Short title: Local CEPR1 activity controls seed size and yield2 1 Abstract 2 The interaction of...

1

Short title: Local CEPR1 activity controls seed size and yield

Author for contact: Professor Michael Djordjevic

Division of Plant Sciences, Research School of Biology, College of Science, The Australian National University, Canberra, ACT, 2601 Australia

Email: [email protected]

The peptide hormone receptor CEPR1 functions in the reproductive tissue to control seed size and yield

1Michael Taleski, 1Kelly Chapman, 2Nijat Imin, 1#Michael A. Djordjevic, 1,3Michael Groszmann

1Division of Plant Sciences, Research School of Biology, College of Science, The Australian National University, Canberra, ACT, 2601 Australia 2School of Biological Sciences, University of Auckland, Auckland, New Zealand

3Australian Research Council Centre of Excellence for Translational Photosynthesis, Division of Plant Sciences, Research School of Biology, The Australian National University, Acton, ACT, 2601 Australia #Corresponding author (email: [email protected])

One sentence summary: CEP receptor signalling in maternal tissues controls delivery of nitrogen to reproductive sinks.

Author contributions: M.G, M.A.D, N.I and M.T conceived and designed experiments. M.G, M.A.D and M.T coordinated the project. M.T performed most of the experiments with assistance from M.G, and K.C contributed some data to Fig. 1. M.T, M.G and M.A.D analysed the data and wrote the manuscript, with contributions from N.I and K.C.

Funding information: This work was funded by Australian Research Council grants to M.A.D (DP150104050 and LP150100826). MG was supported by the Australian Research Council Centre of Excellence for Translational Photosynthesis (CE140100015). MT and KC were supported by Australian Government Research Training Program (RTP) awards. We acknowledge that National Collaborative Research Infrastructure Strategy (NCRIS) of the Australian Government provided The Australian National University with the growth facilities utilised as part of the Australian Plant Phenomics Facility.

Plant Physiology Preview. Published on April 21, 2020, as DOI:10.1104/pp.20.00172

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2

Abstract 1

The interaction of C-Terminally Encoded Peptides (CEPs) with CEP RECEPTOR 1 (CEPR1) 2

controls root growth and development, as well as nitrate uptake, but has no known role in 3

determining yield. We used physiological, microscopic, molecular and grafting approaches to 4

demonstrate a reproductive tissue-specific role for CEPR1 in controlling yield and seed size. 5

Independent Arabidopsis (Arabidopsis thaliana) cepr1 null mutants showed 6

disproportionately large reductions in yield and seed size relative to their decreased 7

vegetative growth. These yield defects correlated with compromised reproductive 8

development predominantly in female tissues, as well as chlorosis, and the accumulation of 9

anthocyanins in cepr1 reproductive tissues. The thinning of competing reproductive organs to 10

improve source-to-sink ratios in cepr1, along with reciprocal bolt-grafting experiments, 11

demonstrated that CEPR1 acts locally in the reproductive bolt to control yield and seed size. 12

CEPR1 is expressed throughout the vasculature of reproductive organs, including in the 13

chalazal seed coat, but not in other seed tissues. This expression pattern implies that CEPR1 14

controls yield and seed size from the maternal tissue. The complementation of cepr1 mutants 15

with transgenic CEPR1 rescued the yield and other phenotypes. Transcriptional analyses of 16

cepr1 bolts showed alterations in the expression levels of several genes of the CEP-CEPR1 17

and nitrogen homeostasis pathways. This transcriptional profile was consistent with cepr1 18

bolts being nitrogen-deficient, and with a reproductive tissue-specific function for CEP-19

CEPR1 signalling. The results reveal a local role for CEPR1 in the maternal reproductive 20

tissue in determining seed size and yield, likely via the control of nitrogen delivery to the 21

reproductive sinks. 22

Introduction 23

Leucine-rich repeat receptor-like kinases (LRR-RLK) are one of the largest gene families in 24

plants, comprising more than 220 members in Arabidopsis (Arabidopsis thaliana) (Gou et al., 25

2010). Research over the past decade has implicated LRR-RLKs and their selective 26

interactions with secreted peptide hormones in a myriad of developmental processes 27

including reproduction, chemotropism, biotic and abiotic stress tolerances, symbiosis, root 28

architecture, regulation of organ number, stomatal function and development, abscission, and 29

general interactions with the environment (Czyzewicz et al., 2013; Delay et al., 2013a; 30

Djordjevic et al., 2015; Santiago et al., 2016; Shabala et al., 2016; Shinohara et al., 2016; 31

Imin et al., 2018; Roy et al., 2018; Chapman et al., 2020). 32



3

A conserved LRR-RLK with a growing list of important roles is C-TERMINALLY 33

ENCODED PEPTIDE RECEPTOR 1 (CEPR1) in Arabidopsis, and its functional orthologue 34

COMPACT ROOT ARCHITECTURE 2 (CRA2) in Medicago (Medicago truncatula). In 35

Arabidopsis, CEPR1’s ectodomain specifically interacts with peptide hormones of the C-36

terminally Encoded Peptide (CEP) family (Tabata et al., 2014). Arabidopsis has 12 canonical 37

CEP genes, each encoding one or more conserved 15-amino acid CEP domains from which 38

the secreted, mature CEP peptide hormones are derived (Ogilvie et al., 2014). Since the 39

identification of CEPR1 as a CEP receptor (Tabata et al., 2014), its developmental and 40

physiological role has been defined primarily in the context of roots. For example, CEP-41

CEPR1/CRA2 signalling controls the extent of root growth and development, root nodule 42

number in legumes, and nitrate uptake in roots (Tabata et al., 2014; Mohd-Radzman et al., 43

2016; Roberts et al., 2016; Taleski et al., 2016; Taleski et al., 2018; Chapman et al., 2019; 44

Delay et al., 2019; Chapman et al., 2020). Grafting and split root studies show that CEPR1 45

influences nitrate uptake in Arabidopsis via a systemic mechanism, and that the rate of nitrate 46

uptake is reduced in cepr1-1 (Tabata et al., 2014). The identification of mature CEPs in the 47

xylem streams of various plants also supports the existence of systemic mechanisms (Tabata 48

et al., 2014; Okamoto et al., 2015; Patel et al., 2018). The interaction of the root-derived 49

CEPs with CEPR1 in the shoot vasculature triggers the upregulation of phloem-mobile shoot-50

to-root signals, namely the glutaredoxins CEP DOWNSTREAM 1 (CEPD1) and CEPD2, that 51

upregulate the level of nitrate transporter expression in roots selectively exposed to high 52

nitrate (Ohkubo et al., 2017). Recently, we demonstrated that local and systemic CEP-CEPR1 53

signalling curtails the expenditure of resources to control lateral root growth in response to 54

elevated shoot-derived carbon (Chapman et al., 2019), and that systemic CEP-CEPR1 55

signalling controls aspects of root system architecture in soil (Chapman et al., 2020). CEP-56

CEPR1 signalling also controls main root growth in Arabidopsis (Delay et al., 2013b; Delay 57

et al., 2019). In Medicago, CRA2 controls root nodulation systemically from the shoot, 58

however a local interaction of CEPs with CRA2 controls the growth of lateral roots (Huault 59

et al., 2014; Mohd-Radzman et al., 2015; Laffont et al., 2019). 60

Whether CEP-CEPR1 signalling plays a role in the growth of shoots has not been thoroughly 61

explored. Aboveground, the cepr1-1 mutant has been described as dwarfed, producing 62

smaller rosettes with pale green leaves and a shorter floral stem that over accumulates 63

anthocyanins (Bryan et al., 2012; Tabata et al., 2014). Since these traits are typical responses 64

to nitrogen deficiency (Vidal and Gutiérrez, 2008; Takatani et al., 2014), it could be 65



4

reasonable to dismiss any cepr1 aboveground defects as simply the result of reduced nitrate 66

acquisition by the cepr1 roots. Our anecdotal observations of two cepr1 null mutants, 67

however, indicated that their yield was reduced much more dramatically than expected based 68

on their modest reduction in vegetative growth. In addition, we observed that the cepr1 69

mutants produced smaller seeds. These phenotypes appear inconsistent with an effect of 70

CEPR1 on nitrate uptake alone, given that wild-type plants grown at low nitrogen, or mutants 71

with impaired nitrate uptake, produce normally sized but fewer seeds such that their yield 72

losses are proportional to the decreases in vegetative growth (Schulze et al., 1994; Masclaux-73

Daubresse and Chardon, 2011). 74

In contrast to plants with impaired root nitrate uptake, an impairment in the remobilisation of 75

assimilated nitrogen from vegetative to reproductive tissues leads to a reduction in both seed 76

size and yield (Guan et al., 2015; Li et al., 2015; Di Berardino et al., 2018; Moison et al., 77

2018). Smaller seeds also result from knocking out particular UMAMIT genes, which encode 78

transporters required for delivering assimilated nitrogen to seeds (Müller et al., 2015). It is 79

not known if CEPR1 signalling affects nitrogen mobilisation and delivery to reproductive 80

sinks, however the phenotypic similarities of cepr1 with mutants impaired in these processes 81

hint at this possibility, and suggest that CEPR1’s control over seed size and yield extends 82

beyond its influence over root nitrate uptake. Supporting this hypothesis, we noted that 83

several Arabidopsis CEPs are expressed in reproductive tissues (Roberts et al., 2013), and 84

that rice (Oryza sativa) CEPs OsCEP5 and OsCEP6 are specifically expressed at defined 85

stages of reproductive development (Ogilvie et al., 2014; Sui et al., 2016). CEPR1 is 86

expressed throughout the shoot and root vasculature (Bryan et al., 2012; Huault et al., 2014; 87

Tabata et al., 2014), suggesting roles in multiple tissues. 88

To explore a potential role for CEP-CEPR1 signalling in reproduction, we addressed several 89

questions. Firstly, what is the physiological basis for yield reduction in cepr1 mutants? 90

Second, can yield losses in cepr1 be restored by complementation with transgenic CEPR1 or 91

by manipulating nutrient allocation from the vegetative tissues? Third, is CEPR1 expressed in 92

reproductive tissues, and is its effect on yield controlled systemically via vegetative tissues or 93

locally in reproductive tissues? Finally, does CEPR1 regulate genes involved in nitrogen 94

homeostasis/nutrient mobilisation in the reproductive tissues? 95

In this study, we demonstrate that CEPR1 has a specific role in reproductive tissues in the 96

promotion of fecundity, seed yield and size. The two cepr1 knockout mutants showed yield 97



5

reductions of between 88% and 98%, which were associated with the production of smaller 98

seeds and a diminished number of reproductive units. These yield defects correlated with 99

poorly developed reproductive tissues as well as chlorosis and the accumulation of 100

anthocyanins in cepr1 reproductive tissues, all of which could be restored by transgenic 101

complementation with CEPR1. Bolt grafting and manipulation of nutrient allocation to 102

reproductive sinks showed that local CEP-CEPR1 signalling underpins the poor fecundity of 103

the cepr1 mutants. We found that CEPR1 expression in the reproductive organs occurred 104

specifically in the vasculature. Notably, CEPR1 expression in the seed was restricted to the 105

chalazal seed coat, the site where nutrients for seed filling are unloaded from the terminating 106

maternal vasculature (Müller et al., 2015). This result supported a local role for CEPR1 in the 107

control of seed size and yield through activity in the mother tissue. Finally, we used 108

transcriptional profiling of key marker genes to demonstrate a perturbation of nitrogen status 109

in cepr1 bolts. Collectively, the results reveal a role for CEP-CEPR1 signalling that involves 110

local activity in the bolt to control nitrogen mobilisation and delivery to reproductive sinks. 111

Results 112

CEPR1 controls vegetative growth, reproductive development and seed yield 113

We explored whether CEPR1 plays a role in vegetative and reproductive development by 114

examining two independent knockout mutant alleles in the No-0 and Col-0 backgrounds 115

(cepr1-1 and cepr1-3, respectively) (Tabata et al., 2014; Chapman et al., 2019). Both cepr1 116

knockout mutants displayed a ~30% retardation in rosette growth (Fig. 1, A-C). Since 117

vegetative leaves mobilise resources to the bolt and other reproductive tissues, we examined 118

whether loss of CEPR1 function affected yield. The cepr1 mutants displayed a reduction in 119

the growth of reproductive tissues (Fig. 1, D and E), and the number of reproductive units 120

(siliques, flowers and buds) on the main inflorescence was reduced by ~10% in cepr1-1 and 121

~40% in cepr1-3 (Supplemental Fig. S1). The diminished reproductive capacity correlated 122

with a substantial reduction in the total seed yield per plant of ~88% and ~98% in cepr1-1 123

and cepr1-3, respectively (Fig. 1, F and G). The reduced seed yield resulted from a lower 124

seed number and a 12-25% reduction in seed weight (Fig. 1, H and I). In general, the limited 125

seeds produced by the cepr1 mutants were smaller and more diverse in size compared to 126

wild-type (WT) seeds (Fig. 1, J and K). These results demonstrate that CEPR1 knockout 127

reduces vegetative growth as well as seed size and yield. 128

CEPR1 activity controls the proper development of reproductive organs 129



6

The severe reductions in cepr1 seed yield (~88-98%) seemed disproportionate to the decrease 130

in vegetative growth (~30%) and reduced number of reproductive units per main 131

inflorescence (~10-40%). Therefore, we examined if CEPR1 knockout mutants had 132

additional effects on reproductive development. An examination of floral development in the 133

cepr1 mutants (Fig. 2) revealed chlorosis in the sepals of the developing buds and those of 134

the open flowers (Fig. 2, A-H), and anthocyanin accumulation in the apical region of the 135

main stem, pedicle and valves of the siliques, especially in cepr1-3 (Fig. 2, E-H). This 136

anthocyanin accumulated in the cepr1 silique valves shortly after fertilisation (stage 14; 137

Smyth et al., 1990), intensified during silique elongation (stages 15-17) and subsided as the 138

silique reached full length (late stage 17) (Fig. 2E-H). 139

We examined the preanthesis floral structure in dissected stage 12 flowers of WT No-0 and 140

cepr1-1 (Fig. 2, I and J). The cepr1-1 flowers were smaller than WT No-0, but retained the 141

relative dimensional ratios between the different floral organs. There was a clear 142

differentiation of the sub-structures of the cepr1-1 gynoecium (i.e. stigma, style, valves and 143

replum), but, like the sepals, these tissues were chlorotic compared to WT No-0 (Fig. 2J). 144

Post-anthesis cepr1-1 flowers (stage 13) were smaller and chlorotic compared to WT No-0, 145

but the anthers still elongated and deposited pollen on the stigma similarly to WT No-0 (Fig. 146

2, M and N). 147

Floral development in the Col-0 cepr1-3 mutant was impaired more severely than in the No-0 148

mutant, and it was not possible to determine floral stage by the conventional landmark 149

developmental events (Smyth et al., 1990). Instead we determined floral buds equivalent to 150

WT Col-0 stage 12, based on the relative position of the bud within the inflorescence from 151

the most recent anthesed flowers. Although the cepr1-3 sepals were of similar size to those 152

of Col-0, there was a severe underdevelopment of the organs in the inner whorls (Fig. 2, K 153

and L). The cepr1-3 gynoecium was typically ‘pear-shaped’ and stunted, with a translucent 154

appearance (Fig. 2L). In cepr1-3, the petals expanded and the anthers elongated and dehisced, 155

however, the stunting of the gynoecium resulted in a state of near hercogamy (i.e. reduced 156

self-pollination; Fig. 2, O and P). We observed only occasional deposition of cepr1-3 pollen 157

from the shorter medial stamens onto the poorly developed stigma. Collectively, these results 158

show that loss of CEPR1 activity perturbs floral and reproductive organ development, with 159

the impact being more severe in Col-0 cepr1-3 compared to No-0 cepr1-1. This suggests that 160



7

background genetic differences between the Col-0 and No-0 accessions modify the severity 161

of the reproductive development defects resulting from a CEPR1 knockout. 162

CEPR1 positively influences seed yield on a per silique basis 163

Since the loss of CEPR1 function affected flower development, we investigated whether 164

there were effects on yield per silique in cepr1 (Fig. 3). First, we assessed siliques of self-165

pollinated plants and observed that cepr1 mutants had a higher incidence of unfertilised 166

ovules, and of seeds that had aborted at various stages of development (Fig. 3, A and B). The 167

reduction in seed set per silique was particularly severe in cepr1-3, and worsened acropetally. 168

Therefore, we quantified seed set across silique positions (Fig. 3, C and D). In WT No-0, 169

seed set steadily improved with increasing silique positions up the stem, reaching a maximum 170

at approximately silique 14 (Fig. 3C). The cepr1-1 mutant also showed an improving seed 171

set with increasing silique position up the main shoot, albeit at a decreased rate compared to 172

WT No-0. Maximum seed set in cepr1-1 was lower compared to WT No-0 (Fig. 3C). Seed 173

set in WT Col-0 was minimal in the first silique, and increased to a maximum at 174

approximately silique 6 (Fig. 3D). In contrast to WT Col-0, cepr1-3 had maximal seed set in 175

the first silique, which decreased with increasing silique position (Fig. 3D). We observed nil 176

seed set from silique number 12 onwards in cepr1-3. For siliques with non-zero fecundity, the 177

average seed set was significantly lower in cepr1-1 and cepr1-3 compared to their respective 178

WT lines (Fig. 3, E and F). Moreover, the frequency of clearly fertilised and then aborted 179

seeds (i.e. late aborting seed) was higher in both cepr1 mutants compared to their respective 180

WT lines, and this phenotype was particularly severe in cepr1-3 (Fig. 3, G and H). 181

We conducted reciprocal crosses to determine whether the more severe seed set reduction in 182

cepr1-3 was due to a male and/or female reproductive defect (Fig. 3I). Pollen from cepr1-3 183

fertilized WT pistils without impairment, which suggested that there was no appreciable 184

decrease in cepr1-3 pollen viability. The reduced fecundity of the cepr1-3 pistil compared to 185

the WT held true regardless of pollen genotype. As mechanical pollination would overcome 186

pollen deposition defects resulting from asynchronous anther-gynoecium development in 187

cepr1-3 (Fig. 2, O and P), we reasoned that a female reproductive defect limits cepr1-3 seed 188

set. 189

To further explore this female fertility defect, we examined fertilisation frequency depending 190

on ovule position in the pistil. Such analysis helps distinguish between problems with pollen 191



8

transmission and ovule-specific defects (Kay et al., 2013; Groszmann et al., 2020). As cepr1 192

mutants in both backgrounds had fewer ovules per pistil than WT (Supplemental Fig. S2), we 193

assessed seed set at normalised ovule positions within the carpels, from position zero (closest 194

to stigma) to position one (closest to gynophore) (Fig. 3, J and K). Compared to WT No-0, 195

cepr1-1 showed a similar, albeit more accentuated, position-dependent fertilisation pattern in 196

the pistil (Fig. 3J). As expected, ovules of WT Col-0 pistils showed a high and mostly 197

position-neutral fertilisation frequency (Fig. 3K). In stark contrast, the fertilisation rate in 198

cepr1-3 was very low at the stigma end and gradually increased towards the proximal region 199

of the pistil, eventually reaching WT Col-0 levels (Fig. 3J). The high fertilisation rate of 200

ovules furthest from the stigma in cepr1-3 demonstrates that pollen tubes can traverse the 201

entire distance of the transmitting tract tissue. This indicates that the defect responsible for 202

the reduced ovule fertility is not in the female pollen transmitting tissues (e.g. stigma and 203

transmitting tract), but rather is specific to the ovules. This fertilisation pattern of cepr1-3 204

correlated spatially with the poor development of the distal region of the gynoecium (Fig. 2 L 205

and P). 206

CEPR1 activity controls seed filling 207

One component of the yield decrease in cepr1 is a reduction in mature seeds per silique due 208

to a reduced ovule number, lower fertility rate and an increased incidence of seed abortion. 209

In addition, cepr1 seeds that successfully progress to maturity are smaller than WT seeds, 210

further contributing to the lower yield. Normally plants with a reduced seed number tend to 211

compensate by having larger seeds, which is due to a greater proportional allocation of the 212

available nutrients being remobilised from the rosette (Bennett et al., 2012). Therefore, the 213

small mature seeds of cepr1 may reflect a deficiency in nutrient supply to the seeds. This 214

may arise due to its smaller source rosette and hence, a proportionately lower per seed 215

availability of nutrients; or alternatively, due to a reduced capacity of cepr1 plants to deliver 216

nutrients from the source rosette to the seed. To test these possibilities, we manipulated 217

nutrient allocation from the rosette (source) by thinning the number of competing 218

reproductive organs (sinks), to improve the source-to-sink ratio in favour of larger seeds in 219

the siliques that remained (Bennett et al., 2012). As expected, we found that seed size 220

increased in response to the thinning of WT plants, however, an increase in seed size did not 221

occur in cepr1-1 despite improving the source-to-sink ratio (Fig. 4). This result suggests that 222



9

CEPR1 is required for the redistribution and/or delivery of resources for seed filling, and in 223

doing so, controls seed size. 224

CEPR1 control of seed size depends on CEPR1 activity in the reproductive bolt 225

We undertook reciprocal bolt grafting between WT and cepr1-1 to elucidate if CEPR1 226

activity in the vegetative tissues or reproductive tissues determined seed size (Fig. 5, A and 227

B; Supplemental Fig. S3). Early observations of established grafted bolts revealed that both 228

the chlorosis, and the accumulation of anthocyanins in the siliques and inflorescence stem, 229

persisted in cepr1 bolts even when grafted onto WT stock (Fig. 5C). This result suggested 230

that juvenile cepr1 bolts derived little or no additional nutritional benefit from the WT stock. 231

At maturity, we harvested the seeds and other dry bolt materials (i.e. stem, cauline leaves, 232

floral and silique material) to assess the effect of graft combination on seed size and yield. 233

We found that the smaller size of seeds produced by cepr1 bolts could not be rescued by 234

grafting to a WT stock (Fig. 5D). In contrast, there was no penalty to the seed size of WT 235

bolts when grafted to cepr1-1 stock (Fig. 5D). Furthermore, the distribution of seed size for 236

WT bolts was more uniform than for cepr1-1 bolts regardless of the stock (Fig. 5E). This 237

suggests that local CEPR1 activity in the bolt controls seed size and its uniformity. A weak, 238

compensatory effect of vegetative CEPR1 activity was observed for cepr1-1 bolts grafted 239

onto a WT stock (i.e. cepr1-1/WT) with mild improvements in seed size uniformity 240

compared to cepr1-1 homografts (Fig. 5E). 241

CEPR1 activity controls total seed yield primarily in the reproductive bolt 242

Since the decrease in total seed yield of the cepr1-1 bolt could not be rescued by grafting to a 243

WT stock (Fig. 6A), a lack of CEPR1 activity in the bolt most likely limits yield in cepr1-1 244

plants. Moreover, there was no yield penalty to a WT bolt when grafted to a cepr1 stock, but 245

rather an apparent increase in total seed yield relative to the WT homografts (Fig. 6A). An 246

examination of the dry mass of harvested bolt material (excluding seed) revealed that WT on 247

cepr1-1 grafts had significantly greater bolt dry mass than the other graft combinations (Fig. 248

6B), consistent with the greater bolt growth observed for this graft combination at 26 days 249

(Fig. 5B). To account for differences in bolt growth, we calculated the ratio of seed yield to 250

total bolt biomass (bolt harvest index) (Fig. 6C). The bolt harvest index of WT on cepr1-1 251

grafts was not different to WT homografts. Compared to the cepr1-1 homografts, the bolt 252

harvest index of cepr1-1 slightly improved when grafted to a WT stock (increasing from 253



10

~37% to ~50% of WT homografts). Therefore, whilst a WT stock could partially compensate 254

for a lack of CEPR1 in the bolt, the bolt harvest index was primarily determined by CEPR1 255

activity in the bolt. These results, together with the seed size data, show that CEPR1 bolt 256

activity controls reproductive development, seed size, and subsequently total yield. 257

CEPR1 is expressed in the vasculature of floral and reproductive organs 258

To help elucidate how CEPR1 influences reproductive development and fecundity, we 259

examined CEPR1 expression in reproductive organs using a 2kb CEPR1 promoter-GUS 260

reporter (pCEPR1:GUS). pCEPR1:GUS was expressed in the vasculature of the 261

inflorescence stem, the base of floral buds, as well as floral and reproductive organs (Fig. 7, 262

A and B). In flowers, expression was detected in the vasculature of well-developed sepals 263

and petals, elongated stamen filaments (Fig. 7; A, C and D), developing gynoecium prior to 264

fertilisation (Fig. 7E), mature gynoecium (Fig. 7F), and the growing silique (Fig. 7G). 265

CEPR1 expression in the maternal reproductive tissues appeared throughout the entire 266

vasculature network including the medial and lateral vascular strands, the terminating 267

vascular bundles in the style, and the vasculature of the funiculus right to the point of 268

termination within the chalazal seed coat (Fig. 7, F-H). We observed CEPR1 expression 269

within the funiculus and chalazal seed coat only after fertilisation (Fig. 7E vs Fig. 7F) and it 270

persisted throughout seed development (Fig. 7, H and I). We detected no expression of 271

CEPR1 in the endosperm or embryo. 272

The restriction of seed pCEPR1:GUS expression to the chalazal seed coat is consistent with 273

publicly available expression data (Fig. 7J) (Belmonte et al., 2013; Arabidopsis eFP browser, 274

https://bar.utoronto.ca/efp/cgi-bin/efpWeb.cgi). CEPR1 expression in the chalazal seed coat 275

is important since it represents the final delivery point of nutrients via the vasculature from 276

the mother tissue prior to their uptake via a variety of transporters to the symplasmically 277

isolated filial tissues (Stadler et al., 2005; Chen et al., 2015; Müller et al., 2015; Phan et al., 278

2020). The lack of pCEPR1:GUS or CEPR1 mRNA expression in the endosperm or embryo 279

tissue indicates that CEPR1 control of seed size occurs strictly through activity in the mother 280

tissue. Consistent with this, restoring WT CEPR1 in only the filial tissue of the cepr1-3 281

mutant via crossing (i.e. cepr1-3 ♀ x WT Col-0 ♂) did not improve seed size (Supplemental 282

Fig. S4). 283

Transgenic CEPR1 rescues cepr1 reproductive and yield defects 284



11

We complemented both cepr1 mutants using a transgene containing CEPR1 driven by the 285

same 2kb upstream sequence used in our GUS reporter expression analysis (Fig. 8). The 286

examination of multiple complemented lines revealed that the transgene rescued several 287

obvious cepr1 developmental defects (e.g. anthocyanin accumulation in stem and silique, 288

smaller chlorotic flowers, and aberrant floral organ morphology; Fig. 8, A and B). Further 289

analysis of two independent complemented lines of each cepr1 allele demonstrated full or 290

substantial rescue of ovule number (Fig. 8, C and G), seed set (Fig. 8, D and H), seed 291

abortion (Fig. 8 E and I), and seed size (Fig. 8 F and J). These results indicate that the 2kb of 292

sequence upstream of CEPR1 is sufficient for native CEPR1 function and imply that a loss of 293

CEPR1 expression in the vasculature is the causal factor leading to the developmental, 294

reproductive, and yield defects associated with the cepr1 mutants. 295

CEPR1 regulates the expression of genes involved in nitrogen homeostasis in the 296

reproductive bolt 297

Anthocyanin accumulation and chlorosis are signs of imbalances in nitrogen and carbon, 298

especially where nitrogen is low and carbon is in proportional excess (Takatani et al., 2014). 299

Therefore, nutritional limitation may account for the cepr1 defects in floral morphology, 300

lower fecundity, the high incidence of seed abortion and its smaller, more variable seed sizes. 301

To investigate this, we harvested bolt and inflorescence tissues and surveyed the expression 302

of several genes involved in the CEP-CEPR1 signalling pathway along with several genes 303

involved in nitrogen and carbon homeostasis (Fig. 9). CEP DOWNSTREAM 1 (CEPD1), 304

which is positively regulated by CEP-CEPR1 signalling in shoots (Ohkubo et al., 2017), was 305

downregulated ~8-fold in the cepr1 bolt tissue (Fig. 9A). Three out of four CEP ligand-306

encoding genes known to be expressed in the bolt (Roberts et al., 2013; Col-0 accession) 307

were also differentially expressed in the cepr1 mutants. CEP5 and CEP9 were strongly 308

upregulated (~32-fold), CEP2 was downregulated in cepr1-3 (~3-fold) and undetectable in 309

the No-0 background, and CEP1 expression was not significantly altered (Fig. 9A). The 310

cepr1 mutants had a ~60% reduction in the expression of GLUTAMINE SYNTHETASE 1;2 311

(GLN1;2) (Fig. 9B), which encodes the main isozyme contributing to glutamine synthetase 312

activity in the shoot (Guan et al., 2016), and is known to be involved in nitrogen mobilisation 313

and yield formation (Diaz et al., 2008; Guan et al., 2016; Moison et al., 2018). The 314

expression of the nitrate reductase gene NITRATE REDUCTASE1 (NIA1), also involved in 315

nitrogen metabolism (Wilkinson and Crawford, 1993), was not significantly different. The 316



12

expression of USUALLY MULTIPLE ACIDS MOVE IN AND OUT TRANSPORTERS 14 317

(UMAMIT14), an amino acid transporter gene linked to seed filling (Müller et al., 2015), was 318

strongly downregulated in the cepr1 mutants (>80% reduction; Fig. 9B). In contrast, 319

UMAMIT11 and UMAMIT18/SILIQUES ARE RED 1 (SIAR1), which also supply assimilated 320

nitrogen as amino acids to reproductive tissues (Ladwig et al., 2012; Müller et al., 2015), 321

were not differentially expressed in the cepr1 mutants (Fig. 9B). Consistent with the 322

observed anthocyanin accumulation in cepr1 stems, there was a substantial upregulation in 323

the cepr1 mutants of one or both of the low nitrogen-induced MYB transcription factors 324

PRODUCTION OF ANTHOCYANIN PIGMENT 1 (PAP1) and PAP2, which are involved in 325

anthocyanin production when nitrogen is limited (Scheible et al., 2004; Lea et al., 2007; 326

Rubin et al., 2009) (Fig. 9B). 327

Unlike some of the nitrogen-associated genes, marker genes responding to elevated carbon 328

(Nunes et al., 2013; Cookson et al., 2016) were not substantially altered in the cepr1 mutants. 329

Specifically, AKINBETA1 and the putative trehalose-6-phosphate synthase (TPS) genes, 330

TREHALOSE PHOSPHATE SYNTHATSE 8 (TPS8) and TPS10, which are normally 331

downregulated in response to elevated carbon levels, were either mildly downregulated or 332

unaltered in the cepr1 mutants (Fig. 9C). The ARABIDOPSIS THALIANA BASIC LEUCINE-333

ZIPPER 11 (bZIP11) and TPS5 genes, which positively respond to elevated carbon levels, 334

remained unchanged (Fig. 9C). Together with the nitrogen-associated transcripts, the 335

expression profiles of cepr1 bolts implies a state of nitrogen limitation with minimal or no 336

perturbations to carbon status. 337

Discussion 338

In this study we demonstrated a function for CEPR1 in controlling seed yield via a local 339

circuit in the reproductive tissues of Arabidopsis. The severely decreased yield of cepr1 340

mutants is due to a loss of vasculature-expressed CEPR1, which compromises bolt growth, 341

female reproductive development, seed set, and mature seed size, and in addition, causes 342

chlorosis and anthocyanin accumulation in inflorescence tissues. The complementation of 343

cepr1 mutants using a CEPR1 genomic fragment rescues these diverse phenotypes. 344

Underpinning these phenotypes of the cepr1 mutants is the apparent common theme of an 345

inability to mobilise nutrients, specifically nitrogen, either from the vegetative tissues to the 346

young bolts or from within bolt tissues to the developing floral organs and seeds. Several 347

lines of evidence support this view. 348



13

First, the cepr1 reproductive tissues showed chlorosis in the bolt tissues and floral organs, 349

and anthocyanin accumulation in the inflorescence stems and siliques. The grafting of young 350

cepr1 bolts onto WT vegetative stocks did not remedy these well-documented phenotypes of 351

nutrient limitation stress, suggesting a compromise of nutrient delivery from the vegetative 352

tissue to the young cepr1 bolt. Concordantly, young WT bolts did not develop chlorosis or 353

accumulate anthocyanins when grafted onto cepr1 vegetative stocks. 354

The grafting of cepr1 bolts onto WT vegetative stocks did not restore yield or a normal seed 355

size distribution, whereas WT bolts had no reduction in yield or seed size when grafted to 356

cepr1 vegetative stocks. In agreement with a role for CEPR1 in seed filling through the 357

control of nitrogen mobilisation and delivery, we found that both GLN1;2 and UMAMIT14 358

were down-regulated in the cepr1 reproductive bolt. The cytosolic glutamine synthetase 359

(GS) encoded by the vasculature-expressed GLN1;2 contributes to nitrogen remobilisation 360

from source tissues for seed filling (Moison et al., 2018), with gln1;2 loss-of-function 361

mutants displaying reduced seed size and yield similar to cepr1 (Guan et al., 2015). The 362

importance of cytosolic GS in seed filling appears conserved across diverse species including 363

maize (Zea mays) (Martin et al., 2006). The UMAMIT14 amino acid transporter is also 364

expressed throughout the plant vasculature, including the chalazal seed coat, where it is 365

required for the unloading of amino acids transported from source tissues to support seed 366

filling. Consistent with the decreased UMAMIT14 expression in the cepr1 mutants, the 367

umamit14 null mutants produce smaller seeds (Müller et al., 2015). 368

Improving nutrient allocation by thinning the number of reproductive units resulted in the 369

expected increased seed size in WT plants, but not in cepr1 mutants. The differential effect 370

of thinning between WT and cepr1 is not due to the smaller cepr1 rosettes, because grafting 371

showed that the cepr1 rosettes support the flourishing of WT bolts. Moreover, this grafting 372

result implies that the cepr1 source rosettes are still able to sufficiently load nutrients such as 373

amino acids into the phloem for export to the developing bolts (Santiago and Tegeder, 2016). 374

Therefore, the seeds of cepr1 plants that were thinned appear unable to receive the expected 375

allocation of surplus nutrient that clearly benefits the seeds of thinned WT plants. 376

CEPR1 expression was detected throughout the vasculature of reproductive tissues, 377

consistent with a function in nutrient mobilisation/delivery. The specific expression of 378

CEPR1 in the chalazal seed coat, but not in any other seed tissues, is pertinent to the cepr1 379

seed size defect since this tissue is the final delivery point of nutrients from the mother tissue 380



14

via the vasculature prior to their uptake via transporters to the symplasmically isolated filial 381

tissues (Müller et al., 2015). This localisation points to CEPR1 playing an important role in 382

nutrient unloading at the seed and indicates that it controls seed development and size strictly 383

through activity in the maternal tissue. An impairment of nutrient delivery to the seed would 384

be consistent with the more variable seed size and higher rates of seed abortion observed in 385

the cepr1 mutants, with seed abortion occurring in instances where early nutrient demands of 386

the embryo are not met (Di Berardino et al., 2018), and with the more variable mature seed 387

sizes reflecting inconsistency in nutrient delivery. 388

Our RT-qPCR data indicates that the nutrient stress caused by a loss of CEPR1 function is 389

related to impaired nitrogen status of the reproductive bolt. Consistent with a low nitrogen 390

state and anthocyanin accumulation, cepr1 bolts displayed a strong upregulation of one or 391

both of the MYB transcription factors PAP1 and PAP2. These PAP genes are highly 392

upregulated in response to nitrogen starvation and positively regulate anthocyanin 393

biosynthesis (Lea et al., 2007; Rubin et al., 2009). The downregulation of the glutamine 394

synthetase gene GLN1;2 and UMAMIT14 would be consistent with decreased levels of 395

assimilated nitrogen compounds (Patterson et al., 2010; Besnard et al., 2016). By contrast, 396

the mild downregulation of carbon-repressed TPS genes and the unchanged expression of 397

carbon-induced transcripts in cepr1 bolts implies a sufficient carbon supply. A decreased 398

nitrogen-state but steady carbon-state in cepr1 mutants is further supported by their 399

accumulation of anthocyanins, which in general is not just a symptom of nitrogen limitation, 400

but rather a symptom of excess levels of carbon relative to nitrogen (Takatani et al., 2014). 401

Moreover, several CEP-CEPR1 pathway genes both upstream (i.e. several CEP genes) and 402

downstream (i.e. CEPD1) of CEPR1 displayed altered expression in cepr1 bolts, consistent 403

with a locally perturbed CEPR1-signalling status involving both feedforward and feedback 404

loops. Similar transcriptional perturbations occur to CEP-CEPR1 pathway genes locally in 405

cepr1 root tissues (Chapman et al., 2019). These transcriptional responses, together with 406

CEPR1 expression in the vasculature of reproductive tissues and the dependence of seed size 407

and yield on local CEPR1 activity, demonstrates that CEPR1 specifically acts in bolt tissues 408

to control aspects of nitrogen mobilisation and delivery to reproductive sinks. 409

Finally, an impairment in the nitrogen economy of the bolt can also explain the cepr1 410

fecundity and silique defects. Nutrient deficiency is consistent with the diminished growth of 411

the bolt and the reduced number of reproductive units produced (i.e. flowers and siliques) 412



15

(Perchlik and Tegeder, 2018). The aberrant and asynchronous development of the cepr1 413

gynoecium and stamens contributing to the reduced seed number on a per silique basis, is 414

comparable with the miscoordination of reproductive development occurring in rice florets 415

when nitrogen is limited by loss-of-function mutations in arginase (OsARG) or ornithine δ-416

aminotransferase (OsOAT) (Ma et al., 2013; Liu et al., 2018). Similar to cepr1, these rice 417

mutants display reduced seed set and smaller seed/grain. The accumulation of anthocyanins 418

observed in cepr1 developing siliques is identical to the phenotype of mutants in the amino 419

acid transporter gene UMAMIT18/ SIAR1 and is likely a stress symptom of inadequate 420

nitrogen provision during the nutrient demanding stages of seed development (Ladwig et al., 421

2012). The miscoordination of reproductive development along with the altered expression 422

of some nitrogen-related genes in the cepr1 bolt, is consistent with CEPR1 acting as one node 423

of a complex network regulating nitrogen homeostasis (Castaings et al., 2010; Tegeder and 424

Masclaux-Daubresse, 2018). 425

Conclusions 426

In this paper, we show that CEPR1 activity in the reproductive tissue is critical for both 427

reproductive development and yield. Our data highlights the importance of CEPR1 activity in 428

the reproductive bolt for the delivery of nutrients for yield formation. The apparent 429

perturbation of nitrogen status in cepr1 bolts suggests that CEPR1 plays a broader role in 430

controlling nitrogen homeostasis at the whole-plant level, beyond roles previously identified 431

in root nitrogen acquisition, root system architecture and nodulation (Huault et al., 2014; 432

Tabata et al., 2014; Mohd-Radzman et al., 2016; Ohkubo et al., 2017; Chapman et al., 2020). 433

The manipulation of CEPR1-dependent outputs could provide a new avenue to improve 434

nutrient delivery from source tissues to reproductive sinks, with the aim of improving traits 435

such as seed yield and nitrogen use efficiency in plants. 436

Material and Methods 437

Plant materials and growth conditions 438

The previously described Arabidopsis (Arabidopsis thaliana) No-0 cepr1-1 (RATM11-2459; 439

RIKEN) (Bryan et al., 2012; Tabata et al., 2014) and Col-0 cepr1-3 (467C01; GABI-Kat) 440

(Kleinboelting et al., 2012; Chapman et al., 2019) mutant lines were used. Sterilised seedlings 441

were grown on solidified media (1% w/v Type M agar) containing ½ strength Murashige–442

Skoog (MS) basal salts (Sigma) at pH 5.7 for 7-10 days until seedlings were transferred to 443



16

soil (seed raising mix; Debco, Bella Vista NSW) supplemented with Osmocote Exact 444

fertiliser and grown in chambers at 22 °C. For the grafting experiment, plants were grown 445

with 200 µmol m-2 s-1 light and an 8 h photoperiod. For all other experiments, plants were 446

grown with 100 µmol m-2 s-1 light and a 16 h photoperiod. 447

Determination of seed size, seed set and yield parameters 448

Inflorescences were covered with microperforated plastic bags to collect seeds. To determine 449

single seed mass, aliquots were weighed and seed number per aliquot counted. Seed area was 450

determined using ImageJ (https://imagej.nih.gov/ij/) using the ‘particle analysis’ function 451

with a consistently applied ‘threshold’ on all microscope images of seeds taken with identical 452

magnification and exposure time within experiments (Herridge et al., 2011). For seed size 453

distributions, the percentage of seeds within bins at 0.002 mm2 intervals was determined and 454

a running average over six bins was plotted. For controlled pollination, preanthesis flowers 455

(Smyth et al., 1990; stage 12) were emasculated using forceps. One day after emasculation, 456

the pollen from the donor genotype was applied to the stigma of the recipient genotype. Seed 457

development and seed set was determined by dissecting developing siliques and dehisced 458

siliques, respectively (Groszmann et al., 2008; Kay et al., 2013). For the grafting experiment, 459

bolt harvest index was determined as the seed mass as a proportion of total bolt biomass (seed 460

mass/total bolt dry mass including seed). 461

Vector Construction 462

To generate the pCEPR1:GUS reporter, the 2 kb of sequence upstream of the start codon of 463

CEPR1 was amplified from Col-0 gDNA, cloned into pENTR/D-TOPO, and then transferred 464

into the pHGWFS7 destination vector (Karimi et al., 2002) by LR recombination. To 465

generate the CEPR1 complementation construct, the kanamycin marker for plant selection in 466

the pBI121 vector was first removed by digestion with PmeI and ApaI and was replaced 467

using Gibson Assembly (NEB) with a Basta selection marker amplified from the MIGS2.1 468

vector (de Felippes et al., 2012). Using Gibson Assembly, the Col-0 CEPR1 genomic 469

fragment and 2 kb of upstream sequence, was cloned upstream of a NOS terminator in the 470

modified pBI121 vector cut with SacI and ClaI. Primer sequences used for cloning are listed 471

in Supplemental Table S1. 472

Plant transformation and introgression of constructs 473


https://imagej.nih.gov/ij/


17

Plants were transformed by floral dipping (Clough and Bent, 1998) with the A. tumefaciens 474

strain LBA4404 harbouring the described vectors to create the pCEPR1:GUS reporter line 475

(No-0 background) and the cepr1-1 complementation lines (comp #1 and comp #2). Due to 476

the severely impaired female fertility in cepr1-3, which prevented the direct transformation of 477

this mutant, the complementation lines in the cepr1-3 background (comp #3 and comp #4) 478

were generated by crossing with WT Col-0 transformed with the complementation construct. 479

Flowers from independent Col-0 lines harbouring the CEPR1 complementation construct 480

were emasculated and then pollinated using cepr1-3 pollen. F2 plants homozygous for the 481

cepr1-3 allele (i.e. no endogenous WT CEPR1) and carrying the CEPR1 transgene were 482

identified using PCR genotyping (see Supplemental Table S1 for primers). 483

Thinning experiment 484

Six-week-old No-0 (WT) and cepr1-1 plants were thinned by removal of siliques and flowers 485

in addition to secondary and lateral apexes so that only three or four open flowers or very 486

early stage siliques remained on the primary stem. Seeds from thinned plants were compared 487

to those from unpruned controls. 488

Inflorescence stem (bolt) grafting 489

Bolt grafting was carried out as described in Nisar et al. (2012). Briefly, young No-0 (WT) 490

and cepr1-1 bolts (~80 mm long) were excised ~20 mm from the base. The end of the donor 491

bolt was cut into a wedge, which was inserted into a vertical incision made in the remaining 492

basal stem section of the recipient stock. The graft junction was stabilised with silicon tubing 493

2-2.5 mm (inner diameter) and covered with parafilm to retain moisture. Plants were kept in a 494

humid environment using a plastic covering until grafted bolts had re-established turgor and 495

growth. Bolts that did not take, or that grew poorly as determined by the appearance of 496

necrotic cauline leaves were discarded. Secondary branches that formed from the stock post 497

grafting were continuously removed so that the final reproductive organs were derived from 498

the donor bolt only. 499

Promoter-GUS Reporter analysis 500

GUS staining and analysis was performed essentially as previously described (Groszmann et 501

al., 2010; Groszmann et al., 2011). Briefly, samples were harvested into cold phosphate 502

buffer (pH 7) with 4% v/v formaldehyde, washed in cold phosphate buffer, transferred into a 503

2mM X-gluc staining solution, incubated at 37°C for specified durations and then cleared for 504



18

24 hrs in 70% ethanol, fixed for 24 hrs in 70% ethanol plus FAA (3.7% (v/v) formaldehyde 505

and 5% (v/v) acetic acid), washed again and stored in 70% ethanol ready for visualisation. 506

Microscopy 507

Microscopic imaging was carried out with a M205 FA stereomicroscope with a DFC550 508

camera (Leica). 509

Complementation analyses 510

T2 complementation lines in the cepr1-1 background (comp #1 and comp #2) were grown 511

alongside WT No-0 and cepr1-1. PCR genotyping identified cepr1-1 plants harbouring the 512

complementation transgene and null (azygous) segregants. Azygous segregants were pooled 513

with the cepr1-1 plants grown in parallel for the analysis. 514

For complementation lines in the cepr1-3 background (comp #3 and comp #4), segregating 515

F2 plants were grown alongside WT Col-0 and cepr1-3. PCR genotyping identified 516

homozygous cepr1-3 plants harbouring the complementation CEPR1 transgene. For the 517

analysis, WT Col-0 and cepr1-3 segregants identified from the F2 populations were pooled 518

with the WT Col-0 and cepr1-3 plants grown in parallel, respectively. See Supplemental 519

Table S1 for genotyping primers used. 520

RT–qPCR analyses 521

WT and cepr1 primary inflorescence tissue (including stem, inflorescence meristem, buds 522

and flowers) was harvested for analyses upon opening of the first flower. The lateral organs 523

(cauline leaves, developing branches and buds) were removed from the harvested tissue 524

before they were snap-frozen in liquid nitrogen. Three biological samples per genotype, each 525

containing two bolts, were used, and total RNA was isolated by a modified Trizol extraction 526

method using columns from the RNeasy Plant Mini Kit (QIAGEN) (Delay et al., 2013b). 527

cDNA synthesis was carried out using oligo(dT)12–18 primers and Superscript III reverse 528

transcriptase (Invitrogen), and was followed by treatment with RNase H (Invitrogen). For 529

RT–qPCR, Fast SYBR Green fluorescent dye (Applied Biosystems) was used and samples 530

were run on a ViiA 7 Real-Time PCR System (Applied Biosystems) following 531

manufacturer’s specifications. Data were analysed using the ΔΔCT method (Livak and 532

Schmittgen, 2001), with EF1α (At1g07920) expression used for normalisation (Czechowski 533

et al., 2005). RT-qPCR primers are listed in Supplemental Table. S1. 534



19

Accession numbers 535

The AGI locus codes for genes discussed in this study are as follows: CEPR1 (AT5G49660), 536

CEPD1 (AT1G06830), CEPD2 (AT2G47880), CEP1 (AT1G47485), CEP2 (AT1G59835), 537

CEP5 (AT5G66815), CEP9 (AT3G50610), UMAMIT11 (AT2G40900), UMAMIT14 538

(AT2G39510), UMAMIT18/SIAR1 (AT1G44800), PAP1 (AT1G56650), PAP2 539

(AT1G66390), NIA1 (AT1G77760), GLN1;2 (AT1G66200), AKINBETA1 (AT5G21170), 540

TPS5 (AT4G17770), TPS8 (AT1G70290), TPS10 (AT1G60140), bZIP11 (AT4G34590). 541

Supplemental data 542

Supplemental Figure S1. CEPR1 mutants have reduced reproductive units per main stem. 543

Supplemental Figure S2. CEPR1 knockout results in a reduced number of ovules per silique 544

Supplemental Figure S3. Rosette diameter of plants grown under a short day (8 hr) 545

photoperiod for bolt grafting. 546

Supplemental Figure S4. CEPR1 controls seed size via activity in the maternal tissue. 547

Supplemental Table S1. List of oligos used. 548

549

Acknowledgements 550

We thank Katia Taylor (Australian National University and University of Zurich) and the 551

Grossniklaus lab (University of Zurich) for helpful discussions, and Nazia Nisar (Australian 552

National University) for bolt grafting technical advice. We thank Bernd Weisshaar, MPI for 553

Plant Breeding Research, Cologne for the T-DNA mutant line 467C01, and RIKEN (Japan) 554

for providing the RATM11-2459 line. We thank Aleu Mani George and Baxter Massey for 555

technical assistance. We acknowledge the National Collaborative Research Infrastructure 556

Strategy (NCRIS) of the Australian Government, for supporting The Australian National 557

University with the growth facilities utilised as part of the Australian Plant Phenomics 558

Facility. 559

Figure legends 560

Figure 1. CEPR1 affects above-ground plant growth, yield and seed size. (A-C) CEPR1 561

mutants show decreased vegetative leaf growth. (A) Rosette diameter after 30 days post 562

germination (dpg) for No-0 and cepr1-1. n= 10. (B) Rosette diameter at 31 dpg for Col-0 and 563

cepr1-3. n=4-8. (C) Representative images of plants in B. Note, cepr1-3 rosette leaves 564

displayed no obvious chlorosis. Scale bar = 5 cm. (D-J) Loss of CEPR1 function results in 565



20

impaired yield. (D) Inflorescence stems of No-0 and cepr1-1 at 50 dpg. (E) Inflorescence 566

stems of Col-0 and cepr1-3 at 59 dpg. Scale bars in D and E = 100 mm. (F, G) CEPR1 567

mutants show reduced yield. Total seed yield per plant for (F) No-0 and cepr1-1 (n=6-10), 568

and for (G) Col-0 and cepr1-3 (n=4-8). (H-I) CEPR1 mutants have reduced seed size. Mass 569

of one seed for (H) No-0 and cepr1-1 (n=3 plants), and for (I) Col-0 and cepr1-3 lines (n=4 570

plants) determined from ~100 seeds per plant. Percentages above bars indicate mean as a 571

percentage of WT. Significant differences were determined by a two-sample t-test; **p˂0.01, 572

*** p˂0.001. Error bars = SE. Distribution of seed size for WT and cepr1 in the (J) No-0 and 573

(K) Col-0 backgrounds. n = 4-7 plants, 60-120 seeds per plant. 574

575

Figure 2. CEPR1 affects the development of reproductive organs. Representative images 576

showing floral and reproductive organ phenotypes of WT and cepr1 mutant plants in the No-577

0 and Col-0 accession. (A-D) Inflorescence of WT and cepr1 mutants. The developing buds 578

of CEPR1 knockout mutants are chlorotic. (E-H) Side view of the inflorescence showing 579

chlorotic sepals (sep.) and anthocyanin accumulation in the siliques, pedicle and main stem of 580

cepr1 (arrows). Arrow head in F indicates the fading of anthocyanin in older siliques. (I-P) 581

Medial view of dissected WT and cepr1 flowers showing the aberrant floral development 582

associated with CEPR1 knockout. (I-L) Preanthesis stage 12 WT and cepr1 flowers. Arrow 583

head in L indicates poorly developed distal end of cepr1-3 gynoecium. (M, N) Post-anthesis, 584

stage-13 flowers of WT No-0 and cepr1-1. (O, P) Post-anthesis, stage-14 flowers of WT Col-585

0 and cepr1-3. Scale bars = 1 mm. 586

587

Figure 3. Loss of CEPR1 function results in decreased seed set and a higher frequency 588

of seed abortion. (A,B) Representative images of dissected siliques from self-pollinated WT 589

and cepr1 lines in the (A) No-0 and (B) Col-0 backgrounds. Arrowheads indicate unfertilised 590

ovules. Asterisks indicate aborted seeds. Scale bars = 1 mm. (C,D) Seed set at silique 591

positions on the main stem (position 1 = first silique produced) for self-pollinated WT and 592

cepr1 lines in the (C) No-0 (n=4-6), and (D) Col-0 (n=3-6) backgrounds. Error bars show SE. 593

For each plant line, two separate linear trendlines were applied to the distinct subset of silique 594

positions before and after a plateau in seed set. (E,F) Average seed set determined from 595

siliques with non-zero seed set irrespective of silique position for self-pollinated WT and 596

cepr1 in the (E) No-0 background (n= 6 plants, 7-14 siliques per plant) and (F) Col-0 597

background (n= 5-6 plants, 2-15 siliques per plant). (G,H) Frequency of aborted seeds 598

observed at fertilised ovule positions for self-pollinated WT and cepr1 in the (G) No-0 599

background (n= 6 plants, 7-14 siliques per plant) and (H) Col-0 background (n= 5-6 plants, 2-600

15 siliques per plant). Significant differences in E-H determined by a two-sample t-test; 601

*p˂0.05, **p˂0.01, ***p<0.001. Error bars show SE. (I) Percentage seed set for controlled 602

pollination between Col-0 and cepr1-3 plants. Preanthesis flowers were emasculated prior to 603

deposition of donor pollen onto recipient pistils. Significant differences determined by 604

ANOVA followed by Tukey HSD test (alpha=0.05). n=4-6 siliques from 3 plants. Error bars 605

show SE. (J,K) Fertilisation frequency at ovule positions for self-pollinated WT and cepr1 in 606

the (J) No-0 background (n= 6 plants, 7-14 siliques per plant) and (K) Col-0 background (n= 607

5-6 plants, 2-15 siliques per plant). Each position is represented as a fraction of the highest 608



21

position observed in at least 3 plants per genotype (0 = stigma end; 1 = gynophore end). 609

Fertilisation frequency was determined from siliques with non-zero seed set. 610

Figure 4. CEPR1 determines the extent of seed filling. The resource availability per silique 611

was increased by thinning the number of reproductive sinks. (A) Images of No-0 (WT) and 612

cepr1-1 before (left) and after (right) thinning. Three to four open flowers or early stage 613

siliques were left at the apex of the main stem. (B) Relative seed area for thinned and 614

untreated plants. ANOVA followed by Tukey HSD test (alpha = 0.05), n=3 plants, 100-200 615

seeds per plant. Error bars show SE. 616

Figure 5. Seed size depends upon CEPR1 activity in the bolt. Young No-0 (WT) and 617

cepr1-1 bolts were excised approximately 2 cm from the base and grafted to a recipient stock, 618

which provided vegetative rosette and root tissues to the transplanted reproductive tissue. 619

Secondary branches that formed from the stock post grafting were continuously removed so 620

that the final reproductive organs were derived from the donor bolt only. The bolt and stock 621

genotypes are labelled above and below the horizontal line, respectively. (A,B) Reciprocal 622

grafting of WT and cepr1-1 plants. Representative images of plants (A) 0 and (B) 26 days 623

after grafting (bolt/stock genotype). Arrow heads in A indicate the graft junction. Scale bars = 624

5 cm. (C) Representative images of inflorescences from hetero-grafted plants. Note the 625

accumulation of anthocyanin in the siliques of cepr1-1 bolt-grafts. (D) Quantification of 626

single seed mass for grafted plants. Statistically significant differences determined by 627

ANOVA followed by Tukey HSD test (alpha = 0.05), n = 6-9. (E) Distribution of seed size. n 628

= 6-9 plants, 100-200 seeds per plant. Error bars show SE. 629

Figure 6. Yield is primarily determined by CEPR1 activity in the reproductive bolt. (A-630

C) Analysis of yield on a per plant basis for reciprocal WT and cepr1-1 bolt grafted plants. 631

Quantification of (A) total seed yield, (B) bolt dry mass (minus seed), and (C) bolt harvest 632

index (the ratio of seed yield to total bolt biomass). Significant differences determined by 633

ANOVA followed by Tukey HSD test (alpha=0.05). Error bars show SE. n = 6-9 plants. 634

Figure 7. CEPR1 expresses in the vasculature of reproductive organs. pCEPR1:GUS 635

expression in the reproductive organs. (A) whole inflorescence, (B) buds, (C) stage 14 636

flower, (D) stage 15 gynoecium and stamens, (E) stage 12 gynoecium, (F) stage 14 637

gynoecium (s.v = style vasculature, m.v = medial vasculature, l.v = lateral vasculature), (G) 638

mature silique, (H) funiculus and chalazal seed coat (CZSC = chalazal seed coat, fun. = 639

funiculus), and (I) mature silique funiculus. Scale bars = 1 mm (A,C-G) or 0.1 mm (B,H,I). 640

Staining carried out for 18 h (A,D,G,I), 24 h (H) or 72 h (B,C,E,F). (J) Microarray expression 641

of CEPR1 in the developing seed from the Arabidopsis eFP browser; 642

https://bar.utoronto.ca/efp/cgi-bin/efpWeb.cgi; Belmonte et al., (2013). 643

Figure 8. Complementation of cepr1 mutants using a CEPR1 genomic fragment. 644

Reproductive development phenotypes were assessed for independent complementation 645

(comp) lines in the No-0 cepr1-1 (#1 and #2) and Col-0 cepr1-3 (#3 and #4) backgrounds 646

compared to their respective cepr1 mutant and WT lines. (A, B) Representative images 647

showing a side view of the inflorescence (upper panels) and dissected post-anthesis flowers 648

(lower panels) for lines in the (A) No-0, and (B) Col-0 ecotypes. (C, G) Quantification of 649

ovule number for siliques with non-zero fecundity for (C) No-0 (n=4-10, 2 siliques per plant), 650

and (G) Col-0 ecotype lines (n=3-11, 1-4 siliques per plant). (D,H) Measurement of seed set 651

for (D) No-0 (n=4-10) and (H) Col-0 ecotype lines (n=3-11). Two siliques were examined per 652



22

plant from positions on the stem corresponding to the phase of WT maximal seed set (see 653

Fig. 3C,D). (E,I) Frequency of aborted seeds observed at fertilised ovule positions for lines in 654

the (E) No-0 (n=4-10, 2 siliques per plant), and (I) Col-0 ecotypes (n=3-11, 1-4 siliques per 655

plant). (F,J) Seed area for (F) No-0 (n=6-11 plants) and (J) Col-0 ecotype lines (n=3-9 plants) 656

determined from 60-120 seeds per plant. Significant differences determined by ANOVA 657

followed by Fisher’s Least Significant Difference test (alpha = 0.05). Error bars show SE. 658

Figure 9. Loss of CEPR1 function affects the expression of genes involved in nitrogen 659

homeostasis in bolt tissue. For RT-qPCR analyses, the primary inflorescence tissue was 660

harvested from WT and cepr1 plants upon first flower opening. The fold change in 661

expression (log2) was determined for cepr1-1 and cepr1-3 relative to WT (No-0 and Col-0, 662

respectively) for a selection of (A) CEP-CEPR1 pathway genes, (B) genes related to nitrogen 663

(N) homeostasis, and (C) genes related to carbon (C) homeostasis. Significant differences 664

were determined by a two-sample t-test; *p<0.05 ,**p˂0.01, *** p˂0.001. Error bars show 665

SE, n=3 biological replicates each consisting of two pooled plants. n.d.; not detected. 666

667

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Parsed CitationsBelmonte MF, Kirkbride RC, Stone SL, Pelletier JM, Bui AQ, Yeung EC, Hashimoto M, Fei J, Harada CM, Munoz MD, et al (2013)Comprehensive developmental profiles of gene activity in regions and subregions of the Arabidopsis seed. Proc Natl Acad Sci 110:E435–E444

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

Bennett E, Roberts JA, Wagstaff C (2012) Manipulating resource allocation in plants. J Exp Bot 63: 3391–3400Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Besnard J, Pratelli R, Zhao C, Sonawala U, Collakova E, Pilot G, Okumoto S (2016) UMAMIT14 is an amino acid exporter involved inphloem unloading in Arabidopsis roots. J Exp Bot 67: 6385–6397


Bryan AC, Obaidi A, Wierzba M, Tax FE (2012) XYLEM INTERMIXED WITH PHLOEM1, a leucine-rich repeat receptor-like kinaserequired for stem growth and vascular development in Arabidopsis thaliana. Planta 235: 111–122


Castaings L, Marchive C, Meyer C, Krapp A (2010) Nitrogen signalling in Arabidopsis: how to obtain insights into a complex signallingnetwork. J Exp Bot 62: 1391–1397


Chapman K, Ivanovici A, Taleski M, Sturrock C, Ng JLP, Mohd-Radzman NA, Frugier F, Bennett M, Mathesius U, Djordjevic MA (2020)CEP receptor signalling controls root system architecture in Arabidopsis and Medicago. New Phytol doi:10.1111/nph.16483


Chapman K, Taleski M, Ogilvie HA, Imin N, Djordjevic MA (2019) CEP–CEPR1 signalling inhibits the sucrose-dependent enhancementof lateral root growth. J Exp Bot 70: 3955–3967


Chen L-Q, Lin IW, Qu X-Q, Sosso D, McFarlane HE, Londoño A, Samuels AL, Frommer WB (2015) A Cascade of Sequentially ExpressedSucrose Transporters in the Seed Coat and Endosperm Provides Nutrition for the Arabidopsis Embryo. Plant Cell 27: 607–619


Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant JCell Mol Biol 16: 735–743


Cookson SJ, Yadav UP, Klie S, Morcuende R, Usadel B, Lunn JE, Stitt M (2016) Temporal kinetics of the transcriptional response tocarbon depletion and sucrose readdition in Arabidopsis seedlings. Plant Cell Environ 39: 768–786


Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible W-R (2005) Genome-Wide Identification and Testing of Superior ReferenceGenes for Transcript Normalization in Arabidopsis. Plant Physiol 139: 5–17


Czyzewicz N, Yue K, Beeckman T, De Smet I (2013) Message in a bottle: small signalling peptide outputs during growth anddevelopment. J Exp Bot 64: 5281–5296


Delay C, Chapman K, Taleski M, Wang Y, Tyagi S, Xiong Y, Imin N, Djordjevic MA (2019) CEP3 levels affect starvation-related growthresponses of the primary root. J Exp Bot 70: 4763–4774


Delay C, Imin N, Djordjevic MA (2013a) Regulation of Arabidopsis root development by small signaling peptides. Front Plant Sci 4: 352Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Delay C, Imin N, Djordjevic MA (2013b) CEP genes regulate root and shoot development in response to environmental cues and arespecific to seed plants. J Exp Bot 64: 5383–5394

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https://scholar.google.com/scholar?as_q=CEP genes regulate root and shoot development in response to environmental cues and are specific to seed plants.&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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https://www.ncbi.nlm.nih.gov/pubmed?term=Di Berardino J%2C Marmagne A%2C Berger A%2C Yoshimoto K%2C Cueff G%2C Chardon F%2C Masclaux%2DDaubresse C%2C Reisdorf%2DCren M %282018%29 Autophagy controls resource allocation and protein storage accumulation in Arabidopsis seeds%2E J Exp Bot 69%3A 1403%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Diaz C%2C Lema�tre T%2C Christ A%2C Azzopardi M%2C Kato Y%2C Sato F%2C Morot%2DGaudry J%2DF%2C Le Dily F%2C Masclaux%2DDaubresse C %282008%29 Nitrogen Recycling and Remobilization Are Differentially Controlled by Leaf Senescence and Development Stage in Arabidopsis under Low Nitrogen Nutrition%2E Plant Physiol 147%3A 1437%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Djordjevic MA%2C Mohd%2DRadzman NA%2C Imin N %282015%29 Small%2Dpeptide signals that control root nodule number%2C development%2C and symbiosis%2E J Exp Bot 66%3A 5171%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=de Felippes FF%2C Wang J%2C Weigel D %282012%29 MIGS%3A miRNA%2Dinduced gene silencing%2E Plant J 70%3A 541%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Gou X%2C He K%2C Yang H%2C Yuan T%2C Lin H%2C Clouse SD%2C Li J %282010%29 Genome%2Dwide cloning and sequence analysis of leucine%2Drich repeat receptor%2Dlike protein kinase genes in Arabidopsis thaliana%2E BMC Genomics&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Groszmann M%2C Bylstra Y%2C Lampugnani ER%2C Smyth DR %282010%29 Regulation of tissue%2Dspecific expression of SPATULA%2C a bHLH gene involved in carpel development%2C seedling germination%2C and lateral organ growth in Arabidopsis%2E J Exp Bot 61%3A 1495%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Groszmann M%2C Chandler PM%2C Ross JJ%2C Swain SM %282020%29 Manipulating gibberellin control over growth and fertility as a possible target for managing wild radish weed populations in cropping systems%2E Front Plant Sci%2E doi%3A 10%2E3389%2Ffpls&dopt=abstract


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https://www.ncbi.nlm.nih.gov/pubmed?term=Guan M%2C M�ller IS%2C Schjoerring JK %282015%29 Two cytosolic glutamine synthetase isoforms play specific roles for seed germination and seed yield structure in Arabidopsis%2E J Exp Bot 66%3A 203%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Huault E%2C Laffont C%2C Wen J%2C Mysore KS%2C Ratet P%2C Duc G%2C Frugier F %282014%29 Local and Systemic Regulation of Plant Root System Architecture and Symbiotic Nodulation by a Receptor%2DLike Kinase%2E PLOS Genet 10%3A e&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Imin N%2C Patel N%2C Corcilius L%2C Payne RJ%2C Djordjevic MA %282018%29 CLE peptide tri%2Darabinosylation and peptide domain sequence composition are essential for SUNN%2Ddependent autoregulation of nodulation in Medicago truncatula%2E New Phytol 218%3A 73%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Ladwig F%2C Stahl M%2C Ludewig U%2C Hirner AA%2C Hammes UZ%2C Stadler R%2C Harter K%2C Koch W %282012%29 Siliques Are Red1 from Arabidopsis Acts as a Bidirectional Amino Acid Transporter That Is Crucial for the Amino Acid Homeostasis of Siliques%2E Plant Physiol 158%3A 1643%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Laffont C%2C Huault E%2C Gautrat P%2C Endre G%2C Kalo P%2C Bourion V%2C Duc G%2C Frugier F %282019%29 Independent Regulation of Symbiotic Nodulation by the SUNN Negative and CRA2 Positive Systemic Pathways%2E Plant Physiol&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Lea US%2C Slimestad R%2C Smedvig P%2C Lillo C %282007%29 Nitrogen deficiency enhances expression of specific MYB and bHLH transcription factors and accumulation of end products in the flavonoid pathway%2E Planta 225%3A 1245%26%23x&dopt=abstract

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Short title: Local CEPR1 activity controls seed size and yield2 1 Abstract 2 The interaction of...

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Transcript of Short title: Local CEPR1 activity controls seed size and yield2 1 Abstract 2 The interaction of...