 1999). 135

Ribosome biosynthesis consumes ~80% of a cell's energy (James et al., 2014). 136

In eukaryotes, ribosome biogenesis begins in the nucleolus with the 137

transcription of a large ribosomal precursor RNA that gives rise to the 90S 138

pre-ribosomal particle. Cleavages of the 90S particle generate two subunits: 139

the pre-40S and pre-60S complexes. The pre-40S and pre-60S subunits 140

mature in the nucleolus and nucleoplasm before being exported to the 141

cytoplasm (Venema and Tollervey, 1999; Fromont-Racine et al., 2003; 142

Granneman and Baserga, 2004). Inhibition of ribosome biogenesis causes 143

developmental defects in yeast, humans and plants (Tschochner and Hurt, 144

2003; Galani et al., 2004; Ruan et al., 2012; Weis et al., 2014; Brooks et al., 145

2014). 146

A great deal of research has revealed that hundreds of 147

ribosomal-biogenesis factors contribute to maturation of the ribosome in 148

eukaryotes (Tschochner and Hurt, 2003; Henras et al., 2008), including three 149

essential AAA-ATPases: Ribosome export (Rix) 7, Ribosome export 150

associated (Rea) 1, and Diazaborine resistance gene (Drg) 1 (Pertschy et al., 151

2007; Kressler et al., 2008; Ulbrich et al., 2009; Bassler et al., 2010; Kressler 152

et al., 2012). Rea1 AAA-ATPase is the best-characterized ATPase in ribosome 153

biogenesis and is conserved from yeast to humans (Bassler et al., 2010; 154

Kressler et al., 2012). Rea1 promotes stripping of other biogenesis factors 155

from the pre-60S particle in the nucleolus and nucleoplasm (Ytm1-Erb1-Nop7 156

and Rsa4) prior to the export of the large ribosomal subunit to the cytoplasm 157

(Bassler et al., 2010). However, there is not a comprehensive understanding of 158

cellular responses to the impaired large ribosomal subunit export. 159

The regulation of mRNA translation is a critical feature of gene expression 160

in eukaryotes (Bailey-Serres, 1999). Previous studies highlight the importance 161

of translational control in determining protein abundance, underscoring the 162

value of measuring gene expression at the level of translation. Mechanisms 163



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that underlie differential mRNA translation are likely to involve nucleotide 164

sequence features and the phosphorylation status of initiation factors 165

(Bailey-Serres and Dawe, 1996; Pop et al., 2014). Transcriptome and 166

translatome analyses of the cellular response to heat shock, cell-cycle arrest 167

and mating pheromone in Saccharomyces cerevisiae (Preiss et al., 2003; 168

Serikawa et al., 2003; MacKay et al., 2004), the hypoxia response of HeLa 169

cells (Blais et al., 2004), and the drought and oxygen deprivation responses in 170

Arabidopsis (Kawaguchi et al., 2004; Branco-Price et al., 2005) have shown 171

the importance of translational regulation. These researchers investigated the 172

correlation between total and poly-ribosome (polysome) -bound mRNA 173

accumulation and provided extensive evidence of variation in the translational 174

regulation of individual mRNAs. These studies showed mRNAs differ in their 175

association with polysomes under different circumstances, and gene 176

expression can be regulated at the translational level without a change in 177

mRNA abundance. 178

Maize (Zea mays) is especially well suited for genetic studies, partly 179

because of the feasibility to generate a wide range of easily observable 180

phenotypes (Neuffer and Sheridan, 1980). Many kernel mutants are known 181

(Neuffer et al., 1968), among which one class is defective kernel (dek) mutants 182

(Neuffer and Sheridan, 1980). dek mutants are good resource to investigate 183

seed development. For example, Dek1 encodes a large membrane protein of 184

the calpain gene superfamily (Lid et al., 2002). In dek1 mutants, 185

embryogenesis is blocked, while the endosperm lacks the aleurone layer and 186

is chalky (Becraft et al., 2002). Other dek mutants offer opportunities to 187

investigate many basic biological processes, because embryo formation is the 188

first developmental process after the fertilization. Such defects in basic 189

biological processes create visible phenotypes during kernel development. 190

In this study, we characterized dek*, a novel mutant with small kernels, 191

and delayed developmental of the embryo, endosperm and seedling. We 192

report the map-based cloning of Dek* and demonstrate it encodes Rea1 in 193

maize. dek* is a weak mutant allele that only partly represses the maturation 194

and export of the 60S ribosomal subunit. Taking advantage of this mutant allele, 195

we were able to obtain comprehensive information about the cellular 196

responses to impaired 60S ribosomal subunit biogenesis. 197



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Results 199

dek* produces small kernels with delayed development 200

The dek* mutant was isolated from an opaque mutant stock obtained from the 201

Maize Genetic Stock Center. It was crossed to the W64A inbred line to 202

produce a F2 population that displayed a 1:3 segregation of dek (dek*/ dek*) 203

and wild type (+/+ and dek*/+) phenotypes (Figure 1A&B). At 15 days after 204

pollination (DAP), homozygous dek* kernels exhibited a small, vague 205

phenotype (Figure 1A), and mature kernels were small and shrunken (Figure 206

1B). The 100-kernel weight of dek* was nearly 39.5% less than wild type 207

(Figure 1C), but there was no significant difference in the total protein and zein 208

content (Figure 1D, Supplemental Figure 1), although, there was a slight 209

increase in the amount of non-zeins (13.5%, Figure 1D). Among zein proteins, 210

the 22kD α-zeins were relatively more abundant in dek* endosperms 211

(Supplemental Figure 1). We found no obvious difference in total starch 212

content and the percentage of amylose in dek* and wild type endosperms 213

(Supplemental Figure 2). We analyzed soluble amino acids to determine if the 214

slight increase of non-zeins in dek* altered their composition. The results 215

showed that the amount of lysine was most significantly increased (23.1%) 216

might due to the slight increase of non-zein content (Figure 1E), for zeins lack 217

lysine residues (Mertz et al., 1964). 218

Wild type and dek* kernels of 15 DAP and 18 DAP were analyzed by light 219

microscopy to compare their development. Longitudinal sections of the 220

embryos indicated development of the plumule and seminal was delayed more 221

than three days in dek* compared to wild type (Figure 1F). To investigate the 222

endosperm development, we observed 15 DAP and 18 DAP immature 223

endosperm cells using optical microscopy. The endosperm cells of dek* 224

kernels were less cytoplasmic dense with fewer starch granules compared to 225

the wild type of the same stage, also indicating more than a three day delay in 226

development (Figure 1G). 227

At 4 and 7 days after germination (DAG), seedlings of dek* showed a 228

three day developmental delay compared to wild type (Figure 1H). By 4 DAG, 229

wild type seedlings had two leaves, one completely expanded and the other 230



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emerging; the dek* seedlings had only one leaf at this stage. The 7 DAG wild 231

type seedlings had three leaves, while the dek* seedlings had only two leaves. 232

The heading stage of the dek* plant was delayed approximately fifteen days 233

compared to wild type, and its height was only 50% of the wild type 234

(Supplemental Figure 3). These results demonstrated that the growth and 235

development of dek* kernels and seedlings is delayed compared to wild type. 236

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Positional cloning of Dek* 238

Genetic fine mapping of Dek* was carried out with the F2 mapping population 239

and the Dek* gene was placed between the simple sequence repeat (SSR) 240

markers, mmc0241 and umc2162, on the long arm of chromosome 6 (Figure 241

2A). After characterizing a mapping population of 864 individuals, Dek* was 242

mapped between the self-created SSR markers 153.7M-2 (19 recombinants) 243

and 155.1M-1 (29 recombinants). Additional markers InDel438, InDel428, 244

SNP064 and SNP165 were developed, and Dek* gene was eventually placed 245

between SNP064 (1 recombinant) and SNP165 (2 recombinants), a region 246

encompassing a physical distance of 101.6kb (Figure 2A). 247

Nucleotide sequence analysis within this region identified ten predicted 248

open reading frames (ORFs) with gene model information (GRMZM2G405052, 249

GRMZM2G387038, GRMZM5G873561, GRMZM5G807823, 250

GRMZM2G361064, GRMZM5G892685, GRMZM2G059268, 251

GRMZM2G059278, GRMZM2G323939 and GRMZM2G128315). Expression 252

analysis revealed no expression of GRMZM5G892685, GRMZM2G059268 253

and GRMZM2G059278 based on reverse transcription (RT)-PCR and 254

expressed sequence tag (EST) information (http://www.maizegdb.org/); 255

consequently, these three might be pseudogenes. DNA sequence analysis 256

revealed GRMZM2G405052, GRMZM2G387038, GRMZM5G873561, 257

GRMZM5G807823, together with GRMZM2G092001 and GRMZM2G149586 258

which are up-stream of the candidate region, produced one huge transcript 259

that was identified as candidate Gene1. There is a single nucleotide 260

polymorphism in Gene1 resulting in an amino acid replacement between the 261

alleles of dek* and wild type. GRMZM2G361064, GRMZM2G323939 and 262

GRMZM2G128315 were identified as candidate Gene2, Gene3 and Gene4, 263

respectively; however, their consideration for Dek* was eliminated due to no 264



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sequence differences between alleles in dek* and wild type (Figure 2A). 265

Therefore, Gene1 appeared to be the best candidate for the Dek* locus. 266

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Dek* encodes the 60S-specific ribosome biogenesis factor Rea1 268

The genomic DNA sequence of candidate Gene1 spans ~50 kb and produces 269

a huge transcript containing a 16,278 bp coding sequence (Figure 2B). 270

Sequence data for this gene has been deposited in GenBank 271

(http://www.ncbi.nlm.nih.gov/ ) as accession number KP137367. Gene1 272

encodes a ~600 kD protein of 5,425 amino acids. BLASTP searches of 273

Genbank indicated that Gene1 encodes a ribosome biogenesis factor, 274

AAA-ATPase Rea1, with several conserved domains in maize (Figure 2B). 275

ZmRea1 contains different kinds of molecular domains: a weakly conserved 276

N-terminal region, a dynein-like tandem array of six AAA-type ATPase domains 277

(Neuwald et al., 1999), a large linker, a D/E rich region and a metal ion 278

dependent adhesion site (MIDAS) domain (Figure 2B). Rea1 promotes release 279

of Ytm1 which associates with nucleolar pre-60S particles, and later also 280

promotes release of Rsa4 associates with nucleoplasmic pre-60S particles via 281

the MIDAS-MIDAS interacting domain (MIDO) using the mechanical force 282

created by the ATPase ring domain for the export of the large ribosomal 283

subunit to the cytoplasm (Ulbrich et al., 2009; Bassler et al., 2010). The 284

mutation in the dek* allele of ZmRea1 is a single nucleotide polymorphism in 285

the 2,359th codon of ZmRea1, which results in Ala (GCC) replaced by Val 286

(GTC; Figure 2B). This mutation alters the highly conserved region between 287

the dynein-like array of six AAA-type ATPases and the large linker, which could 288

affect transduction of the mechanical force created by the ATPase ring domain 289

to the large tail for release of the ribosome biogenesis factors. 290

To confirm if ZmRea1 is the Dek* gene, we carried out an allelism test 291

with a Mu induced mutant of ZmRea1 (Figure 2B&C). A UniformMu insertion 292

mutant (rea1-Mu) stock for GRMZM2G092001 was obtained from the Maize 293

Genetics Stock Center. This mutant has a Mutator-8 insertion after the 4th 294

nucleotide of the ZmRea1 coding sequence and is not viable (Figure 2B). The 295

allelism test was done by crossing dek* F1 (dek*/+) and rea1-Mu F1 (rea1-Mu 296

/+). The kernel phenotypes in the F2 ears displayed a 1:3 segregation of 82 297

dek (dek*/rea1-Mu) and 249 wild type phenotype kernels (Figure 2C), 298



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indicating that rea1-Mu can’t complement dek*. Therefore, Gene1 (ZmRea1) is 299

indeed the Dek* gene. We hence named dek* as rea1-ref. 300

Maize endosperm is a triploid tissue with 2 maternal and 1 paternal 301

genomes. The mutant kernels in rea1-ref/+ (maternal) X rea1-Mu/+ (paternal) 302

F2 ear are small and shallow, similar to homozygous rea1-ref kernels. The 303

mutant kernels in rea1-Mu/+ (maternal) X rea1-ref /+ (paternal) F2 ears display 304

an even more severe phenotype with dramatically shrunken kernels. The 305

mutant kernels from rea1-Mu/+ selfing are non-viable (Figure 2C). Thus, 306

results of the allelism test show rea1-ref is a weak allele compared to rea1-Mu, 307

which has a lethal phenotype. 308

To examine Rea1 mRNA expression in rea1-ref, we performed 309

quantitative RT-PCR (qRT-PCR) with the total RNA extracted from 15 and 18 310

DAP mutant and wild type kernels. Surprisingly, mRNA expression of Rea1 311

was significantly up-regulated in rea1-ref (Figure 2D). Because ZmRea1 is too 312

large (~600kD) to perform a regular western blot analysis, we used 313

dot-immunoblot analysis on quantified and gradient diluted total protein 314

samples with Rea1-specific antibody to detect its existence in 15 and 18 DAP 315

rea1-ref and wild type kernels (Figure 2E). The results demonstrated that Rea1 316

is present in rea1-ref and accumulates in rea1-ref at normal levels, but might 317

be only partly functional. 318

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Rea1 is highly conserved in different organisms and is constitutively 320

expressed in maize 321

Rea1 was first identified as a component of pre-60S ribosome complex in 322

yeast and is conserved from yeast to humans (Bassler et al., 2001; Bassler et 323

al., 2010; Kressler et al., 2012). We constructed a phylogenetic tree on the 324

basis of the ZmRea1 full length protein sequence and Rea1 protein sequences 325

from Brachypodium distachyon, Triticum, Oryza sativa, Setaria, Arabidopsis 326

thaliana, Populus, Glycine-max, Dictyostelium, Monodelphis domestica, 327

Saprelegnia, Mortierella, and Saccharomyces Cerevisiae. The results 328

suggeste that ZmRea1 is highly conserved with the Rea1 proteins in other 329

plants as well as the Rea1 proteins of yeast, mammals and micro-organisms 330

(Figure 3A). 331

Quantitative RT-PCR analysis revealed ZmRea1 is expressed in a broad 332



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range of maize tissues, including silk, tassel, ear, root, husk, stem, leaf and 333

kernel (Figure 3B). During kernel development, expression of Rea1 occurs 334

before 5 DAP and continues later than 25 DAP (Figure 3C). Dot-immunoblot 335

analysis on quantified and gradient diluted total nuclear and cytoplasmic 336

proteins detected Rea1 in these subcellular fractions, and it was predominantly 337

found in the nuclear fraction, consistent with Rea1 localization in the nucleus 338

(Figure 3D). 339

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rea1-ref affects the biogenesis of 60S ribosomal subunits 341

To investigate the effect of rea1-ref on ribosomal subunit biogenesis and the 342

formation of monosome and polysome complexes, polysome profiles of 15 343

DAP rea1-ref and wild type kernel extracts were analyzed by 15-45% (w/v) 344

sucrose gradient centrifugation. Two independent biological replicates were 345

performed. This analysis revealed a significant reduction of 60S ribosomal 346

subunits, as compared to 40S ribosomal subunits, in the mutant (Figure 4A). 347

To compare the levels of monosomes and polysome complexes, calculation of 348

the peak areas of A254 absorbance revealed that about 40.2% of the 349

ribosomes in wild type kernel extracts were in polysomes, while the level of 350

polysome complexes in rea1-ref kernel extracts was 57.2 % (Figure 4A). Thus, 351

there are 1.4-Fold greater polysomes/total ribosomes in rea1-ref. The 352

decrease in 60S subunits and increase in polysomes is consistent with 353

inhibition of large ribosomal subunit export and promotion in initiation of protein 354

synthesis as a consequence of down-regulated ribosome biogenesis in 355

rea1-ref. 356

To confirm that maturation and export of 60S subunits is reduced in 357

rea1-ref, immunoblot analysis with 60S and 40S subunit antibodies was 358

performed on nuclear and cytoplasmic fractions from 15 and 18 DAP rea1-ref 359

or wild-type kernels. Nuclear and cytoplasmic fractions were subjected to 360

immunoblot analysis with antibodies against Bip (cytoplasm marker), and 361

histone (nucleus marker). Tubulin and TATA-box binding protein (TBP) served 362

as sample loading controls of cytoplasmic and nuclear proteins, respectively. 363

The level of eRPL13 was examined using a L13-specific antibody. L13 protein 364

was markedly decreased in both the nuclear and cytoplasmic fractions of 365

rea1-ref compared to wild-type kernels (Figure 4B). The level of eRPS14 was 366



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also examined using a specific antibody, and its content was the same in both 367

the nuclear and cytoplasmic fractions of rea1-ref and wild-type kernels (Figure 368

4B). Meanwhile, we also observed slight decrease of histone protein in 369

rea1-ref nuclear fraction (Figure 4B). 370

A reduction of 60S ribosomal subunits in the cytoplasm of 15 and 18 DAP 371

rea1-ref and wild-type endosperms was also observed by Transmission 372

Electron Microscopy (TEM) analysis. There were fewer ribosomes on rough 373

ER (RER), and the RER around protein bodies (PBs, Supplemental Figure 4). 374

Nucleolus stress due to ribosomal failure alters the morphology and increases 375

the surface area of nucleolus in humans (Bailly et al., 2015). This stress, which 376

misshapes and expands nucleolus, was also observed in rea1-ref endosperm 377

by TEM (Figure 4C). All these data are consistent with a biogenesis defect of 378

60S subunits and demonstrates it is specific to the 60S maturation and export 379

pathway. 380

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rea1-ref affects transcription of ribosome biogenesis, translational 382

elongation and nucleosome-related genes 383

We compared the transcript profile of 15 DAP rea1-ref and wild type 384

endosperm using RNA sequencing (RNA-seq). Among the 45,730 gene 385

transcripts detected by RNA-seq, significantly differentially transcribed genes 386

(DTGs) were identified as those with a threshold fold change>2 and 387

p-value<0.05. Based on this criterion, 2,076 genes showed significant altered 388

expression between rea1-ref and the wild type. There were 1,518 genes with 389

increased transcription, while 558 genes showed decreased transcription. 390

Within the 2,076 DTGs, 39.9% could be functionally annotated 391

(annotations were found using BLASTN and BLASTX analyses against the 392

Genbank (http://www.ncbi.nlm.nih.gov/) database). Gene Ontology (GO; 393

http://bioinfo.cau.edu.cn/agriGO/) and the Kyoto Encyclopedia of Genes and 394

Genomes (http://www.genome.jp/kegg/) pathway analysis indicated that 828 395

DTGs were mostly related to four GO terms: GO: 0005840 (ribosome, 396

p-value=2.34E-130); GO: 0006414 (translational elongation, 397

p-value=2.30E-17); and GO: 0000786 (nucleosome, p-value= 8.22E-29); GO: 398

0045735 (nutrient reservoir activity, p-value=6.47E-33). This analysis is 399

illustrated in Figure 5A and Supplemental Table 1. 400



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Ninety-eight DTGs classified to GO: 0005840 (ribosome) could be divided 401

into three categories: small ribosomal subunit proteins, e.g., eRPS6 402

(GRMZM5G851698), eRPS13 (GRMZM2G130544); large ribosomal subunit 403

proteins, e.g. eRPL14 (GRMZM2G168330), eRPL18 (GRMZM2G030731); 404

and ribosome biogenesis factors. Transcription of all the genes related to 405

ribosome biogenesis was increased in rea1-ref endosperm. rea1-ref also has a 406

strong impact on translational elongation. The twenty DTGs involved in GO: 407

0006414 (translational elongation) could be divided into two categories: 60S 408

acidic ribosomal proteins, e.g. eRPLP0 (GRMZM2G066460), eRPLP1 409

(GRMZM2G157443); and translation elongation factors, e.g. eEF1α 410

(GRMZM2G151193), eEF1β (GRMZM2G122871). These genes were also 411

up-regulated. Fifty-two DTGs related to GO: 0000786 (nucleosome) could be 412

divided into two categories: histones, e.g., H2A (GRMZM2G056231), H2B 413

(GRMZM2G401147); and nucleosome assembly protein (NAP, 414

GRMZM2G176707). Transcription of these genes, which are related to 415

nucloesome assembly and cell cycle, was markedly induced in rea1-ref 416

endosperm. DTGs involved in GO: 0045735 (nutrient reservoir activity) were 417

storage proteins, including 22kD α-zein (GRMZM2G346897), and 19kD α-zein 418

(GRMZM2G059620), e.g. these genes were down-regulated. To validate the 419

differences observed by RNA-Seq, we performed qRT-PCR on the most 420

significant DTGs from each GO category, and the results confirmed similar 421

differences of mRNA accumulation (Figure 5B). 422

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rea1-ref exhibits uncoordinated expression of distinct groups of genes at 424

the translational level 425

The increase in polysomes in rea1-ref indicated promotion in initiation of 426

protein synthesis in response to down-regulated ribosome biogenesis. The 427

mechanisms that underlie differences of mRNA translation involve sequence 428

features of individual mRNAs and the phosphorylation status of translation 429

initiation factors (Bailey-Serres and Dawe, 1996). General Control 430

Non-derepressing kinase-2 (GCN2) was reported to phosphorylate eukaryotic 431

initiation factor 2α (eIF2α) to down-regulate translation (Zhang et al., 2008). 432

We firstly measured the phosphorylation levels of eIF2α in 15 and 18 DAP 433

rea1-ref and wild-type cytoplasms by protein gel blot analysis with P-eIF2α and 434



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eIF2α (total eIF2α as control) antibodies. Compared with wild type, eIF2α in 435

rea1-ref was significantly less phosphorylated, while the eIF2α protein level 436

was not altered (Figure 6A). The level of eEF1α protein in rea1-ref and 437

wild-type cytoplasms was examined using specific antibody. eEF1α was 438

markedly increased in rea1-ref (Figure 6A). These results indicated that 439

initiation and elongation of translation are promoted in rea1-ref. 440

The level of an mRNA in polysomes reflects its translation (Branco-Price 441

et al., 2005). To examine the effects of rea1-ref on translational regulation of 442

individual mRNAs, we evaluated the amount of RNA in polysomes, relative to 443

the total amount of transcript in 15DAP rea1-ref and wild type kernels. Kernel 444

extracts were centrifuged (170,000 g) to obtain a polysome pellet for 445

comparing total extract and polysome-bound RNA samples by RNA-Seq 446

analysis. The polysome-bound/total RNA ratios in 15DAP rea1-ref and wild 447

type kernels were 36.4% and 25.6%, respectively. Consequently, there was a 448

1.4-Fold increase of polysome-bound/total RNA in rea1-ref, which is consistent 449

with the polysome complexes/total ribosomes A254 absorbance by ribosome 450

profile analysis. 451

Within the 30,188 gene transcripts detected by RNA-seq, significantly 452

differentially translated RNAs (DTRs) were identified as those with a 2nP/T 453 (normalized polysome-bound/total)×100% (see Methods) between rea1-ref and wild type, fold 454

change>2.0 or <0.5. Based on this criterion, 1,802 genes showed significantly 455

increased translation in rea1-ref compared to the wild type, while 2,959 genes 456

showed decreased translation. To confirm the differences between wild type 457

and rea1-ref endosperm observed by RNA-Seq, we performed qRT-PCR on 458

the most significantly increased or decreased DTRs selected from each 459

category and the results were consistent (Figure 6B&C). We also performed 460

puromycin treatment for the releasing of polysome as negative control 461

(Supplemental Figure 5). No significant difference of sequence features was 462

observed between the up-regulated and down-regulated DTRs (Supplemental 463

Table 2). 464

Within the increased DTRs, 687 could be functionally annotated. GO 465

analysis indicated these RNAs are mostly related to three GO terms, GO: 466

0045449 (Regulation of transcription, p-value=1.33E-03), GO: 0045735 467

(Nutrient reservoir activity, p-value=3.51E-12) and GO: 0006414 (Translational 468



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elongation, p-value= 1.17E-07). For the decreased DTRs, 601 could be 469

functionally annotated, belonging to GO: 0006334 (Nucleosome assembly, 470

p-value=6.59E-10), GO: 0006260 (DNA replication, p-value=1.18E-03) and 471

GO: 0033279 (Ribosomal subunits, p-value= 1.16E-03). Ten most strongly 472

up-regulated or down-regulated DTRs of each classification are illustrated in 473

Table 1 and all DTRs are shown in Supplemental Table 2. 474

Transcriptional factors (e.g. NAC domain transcription factors, MADS-box 475

transcription factors) and translation elongation-related genes had a markedly 476

higher translation level in rea1-ref. Although the expression of zeins was 477

down-regulated in rea1-ref (Figure 5), surprisingly their translation level is 478

significantly increased (Table 1& Supplemental Table 2). There is significant 479

overlap (p-value=2.23E-16, chi-sq test) for zeins between transcriptional 480

down-regulated genes and translational up-regulated genes (Figure 6E). 481

Meantime, although the expression of histone RNAs was up-regulated in 482

rea1-ref (Figure 5), their translation level was dramatically reduced. There is 483

also significant overlap (p-value=1.57E-14, chi-sq test) for histones between 484

transcriptional up-regulated genes and translational down-regulated genes 485

(Figure 6E). DNA replication related genes (e.g. DNA polymerase subunits, 486

minichromosome maintenance proteins (MCMs)) had lower translation level in 487

rea1-ref. Histones and DNA replication related genes are both related to 488

nucloesome assembly and cell cycle. Although the transcription of ribosomal 489

subunit proteins is up-regulated in rea1-ref (Figure 5), their translation level is 490

dramatically down-regulated. There is overlap between transcriptional 491

up-regulated genes and translational down-regulated genes for ribosomal 492

proteins (Figure 6E). These results demonstrate that the transcriptional and 493

translational regulation of individual genes responding to reduced 60S 494

ribosome exportation is not always consistent. 495

We measured the level of 22kD α-zeins in 470 ng and 1,190 ng total 496

proteins of 15 DAP rea1-ref and wild-type kernels, respectively, by protein gel 497

blot analysis with 22kD α-zein antibodies. Compared with the wild type, 22kD 498

α-zeins in rea1-ref are significantly increased. Meanwhile, there is no effect on 499

19kD α-zein content (Figure 6D). Increased eEF1α protein content (Figure 6A) 500

and lower protein content of histone (Figure 4B) in rea1-ref also confirmed 501

their increased or decreased translation level. 502



16

503

rea1-ref inhibits cell proliferation and cell growth 504

The synthesis of nucloesome assembly proteins that related to cell cycle 505

transition is markedly reduced in rea1-ref (Table1&Figure 6). This mutant 506

exhibits a slow growth phenotype for both kernels and seedlings. There was a 507

more than three days’ delay in endosperm development (Figure 1). 508

Endoreduplication is a general feature of endosperm development in maize, 509

involving replication of the nuclear genome without cell division, and leading to 510

elevated nucleic acid content (Sabelli and Larkins, 2009). Endoreduplication 511

includes only G1 and S phase, which is different from the mitotic cell cycle 512

(G1-S-G2-M). 513

Flow cytometry (FCM) analysis of 15 DAP rea1-ref and wild type 514

endosperms showed endoreduplicated nuclei with C-values of 12C or greater, 515

accounting for 18.1% of the DNA in 15 DAP endosperm of rea1-ref, and 22.2% 516

of the DNA in 15 DAP wild-type endosperm (Figure 7A). At 18 DAP, there are 517

19.3 and 24.2% endoreduplicated nuclei with C-values of 12C or greater in 518

rea1-ref and wild-type endosperm, respectively (Figure 7B). The mitotic cell 519

cycle was also assessed in 7 DAG seedlings by FCM. The result showed that 520

63.3% of the nuclei are with 2C DNA content in rea1-ref 7 DAG seedlings, 521

while 45.1% of the nuclei in the wild type seedlings are with 2C DNA content 522

(Figure 7C). These results demonstrate that mutation of rea1-ref affects the 523

cell proliferation. The first leaf of 7 DAG rea1-ref and wild-type seedlings was 524

analyzed by scanning electron microscopy (SEM) to observe the cell size of 525

lower epidermis (Figure 7D). There was significantly smaller cell size in 526

rea1-ref seedling than wild type; with cell width and cell length both decreased 527

(Figure 7E). These results demonstrate that cell growth and cell proliferation 528

are suppressed as a result of impaired 60S ribosome maturation, resulting in a 529

developmental delay. 530

531

Discussion 532

rea1-ref/dek* is a weak mutant allele that functionally suppresses 533

ZmRea1 and affects 60S ribosome biogenesis 534

Rea1 is a highly conserved ribosome biogenesis factor first identified in the 535



17

Nug1-purified pre-60S subunit in yeast, which is the pre-ribosomal particle at 536

the export from the nucleolus to the nucleoplasm (Bassler et al., 2001). The six 537

ATPase modules of Rea1 create a ring domain, while the large linker and the 538

MIDAS domain compose the tail structure (Ulbrich et al., 2009). Rea1 attaches 539

the pre-ribosome at the Rix1 complex (Rix1-Ipi3-Ipi1) via the ATPase ring 540

domain (Nissan et al., 2002; Nissan et al., 2004; Galani et al., 2004). The tail of 541

Rea1 containing the MIDAS domain contacts the pre-ribosome at other 542

positions where the pre-60S factor, Rsa4 or Ytm1, is located. Ytm1 associates 543

with nucleolar pre-60S particles, while Rsa4 associates with nucleoplasmic 544

particles (Bassler et al., 2001; Miles et al., 2005; De la Cruz et al., 2005; 545

Ulbrich et al., 2009). The MIDAS domain of Rea1 interacts with the MIDO 546

domain of Ytm1or Rsa4; this interaction is essential for 60S unit maturation 547

and export from the nucleolus to the nucleoplasm, or from the nucleoplasm to 548

cytoplasm, respectively (Bassler et al., 2001; Ulbrich et al., 2009). Rea1 is 549

bound to the pre-60S ribosome at two distinct sites: one is mediated via the 550

motor ring domain and the other via MIDAS interaction with Ytm1 or Rsa4, 551

creating a mechanochemical device to release Ytm1 or Rsa4 for 60S ribosome 552

export (Kressler et al., 2012). 553

Compared to dek1, which creates severe effects on kernel development 554

(Becraft et al., 2002), dek* causes only mild effects. The mutant kernels have 555

an obvious small phenotype and decreased seed weight (Figure 1), with a 556

delay of embryo, endosperm and seedling development (Figure 1). 557

rea1-ref/dek* is a weak, non-lethal mutant allele, where the 2,359th Ala (GCC) 558

of ZmRea1 is replaced by Val (GTC, Figure 2). The rea1 mutant allele derived 559

from a Mutator transposon insertion in the coding region has a defective 560

phenotype and is lethal. rea1-ref is defective at the highly conserved linkage 561

region and might suppress function of ZmRea1 by affecting the mechanical 562

force of the ATPase ring domain to the MIDAS tail that releases Rsa4 or Ytm1 563

factors. The expression of Rea1 is increased at the transcript level in rea1-ref, 564

which might be a response to its functional suppression (Figure 2). 565

The characterization of dek* provides the first description of Rea1 in 566

maize. A significant reduction of mature 60S subunits were observed in yeast 567

rea1 mutants at restrictive conditions (Garbarino and Gibbons, 2002; Galani et 568

al., 2004). Rea1 homologous gene in arabidopsis is essential for female 569



18

gametophyte development (Chantha et al., 2010). Rea1 AAA-ATPase is 570

conserved from yeast to humans (Bassler et al., 2010). Phylogenetic analysis 571

of ZmRea1 suggests Rea1 protein is highly conserved in plants, and is 572

homologous to proteins in yeast, mammals and micro-organisms (Figure 3). A 573

significant reduction of mature 60S ribosomal subunits is observed in the 574

rea1-ref mutant, consistent with the effects observed in yeast rea1, indicating 575

an biogenesis defect specific to the 60S subunit maturation pathway; 576

maturation and export of 40S subunits is not affected (Figure 4). This indicates 577

conserved function on 60S subunit biogenesis of Rea1 in yeast and plants. 578

There is reduction of mature 60S subunits in cytoplasm and pre-60S subunits 579

in nucleus (Figure 4&8), indicating the nucleus detained pre-60S subunits 580

might be degraded, for pre-mature ribosomal particles with biogenesis failure 581

would be dispersed and degraded in the nucleoplasm (Andersen et al., 2005; 582

Lam et al., 2007). 583

584

Impaired ribosome biogenesis enhances ribosome use efficiency 585

Regulation of protein synthesis is a key control point in cellular responses to 586

distinct stresses (Faye et al., 2014). The proportion of actively translating 587

ribosomes is reflected by the percentage of polysome complexes/total 588

ribosomes (Branco-Price et al., 2005; Faye et al., 2014). We observed a 589

1.4-Fold increase of polysome complexes/total ribosomes in rea1-ref (Figure 590

4). This increase in polysomes in rea1-ref is indicative of a promotion in the 591

initiation of protein synthesis. The proportion of actively translating ribosomes 592

might be in response to the down-regulation of ribosome biogenesis. 593

The results of our study of rea1-ref suggest suppressed ribosome export 594

enhances ribosome use efficiency and cellular translational efficiency. mRNA, 595

the 40S ribosomal subunit and eIF2α comprise the 43S pre-initiation complex, 596

termed “half-mer”, before attachment of the 60S ribosomal subunit (Helser et 597

al., 1981; Moy et al., 2002). Multiple eukaryotic protein kinases each of which 598

responds to different signals are known to phosphorylate eIF2α and 599

down-regulate general translation initiation, (Chen and London, 1995; Harding 600

et al., 1999; Williams, 1999; Harding et al., 2000; Huizen et al., 2003). GCN2 is 601

the only eIF2α kinase found in all eukaryotes, including plants like Arabidopsis 602

(Berlanga et al., 1999; Zhang et al., 2008). Phosphorylation of eIF2α is 603



19

significantly reduced in rea1-ref (Figure 6), indicating increased formation of 604

pre-initiation complexes for protein synthesis, consistent with an increased 605

proportion of actively translating ribosomes. Further more, the level of eEF1α 606

protein is markedly increased in rea1-ref (Figure 6), suggesting a promotion of 607

both initiation and elongation of translation in rea1-ref. Consequently, there is 608

evidence for increased efficiency of ribosome usage during translation in 609

rea1-ref to ensure normal rates of protein synthesis (Figure 8). 610

611

Impaired ribosome biogenesis triggers distinct transcriptional and 612

translational cellular responses 613

We have found the suppressed ribosome maturation associated with rea1-ref 614

brings about global changes in transcription and translation. Translation of 615

individual mRNAs is regulated, producing discrepancies between mRNA and 616

protein levels. mRNAs have a distinct pattern of ribosome loading under 617

certain conditions, resulting in altered translational efficiencies (Branco-Price 618

et al., 2005; Gawron et al., 2014). Thus, analysis of transcript level is 619

insufficient to completely describe cellular responses under different conditions. 620

There is also alternative translation that contributes to the complexity of 621

proteomes (Preiss et al., 2003; Serikawa et al., 2003; MacKay et al., 2004; 622

Blais et al., 2004; Kawaguchi et al., 2004; Branco-Price et al., 2005; Lin et al., 623

2014). According to our transcriptome and translatome analysis, there is 624

evidence for consistent and inconsistent transcriptional and translational 625

regulation of genes in rea1-ref endosperm (Figure 8). The large amount of 626

transcriptionally up-regulated genes is not the consequence of developmental 627

delay, according to the expression data for developing maize kernels (Chen et 628

al., 2014). Our transcriptome analysis revealed immediate cellular responses, 629

while the translatome revealed specific protein changes that are independent 630

of transcriptional regulation for efficient use of limited ribosomes and energy. 631

For nucleus located proteins, transcription of small and large ribosomal 632

subunit proteins is increased in rea1-ref endosperm (Figure 5), whereas their 633

translation is down-regulated (Table 1). The transcriptional up-regulation of 634

ribosomal proteins might be a response to a decreased level of mature 635

ribosomes in the cytoplasm in rea1-ref (Figure 4). But increased transcription 636

is incapable of rescuing 60S ribosome export in rea1-ref. Consequently, the 637



20

percentage of polysome-bound RNA of these genes might be reduced for 638

more efficient usage of limited ribosomes. Similar to ribosomal proteins, there 639

is also a discrepancy in expression of nucleosome assembly-related genes. 640

Transcription of histones is increased in rea1-ref (Figure 5), while their 641

translation is down-regulated (Table 1). DNA replication-related genes also 642

have reduced translation in rea1-ref (Table 1). The polysome-bound RNA of 643

histone- and DNA replication- related genes are markedly decreased (Figure 644

6); and the histone protein content is down-regulated in rea1-ref (Figure 4). 645

Up-regulation of histone transcription might be a response to decreased 646

growth vigor of rea1-ref (Figure 1), in order to accelerate growth rate. But 647

accelerated growth might be lethal due to ribosome shortage. Different kinds of 648

transcriptional factors have markedly higher translation in rea1-ref (Table 1), 649

including auxin-signaling related genes (GRMZM2G081930 and 650

GRMZM5G809195, Zhang et al., 2014). Among cytosol-located proteins, 651

transcription and translation of translation elongation-related genes are both 652

up-regulated in rea1-ref (Figure 5&Table 1). The final polysome-bound RNA 653

content of eEF1α and eEF-Tu, as well as the protein level of eEF1α are 654

markedly increased in rea1-ref (Figure 6). There is also inconsistent 655

transcriptional and translational levels of Rea1 itself (Figure 2), and it might be 656

a developmental stage-dependent translational regulation 657

In maize kernel, the most abundant protein is zein storage protein, that 658

accounts for 50%-70% of the total protein (Holding and Larkins, 2009), and 659

α-zein is the largest class of zein protein (Heidecker and Messing, 1986). The 660

transcriptionally down-regulated zeins might be the consequence of 661

developmental delay. α-zeins have an increased translation level (Table 1), 662

especially the 22kD α-zeins show markedly increased protein in both 663

SDS-PAGE and immunoblot analysis (Figure 1&Figure 6). The percentage of 664

α-zein polysome-bound RNA might be increased to ensure basic protein 665

storage in rea1-ref. 666

The mechanisms that underlie variation in translation of individual genes 667

are likely to involve features of the mRNA sequence (Bailey-Serres and Dawe, 668

1996). Evaluation of highly translated genes under hypoxia in Arabidopsis 669

showed mRNA sequences with a low GC nucleotide content in the 670

5’-untranslated region (UTR) (Branco-Price et al., 2005). RNA 5’- UTR GC 671



21

content, 5’- UTR length, and ORF length were also observed to affect 672

ribosome loading (Jiao and Meyerowitz, 2010; Yángüez et al., 2013). When 673

we analyzed sequence features that might affect ribosome loading of 674

individual gene transcripts affected by shortage of 60S ribosome subunits 675

(Supplemental Table 3), no significantly different features were observed 676

between the 1,802 up-regulated DTRs and 2,959 down-regulated DTRs, 677

compared to 3,000 randomly selected control genes. However, there might be 678

other feedback pathways for independent regulation at the transcriptional and 679

translational levels. 680

681

Impaired ribosome biogenesis affects cell growth and proliferation 682

Cell growth and proliferation are tightly linked, as enhanced protein synthesis 683

is required for cell proliferation (Thomas, 2002). The increase in protein 684

synthesis is accomplished by an enhanced rate of ribosome biogenesis in 685

support of the metabolic effort for cell proliferation (Sollner-Webb and Tower, 686

1986). Normal mitosis includes four successive phases: G1 (postmitotic 687

interphase), S (DNA synthesis phase), G2 (postsynthetic phase), and M 688

(mitosis) (Fowler et al., 1998; Riou-Khamlichi et al., 2000), where as 689

endoreduplication of endosperm includes only G1 and S phases (Sabelli and 690

Larkins, 2009). rea1-ref exhibits slower growth and cell proliferation (Figure 7), 691

indicating an intrinsic link between ribosome biogenesis and cell cycle 692

transition. Based on our analysis, this linkage is through regulation of DNA 693

replication and nucleosome assembly. 694

In mammalian cells, the tumor suppressor, p53, has been shown to arrest 695

the cell cycle at the G1–S transition in response to impaired ribosome 696

biogenesis, while p53-independent cell cycle arrest in response to alteration of 697

ribosome biogenesis has also been described (Mayer and Grummt, 2005; 698

Zhang and Lu, 2009; Deisenroth and Zhang, 2010; Grimm et al., 2006; Donati 699

et al., 2011). p53 stabilization leads to cell cycle arrest through the regulation 700

of cyclins and cyclin-dependent kinases (CDKs) (Sherr and McCormick, 2002). 701

But the expression level of cyclins does not appear to be affected in rea1-ref 702

according to our trancriptome and translatome analysis. The target of 703

rapamycin (TOR) kinase is evolutionarily conserved among plant, yeast, and 704

animal cells, and is reported to integrate nutrient and energy signaling partly 705



22

through the phosphorylation of RPS6 to promote ribosome biogenesis, 706

polysome accumulation, translation initiation, cell growth and cell proliferation 707

(Xiong and Sheen, 2014). The transcription and translation level of TOR 708

signaling-related genes does not appear to be affected in rea1-ref, but there 709

might be an altered phosphorylation level of RPS6 or other post-translational 710

level regulation that is responsible for immediate transcriptional up-regulation 711

of genes in rea1-ref. The underlying mechanisms merit further explorations. 712

S phase is the period for DNA replication, histone synthesis and 713

nucleosome assembly. Nucleosome assembly is essential for a variety of 714

biological processes, such as cell cycle progression, development and 715

senescence (Gal et al., 2015). The synthesis of nucleosome assembly-related 716

proteins (histones and DNA replication-related enzymes) might be reduced to 717

decelerate the growth rate for survival under the suppressed ribosome 718

biogenesis condition in rea1-ref (Table 1&Figure 6). As a result, the 719

nucleosome assembly process during S phase would be dramatically 720

suppressed. The cell proliferation is slowed in rea1-ref (Figure 7), thus 721

together with impaired cell growth kernel and seedling development are 722

slowed for more than three days (Figure 1). 723

724

rea1-ref/dek* as a non-lethal maize small kernel mutant offered an 725

opportunity to explore comprehensive cellular responses to impaired 60S 726

ribosome biogenesis. Based on our results, we propose reduced 60S 727

ribosome biogenesis lead to differentially regulating the transcription and 728

translation of distinct groups of genes that affect translation efficiency and cell 729

proliferation (Figure 8). Firstly, there is increased efficiency of translation 730

initiation and ribosome usage. Secondly, there is selective translational 731

regulation of different groups of genes for intensive usage of quantitatively 732

limited mature ribosome. Finally, there is inhibited cell proliferation, leading to 733

slower growth and survival. 734

735

Materials and Methods 736

Plant Materials 737

The o*-N1117 mutant stock was obtained from the Maize Genetics Cooperation stock 738



23

center and identified as an EMS-induced allele of the opaque15 mutant. The dek* 739

mutation was separated from the o*-N1117 stock as an independent mutant. The dek* 740

mutant was crossed to the W64A inbred line and a F1 and F2 was produced to generate a 741

mapping population. All plants were cultivated in the field at the campus of Shanghai 742

University. Seeds were harvested at 5, 9, 13, 15, 17, 18, 21, 25 and 36 DAP. 743

744

Paraffin and resin sections 745

The 15 and 18 DAP embryos were fixed at 4°C overnight in FAA [ethanol 50% (v/v), acetic 746

acid 5.0% (v/v) and formaldehyde 3.7% (v/v)]. After embedding in paraffin, 10 μm 747

microtome sections on glass slides were dewaxed in xylene, rehydrated, and stained with 748

fuchsin. The 15 and 18 DAP endosperm tissues were fixed at 4°C overnight in FAA 749

[ethanol 50% (v/v), acetic acid 5.0% (v/v) and formaldehyde 3.7% (v/v)]. After embedding 750

in Spurr’s epoxy resin, thin sections (1μm) were heat fixed to glass slides and stained with 751

fuchsin. Stained sections were rinsed in water three times and air dried. Bright-field 752

photographs of the sections were taken using a Leica microscope. 753

754

Transmission Electron Microscopy 755

The 15 and 18 DAP kernels of rea1-ref and wild type were prepared according to Lending 756

and Larkins, (1992), with some modifications: kernels were fixed in paraformaldehyde and 757

post-fixed in osmium tetraoxide. After dehydration in an ethanol gradient, samples were 758

transferred to a propylene oxide solution and gradually embedded in acrylic resin (London 759

Resin Company). Sections (70 nm) were made with a diamond knife microtome (Reichert 760

Ultracut E). Sample sections were stained with uranyl acetate, post-stained with lead 761

citrate, and observed with a Hitachi H7600 transmission electron microscope. 762

763

Scanning Electron Microscopy 764

The first leaf mature region of 7 DAG rea1-ref and wild-type seedlings was fixed at 4°C 765

overnight in FAA [ethanol 50% (v/v), acetic acid 5.0% (v/v) and formaldehyde 3.7% (v/v)]. 766

Samples were critically dried and spray coated with gold. Gold-coated samples were then 767

observed with a scanning electron microscope (S3400N; Hitachi). 768

769

Protein Quantification 770

Mature kernels of rea1-ref and wild type were soaked in water and endosperm was 771

separated from the embryo and pericarp. Endosperm samples were critically dried to 772

constant weight, powdered in liquid N2, and measured according to (Wang et al., 2011). 773

Proteins were extracted from 50 mg of 3 pooled endosperm flour samples. Extracted 774

proteins were measured using a bicinchoninic acid protein assay kit (Pierce) according to 775

instructions. Measurements of all samples were replicated three times. 776



24

777

Measurement of starch 778

Mature kernels of rea1-ref and wild type were soaked in water, and endosperm was then 779

separated from the embryo and pericarp. Endosperm samples were dried to constant 780

weight, pulverized in liquid N2, and starch was extracted and measured using an 781

amyloglucosidase /α- amylase method starch assay kit (Megazyme) according to the 782

instructions adapted as: add 0.2 mL of aqueous ethanol (80 % v/v) to 100 mg sample and 783

aid dispersion; immediately add 3 mL of thermostable α-amylase. Incubate the tube in a 784

boiling water bath for 6 min; place the tube in a bath at 50°C; add 0.1 mL 785

amyloglucosidase; stir the tube on a vortex mixer and incubate at 50°C for 30 min; 786

transfer duplicate aliquots (0.1 mL) of the diluted solution to the bottom, add 3.0 mL of 787

GOPOD reagent and incubate the tubes at 50°C for 20 min; read the absorbance for each 788

sample, and the D-glucose control at 510 nm against the reagent blank. The percentage 789

of starch content in per mg dried sample was analyzed. 790

791

Soluble amino acids analysis 792

Soluble amino acids were analyzed according to (Holding et al., 2010): 3 mg samples 793

were refluxed for 24 hr in 6N HCl. Samples were hydrolyzed at 110℃ for 24 hr. Sample 794

hydrolysates were critically dried and dissolved in 10 ml of citrate buffer. The amino acids 795

were analyzed with a Hitachi-L8900 amino acid analyzer at Shanghai Jiaotong University. 796

On the wt and dek kernels analyses were replicated three times. 797

798

Map-Based Cloning 799

The Dek* locus was mapped using 864 individuals from a F2 mapping population of the 800

cross between the dek* and the W64A inbred line. For preliminary mapping, molecular 801

markers distributed throughout maize chromosome 6 were used. SSR 155.1M-1, 802

SSR153.7M-2, SSR154.7M-3, InDel438, InDel428, SNP064 and SNP165 (see 803

Supplemental Table 4 online) as additional molecular markers for fine mapping, were 804

developed to localize the Dek* locus to a 101.6 kb region. 805

806

RNA Extraction and real-time PCR Analysis 807

Total RNA was extracted with TRIzol reagent (Tiangen) and DNA was removed by a 808

treatment with RNase free DNase I (Takara). Using ReverTra Ace reverse transcriptase 809

(Toyobo), RNA was reverse transcribed to cDNA. Quantitative real-time PCR was 810

performed with SYBR Green Real-Time PCR Master Mix (Toyobo) using a Mastercycler 811

ep realplex 2 (Eppendorf) according to the standard protocol. Specific primers were 812

designed (see Supplemental Table 4 online) and the experiments were performed with 813

two independent RNA samples sets with ubiquitin as the reference gene. From a pool of 814



25

kernels collected from three individual plants, a RNA sample was extracted, for which 815

three technical replicates were performed. A final volume of 20 mL contained 1 mL 816

reverse transcribed cDNA (1 to 100 ng), 10 mL 23 SYBR Green PCR buffer, and 1.8 mL 817

10 mM/L forward and reverse primers for each sample. Relative quantifiable differences in 818

gene expression were analyzed as described previously (Livak and Schmittgen, 2001). 819

820

Fractionation of cytoplasmic and nuclear proteins 821

Pulverized tissue was hydrated in cold harvest buffer [10mM HEPES (PH 7.9), 50mM 822

NaCl, 0.5M sucrose, 0.1mM EDTA, 0.5% Triton X-100, 1mM DTT, 10mM tetratsodium 823

pyrophosphate, 100mM NaF, 17.5mM beta-glycrophosphate, 1mM PMSF, 4μg/ml 824

Aprotinin, 2μg/ml Pepstatin A ] incubated on ice for 5 min, and nuclei was pelleted (1,000 825

rpm, 10 min). After transfer of the supernatant to a new tube for extracting cytoplasmic 826

proteins, the pellet of nucleic was washed and resuspended by Buffer A [10mM HEPES 827

(PH7.9), 10mM KCl, 0.1mM EDTA, 0.1mM EGTA, 1mM DTT, 1mM PMSF, 4μg/ml 828

Aprotinin, 2μg/ml Pepstatin A] and pelleted again (1,000 rpm, 10 min). Nuclei were 829

washed and resuspended in Buffer C [10mM HEPES (PH7.9), 500mM NaCl, 0.1mM 830

EDTA, 0.1mM EGTA, 0.1% NP-40, 1mM DTT, 1mM PMSF, 4μg/ml Aprotinin, 2μg/ml 831

Pepstatin A] and vortexed (4℃, 15 min), pelleted again (14,000 rpm, 4℃, 10 min), and 832

transfered to a new tube for extracting nuclear proteins. 833

834

Polyclonal Antibodies 835

For anti-Rea1 antibody production, the 12,478-16,038 bp cDNA fragment was cloned into 836

pGEX-4T-1 (Amersham Biosciences), and GST–tagged fusion protein was purified with 837

the AKTA purification system (GE Healthcare) using a GSTrap FF column. Protein 838

expression and purification followed established procedures. Antibodies were produced in 839

rabbits according to standard protocols of Shanghai ImmunoGen Biological Technology. 840

For 22kD α-zein and 19kD α-zein antibody production, regions of low similarity of 22kD 841

α-zein and 19kD α-zein were selected according to a previous study (Woo et al., 2001). 842

The cDNAs responsible for selected polypeptides were cloned into pGEX-4T-1 843

(Amersham Biosciences), and GST–tagged fusion protein was purified with the AKTA 844

purification system (GE Healthcare) using a GSTrap FF column. Protein expression and 845

purification followed established procedures. Antibodies were produced in rabbits 846

according to standard protocols of Shanghai ImmunoGen Biological Technology. 847

848

Immunoblot Analysis 849

Proteins extracted from rea1-ref and wild type mature kernels were separated by 850

SDS-PAGE. Separated protein samples were then transferred to polyvinylidene difluoride 851

membrane (0.45 mm; Millipore). The membrane with a protein sample attached on it was 852



26

incubated with primary and secondary antibodies. Using the Super Signal West Pico 853

chemiluminescent substrate kit (Pierce) the signal was visualized according to the 854

manufacturer’s instructions. The purified anti-Rea1 antibody was used at 1: 500; the 22kD 855

α-zein and 19kD α-zein antibodies were used at 1: 5000; the α-tubulin antibody 856

(Sigma-Aldrich) was used at 1: 5000; the BIP (at-95) antibody (Santa Cruz Biotechnology), 857

Histone antibody (Cell signaling), eRPL13 antibody (Agrisera), eIF2α antibody (Cell 858

signaling), and P- eIF2α antibody (Cell signaling) were used at 1: 1000, and the TBP 859

antibody (Santa Cruz Biotechnology), eRPS14 antibody (Santa Cruz Biotechnology), and 860

eEF1α antibody (Santa Cruz Biotechnology) were used at 1:500. 861

862

Phylogenetic Analysis 863

Related sequences were identified in the NCBI nr (nonredundant protein sequences) 864

database by performing a BLASTp search with ZmRea1 protein sequences. Amino acid 865

sequences were aligned with the MUSCLE method in the MEGA5.2 software package 866

using their default settings for protein multiple alignment. A rooted phylogenetic tree of 867

Rea1 from maize, Brachypodium distachyon, Triticum, Oryza sativa, Setaria, Arabidopsis 868

thaliana, Populus, Glycine-max, Dictyostelium, Monodelphis domestica, Saprelegnia, 869

Mortierella, and Saccharomyces Cerevisiae was constructed by the neighbor-joining 870

method using the MEGA5.2 software package. The evolutionary distances were 871

computed using the Poisson correction analysis. 872

873

RNA-seq Analysis 874

Total RNA (10 μg) was extracted from endosperm of rea1-ref and wild type kernels 875

harvested at 15 DAP, and three rea1-ref or wild type biological samples were pooled 876

together. The poly-A selected RNA-Seq library was prepared according to Illumina 877

standard instruction (TruSeq Stranded RNA LT Guide). Library DNA was checked for 878

concentration and size distribution in an Agilent2100 bioanalyzer before sequencing with 879

an Illummina HiSeq 2500 system according to the manufacturer’s instructions (HiSeq 880

2500 User Guide). Single-end reads were aligned to the maize B73 genome build Zea 881

mays AGPv2.15 using TopHat 2.0.6 (Langmead et al., 2009). Data were normalized as 882

fragments per kilobase of exon per million fragments mapped (FPKM), for the sensitivity 883

of RNA-seq depends on the transcript length. Significant differentially transcribed genes 884

(DTGs) were identified as those with a fold change and P-value of differential expression 885

above the threshold (Fold change>2.0, P<0.05). 886

887

Ribosome profile and isolation of polysomal RNA 888

For the ribosome profile, approximately 2.5ml of pulverized tissue (approx. twenty 15 DAP 889

kernels) was hydrated in two volumes of polysome extraction buffer (PEB) [200mM 890



27

Tris–HCl (pH 9.0), 200mM KCl, 25mM EGTA, 35mM MgCl2, 1% (w/v) Brij-35, 1% (v/v) 891

Triton X-100, 1 % (v/v) Tween-20, 1% (v/v) Igepal CA–630, 1% (w/v) deoxycholic acid, 1% 892

(v/v) polyethylene-10-tridecylether, 1mM Phenylmethylsulfonyl fluoride (PMSF), 0.5mg/ml 893

heparin, 5mM dithiothreitol (DTT), 50 mg/ml cycloheximide, 50 mg/ml chloramphenicol] 894

(Kawaguchi et al., 2004), homogenized, filtered through two layers of sterile Miracloth 895

(Calbiochem, La Jolla, CA), and cleared by centrifugation (16,000 g, 4℃, 15 min). Four 896

hundred A260 units of the supernatant was layered over a 15–45% (w/v) sucrose density 897

gradient, centrifuged (237,000 g, 2.5h, at 4℃, Beckman Optima™ L-100 XP) and the 898

A254 nm absorbance profile was recorded with chart recorder by using a gradient 899

fractionator connected to a UA-5 detector (BIOCOMP，Canada) as described previously 900

(Kawaguchi et al., 2003, 2004). Two independent biological replicates were performed. 901

For isolation of polysomal RNA, approximately 5 ml of pulverized tissue powder 902

(approx. forty 15 DAP kernels) was hydrated in two volumes of PEB, homogenized, 903

filtered through two layers of sterile Miracloth (Calbiochem, La Jolla, CA), and cleared by 904

centrifugation (16,000 g, 4℃, 15 min). The supernatant was layered over a 1.75 M 905

sucrose cushion [400mM Tris–HCl (pH 9.0), 200mM KCl, 30mM MgCl2, 1.75 M sucrose, 906

5mM DTT, 50 mg/ml chloramphenicol, 50 mg/ml cycloheximide], and centrifuged at 907

170,000 g, at 4 ℃ for 3 h (modified from Fennoy and Bailey-Serres, 1995). The polysome 908

pellet was washed with sterile water and resuspended in 700 μl PEB lacking heparin and 909

detergents. Total or polysome-bound RNA was precipitated from total supernatant or the 910

ribosome fraction of the same amount of sample powder, by addition of 2.5 vol of 8 M 911

guanidine chloride and 3.5 vol of 99% (v/v) ethanol, and extracted by use of Qiagen Plant 912

RNeasy mini kit (Qiagen, Valencia, CA, USA) according to the manufacturer’s protocol. 913

For negative control, same amount of pulverized tissue powder was hydrated in two 914

volumes of PEB buffer with 2mM puromycin. 915

The polysome-bound/total RNA value for individual genes was determined from the 916

ratio of the signal in the polysome RNA sample divided by the signal in the total RNA 917

sample. Due to the required use of an equal RNA quantity in each RNA-Seq reaction, in 918

spite of the unequal proportion of RNA in the polysome fraction under the two conditions, 919

it was necessary to normalize the signal values obtained for polysome RNA. 920

Normalization was performed according to Branco-Price et al., 2005. Polysomes 921

accounted for 57.2% and 40.2% of the total absorbance in rea1-ref and wild type kernels, 922

respectively. The percentage of an individual mRNA species in polysomes was calculated 923

as, 2nP/T (normalized polysome-bound/total)×100%. 924

Normalized polysome-bound/total in rea1-ref: 925

926



28

Normalized polysome-bound/total in wild type: 927

928 929

FCM Detection 930

For extraction of nuclei, endosperm and seedling tissues were finely chopped with a sharp 931

razor blade in Beckman lysis buffer. The resulting slurry was filtered through a 30 μm 932

nylon filter to eliminate cell debris and the suspension containing nuclei was immediately 933

measured using an Accuri C6 (BD) flow cytometer equipped with an argon-ion laser tuned 934

at a wavelength of 488 nm. For each sample, at least 15,000 nuclei were collected and 935

analyzed using a logarithmic scale display. Each flow cytometric histogram was saved 936

and analyzed using BD Accuri C6 Software 1.0.264.21. 937

938

Accession numbers 939

Sequence data from this article can be found in the GenBank/EMBL data libraries under 940

the following accession numbers: Zm Rea1, KP137367; Zm BIP1, NM_001112423, 941

GRMZM2G114793; Zm eRPS6, NM_001112164, GRMZM5G851698; Zm eEF1α, 942

NM_001112117, GRMZM2G153541; Zm Histone H4, NM_001138113, 943

GRMZM2G084195; Zm DNA polymerase epsilon subunit 2, NM_001153609, 944

GRMZM2G154267, Zm MCM6, NM_001111819, GRMZM2G021069. RNA-seq data is 945

available from the National Center for Biotechnology Information Gene Expression 946

Omnibus (www.ncbi.nlm. nih.gov/geo) under the series entry GSE67103. 947

948

Supplemental data 949

The following materials are available in the online version of this article. 950

Supplemental Figure 1, SDS–PAGE analysis of total (A), zein (B), and nonzein (C) 951

proteins from dek*/ rea1-ref and WT mature endosperm. 952

Supplemental Figure 2, Comparison of total starch content and the percentage of 953

amylose in wild type and rea1-ref mature endosperm. 954

Supplemental Figure 3, Phenotype of rea1-ref and WT plants (90 DAG). 955

Supplemental Figure 4, Ultrastructure of developing endosperms of wild type and 956

rea1-ref (15 DAP and 18 DAP). 957

Supplemental Figure 5, qRT-PCR confirmation of DTRs with increased or decreased 958

translation level. 959

Supplemental Table 1, Gene ontology classifications of DTGs with functional annotation. 960

Supplemental Table 2. Gene ontology classifications of DTRs with functional annotation. 961

Supplemental Table 3, Sequence feature analysis of DTRs. 962

Supplemental Table 4, Primers used in these experiments. 963



29

964

Acknowledgements 965

This work was supported by the Major Research plan of the National Natural Sciences 966

Foundation of China (91335208 and 31425019), and the Ministry of Science and 967

Technology of China (2014CB138204). We thank Dr.Yuanyuan Ruan (Fudan University) 968

for technical support on ribosome profile experiment and Dr. Brian A. Larkins (University 969

of Nebraska, Lincoln) for critical reading the article. 970

971

Author contributions 972

R.S., W.Q., and J.Z. designed the experiment. J.Z., W.Q., Qiao.W., Qun.W., X.L., D.Y., 973

and Y.J. performed the experiments. W.Q., J.Z. Gang. W., Gui. W. and R.S. analyzed the 974

data. W.Q. and R.S. wrote the article. 975

976

Tables 977

Table 1. Ten most strongly up-regulated or down-regulated DTRs of each Gene 978

ontology classification. 979

GO ID P-value Gene Description Polysome/Total

in WT Polysome/Total

in rea1 Fold

change Genes with increased ratio of polysome-bound mRNA (% of total)

GO:0045449

Regulation of

transcription

1.33E-03 GRMZM2G081930 NAC1 0.1437 0.6978 4.86

GRMZM2G167018 NAC domain transcription factor 0.0336 0.3461 10.31

GRMZM2G134717 NAC domain transcription factor 0.0291 0.2145 7.36

GRMZM2G170079 BZIP-type transcription factor 0.0165 0.1979 12.03

GRMZM5G812272 WRKY DNA-binding domain

superfamily protein 0.0106 0.1038 9.76

GRMZM2G327059 BEL1-related homeotic protein 0.0316 0.2861 9.05

GRMZM2G021339 leucine zipper domain protein 0.0158 0.1272 8.07

GRMZM2G126239 Homeobox-leucine zipper protein

ATHB-4 0.0142 0.2754 19.38

GRMZM2G087741 Homeobox protein liguleless 3 0.0480 0.3018 6.29

GRMZM5G809195 IAA14-auxin-responsive Aux/IAA

family member 0.0451 0.4536 10.06

GO:0045735

Nutrient reservoir

activity

3.51E-12 GRMZM2G346897 22kD alpha zein 0.2875 0.7691 2.68

GRMZM2G353272 22kD alpha zein 0.2442 0.9829 4.03




30



GRMZM2G008341 Zein-alpha 19kD z1A 0.2862 0.9428 3.29

GRMZM2G353268 Zein-alpha 19kD z1A 0.2504 0.8631 3.45

AF546188.1_FG003 Zein-alpha 19kD z1B 0.2120 0.7470 3.52

AF546188.1_FG007 Zein-alpha 19kD z1B 0.2578 0.8318 3.23

AF546187.1_FG007 Zein-alpha 19kD z1D 0.2429 0.9263 3.81

GO:0006414

Translational

elongation

1.17E-07 GRMZM5G859846 Elongation factor Tu 0.0476 0.1744 3.67

GRMZM2G007038 Elongation factor Tu 0.2158 0.6634 3.07

GRMZM2G407996 Elongation factor Tu 0.3131 0.6392 2.04

GRMZM2G110509 Elongation factor 1-alpha 0.1984 0.4218 2.13



Genes with reduced ratio of polysome-bound mRNA (% of total) GO:0006334

Nucleosome

assembly

6.59E-10 GRMZM5G883764 Histone H2A 0.5549 0.0717 0.13

GRMZM2G355773 Histone H3.2 0.9458 0.0945 0.09

GRMZM2G447984 Histone H3.2 0.8418 0.1126 0.13

GRMZM2G130079 Histone H3.2 0.6460 0.0847 0.13

GRMZM2G349651 Histone H4 0.7069 0.0850 0.12

GRMZM2G073275 Histone H4 0.5894 0.0784 0.13

GRMZM2G479684 Histone H4 0.9550 0.1012 0.11

GRMZM2G084195 Histone H4 0.3357 0.0266 0.08

GRMZM2G421279 Histone H4 0.9435 0.1030 0.11

GRMZM2G149178 Histone H4 0.5823 0.0750 0.13

GO:0006260

DNA replication 1.18E-03 GRMZM5G825512 Origin recognition complex subunit 6 0.4301 0.1093 0.25

GRMZM5G872710 DNA polymerase 0.4674 0.1236 0.26

GRMZM2G154267 DNA polymerase epsilon subunit 2 0.7544 0.0657 0.09

GRMZM2G100639 DNA replication licensing factor

MCM3 homolog 2 0.6059 0.0796 0.13

GRMZM2G117238 Origin recognition complex subunit 2 0.6233 0.1285 0.21

GRMZM2G162445 mini-chromosome maintenance

(MCM) complex protein family 0.8304 0.0891 0.11

GRMZM2G086934 Replication protein A 70 kDa

DNA-binding subunit 0.5513 0.1185 0.22

GRMZM2G021069 Minichromosome maintenance

protein 0.7020 0.0859 0.12

GRMZM2G108712 Proliferating cell nuclear antigen 0.8651 0.1292 0.15

GRMZM2G304362 Ribonucleoside-diphosphate

reductase 0.6543 0.0827 0.13



31

GO:0033279

Ribosomal subunits 1.16E-03 GRMZM2G099352 40S ribosomal protein S3 0.3527 0.1547 0.44

GRMZM2G078985 40S ribosomal protein S5 0.3491 0.1649 0.47






GRMZM5G868433 60S ribosomal protein L7-2 0.5257 0.2523 0.48

GRMZM2G119169 60S ribosomal protein L17 0.3371 0.1421 0.42

GRMZM2G091921 60S ribosomal protein L32 0.5604 0.2650 0.48

980

Figure legends 981

Figure 1. Phenotypic features of maize dek*/rea1-ref mutants. 982

A. A 15 DAP F2 ear of dek* ×W64A and randomly selected 15 DAP dek* and wild type 983

(WT) kernels in segregated F2 population, red arrow identifies the dek* kernel, Bar = 984

5mm. 985

B. Mature F2 ear of dek*×W64A and randomly selected mature dek* and WT kernels in 986

segregated F2 population, red arrow identifies the dek* kernel, Bar = 5mm. 987

C. Comparison of 100-grain weight of randomly selected mature dek* and WT kernels in 988

segregated F2 population. Values are the mean values with standard errors, n= 3 989

individuals (***P<0.001, Student’s t-test). 990

D. Comparison of total, zein, and nonzein proteins from dek* and WT mature endosperm. 991

The measurements were done on per mg of dried endosperm. Values are the mean 992

values with standard errors, n= 3 individuals (ns refers to not significant, **P<0.01, 993

Student’s t-test). 994

E. The soluble amino acids with different content in dek* and WT mature endosperm. 995

Values are the mean values with standard errors, n= 3 individuals (*P<0.05, **P<0.01, 996

***P<0.001, Student’s t-test). 997

F. Paraffin sections of 15 DAP and 18 DAP dek* and WT embryo. Bars = 200μm. 998

G. Microstructure of developing endosperms of dek* and WT (15 DAP and 18 DAP), SG, 999

starch granule. Bars = 100μm. 1000

H. Phenotype of dek* and WT seedlings (4 DAG and 7 DAG). Bar = 5 cm. 1001

1002

Figure 2. Map-based cloning and identification of Rea1. 1003

A. The Dek* locus was mapped to a 101.6kb region between molecular markers SNP064 1004

and SNP165 on chromosome 6, which contained four candidate genes. See 1005

Supplemental Table 3 online for primer information. 1006

B. Protein structure of ZmRea1 and mutation sites in the ZmRea1 gene. 1007



32

C.Heterozygous rea1-ref / dek* and rea1-Mu were used in allelism test because 1008

homozygous rea1-Mu were lethal. Top, heterozygous rea1-ref X heterozygous rea1-Mu; 1009

Middle, heterozygous rea1-Mu X heterozygous rea1-ref; Bottom, heterozygous rea1-Mu X 1010

heterozygous rea1-Mu. Red arrows identify the rea1 kernel. 1011

D. qRT-PCR comparing expression level of ZmRea1 gene in the 15 DAP and 18 DAP 1012

rea1-ref and WT kernels. Ubiquitin was used as internal control. Values are the mean 1013

values with standard errors, n= 3 individuals (***P<0.001, Student’s t-test). 1014

E. Dot-immunoblot comparing accumulation of ZmRea1 protein in the 15 DAP and 18 1015

DAP rea1-ref and WT kernels. 720 ng, 360 ng and 180 ng 15 DAP and 18 DAP rea1-ref 1016

and WT kernel proteins were subjected to immunoblot analysis with antibodies against 1017

ZmRea1. 1018

1019

Figure 3. Phylogenetic analysis, expression pattern and sub-cellular localization of 1020

ZmRea1. 1021

A. Phylogenetic relationships of ZmRea1 and its homologs. Maize Rea1 and identified 1022

Rea1 proteins in Brachypodium distachyon, Triticum, Oryza sativa, Setaria, Arabidopsis 1023

thaliana, Populus, Glycine-max, Dictyostelium, Monodelphis domestica, Saprelegnia, 1024

Mortierella, and Saccharomyces Cerevisiae were aligned by MUSCLE method in MEGA 1025

5.2 software package. The phylogenetic tree was constructed using MEGA 5.2. The 1026

numbers at the nodes represent the percentage of 1000 bootstraps. 1027

B. RNA expression level of ZmRea1 in various tissues. Ubiquitin was used as an internal 1028

control. Representative results from two biological replicates are shown. For each RNA 1029

sample, three technical replicates were performed. Values are the mean values with 1030

standard errors, n= 6 individuals. 1031

C. Expression profiles of ZmRea1 during maize kernel development. Ubiquitin was used 1032

as an internal control. Representative results from two biological replicates are shown. For 1033

each RNA sample, three technical replicates were performed. Values are the mean 1034

values with standard errors, n= 6 individuals. 1035

D, Dot-immunoblot analysis of ZmRea1 protein accumulation. Rea1 is predominantly 1036

associated with the nuclear protein fraction. 720 ng, 360 ng and 180 ng nuclear (Histone 1037

as nuclear marker) and cytoplasmic (Bip as cytoplasm marker) fraction proteins were 1038

subjected to immunoblot analysis with antibodies against ZmRea1. 1039

1040

Figure 4. Production of mature 60S subunits is reduced in rea1-ref kernels. 1041

A. Analysis of ribosome profiles (A254 nm) was performed by sedimentation 1042

centrifugation in 15-45% sucrose density gradients: 40 S, 60 S, 80 S ribosomes and 1043

polysomes are indicated. 1044

B. Immunoblot analysis of ribosome proteins accumulated in nuclear and cytoplasmic 1045



33

fractions. Nuclear and cytoplasmic fraction proteins of 15 and 18 DAP rea1-ref and wild 1046

type kernels were subjected to immunoblot analysis with antibodies against eRPL13 (60S 1047

ribosomal subunit marker), eRPS14 (40S ribosomal subunit marker), Bip (cytoplasm 1048

marker), Histone (nuclear marker), Tubulin (cytoplasm sample loading control), and TBP 1049

(nuclear sample loading control). 1050

C. Ultrastructure of developing endosperms of wild type and rea1-ref (15 DAP) for nucleus 1051

observation. There was nucleolus stress, as shown by the expended nucleolus in rea1-ref. 1052

Bars = 2μm. NL, Nucleolus; NP, Nucleoplasm; SG, Starch granule. The nucleolus size/ 1053

nucleus size measurements were done on TEM results. Values are the mean values with 1054

standard errors, n= 10 individuals (**P<0.01, Student’s t-test). 1055

1056

1057

Figure 5, GO classification for genes with altered expression in rea1-ref kernels. 1058

A. The most significantly related GO terms of the 828 functional annotated DTGs. The 1059

significance and number of genes classified within each GO term is shown. 1060

B. qRT-PCR confirmation of DTGs associated with each category, including small 1061

ribosomal subunit proteins (GRMZM5G851698, GRMZM2G120432, GRMZM2G130544, 1062

GRMZM2G156110, GRMZM2G151252); large ribosomal subunit proteins 1063

(GRMZM2G132968, GRMZM2G100403, GRMZM2G168330, GRMZM2G030731, 1064

GRMZM2G010991); ribosome biogenesis factors (GRMZM2G063700, 1065

GRMZM2G110233, GRMZM2G468932); 60S acidic ribosomal proteins 1066

(GRMZM2G157443, GRMZM2G077208); translation elongation factors 1067

(GRMZM2G151193, GRMZM2G153541, GRMZM2G122871, GRMZM2G029559); 1068

histones (GRMZM2G056231, GRMZM2G401147, GRMZM2G078314, 1069

GRMZM2G479684, GRMZM2G164020); nucleosome assembly protein 1070

(GRMZM2G176707); nutrient reservoir activity (GRMZM2G346897, GRMZM2G059620, 1071

GRMZM2G138727). Ubiquitin was used as an internal control. Values are the mean 1072


1074

Figure 6. Induced general translation efficiency and specific regulation of 1075

translation of individual mRNAs in rea1-ref kernels. 1076

A. Immunoblot comparing the phosphorylated eIF2α accumulation in wild type and 1077

rea1-ref kernels (15 DAP and18 DAP). Anti- eIF2α was used as control. And immunoblot 1078

comparing the accumulation of eEF1αin wild type and rea1-ref kernels at the same stage. 1079

Anti-Tub was used as sample loading control. 1080

B and C. qRT-PCR confirmation of DTRs with increased or decreased translation level: 1081

DTRs with increased translation level (GRMZM2G081930, GRMZM2G007038, 1082

GRMZM2G110509) and DTRs with decreased translation level (GRMZM2G084195, 1083



34

GRMZM2G154267, GRMZM2G021069). Samples were mRNA preps from the polysome 1084

fractions. Ubiquitin was used as an internal control. Values are the mean values with 1085

standard errors, n= 6 individuals (*P<0.05, **P<0.01, Student’s t-test). 1086

D. Immunoblot comparing the accumulation of 22kD and 19kD α-zein in 470 ng and 1,190 1087

ng total protein of 15 DAP rea1-ref and wild-type kernels by protein gel blot analysis with 1088

22kD and 19kD α-zein specific antibodies. 1089

E. The overlap between transcriptional up-regulated genes and translational 1090

down-regulated genes for ribosomal proteins and histones, and the overlap between 1091

transcriptional down-regulated genes and translational up-regulated genes for zeins. 1092

1093

Figure 7. Evidence of inhibited cell proliferation and cell growth in rea1-ref kernels. 1094

A and B. Cell proliferation analysis of 15 DAP and 18 DAP endosperms of the wild type 1095

and rea1-ref. The small graph inserted is the cell cycle diagrams analyzed by flow 1096

cytometry. The 3C and 6C are DNA contents of the nuclei at stage G1 and S phase of 15 1097

DAP and 18 DAP endosperms. The 12C and 24C are DNA contents of endoreduplicated 1098

nuclei at stage S phase of 15 DAP and 18 DAP endosperms. For each sample, three 1099

independent biological replicates were performed. Values are the mean values with 1100

standard errors, n= 3 individuals (**P<0.01, ***P<0.001, Student’s t-test). 1101

C. Cell proliferation analysis of 7 DAG seedlings of the wild type and rea1-ref. The small 1102

graph inserted is the cell cycle diagrams analyzed by flow cytometry. The 2C and 4C are 1103

DNA contents of the nuclei at stage G1/S phase and G2/M phase of 7 DAG seedlings. For 1104

each sample, three independent biological replicates were performed. Values are the 1105

mean values with standard errors, n= 3 individuals (**P<0.01, Student’s t-test). 1106

D. Scanning electron microscopy analysis of the lower epidermis of the first leaf mature 1107

region of 7 DAG rea1-ref and wild-type seedlings. Bars = 50μm. S,stoma. 1108

E. Comparison of cell width and cell length of lower epidermis in wild type and rea1-ref 7 1109

DAG seedlings. The measurements were done on SEM results. Values are the mean 1110


1112

Figure 8. Suppressed 60S ribosome biogenesis promotes translation initiation and 1113

ribosome usage, as well as inconsistently regulates the transcription and 1114

translation of individual genes that affects general translation efficiency and cell 1115

proliferation. 1116

1117

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

http://scholar.google.com/scholar?as_q=The AAA ATPase Rix7 powers progression of ribosome biogenesis by stripping Nsa1 from pre-60S particles, J&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://scholar.google.com/scholar?as_q=Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.&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=Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Langmead&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

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http://search.crossref.org/?page=1&rows=2&q=Lending CR, Larkins BA (1992) Effect of the floury-2 locus on protein body formation during maize endosperm development. Protoplasma 171: 123-133

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http://scholar.google.com/scholar?as_q=Effect of the floury-2 locus on protein body formation during maize endosperm development&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=Effect of the floury-2 locus on protein body formation during maize endosperm development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lending&as_ylo=1992&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Proc%2E Natl%2E Acad%2E Sci%2E USA%5BTitle%5D%29 AND 99%5BVolume%5D AND 5460%5BPagination%5D AND Lid SE%2C Gruis D%2C Jung R%2C Lorentzen JA%2C Ananiev E%2C Chamberlin M%2C Niu X%2C Meeley R%2C Nichols S%2C Olsen OA%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Lid SE, Gruis D, Jung R, Lorentzen JA, Ananiev E, Chamberlin M, Niu X, Meeley R, Nichols S, Olsen OA (2002) The defective kernel 1 (dek1) gene required for aleurone cell development in the endosperm of maize grains encodes a membrane protein of the calpain gene superfamily. Proc. Natl. Acad. Sci. USA 99, 5460-5465

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

http://scholar.google.com/scholar?as_q=The defective kernel 1 (dek1) gene required for aleurone cell development in the endosperm of maize grains encodes a membrane protein of the calpain gene superfamily&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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Zhang Y, Paschold A, Marcon C, Liu S, Tai H, Nestler J, Yeh CT, Opitz N, Lanz C, Schnable PS, Hochholdinger F (2014) The Aux/IAAgene rum1 involved in seminal and lateral root formation controls vascular patterning in maize (Zea mays L.) primary roots J ExpBot. 65:4919-30



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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Oncogene%5BTitle%5D%29 AND 18%5BVolume%5D AND 6112%5BPagination%5D AND Williams BRG%5BAuthor%5D&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28The Role of Target of Rapamycin Signaling Networks in Plant Growth and Metabolism%5BTitle%5D%29 AND 164%5BVolume%5D AND 499%5BPagination%5D AND Xiong Y%2C Sheen J%5BAuthor%5D&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Analysis of Genome%2DWide Changes in the Translatome of Arabidopsis Seedlings Subjected to Heat Stress%2E%5BTitle%5D%29 AND Y�ng�ez E%2C Castro%2DSanz AB%2C Fern�ndez%2DBautista N%2C Oliveros JC%2C Castellano MM%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=Analysis of Genome-Wide Changes in the Translatome of Arabidopsis Seedlings Subjected to Heat Stress.&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 Genome-Wide Changes in the Translatome of Arabidopsis Seedlings Subjected to Heat Stress.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Y�ng�ez&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28J%2E Exp%2E Bot%5BTitle%5D%29 AND 59%5BVolume%5D AND 3131%5BPagination%5D AND Zhang Y%2C Wang Y%2C Kanyuka K%2C Parry MAJ%2C Powers SJ%2C Halford NG%5BAuthor%5D&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28 primary roots J Exp Bot%5BTitle%5D%29 AND 65%5BVolume%5D AND 4919%5BPagination%5D AND Zhang Y%2C Paschold A%2C Marcon C%2C Liu S%2C Tai H%2C Nestler J%2C Yeh CT%2C Opitz N%2C Lanz C%2C Schnable PS%2C Hochholdinger F%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=The Aux/IAA gene rum1 involved in seminal and lateral root formation controls vascular patterning in maize (Zea mays 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 Aux/IAA gene rum1 involved in seminal and lateral root formation controls vascular patterning in maize (Zea mays L&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1


1 running title: characterization of maize rea1 mutant 2dec 08, 2015 · rea1 is an aaa-atpase that...

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