running title: cloning of a kernel size qtl in maize · 81 in one large-scale qtl study in maize,...

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Running Title: Cloning of a kernel size QTL in maize 1

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Correspondence to: Jianbing Yan (email: [email protected]) and David Jackson 3

([email protected]) 4

Tel: +86 27 87280110 5

National Key Laboratory of Crop Genetic Improvement, No.1 Shizishan Street, Hongshan 6

District, Wuhan, Hubei 430070, China. 7

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Article title 9

qKW9 encodes a pentatricopeptide repeat protein affecting photosynthesis and grain filling in 10

maize 11

Authors 12

Juan Huang1, Gang Lu1, Lei Liu1,2, Mohammad Sharif Raihan1, Jieting Xu1,3, Liumei Jian1, 13

Lingxiao Zhao4,5, Thu M. Tran2,6, Qinghua Zhang1, Jie Liu1, Wenqiang Li1, Cunxu Wei4, David 14

M. Braun6, Qing Li1, Alisdair R. Fernie7, David Jackson1,2,*, Jianbing Yan1,* 15

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1National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, 17

Wuhan 430070, China 18

2Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA. 19

3Wimi Biotechnology Co., Ltd, 4th Floor, Kejizhuanhua building, No. 3 Meishan Road, 20

Xinbei District, Changzhou City, Jiangsu Province, China 21

4Jiangsu Key Laboratory of Crop Genetics and Physiology, Co-Innovation Center for Modern 22

Production Technology of Grain Crops, Yangzhou University, Yangzhou 225009, China 23

5Jiangsu Xuzhou Sweetpotato Research Center, Xuzhou, Jiangsu, China 24

6Division of Biological Sciences, Interdisciplinary Plant Group, Missouri Maize Center, 25

University of Missouri, Columbia, MO 65211, USA 26

7Department of Molecular Physiology, Max-Planck-Institute of Molecular Plant Physiology, 27

Am Mühlenberg 1, 14476 Potsdam-Golm, Germany 28

.CC-BY-NC-ND 4.0 International licenseis made available under aThe copyright holder for this preprint (which was not peer-reviewed) is the author/funder. It. https://doi.org/10.1101/847145doi: bioRxiv preprint

https://doi.org/10.1101/847145

http://creativecommons.org/licenses/by-nc-nd/4.0/

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One sentence summary 30

A pentatricopeptide repeat protein exerts quantitative effect on maize kernel weight and size 31

by affecting photosynthesis and grain filling. 32

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Funding information 34

This work was supported by the National Key Research and Development Program of China 35

(2016YFD0100303), the National Natural Science Foundation of China (31525017, 36

31961133002), and NSF grant IOS-1546837 to DJ; Juan Huang was sponsored by China 37

Scholarship Council to visit Cold Spring Harbor Laboratory and study in Prof. David Jackson’s 38

lab from March 2018 to March 2019 (File No. 201706760027). 39

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Author Contributions 41

J.Y. designed and supervised this study. D.J. supervised the study in US side. J.H., G.L., and 42

T. T finished most of the mentioned experiments. Lei. L conducted RNA sequence data 43

analysis. M. S. R. and Jie. L involved in the initial QTL mapping. J.H., G.L. and W. L. 44

performed the field experiments. J.X. and L.J. conducted the transgenic transformation. L.Z. 45

and C.W. performed cytological experiments. Q.Z. constructed the RNA sequencing library 46

and finished the sequencing. J.H., D.B., Q.L., A.F., D.J., and J.Y. contribute a lot of 47

constructive discussions and wrote or revised the manuscript. 48

Competing financial interests 49

The authors declare no competing financial interests. 50

Abstract (<250 words) 51

Kernel weight is an important yield component in maize that was selected during 52

domestication. Many kernel weight genes have been identified through mutant analysis, and 53

are mostly involved in the biogenesis and functional maintenance of organelles or other 54

fundamental cellular activities. However, only a limited number of loci underlying quantitative 55

variation in kernel weight have been cloned. Here we characterize a maize kernel weight QTL, 56


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qKW9 and find that it encodes a DYW motif pentatricopeptide repeat protein involved in 57

C-to-U editing of NdhB, a subunit of the chloroplast NADH dehydrogenase-like complex. In a 58

null qKW9 background, C-to-U editing of NdhB was abolished, and photosynthesis was 59

reduced, suggesting that qKW9 regulates kernel weight by controling the maternal source of 60

photosynthate for grain filling. Characterization of qKW9 highlights the importance of 61

optimizing photosynthesis on maize grain yield production. 62

Keywords 63

Kernel weight; maize yield; QTL; photosynthesis; Cyclic electron transport; C-to-U editing; 64

NDH complex 65

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INTRODUCTION 67

Maize (Zea mays) is one of the most important crops in the world, producing grain vital for 68

our survival. Along with population growth, environmental deterioration, the decline of arable 69

land and climate change challenge us to increase maize grain production. Therefore, the 70

improvement of maize yield is of great importance to the sustainable development of human 71

society. 72

The grain yield of maize is comprised of several components, including ear number per 73

plant, kernel number per cob, and kernel weight. As an essential yield component, kernel 74

weight is positively correlated with yield, and is determined during development by kernel 75

size and the degree of kernel filling (Scanlon and Takacs, 2009). To dissect the genetic 76

architecture of maize kernel weight, numerous studies have identified hundreds of 77

quantitative trait loci (QTL) for kernel traits (www.maizegdb.org/qtl). However, only a few 78

kernel size QTL have been cloned and studied, and some maize kernel weight genes have 79

been identified as homologs of rice genes(Li et al., 2010a; Li et al., 2010b; Liu et al., 2015). 80

In one large-scale QTL study in maize, 729 QTL regulating kernel weight-related traits were 81

identified, and 24 of 30 genes were in, or tightly linked to, 18 rice grain size genes, suggesting 82

conserved genetic architecture of kernel weight(Liu et al., 2017b). One example is teosinte 83

glume architecture1 (tga1), the causal gene underlying the change from encased kernels in 84


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the wild progenitor teosinte to naked kernels in maize(Wang et al., 2005; Wang et al., 2015). 85

Reducing expression of tga1 in maize by RNAi greatly increases kernel size and weight, 86

suggesting that the removal of glumes from teosinte could release growth constraints, and 87

provide more space to allow larger kernels to develop (Wang et al., 2015). Another kernel 88

size gene, ZmSWEET4c, affects kernel weight in a different manner, with its product 89

mediating sugar transport across the basal endosperm transfer cell layer, and shows signals of 90

selection during domestication (Sosso et al., 2015). Recently a further gene, BARELY ANY 91

MERISTEM1d (ZmBAM1d) was identified as an additional QTL responsible for kernel weight 92

variation in maize (Yang et al., 2019). 93

Despite limited progress on our understanding of the quantitative variation in maize 94

kernel weight, numerous kernel mutants have been identified (Neuffer and Sheridan, 1980; 95

Clark and Sheridan, 1991). These mutants have been grouped into three categories: (i) 96

defective kernel (dek) mutations, including empty pericarp (emp) mutants that affect both 97

endosperm and embryo; (ii) embryo-specific (emb) mutations with healthy endosperm 98

formation; and (iii) endosperm-specific mutations (McCarty, 2017). Mutants in categories i 99

and ii have detrimental effects, leading to significant loss of kernel weight. Several of these 100

maize kernel development genes have been identified. For instance, EMP10(Cai et al., 2017), 101

EMP11 (Ren et al., 2017), EMP12 (Sun et al., 2019), EMP16 (Xiu et al., 2016), DEK35 (Chen 102

et al., 2017), and DEK37 (Dai et al., 2018) are involved in intron splicing of mitochondrial 103

genes. In contrast, MPPR6 functions in maturation and translation initiation of mitochondrial 104

ribosomal protein subunit mRNA(Manavski et al., 2012). Mutations of these genes impair 105

mitochondral function, leading to defective kernels. Other genes, including EMP7 (Sun et al., 106

2015), DEK10 (Qi et al., 2017), DEK39 (Li et al., 2018), PPR2263/MITOCHONDRIAL 107

EDITING FACTOR29 (Sosso et al., 2012), and SMALL KERNEL1 (Li et al., 2014) function in 108

C-to-U editing of transcripts in mitochondria and chloroplasts. 109

Many kernel size genes encode pentatricopeptide repeat (PPR) proteins, a large family 110

of RNA-binding proteins in land plants, with more than 400 members in Arabidopsis 111

(Arabidopsis thaliana), rice (Oryza sativa), and maize (Zea mays) (Lurin et al., 2004; 112


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Schmitz-Linneweber and Small, 2008; Barkan and Small, 2014). Members of the PPR family 113

are characterized by tandem arrays of a degenerate 35-amino-acid motif (PPR motif), and the 114

PPR family is divided into P and PLS subfamilies, according to the nature of the PPR motifs. 115

Members of the P subfamily function in various processes of RNA maturation in organelles, 116

including RNA stabilization, splicing, intergenic RNA cleavage, and translation (Barkan and 117

Small, 2014). The PLS subfamily contains canonical PPR (P) motifs, as well as long (L) and 118

short (S) PPR-like motifs, in a P-L-S pattern. This subfamily is further divided into PLS, 119

E/E+, and DYW classes, based on their C-terminal domains (Barkan and Small, 2014). PLS 120

subfamily members function in RNA editing (Barkan and Small, 2014), a post-transcriptional 121

modification of organelle transcripts, including C-to-U, U-to-C and A-to-I editing 122

(Chateigner-Boutin and Small, 2010; Ruwe et al., 2013; Ruwe et al., 2019). 123

Kernel size and carbohydrate import into kernels directly determine the grain yield of 124

maize, therefore, elucidation of the genetic basis of kernel traits could provide favorable 125

alleles to enhance maize breeding. In a previous study, a maize recombinant inbred line (RIL) 126

population was developed from a cross between two diverse parents, Zheng58 and SK (Small 127

Kernel), which show dramatic variation in kernel weight; and a major kernel weight QTL, 128

qKW9, was identified (Raihan et al., 2016; Yang et al., 2019). In this study, we mapped and 129

cloned the causative gene underlying qKW9, and identified it as a PLS-DYW type PPR protein. 130

We found that qKW9 is required for C-to-U editing at position 246 of NdhB, a 131

chloroplast-encoded subunit of the NDH complex. Functional characterization revealed that 132

C-to-U editing of NdhB is crucial for the accumulation of its protein product as well as the 133

activity of the NDH complex. Impairment of this complex led to lower photosynthetic 134

efficiency and a corresponding yield loss of maize in field trials. 135

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RESULTS 137

Fine mapping and validation of qKW9 138

qKW9 is a major QTL regulating maize kernel weight identified in the ZHENG58×SK RIL 139

population (Raihan et al., 2016). Near-isogenic lines (NILs) harboring the qKW9 allele from 140

SK or ZHENG58 were screened from RIL-derived heterogeneous inbred families (HIFs) and 141

used to fine map qKW9. In contrast to dek mutants, which have dramatic kernel weight loss 142

due to defects in the embryo and/or endosperm, the NIL-SK kernels weighed only about 3g 143

less per hundred kernels, compared to NIL-ZHENG58, and their kernel morphology, starch 144

granule structure and plant morphology were similar (Figure 1, Table S1). Thus, the kernel 145

development of NIL-SK plants was not strongly affected. Interestingly, two-week-old 146

seedlings of NIL-SK were smaller than NIL-ZHENG58, possibly as a result of less nutrition 147

from smaller kernels for their heterotrophic growth (Figure1B). However, at the mature stage, 148

NIL-SK, and NIL-ZHENG58 plants had similar plant architecture(Figure 1A and 1C). 149

NIL-SK plants had the same kernel row number but fewer kernels per row compared to 150

NIL-ZHENG58 plants , resulting in smaller ears with fewer kernels (Figure 1D and Table 1). 151

In previous study, line KQ9-HZAU-1341-1 from ZHENG58×SK RIL population with 152

residual heterozygosity was used as founder line to fine map qKW9.2(Raihan et al., 2016; Liu 153

et al., 2018). After three generations self-cross and screening against descendents of 154

KQ9-HZAU-1341-1, several recombinant HIFs were obtained. Among the HIFs, F1H5 was 155

used to generate recombination populations to screen for new recombinants to fine map qKW9 156

in this study. Eight recombinants was identified by screening 685 F1H5 descendents and they 157

were self-crossed for further analysis (Figure S1). By comparing Hundred Kernel Weight 158

(HKW) of the homozygous progenies from all recombinants, qKW9 was fine mapped to a ~ 159

20kb region defined by markers M3484 and M3506 (156.65Mb and 156.67Mb, respectively in 160

B73 RefGen v4) (Figure 2A and Fig S1). Three genes (Zm00001d04850, Zm00001d048451, 161

and Zm00001d048452) were annotated within this region in B73 RefGen v4 (Figure 2B). 162

Several SNPs were found in Zm00001d04850, however they were all synonymous. The second 163

gene, Zm00001d048451, had a 13bp-CDS-deletion in SK, possibly leading to loss of function 164


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(Figure 2C). We failed to amplify the third gene, Zm00001d048452, from both SK and 165

ZHENG58, and therefore, screened SK and ZHENG58 BAC libraries to search for sequence 166

variation. However, sequence alignment and annotation revealed that Zm00001d048452 was 167

absent from both SK and ZHENG58, and there were no additional annotated genes within the 168

qKW9 locus, although there were some large-fragment insertions or deletions in the intergenic 169

regions (Figure 2B). These results were further verified using the assembled SK genome (Yang 170

et al., 2019). Of the two remaining candidates, Zm00001d048450 displayed neither change in 171

expression level nor pattern (Figure S2A), which together with its lack of non-synonymous 172

SNPs suggested Zm00001d048451 to be the causative gene of qKW9. 173

To validate Zm00001d048451 as the gene underlying qKW9, we adopted the 174


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CRISPR/Cas9 system to create knockout mutants (Figure 2C). Editing of qKW9 was 175

identified by Sanger sequencing of T0 transgenic plants, and two null mutants, qKW9-cr1, 176

carrying a 1bp-deletion, and qKW9-cr2, carrying a 4bp-deletion, were used for subsequent 177

analysis (Figure 2C and Figure 3). For both alleles, we found that kernel weight and ear 178

weight were reduced compared to their corresponding wild type (Figure 3), demonstrating 179


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that Zm00001d048451 was indeed the causative gene of qKW9. 180

qKW9 is highly expressed in leaf, and encodes a chloroplast protein involved in NdhB 181

RNA editing 182


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Zm00001d048451/qKW9 is predicted to encode a DYW subgroup pentatricopeptide repeat 183

(PPR) protein with eight putative PPR motifs (Figure 2C). An Arabidopsis ortholog, 184

AT5G66520 (Figure 4A) encodes a DYW subgroup protein with ten PPR motifs and was 185

designated Chloroplast RNA Editing Factor 7 (CREF7), functioning in Ndh editing (Yagi et al., 186

2013). In order to address if qKW9 is also involved in chloroplast RNA editing, we analyzed its 187

expression and subcellular localization. Real-time PCR of qKW9 revealed a considerably 188

higher expression level in leaf than in other tissues (Figure S2B). qKW9 expression was 189

detected in all leaf-related tissues, and its expression level (13.9-87.6 FPKM) was much higher 190

than in other tissues (0-12.8 FPKM) (Stelpflug et al., 2016). To test the subcellular localization 191

of qKW9, we transiently expressed a qKW9-GFP fusion protein in tobacco, and found 192

localization in the stroma of chloroplasts (Figure4B-4E), agreeing with a chloroplast prediction 193

by TargetP (Emanuelsson et al., 2007). 194

To evaluate RNA editing by qKW9, leaves from NIL-SK and NIL-ZHENG58 plants 195

before and after pollination were collected for total RNA sequencing. By comparing editing 196

frequencies between NIL-SK and NIL-ZHENG58, six loci putatively edited by qKW9 were 197


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identified with p-value < 0.05 and mean editing frequency difference > 5% (Table 2). Three of 198

these loci at chloroplast genome positions 90736, 132001, and 65407 (B73 RefGen v4), had 199

striking editing differences between NIL-SK and NIL-ZHENG58, with close to 100% editing 200

in NIL-ZHENG58 but almost none in NIL-SK at all stages tested (Table 2). Position 65407 is 201

in an intergenic region, whereas positions 90736 and 132001 are in the 246th codon of 202

GRMZM5G876106 and GRMZM5G810298, respectively (Table 2). These genes are the two 203

copies of NdhB in the chloroplast genome, and their C-to-U editing changes the 246th amino 204

acid from proline to leucine. Thus, the sites edited by qKW9 were designated as NdhB-246. 205

We confirmed the NdhB-246 editing difference by Sanger sequencing in NIL-SK and 206

NIL-ZHENG58 (Figure 4F). We also investigated the editing frequency of NdhB-246 in 207

leaves of our two CRISPR/Cas9 null mutants, as expected, NdhB-246 editing being abolished 208

in both mutants (data not shown). These results demonstrate that qKW9 is essential for 209

NdhB-246 editing. 210

RNA editing defects may directly alter protein function or affect its ability to form 211

complexes with other proteins (Hammani et al., 2009). NdhB encodes a subunit of the NDH 212

complex (Laughlin et al., 2019), so we asked if this complex accumulates in the null qKW9 213

background using protein blots probed with antibodies against NdhH to monitor 214

accumulation of the complex. In NIL-SK, the level of NdhH was reduced to less than 25% of 215

NIL-ZHENG58 (Figure 5), suggesting that NdhB-246 RNA editing by qKW9 is important for 216

normal accumulation of the NDH complex. 217

C-to-U editing of NdhB-246 is essential for optimal activity of NDH complex, electron 218

transport rate and non-photochemical quenching induction 219

The chloroplast NADH dehydrogenase (NDH) complex transfers electrons originating 220

from Photosystem I (PSI) to the plastoquinone pool, while concomitantly pumping protons 221

across the thylakoid membrane (Strand et al., 2017). Its activity can be monitored as a 222

transient increase in chlorophyll fluorescence, reflecting plastoquinone reduction after turning 223

off actinic light (AL) (Burrows et al., 1998; Shikanai et al., 1998). In Arabidopsis, several 224

nuclear mutants affecting NDH activity function in RNA processing of NDH subunit 225


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transcripts. For instance, Chlororespiratory Reduction 2 (CRR2) functions in the intergenic 226

processing of chloroplast RNA between rps7 and NdhB (Hashimoto et al., 2003). A null allele 227

of CRR2 lacks NDH activity, and the post-illumination increase in chlorophyll fluorescence is 228

undetectable, with a similar phenotype being observed in the tobacco NdhB mutant 229

(Hashimoto et al., 2003). 230


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To check whether qKW9 impaired NDH activity, we monitered chlorophyll fluorescence 231

using the post-illumination method (Burrows et al., 1998; Shikanai et al., 1998). Figure 6A 232

shows a chlorophyll fluorescence trace from wild-type maize and qkw9-cr1 and qkw9-cr2. In 233

both qkw9-cr1 and qkw9-cr2, the post-illumination increase of chlorophyll fluorescence was 234

reduced, indicating that NDH activity was diminished in the null qKW9 background, and that 235

the Leu residue at position 246 of NdhB protein is required for NDH accumulation and 236

activity. We next measured non-photochemical quenching (NPQ), a chlorophyll fluorescence 237

parameter indicative of the level of thermal dissipation. NPQ was induced with increasing light 238

intensity in both qkw9-cr1 and wild type prior to saturation of the ETR (Figure 6B). However, 239

its induction in qkw9-cr1 was significantly lower at light intensities of 2413 μmols-2m-1, 240


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indicating that thermal dissipation was impaired in qkw9-cr1(Figure 6B). ETR represents the 241

relative flow of electrons through PSII during steady-state photosynthesis. It increases with 242

increases in light intensity until a point at which it cannot be further increased – termed its 243

saturation point. For both wild-type and qkw9-cr1, the saturation point was over 400 244

μmol/m2s (Figure 6C). Whilst, ETR was not affected in qkw9-cr1 at a low light intensities of 245

~100 μmols-2m-1 (Figure 6C), it tended to be lower in qkw9-cr1 at intensities above this 246

(significantly so at 200 and 2400 μmols-2m-1). These altered ETR activities are consistent 247

with the overall reduced grain yield in NIL-SK considering that light intensity is far in excess 248

of 100 μmols-2m-1 in the field. These findings considerably differ from studies in Arabidopsis 249


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and tobacco, since multiple mutant analyses have demonstrated that NDH does not function 250

to trigger thermal dissipation in PSII in these species (Burrows et al., 1998; Munekage et al., 251

2004). 252

qKW9 controls kernel weight by regulating photosynthesis 253

Genetic evidence suggests that physiological functions of cyclic electron transport (CET) 254

around Photosystem I (PSI) are essential for efficient photosynthesis and plant growth 255

(Munekage et al., 2004). The physiological role of CET is to protect PSII under intense light 256

via ΔpH-dependent thermal dissipation in PSII, as well as to act as an ATP generator in 257

photosynthesis (DalCorso et al., 2008; Alric and Johnson, 2017). Our results suggest that 258

reduced activity of the NDH complex in maize affected NPQ and ETR. We therefore asked 259

how photosynthesis and carbon assimilation were affected by changes in NDH activity? We 260

measured the fresh weight of developing kernels of NIL-SK and NIL-ZHENG58 under field 261

conditions, and investigated several photosynthesis-related parameters (Figure 7). Fresh 262

weight of NIL-SK kernels was similar to NIL-ZHENG58 before 30 DAP (Figure 7A). 263

However, kernels of NIL-SK reached their maximum fresh weight at 30DAP, while 264

NIL-ZHENG58 kernels continued to gain weight until 35 DAP, suggesting that carbon 265

deposition in kernels was greater in NIL-ZHENG58 at 35 DAP (Figure 7A). Consistent with 266

this observation, leaves of NIL-SK had more severe senescence at 30 DAP compared to 267

NIL-ZHENG58, indicating decreased source strength in the NIL-SK plants (Figure 1C). 268

NIL-SK also had significantly lower net photosynthesis than NIL-ZHENG58 at 22DAP and 269

30DAP (Figure 7B). Consistently, stomatal conductance and transpiration rate were similarly 270

lower in NIL-SK than in NIL-ZHENG58 (Figure 7C-7D). The lower photosynthetic capacity 271

of NIL-SK, coupled with the potential compensatory fact that less kernels were produced per 272

ear in this line (Table 1), may explain why the fresh weight of NIL-SK were not significantly 273

lower than NIL-ZHENG58 at 22DAP and 30DAP (Figure 7A). In addition, the chlorophyll 274

content (SPAD value) and the maximum photochemical efficiency (Fv/Fm) were invariant 275

between the NILs (Figure 7E-7F), indicating that the differences in the net photosynthetic 276

rates might not result from a different level of photosynthesis potential. Accordingly, the 277


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photosynthetic rate was also significantly lower in qKW9-cr1 than WT at 30DAP under field 278

conditions (qKW9-cr1: 17.35±2.10 μmol CO2m-2s-1, Wild type: 29.68±3.56μmol CO2 m

-2s-1, 279

n=6). We conclude that impaired NDH activity affected both net photosynthesis and the 280

duration of active photosynthesis, resulting in smaller ears and kernels in NIL-SK. 281

282


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DISCUSSION 283

qKW9 encodes a PPR gene responsible for C-to-U editing of NdhB 284

The maize kernel has been of interest to researchers as a model system for the study of 285

development and genetics for a century. Numerous kernel mutants have been identified 286

(Neuffer and Sheridan, 1980; Sheridan and Neuffer, 1980; Clark and Sheridan, 1991), and in 287

recent years, many mutants that result in dramatically reduced kernel size, and seedling 288

lethality have been identified. In many cases, PPR genes are responsible for these phenotypes, 289

due to their function in organellar gene expression. Generally, null alleles of PPR genes in 290

previous studies produce kernels that are with obvious development abnormality at early stages 291

and are easily distinguished from normal kernels on self-crossed F1 ears due to their smaller 292

size, pale pericarp, flat or shrunken appearance (Manavski et al., 2012; Sosso et al., 2012; Li et 293

al., 2014; Sun et al., 2015; Xiu et al., 2016; Cai et al., 2017; Chen et al., 2017; Qi et al., 2017; 294

Ren et al., 2017; Dai et al., 2018; Li et al., 2018; Sun et al., 2019). Unlike these kernel mutants, 295

kernels produced by null allele of qKW9 are similar in appearance and viability although 296

smaller in size comparing to wild type, and kernel weight is determined by genotype of 297

maternal plant rather than kernel genotype. qKW9 is the first identified C-to-U editing factor in 298

the maize chloroplast that has a quantitative rather than qualitative effect on kernel and ear size. 299

This difference stems from the involvement of qKW9 in the abundance of the NDH complex, 300

which in known to play a regulatory role in photosynthesis (Nashilevitz et al., 2010; Peltier et 301

al., 2016). Based on results from this study, it is possible that variants of other yet-unidentified 302

RNA editing factors responsible for the 11 C-to-U editing sites in maize ndh transcripts will 303

also affect kernel and ear size in a quantitative way. Indeed, studies in Arabidopsis have 304

identified many PPR genes affecting ndh expression, by focusing on changes in chlorophyll 305

fluorescence related to NDH activity (Kotera et al., 2005; Okuda et al., 2007; Hammani et al., 306

2009; Okuda et al., 2010). Similar research in maize may help us rapidly identify potential 307

QTL, circumventing the tedious work of fine mapping. 308

Grains are typical sink organs -i.e. they are net receivers of photoassimilates from 309

photosynthetically active source tissues - and a considerable number of studies suggest that 310


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enhancing photosynthetic efficiency could increase the productivity of crops (Sonnewald and 311

Fernie, 2018; South et al., 2019; Wu et al., 2019). In the light reactions of photosynthesis, 312

linear electron transport (LET) from water to NADP+ does not fully satisfy the ATP/NADPH 313

production ratio required by the Calvin-Benson cycle and photorespiration (Yin and Struik, 314

2018). Cyclic electron transport (CET) around photosystem I (PSI) has, therefore, been 315

considered as a candidate for augmented ATP synthesis in response to fluctuating demand 316

during photosynthesis (Rumeau et al., 2007; DalCorso et al., 2008; Nakamura et al., 2013). In 317

PSI CET, electrons are recycled around PSI generating ΔpH and consequently ATP without a 318

concomitant accumulation of NADPH (Shikanai, 2007; Munekage and Taniguchi, 2016). In 319

Arabidopsis, two CET pathways have been identified by genetics. The main pathway depends 320

on PROTON GRADIENT REGULATION 5 (PGR5)/PGR5-LIKE PHOTOSYNTHETIC 321

PHENOTYPE 1 (PGRL1) proteins, whereas the minor pathway is mediated by the 322

chloroplast NADH dehydrogenase-like (NDH) complex (Munekage et al., 2004). The 323

Arabidopsis pgr5 mutant is defective in PSI CET and was discovered by screening for 324

reduced non-photochemical quenching (NPQ) of chlorophyll fluorescence (Munekage et al., 325

2002; DalCorso et al., 2008). However, as in tobacco, the Arabidopsis chlororespiratory 326

reduction (crr) mutants and organelle transcript processing (otp)mutants defective in 327

chloroplast NDH did not show any marked phenotype (Burrows et al., 1998; Hashimoto et al., 328

2003; Munekage et al., 2004; Hammani et al., 2009; Okuda et al., 2010). 329

Plastid genomes encode 11 subunits (NdhA to NdhK) forming the core of the membrane 330

arm of the L-shaped structure of the NDH complex (Laughlin et al., 2019). Multiple PPR 331

genes regulate expression of ndh genes in Arabidopsis. These PPR genes are either 332

responsible for splicing of polycistronic transcripts, or site-specific C-to-U RNA editing 333

(Hashimoto et al., 2003; Munekage et al., 2004; Kotera et al., 2005; Okuda et al., 2007; 334

Hammani et al., 2009; Okuda et al., 2009; Okuda et al., 2010). C-to-U RNA editing is 335

important in organelle gene expression in various organisms, although the efficiency varies in 336

different organs and at different developmental stages (Maier et al., 1995; Peeters and Hanson, 337

2002). C-to-U RNA editing in Arabidopsis can generate translational initiation codons, as in 338


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CRR4 (Kotera et al., 2005) or cause amino acid alterations, as in CRR21, CRR22, CRR28, 339

OTP82, OTP84 and OTP85 (Okuda et al., 2007; Hammani et al., 2009; Okuda et al., 2009; 340

Okuda et al., 2010). Editing of NdhB-246 in leaf tissues is near 100% in maize, suggesting that 341

it is important for the function of NdhB protein (Peeters and Hanson, 2002). NdhB-246 editing 342

also occurs in tobacco and rice (Tsudzuki et al., 2001). Therefore, C-to-U editing of NdhB-246 343

appears crucial to its function. The qKW9 QTL characterized in our study is the first RNA 344

editing factor that has been linked to C-to-U editing of NdhB-246. Our results clearly indicate 345

that the abolition of C-to-U editing in NdhB-246 impairs accumulation of the NDH complex in 346

vivo. 347

Cyclic electron transport via NDH complex in C4 and C3 348

Chloroplast NDH mediation of CET around PSI was first reported in tobacco following 349

disruption of NdhB (Shikanai et al., 1998). Knockout lines of ndh genes were created by 350

plastid transformation in tobacco. Mutants defective in expression of chloroplast ndh genes 351

were isolated in Arabidopsis (Hashimoto et al., 2003). However, both knockout lines of ndh 352

genes in tobacco and mutants with impaired NDH activity in Arabidopsis lack morphological 353

phenotypes (Hashimoto et al., 2003; Munekage et al., 2004; Okuda et al., 2007; Hammani et 354

al., 2009; Okuda et al., 2009; Okuda et al., 2010). So, the general conclusion has been that 355

mutants defective in NDH do not show a clear phenotype and NDH is dispensable at least 356

when plants are grown in controlled environments. Analysis of this observation leads to the 357

conclusion that NDH does not function to generate a pH gradient in order to trigger thermal 358

dissipation in PSII. The observations we present here, where we found that qKW9 is required 359

for the expression of NdhB and optimal activity of the NDH complex in maize, suggest that 360

this conclusion may not hold in all species. Namely in the null mutant genotypes, light 361

intensity-dependent ETR and NPQ were obviously affected. We additionally observed more 362

severe leaf senescence in NIL-SK, a phenonomon that may result from impaired thermal 363

dissipation, since NPQ induction under high-intensity light is suppressed as compared with 364

NIL-ZHENG58. Moreover, the overall rate of photosynthesis was also reduced in the null 365

qKW9 mutant, leading to significantly reduced ear and kernel size. 366


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Our study of qKW9 provides a possible explanation for the apparent contradiction of 367

these observations, in suggesting that CET via the NDH complex is more important in C4 368

than in C3 plants. CET around photosystem I is critical for balancing the photosynthetic 369

energy budget of the chloroplast by generating ATP without net production of NADPH 370

(Ishikawa et al., 2016a). C4 plants have higher ATP requirements than C3 plants (Ishikawa et 371

al., 2016b), rendering the ATP supply by CET particularly important, imply that during the 372

evolution of NADP-malic enzyme-type C4 photosynthesis in the C4-like genus Flaveria, CET 373

was promoted by markedly increasing expression of both PGR5/PGRL1 and NDH subunits 374

(Nakamura et al., 2013). The NDH subunit, however, increases markedly in bundle sheath 375

cells with the activity of the C4 cycle while PGR5/PGRL1 increases in both mesophyll and 376

bundle sheath cells in Flaveria and other C4 species, implying that the NDH complex 377

provides a considerable role in the establishment of C4 photosynthesis (Nakamura et al., 378

2013). Previously, it was also shown that NDH plays a central role in driving the 379

CO2-concentrating mechanism in C4 photosynthesis (Takabayashi et al., 2005; Andrews, 380

2010). In addition, the NDH complex has been experimentally demonstrated to be a 381

high-efficiency proton pump, increasing ATP production by cyclic electron transport (Strand 382

et al., 2017). Ishikawa et al. report that NDH-suppressed C4 plants are characterized by 383

consistently decreased CO2 assimilation rates, impaired proton translocation across the 384

thylakoid membrane and reduced growth rates (Ishikawa et al., 2016a). Results from our 385

study provide direct evidence that the NDH complex is important to C4 photosynthesis. As 386

such comparison of our data with that from a recent study in Arabidopsis which showed that 387

NDH-dependent cyclic electron transport around PSI contributes to the generation of proton 388

motive force only in the weak mutant of pgr5 (Nakano et al., 2019), suggests that it is more 389

important to C4 than C3 photosynthesis. 390

An alternative explanation could be the difference in the study conditions. In our study, 391

growth and photosynthesis measurement are conducted in the field where the plants 392

experience naturally fluctuating light, humidity, temperature, etc. Fluctuating elements may 393

give rise to stress to photosystems. Impairment of NDH-dependent PSI cyclic electron 394


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transport causes a reduction in photosynthetic rate under fluctuating light, leading to 395

photoinhibition at PSI and consequently to reductions in plant biomass in rice (Yamori et al., 396

2016). It is worth noting that there are studies stressing the role that NDH complex plays in 397

CET under stresses (Horváth et al., 2000; Wang et al., 2006; Yamori et al., 2015). Indeed the 398

conclusions that the NDH complexs role in CET is dispensable come from studies of tobacco 399

and Arabidopsis grown in growth chambers rather than the field, resulting in an 400

under-estimation of the importance of the NDH complex’s regulatory effect on 401

photosynthesis. 402

In summary, our study identified a maize kernel size QTL which is caused by allelic 403

variation in qKW9, a PLS-DYW type PPR protein. We found that qKW9 is required for C-to-U 404

editing at 246th codon of NdhB, a chloroplast-encoded subunit of the NDH complex. With this 405

editing pattern previously being recorded occuring concomitantly with the onset of 406

photosynthetic activity in tobacco (Karcher and Bock, 2002). Functional characterization 407

revealed that C-to-U editing of maize NdhB is crucial for the accumulation of its protein 408

product as well as the activity of the NDH complex. This study thus challenges current models 409

of the role of the NDH in photosynthesis, revealing new insights into the regulation of C4 410

photosynthesis and suggesting a novel potential target for crop improvement. 411

METHODS AND MATERIALS 412

Fine mapping of qKW9 413

Multiple major QTL regulating kernel-size-related traits were identified by 414

multi-environment QTL analysis in ZHENG58×SK RIL population and a major QTL on 415

chromosome 9 regulating kernel width was designated as qKW9 in a previous report (Raihan et 416

al., 2016). To fine-map qKW9, the heterogeneous inbred family (HIF) was screened against the 417

RIL population and RIL line KQ9-HZAU-1341-1 was heterozygous between Marker M2682 418

(155.83Mb in B73 Ref Gen v4) and Marker M3671 (156.83Mb in B73 RefGen v4) was used 419

as the founder HIF (Raihan et al., 2016). In a nursery grown in Hainan in 2015, two groups of 420

homozygous progenies of F1H5, which was a descendant of line KQ9-HZAU-1341-1, were 421

significantly different in hundred kernel weight (HKW), kernel length (KL), and kernel width 422


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(KW). Thus, F1H5 was used as the starting HIF to fine map qKW9 in this study. In the summer 423

of 2016, recombinants between Marker M2795 and Marker M3671 were screened against the 424

F1H5 population. In the winter of 2016, progeny tests were conducted on those recombinant 425

populations. 426

For genotyping, genomic DNA extraction from young leaf was conducted using the CTAB 427

protocol for plant tissues. To detect SNP and Indel markers, PCR was conducted in 10 μL 428

reactions with KASP master mix (cat no: KBS-1030-002, LGC), self-made KASP array mix, 429

and DNA template in 96 well non-transparent plates. KASP array mix was made by mixing 430

equal volumes of primer F1 (36 μM), F2 (36 μM), and R (90 μM) of a specific SNP marker. For 431

each reaction, 0.14 μL array mix, 1×master mix, and 20~200 ng DNA were used. Thermal 432

cycling was 94 ℃ for 15 minutes to activate the enzyme, followed by 10 cycles of touch down 433

PCR (denature at 94 ℃ for 20 s, annealing/elongation start with 61 ℃ for 60 s, drop 0.6 ℃ per 434

cycle), then annealing/elongation for another 26-36 cycles depending on the quality of primers 435

(denature at 94 ℃ for 20 s, annealing/elongation at 55 ℃ for 60 s). Upon the completion of the 436

KASP PCR, reaction plates were read by CFX96 TouchTM Real-time PCR detection system 437

and the data was then analysed with the Allelic Discrimination module of BioRad CFX 438

Manager 3.0. Detected signals were plotted against FAM and HEX fluorescence intensity as a 439

graph, with samples of the same genotype clustering together. To detect SSR markers, PCR 440

products were detected by AATI Fragment Analyzer following the manufacturer’s instructions. 441

Maize plants were examined under natural field conditions in the experimental fields of 442

Wuhan (30°N, 114°E), Sanya (18°N, 109°E), and Baoding (39°N, 115°E) in China. The 443

planting density was 25 cm between adjacent plants in a row and the rows were 60 cm apart. 444

Field management, including irrigation, fertilizer application, and pest control, essentially 445

followed the normal agricultural practices. Harvested maize ears were air-dried and then 446

fully-developed ears were shelled for measuring HKW, KL, and KW as previously reported 447

(Raihan et al., 2016). 448

BAC screen, sequence, and de novo assembly 449

BACs covering qKW9 of both parent lines-SK and ZHENG58- were screened. BAC DNA 450


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was prepared using the QIAGEN Large-Construct Kit (Cat no: 12462) following the 451

manufacturer’s instructions but with 150ml overnight-cultured bacterial input. The recovered 452

DNA was sent to a company (Nextomics Bioscience Co., Ltd, Wuhan, China) for quality 453

control and library construction. The resulting sequence data was assembled by PacBio’s 454

open-source SMRT Analysis software. 455

Fresh weight during the filling stage 456

NILs derived from homozygous progenies of HIF-p11 were used to analyze the grain 457

filling rate of developing kernels after pollination. NILs with the qKW9 allele of SK designated 458

as NIL-SK while NILs with the qKW9 allele of ZHENG58 designated as NIL-ZHENG58. 459

Starting from 6 days after pollination (DAP), 50 fresh kernels were harvested and weighted 460

from 6 ears of each NIL every other day until 30 DAP. At 35 DAP and upon harvest fresh 461

kernels were also weighed. 462

Mutagenesis of qKW9 with CRISPR/Cas9-based gene editing 463

Two guide RNA sequences (cggtggtggacatgtactg and ctgttctggggatccagct) against qKW9 464

were designed by CRISPR-P 2.0 (http://crispr.hzau.edu.cn/CRISPR2/) then cloned into a 465

CRISPR/Cas9 plant expression vector (Liu et al., 2017a). The backbone of the vector was 466

provided by WIMI Biotechnology Co., Ltd (Changzhou, China). The vector allows expression 467

of single guide RNA by the ZmU61 promoter and Cas9 by a maize UBI promoter. The 468

resulting binary plasmids were transformed into the Agrobacterium tumefaciens strain 469

EHA105 and used to transform maize inbred C01. All constructs were sequence-verified. 470

Light Microscopy 471

Whole sections of mature kernels were stained with iodine solution using the method in a 472

previous report (Zhao et al., 2016). Three different regions of endosperm were examined for 473

the morphology of starch. 474

Subcellular localization of qKW9 475

Zm00001d048451 was predicted to locate in chloroplast by TargetP (Emanuelsson et al., 476

2007). To verify this, a codon-optimized CDS (optimized by a web tool - 477

https://www.genscript.com/codon_opt_pr.html) was fused with green fluorescent protein (GFP) 478


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and driven by expression from the cauliflowner mosaic virus 35S promoter. The binary 479

vector-pK7FWG2.0-was obtained from Dr. Hannes Claeys (Cold Spring Harbor Laboratory, 480

USA). The plasmids containing the chimeric genes were transferred into Agrobacterium 481

tumefaciens strain GV3101. The resulting strain was co-infiltrated into Nicotiana benthemiana 482

leaves with a strain harboring P19 which was obtained from Dr. Edgar Demesa Arevalo (Cold 483

Spring Harbor Laboratory, USA) (Lindbo, 2007). Fluorescence signals were detected using 484

LSM780. DAPI (4,6-diamidino-2-phenylindole) staining solution 485

(http://cshprotocols.cshlp.org/content/2007/1/pdb.rec10850.full?text_only=true) was injected 486

to the leaf before observing the fluorescence signals. Agrobacterium growth and injection 487

followed the steps described in a previous report (Xu et al., 2015). 488

Phylogenetic analysis 489

To identify the PPR genes in maize B73 RefGen v4, protein sequences of B73 RefGen 490

v4 genes were downloaded from ftp://ftp.gramene.org/pub/gramene/ (B73 RefGen v4.59). 491

Then HMMER 3.0 software (Finn et al., 2011) was used to scan all of the annotated 492

Pentatricopeptide Repeat genes in B73 RefGen v4 with the Midden Markov (HMM) profile 493

of PPR domain (PF01535.20, http://pfam.sanger.ac.uk/) (E-value < 1). Based on the 494

C-terminal domain structure, the HMM profiles of E, E+, and DYW domain were rebuilt 495

using the previously predicted PPR genes in B73 RefGen v3. Then these HMM profiles were 496

used to scan the PPR genes annotated in B73 RefGen v4 497

(ftp://ftp.gramene.org/pub/gramene/CURRENT_RELEASE/gff3/zea_mays/gene_function). 498

Then TargetP version 1.1 (http://www.cbs.dtu.dk/services/TargetP/) was used to predict the 499

organelle targeting of these E, E+, and DYW types PPR proteins. Only the chloroplast 500

targeting genes were kept to conduct the evolutionary analysis with their orthologous genes 501

in Arabidopsis and rice 502

(https://download.maizegdb.org/Zm-B73-REFERENCE-GRAMENE-4.0/Orthologs/). The 503

evolutionary history was inferred using the Neighbor-Joining method (Saitou and Nei, 1987) 504

by MEGAX (Kumar et al., 2018). The bootstrap consensus tree inferred from 500 replicates 505

was taken to represent the evolutionary history of the taxa analyzed (Felsenstein, 1985). 506


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Photosynthetic parameters and chlorophyll content measurements 507

Carbon dioxide assimilation rate, stomatal conductance, and transpiration rate were 508

measured on fully-expanded maize leaves grown in the field using a portable gas exchange 509

system (LI‐6400XT, LI‐COR Inc., USA) as described (Huang et al., 2009; Bihmidine et al., 510

2013). The measurements were conducted at an ambient CO2 concentration of 400 μmol 511

mol−1 and light saturation of 2000 μmol m−2 s−1. Leaf photochemical efficiency (Fv/Fm) was 512

measured on dark-adapted leaves using the FlourPen FP100 chlorophyll fluorescence meter 513

(Photon System Instruments, Czech Republic). Leaf chlorophyll content was measured using 514

a chlorophyll meter (SPAD-502, Konica Minolta, Japan). The measurements were performed 515

before pollination and at 22, 30, and 35 days after pollination (DAP) on eight NIL-SK plants 516

or NIL-ZHENG58 plants. Means and standard errors (SE) were calculated using Microsoft 517

Excel. Differences in chlorophyll content and photosynthetic parameters were assessed using 518

the Student's t-test embedded in the Microsoft Excel program, at the P-value ≤ 0.05 level. 519

RNA sequencing 520

To explore the possible RNA editing in leaf by the PPR gene, the ear leaves from NIL-SK 521

and NIL-ZHENG58 plants before pollination and after pollination (22 days and 30 days) were 522

collected. Total RNA was isolated from these samples using Direct-zol RNA MiniPrep Plus kit 523

(Cat no: R2072, ZYMO Research, USA). Libraries were constructed using the Illumina 524

TruSeq Stranded RNA Kit (Illumina, San Diego, CA, USA) following the manufacturer's 525

recommendations. Strand‐specific sequencing was performed on the Illumina HiSeq 2000 526

system (paired‐end 100‐bp reads). The raw reads were trimmed by Trimmomatic v0.36 (Bolger 527

et al., 2014) to gain high-quality clean reads, and the quality of the clean reads was checked 528

using the FASTQC program (Andrews, 2010). Next the clean reads were aligned to maize B73 529

RefGen v4 chloroplast genome by Hisat2 (Kim et al., 2015). Picard tools were subsequently 530

used to add read groups, sort, mark duplicates, and create index 531

(http://broadinstitute.github.io/picard/). Then the GATK was used to call the sequence variants 532

by HaplotypeCaller (McKenna et al., 2010). The ratio of edited allele reads count/total reads 533


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count served as editing frequency for each site and the significance of editing frequency 534

difference between NIL-SK and NIL-ZHENG58 was estimated by pairwise t-test with a 535

threshold P-value < 0.05. Only the loci with a mean editing frequency difference over 5% 536

between NIL-SK and NIL-ZHENG58 were treated as possibly RNA editing sites being 537

affected by qKW9. 538

RNA extraction and qRT-PCR 539

Total RNA was extracted from various plant tissues except leaf using RNA extraction kit 540

(Cat no: 0416-50, Huayueyang, China). cDNA was synthesized from the extracted RNA using 541

the TransScript One-Step gDNA Removal and cDNA Synthesis SuperMix (Cat no: AT311, 542

TransGen Biotech, China). qRT-PCR was carried out in a total volume of 20 μl containing 2 μl 543

of 10x-diluted reverse-transcribed product, 0.2 mM gene-specific primers, and 10 μl KAPA 544

SYBR® FAST qPCR Master Mix (Cat no: KK4607), using a Bio-Rad CFX96 TouchTM 545

Real-time PCR detection system according to the manufacturer's instructions. Quantitative 546

PCR was performed for the gene expression using QPIG, QPPR, and ACTIN primers (Table 547

S1). 548

Immunoblot Analysis 549

Chloroplast membrane proteins were isolated from the leaves of around 2-week-old 550

maize plants using kits (Cat no: BB-3175, BestBio, China). Protein samples were quantified 551

with BCA protein assay. The protein samples were separated by 12% SDS-PAGE. After 552

electrophoresis, the proteins were transferred onto a PVDF membrane (0.2 µm, Bio-Rad) 553

using Bio-Rad Semi-Dry Transfer Cell. The blot was blocked with 5% milk in TBST for 1h at 554

room temperature (RT) with agitation and then incubated in the primary antibody (from 555

Agrisera, AS16 4065) at a dilution of 1: 500 overnight in +4°C. The antibody solution was 556

decanted, and the blot was washed briefly with TBST at RT with agitation. The blot was 557

incubated in secondary antibody (anti-rabbit IgG horseradish peroxidase conjugated, from 558

Agrisera, AS09 602) diluted to 1:10 000 in 1% milk/TBST for 30min at RT with agitation. 559

The blot was washed briefly in TBST at RT with agitation and developed for 2 min with ECL 560

according to the manufacturer's instructions (Cat no: SL1350, Coolaber, China). The signals 561


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were visualized by a GeneGnome chemiluminescence analyzer (Syngene). 562

ASSESSION NUMBERS 563

Sequence data from this article can be found in the GenBank/NCBI databases under the 564

SRA accession number: PRJNA588870. 565

SUPPLEMENTARY DATA 566

Supplemental Figure S1 Schematic representation of genotypes and kernel weights of 567

recombinant families derived from F1H5. 568

Supplemental Figure S2 qPCR analysis of Zm00001d048450 and Zm00001d048451 569

expression. 570

Table S1 Primer sequences used in this study. 571

ACKNOWLEDGEMENTS 572

This work was supported by the National Key Research and Development Program of China 573

(2016YFD0100303), the National Natural Science Foundation of China (31525017, 574

31961133002), and NSF grant IOS-1546837 to DJ; Juan Huang was sponsored by China 575

Scholarship Council to visit Cold Spring Harbor Laboratory and study in Prof. David Jackson’s 576

lab from March 2018 to March 2019 (File No. 201706760027). We thank Dr. Yali Zhang from 577

Shihezi University for suggestions on measurements of chlorophyll fluorescence. We thank Dr. 578

Edgar Demesa Arevalo’s help in taking confocal images and for providing for P19 containing 579

strain. We thank Dr. Hannes Claeys for providing pK7FWG2.0 containing strain. We thank 580

Felix Fritschi for use of the chlorophyll fluorescence meter. 581

FIGURE LEGENDS 582

Figure 1. Plant and kernel morphology of NIL-SK and NIL-Zheng58. (A) NIL-SK (NS) 583

and NIL-Zheng58 (NZ) had very similar plant architecture, Bar=20cm. (B) NIL-SK (NS) 584

two-week old seedlings were smaller than NIL-Zheng58 (NZ). Bar=4cm. (C) Leaf senescence 585

was greater in NIL-SK (NS) at 30 days after pollination compared to NIL-Zheng58. Bar=10cm. 586

(D) Ears of NIL-SK (NS) were smaller than in NIL-Zheng58 (NZ). Bar=1cm. (E) to (J) 587


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28

Mature kernels of NIL-SK (E-G) were smaller that in NIL-Zheng58 (H-J). Whole kernels of 588

NIL-SK and NIL-Zheng58 ([E] and [H]). Bar=2mm; transverse section of kernel of NIL-SK 589

and NIL-Zheng58([F] and [I]). Bar=2mm; Longitudinal section of kernel of NIL-SK and 590

NIL-Zheng58([G] and [J]). Bar=2mm; (K) to (R) Similar starch structure in endosperms of 591

mature kernels of NIL-SK and NIL-Zheng58. Whole longitudinal section stained with iodine 592

solution of kernels of NIL-SK and NIL-Zheng58 ([K] and [O]), 1, 2, 3 indicate the crown, 593

farinaceous and keratin endosperm regions, respectively. Bar=1mm; (L) to (N) correspond to 594

regions 1, 2, 3 in (K); and (P) to (R) correspond to regions 1, 2, 3 in (O). Bar=10μm. 595

596

Figure 2. Fine mapping and gene structure of qKW9. (A) Mapping delimits qKW9 to the 597

region between M3484 and M3506 on chromosome 9. F1H5 which derives from ZHENG58 × 598

SK RIL population is the founder line for screening heterozygous inbred families (HIFs) for 599

fine mapping qKW9. Progeny tests of kernel weight were conducted on the resulting 600

recombinant families. White bar represents the homozygous chromosomal segment for SK, 601

grey bar represents the heterozygous chromosomal segment for ZHENG58 × SK, black bar 602

represents the homozygous chromosomal segment for ZHENG58. The graphical genotype 603

represents F1H5. Numbers between markers represent physical distances (Kb) between the 604

adjacent markers and numbers in brackets represent the number of recombinants. (B) Gene 605

annotations in the region of qKW9 of B73, SK, and Zheng58. Sequences were obtained by 606

sequencing BACs covering qKW9 from SK and ZHENG58 genome BAC libraries, 607

respectively. Zm00001d048452 was absent in both SK and ZHENG58. Two candidate 608

genes-Zm00001d048450 and Zm00001d048451- were identified in qKW9. (C) 609

Zm00001d048451 is a 1.8kb intron-less gene with 8 pentatricopeptide repeats and a 610

13bp-deletion was identified in coding region of Zm00001d048451 in SK. CRISPR/Cas9 was 611

used to create knockout mutants with a single guide sequence (the 20bp sequence adjacent to 612

PAM) targeting Zm00001d048451 in the inbred C01. Two mutated alleles - qkw9-cr1 and 613

qkw9-cr2 - were identified by sequencing the first-generation (T0) plants and used for further 614

genetic analysis. 615


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29

616

Figure 3. Two CRISPR/Cas9 knockout mutants of Zm00001d048451-qkw9-cr1 and 617

qkw9-cr2-produced smaller ears and smaller kernels than wild type. Each mutant is shown 618

alongside its corresponding wild type segregant from a single Cas9-free T1 generation plant. (A) 619

and (B) comparison of ears produced by CRISPR/Cas9 mutants (left) and WT (right). 620

qkw9-cr1 (left) and wild type (right) in (A) and qkw9-cr2 (left) and wild type (right) in (B). 621

Bar=1cm. (D) and (E) kernels produced by CRISPR/Cas9 mutants (lower row) were smaller 622

than WT (upper row). qkw9-cr1 (lower) and wild type (upper) in (D) and qkw9-cr2 (lower) 623

and wild type (upper) in (E). Bar=1cm. (C) and (F) show reductions in ear weight (C) and 624

kernel weight (F) of CRISPR/Cas9 knockout mutants. Data are shown as mean ± SD (n=6). 625

*** P < 0.001. 626

627

Figure 4. Characterization of qKW9/Zm00001d048451. (A) Phylogenetic tree of maize, 628

Arabidopsis and rice PLS-E, PLE-E+, and PLS-DYW Pentatricopeptide Repeat genes 629

predicted to localize in chloroplast/plastid by TargetP . (B) Autofluorescence of chlorophyll 630

(red). (C) qKW9-GFP fusion protein (green) in green puncta within plastids (D) DAPI 631

staining (blue) of nuclei (E) Overlay of (B), (C) and (D). Scale bar=5 µm. (F) Allele in 632

NIL-SK of Zm00001d048451 fails to edit C to U in 246th codon of NdhB gene. C-to-U editing 633

in NdhB-246 results in amino acid change from proline to leucine. Pro, proline; Leu, leucine. 634

635

Figure 5. Protein blot analysis of the NDH complex. Chloroplast membrane protein was 636

extracted with a commercial kit and protein samples were quantified with BCA protein assay. 637

1× sample amount equals 40 µg protein. Antibody against NdhH was used to indicate the 638

amout of NDH complex. Chloroplast membrane protein from NIL-ZHENG58 was loaded a 639

series of dilutions as indicated. Specific bands corresponded in size of NdhH protein 640

(expected in 45 kDa, apparent in 49 kDa). Signals in NIL-ZHENG58 declined along with the 641

dilution. The level of NdhH in NIL-SK was reduced to less than 25% of NIL-ZHENG58. 642

Coomassie R-250 staining was used to show the proteins separated by electropheris as a 643


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loading control. 644

645

Figure 6. NDH activity monitoring and NPQ and ETR in null mutants of qKW9. (A) 646

Monitoring of NDH activity using chlorophyll fluorescence analysis for qkw9-cr1 and 647

qkw9-cr2 mutants. The curve shows the typical change trace of chlorophyll fluorescence in 648

vivo as the NDH complex catalyzes the post-illumination reduction of the plastoquinone pool 649

(Okuda et al., 2007). The change in post-illumination fluorescence ascribed to NDH activity 650

was different between WT and mutants. Insets are magnified traces from the boxed area. ML, 651

measuring light; AL, actinic light; SP, a saturating pulse of white light. (B) NPQ was induced 652

by light intensity in both cr1 and WT, but it was significantly lower in cr1 under photon flux 653

density of 2413 μmol of photons m-2s-1. (C) relative ETR (rETR) under different photon flux 654

densities. rETR in cr1 and WT reached maximum when the light intensity was 422 μmol of 655

photons m-2s-1. It was significantly lower in cr1 under the photon flux density of 206 μmol of 656

photons m-2s-1 and 2413 μmol of photons m-2s-1. The rETR is depicted relative to a maximal 657

value of φPSII × PPFD (photon flux density, μmol of photons m-2s-1). Data are shown as mean ± 658

SD (n=6). 659

660

Figure 7. Grain filling and photosynthesis measurement in NIL-SK and NIL-Zheng58. 661

(A) Time courses of fresh weight of 50 kernels of NIL-SK and NIL-Zheng58. The fresh weight 662

of NIL-SK and NIL-ZHEGN58 reached the maximum at 30 DAP and 35 DAP, respectively. (B) 663

to (E) Time courses of photosynthesis-rate related parameters of NIL-SK and NIL-Zheng58. 664

Net photosynthesis (B), stomatal conductance(C), and transpiration rate (D) were significantly 665

lower in NIL-SK than NIL-ZHENG58 at 22 DAP and 30 DAP; (E) chlorophyll content and (F) 666

maximum photochemical efficiency did not show significant between genotype differences at 667

any of the four stages tested. Data are shown as mean ± SD (n=6). 668

669

670


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Table 1. Ear related and agronomic traits in NIL-SK and NIL-Zheng58. 671

Trait NIL-SK NIL-Zheng58

P-value Mean ± SDa Nb Mean ± SD N

Hundred Kernel Weight/g 15.59 ± 2.01 27 18.57±1.21 30 6.07ｘ10-9

Ear Length/cm 9.75 ± 0.75 31 10.68±0.76 37 3.72ⅹ10-6

Kernel Number per Row 22.00±2.99 27 24.03±2.28 32 4.47ⅹ10-3

Ear Row Number 12.43±1.00 28 12.39±0.80 36 0.86

Kernel Number per Ear 249.22±39.45 27 279.39±34.28 31 2.89ⅹ10-3

Ear Weight/g 43.79±7.60 30 57.33±8.35 36 3.74ⅹ10-9

Kernel Weight per Ear/g 38.84±6.60 19 53.68±7.44 17 3.07ⅹ10-7

Plant Height/cm 190.73±10.52 92 195.29±10.12 91 3.22ⅹ10-3

Ear Height/cm 84.48±7.19 92 83.65±9.68 91 0.51

Days to Shedding/Day 63.38±1.81 68 60.16±1.21 70 6.72ⅹ10-24

a SD=standard deviation; bN, number of observed individuals. 672

673


https://doi.org/10.1101/847145


32

674


https://doi.org/10.1101/847145


33

Table 2 C-to-U editing sites in plastid genes with significant editing frequency difference 675

between NIL-SK and NIL-Zheng58. 676

Locus(transcript) Genome

position Feature

Developing

Stages

Editing level% P-value

Editing

difference % NIL-SK NIL-Zheng58

GRMZM5G876106(N

dhB)

90736 CDS, P>L

Before

Pollination0.00 100.00

NA 100.00 22 DAPa 0.00 100.00

30 DAP 0.00 100.00

GRMZM5G810298

(NdhB) 132001 CDS, P>L

Before

Pollination 0.00 97.05

2.00E-05 98.15 22 DAP 0.00 98.79

30 DAP 0.00 98.60

intergenic 65407

Before


0.0041 87.21 22 DAP 0.00 88.89

30 DAP 0.00 100.00

GRMZM5G866064 139970

CDS,

synonymou

s

Before


0.024 8.96 22 DAP 18.52 30.60

30 DAP 27.87 32.95

GRMZM5G856777 8558 5'UTR

Before


0.044 5.82 22 DAP 31.63 39.61

30 DAP 35.50 37.63

GRMZM5G845244

(rps8) 78717 CDS, S>L

Before


0.048 5.79 22 DAP 98.08 100.00

30 DAP 92.11 100.00 a DAP= days after pollination. 677

678

679

680


https://doi.org/10.1101/847145


34

681


https://doi.org/10.1101/847145


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https://scholar.google.com/scholar?as_q=EMPTY PERICARP16 is required for mitochondrial nad2 intron 4 cis-splicing, complex i assembly and seed development in maize.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Xiu&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

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https://doi.org/10.1101/847145


running title: cloning of a kernel size qtl in maize · 81 in one large-scale qtl study in maize,...

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