Short title: Movement of tobacco PEBP mRNA 2 · 44 NCH; TSY and NCH conceived and designed the...

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Short title: Movement of tobacco PEBP mRNA 1

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Corresponding author: 3

Tien-Shin Yu 4

Institute of Plant and Microbial Biology, Academia Sinica, Taipei, 11529, Taiwan 5

Phone: 886-2-27871159 6

Fax: 886-2-27827954 7

Email: [email protected] 8

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Plant Physiology Preview. Published on August 27, 2018, as DOI:10.1104/pp.18.00725

Copyright 2018 by the American Society of Plant Biologists

www.plantphysiol.orgon October 20, 2018 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

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Mobility of antiflorigen and PEBP mRNAs in tomato-tobacco heterografts 24

Nien-Chen Huang, Kai-Ren Luo, and Tien-Shin Yu* 25

Institute of Plant and Microbial Biology, Academia Sinica, Taipei, 11529, Taiwan 26

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One-sentence summary 29

Long-distance movement of tobacco NsCET1 and PEBP mRNAs suggests that 30

acquisition of RNA mobility is an early evolutionary event. 31

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Funding information 34

This work was supported by grants from the National Science Council, Taiwan. 35

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*For correspondence: E-mail: [email protected] 37

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Author contributions 42

NCH performed most of the experiments; TSY and KRL provided technical assistance to 43

NCH; TSY and NCH conceived and designed the experiments; TSY wrote the article 44

with contributions of NCH and KRL. 45

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Abstract 47

Photoperiodic floral induction is controlled by the leaf-derived and 48

antagonistic mobile signals florigen and antiflorigen. In response to photoperiodic 49

variations, florigen and antiflorigen are produced in leaves and translocated through 50

phloem to the apex, where they counteract floral initiation. Florigen and antiflorigen are 51

encoded by a pair of homologues belonging to FLOWERING LOCUS T (FT)- or 52

TERMINAL FLOWER1 (TFL1)-like clades in the phosphatidylethanolamine binding-53

domain protein (PEBP) family. The PEBP gene family contains FT-, TFL1-, and 54

MOTHER OF FT AND TFL1 (MFT)-like clades. Evolutionary analysis suggests that FT- 55

and TFL1-like clades arose from an ancient MFT-like clade. Protein movement of PEBP 56

family is an evolutionarily conserved mechanism in many plants; however, mRNA 57

movement of PEBP family remains controversial. Here, we examined the mRNA 58

movement of PEBP genes in different plant species. We identified a tobacco (Nicotiana 59

sylvestris) CENTRORADIALIS-like 1 gene, denoted NsCET1, and showed that NsCET1 is 60

an ortholog of Arabidopsis antiflorigen ATC. In tobacco, NsCET1 acts as a mobile 61

molecule that non-cell-autonomously inhibits flowering. Grafting experiments showed 62

that endogenous and ectopically expressed NsCET1 mRNAs move long distances in 63

tobacco and Arabidopsis thaliana. Heterografts of tobacco and tomato (Lycopersicon 64

esculentum) showed that in addition to NsCET1, multiple members of the FT-, TFL1-, 65

and MFT-like clades of tobacco and tomato PEBP gene families are mobile mRNAs. Our 66

results suggest that the mRNA mobility is a common feature of the three clades of PEBP-67

like genes among different plant species. 68

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Introduction 71

Cell-to-cell and inter-organ communication are crucial in synchronizing plant 72

developmental programs with external cues. To integrate environmental stimuli perceived 73

in distal tissues, plants have evolved many elegant systems to sense and convert the 74

stimuli into mobile molecules. These mobile molecules are translocated through phloem 75

to the target tissues to exert their non-cell-autonomous functions (Ham and Lucas, 2017; 76

Lacombe and Achard, 2016). In addition to hormones, proteins, and metabolites, many 77

plants recruit mRNAs as mobile molecules for long-distance communication (Kim et al., 78

2001; Haywood et al., 2005; Banerjee et al., 2006; Lu et al., 2012; Huang et al., 2012). 79

Upon translocating to target tissues, the mobile mRNAs are believed to serve as a 80

template to translate into many proteins. Thus, this mRNA-based regulatory network 81

provides an efficient and specific communication system to transmit environmental 82

stimuli perceived in distal tissues. It has been demonstrated that many mobile mRNAs are 83

trafficked through phloem, probably by forming an RNA-protein complex to allow the 84

stable translocation of mRNA molecules (Lucas et al., 2001; Ham and Lucas, 2017). 85

Transcriptome profiling of phloem sap or heterografting experiments identified several 86

thousand mobile mRNAs (Ruiz-Medrano et al., 1999; Guo et al., 2013; Thieme et al., 87

2015; Yang et al., 2015; Xia et al., 2018), suggesting that the use of mobile mRNAs as 88

systemic signals may be a prevalent mechanism in plants to cope with environmental 89

dynamics. 90

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Photoperiodic floral regulation is mediated by two counteracting mobile 92

molecules, namely florigen and antiflorigen, which are encoded by a pair of functionally 93

opposite homologues belonging to different clades in the phosphatidylethanolamine 94

binding-domain protein (PEBP) gene family (Zeevaart, 1976; Lang et al., 1977; 95

Corbesier et al., 2007; Tamaki et al., 2007; Zeevaart, 2008; Huang et al., 2012; 96

Matsoukas et al., 2012; Higuchi et al., 2013). In Arabidopsis thaliana, florigen and 97

antiflorigen are encoded by FLOWERING LOCUS T (FT) and ARABIDOPSIS 98

THALIANA CENTRORADIALIS homolog (ATC), respectively. The expression of FT or 99

ATC is induced under long-day (LD) or short-day (SD) conditions, respectively 100

(Kardailsky et al., 1999; Kobayashi et al., 1999; Huang et al., 2012). FT and ATC both 101

regulate the expression of the same downstream meristem identity gene, APETALA1, by 102

interacting with the transcription factor, FD (Abe et al., 2005; Wigge et al., 2005; Huang 103

et al., 2012). The antagonistic function of FT and ATC may be attributed to competition 104

between FT and ATC for the same binding site on FD, because the deletion of 40 amino 105

acids at the C-terminus of FD abolished the binding of FD with FT and ATC (Huang et 106

al., 2012). The expression of FT and ATC is mainly in vascular tissues and is absent in 107

the apex (Takada and Goto, 2003; Huang et al., 2012), whereas the expression of FD is 108

exclusively in shoot and root apices (Abe et al., 2005; Wigge et al., 2005), which 109

suggests that the movement of FT and ATC from the vasculature to the apex is required 110

for their functions. Through grafting experiments and tissue-specific expression, the 111

protein and mRNA movement of FT and ATC has been demonstrated (Corbesier et al., 112

2007; Jaeger and Wigge, 2007; Mathieu et al., 2007; Lu et al., 2012; Huang et al., 2012). 113

The movement of FT protein from companion cells (CCs) to sieve elements (SEs) is 114



6

mediated through the endoplasmic reticulum-localized protein FT-INTERACTING 115

PROTEIN 1 (FTIP1) and the heavy-metal-associated domain-containing protein 116

SODIUM POTASSIUM ROOT DEFECTIVE 1 (NaKR1) (Liu et al., 2012; Zhu et al., 117

2016). However, deletion analysis of Cucurbita moschata FT protein suggested that the 118

transport of FT protein in CCs-SEs is also governed by a diffusion-based system (Yoo et 119

al., 2013). Although ATC protein is detected in grafted scions, direct evidence to support 120

the long-distance movement of ATC protein is lacking (Huang et al., 2012). In addition 121

to protein movement, it has been reported that Arabidopsis FT and ATC are phloem-122

mobile mRNAs (Li et al., 2009; Lu et al., 2012; Huang et al., 2012). After transcription in 123

leaves, FT and ATC mRNA is selectively targeted to plasmodesmata (PD) for cell-to-cell 124

movement (Luo et al., 2018). However, the mRNA movement of florigen and 125

antiflorigen has only been observed in Arabidopsis, because previous tomato 126

(Lycopersicon esculentum) grafting experiments failed to support long-distance 127

trafficking of SINGLE FLOWER TRUSS (SFT) mRNA, a tomato FT ortholog (Lifschitz 128

et al., 2006). Thus, whether the mRNA of florigen and antiflorigen are mobile in different 129

plant species remains to be elucidated. 130

131

The PEBP gene family is an evolutionarily conserved gene family across 132

different kingdoms. In angiosperms, PEBP genes are grouped into three clades, namely 133

FT-, TERMINAL FLOWER1 (TFL1)-, and MOTHER OF FT AND TFL1 (MFT)-like 134

clades (Chardon and Damerval, 2005). However, in gymnosperms, phylogenetic analysis 135

revealed that only MFT- and FT/TFL1-like genes are present, with only MFT-like genes 136

in bryophytes and lycopods, which suggests the MFT-like clade is the ancestor of all 137



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PEBP genes (Hedman et al., 2009; Karlgren et al., 2011). Evolutionary analysis of the 138

PEBP family indicated that two ancient PEBP duplication events occurred in the common 139

ancestor after the angiosperms split from gymnosperms. The first duplication event gave 140

rise to the MFT-like clade and the ancient lineage of the TFL1/FT-like clade, which was 141

subsequently confronted with a second duplication event forming the TFL1-like and FT-142

like clades (Hedman et al., 2009; Karlgren et al., 2011; Wang et al., 2015). The analysis 143

of florigen movement in different plants indicates that the protein movement of PEBP 144

genes is evolutionarily conserved in many plants (Conti and Bradley, 2007; Zeevaart, 145

2008; Turnbull, 2011); however, little is known about the mRNA movement of PEBP 146

genes in different plant species. In addition, how florigen and antiflorigen have evolved 147

to acquire mobility remains to be investigated. 148

149

In tobacco (Nicotiana sp.), many PEBP genes belonging to FT- or TFL1-like 150

clades have been identified (Amaya et al., 1999; Harig et al., 2012). Unlike Arabidopsis, 151

in which all FT-like genes are floral activators, functional analysis of Nicotiana tabacum 152

FT-like genes showed that three FT-like genes (NtFT1, NtFT2, and NtFT3) act as floral 153

inhibitors, whereas NtFT4 is a tobacco florigen homolog (Harig et al., 2012). NtFT1, 154

NtFT2, and NtFT3 are expressed in leaves under SD conditions, probably in phloem 155

companion cells (Harig et al., 2012). However, whether these FT-like genes and the 156

members of TFL1- or MFT-like genes are mobile mRNAs remains unknown. In this 157

study, we investigated the mRNA movement of PEBP genes in tobacco. We identified 158

three Nicotiana sylvestris TFL1-like genes, NsCET1, NsCET2, and NsCET10, which act 159

non-cell-autonomously to inhibit floral initiation. Functional analysis suggested that 160



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NsCET1 is an ortholog of Arabidopsis antiflorigen ATC. Analysis of heterografts showed 161

that NsCET1 mRNA is mobile in Arabidopsis and tobacco, which suggests that mRNA 162

movement of antiflorigen is a conserved mechanism across different plant species. 163

Further heterografting experiments showed that the mRNA of multiple PEBP genes, 164

including the members of FT-, TFL1-, and MFT-like genes, is mobile in tobacco and 165

tomato. Thus, the movement of PEBP genes mRNA may be a conserved mechanism 166

across different plant species. 167

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Results 170

Tobacco NsCET genes act non-cell-autonomously to inhibit flowering in Arabidopsis 171

and tobacco 172

To explore mRNA movement of antiflorigen in different plant species, we 173

identified tobacco ATC orthologues to examine their mRNA movement. By combining 174

database searches and RT-PCR analysis, we identified five TFL1-like genes, namely 175

NsCET1, NsCET2, NsCET5, NsCET9, and NsCET10, from an obligate LD tobacco 176

variety (Nicotiana sylvestris). Phylogenetic analysis showed that NsCET5 and NsCET9 177

were grouped with Arabidopsis TFL1 (Supplemental Fig. S1A), which is consistent with 178

previous results that NsCET5 is an ortholog of TFL1 (Amaya et al., 1999). Because our 179

previous experiments revealed that ectopic expression of Arabidopsis TFL1 in companion 180

cells is not sufficient to affect flowering (Huang et al., 2012), we investigated the 181

remaining CET genes, specifically NsCET1, NsCET2, and NsCET10. Sequence 182

comparison revealed that NsCET1, NsCET2 and NsCET10 contain the key amino acids 183

required for the activity of floral inhibitors (His 88 and Asp 144, Ahn et al., 2006). The 184

flowering time of Arabidopsis transformants harboring these CET transgenes was delayed 185

as compared to that of wild-type plants (Table I), which indicates that NsCET1, NsCET2, 186

and NsCET10 are floral inhibitors. In addition, expression of NsCET1, NsCET2, and 187

NsCET10 by the SUCROSE TRANSPORTER 2 (SUC2) promoter, a companion cell-188

specific promoter, showed that these CETs acted non-cell-autonomously to inhibit 189

flowering in Arabidopsis (Table I). Among CET transformants, ectopic expression of 190

NsCET1 exhibited the most severe late-flowering phenotype (Supplemental Fig. S1, B–E). 191

The flowers of NsCET1 transformants produced leafy-like bracts, which resembled the 192



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phenotypes of Arabidopsis ATC-overexpression lines (Supplemental Fig. S1, C–E; 193

Huang et al., 2012). Similarly, Arabidopsis transformants harboring NsCET2 or NsCET10 194

transgenes showed moderate late-flowering and leafy-like bracts phenotypes (Table I, 195

Supplemental Fig. S1, F–I), which suggests that the functions of NsCET1, NsCET2, and 196

NsCET10 are partially redundant, but NsCET1 functions similar to Arabidopsis ATC. 197

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To further examine the function of NsCET1 in tobacco, we introduced P35S-199

NsCET1 or PSUC2-NsCET1 into tobacco. The obligate LD variety (N. sylvestris) or day-200

neutral variety tobacco (N. tabacum) harboring P35S-NsCET1 or PSUC2-NsCET1 201

transgenes showed a late-flowering phenotype (Fig. 1), which suggests that NsCET1 acts 202

as a non-cell-autonomous floral inhibitor in tobacco. Tobacco transformants with extreme 203

late-flowering phenotypes produced a substantial number of leaves. A number of 204

transformants did not flower at 5 months after transfer to soil from rooting medium (Fig. 205

1, A and B, black circles). In addition to exhibiting a late-flowering phenotype, these 206

tobacco transformants had a short-internode phenotype, which was easily recognized in N. 207

tabacum transformants (Supplemental Fig. S2, A and B). However, unlike Arabidopsis 208

P35S-NsCET1 or PSUC2-NsCET1 transformants, the floral organs of tobacco P35S-209

NsCET1 transformants were similar to those of wild-type plants (Supplemental Fig. S2, C 210

and D), which indicates functional specificity for tobacco NsCET1. 211

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In N. sylvestris leaves, the mRNA accumulation of NsCET1, NsCET2, and 213

NsCET10 was significantly induced under SD conditions (Fig. 2A; Supplemental Fig. S3), 214

which is consistent with the production of antiflorigen under SD conditions (Lang et al., 215



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1977; Huang et al., 2012). To examine the expression pattern of NsCET1 in tobacco, the 216

NsCET1 promoter were PCR-amplified and fused with a GUS reporter gene. 217

Histochemical analysis showed that in N. sylvestris and Arabidopsis transformants, GUS 218

activity was mainly detected in leaves and in root vascular tissue (Fig. 2, B and C, E–F, 219



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Supplemental Fig. S4), but not in the shoot apex (Fig. 2C; Supplemental Fig. S4B), 220

suggesting that the regulatory mechanism of NsCET1 expression is conserved in 221

Arabidopsis and tobacco. In agreement with the non-cell-autonomous function of 222

NsCET1, our bimolecular fluorescence complementation (BiFC) analysis revealed that 223



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NsCET1 interacted with FD (Fig. 2D), which is a bZIP transcription factor specifically 224

expressed in the apex (Abe et al., 2005; Wigge et al., 2005). Thus, NsCET1 may 225

translocate from the leaf to the shoot apex to inhibit flowering. 226

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Knockdown of NsCET expression promotes flowering in tobacco 228

To investigate the contribution of CET genes to floral initiation in tobacco, 229

we knocked down the expression of NsCET1, NsCET2, and NsCET10 using an artificial 230

microRNA (amiR-CETs). Because the sequences of NtCET1, NtCET2, and NtCET10 in N. 231

tabacum were identical to those of respective CETs in N. sylvestris, the same amiR-CETs 232

construct with expression driven by a CaMV35S promoter was introduced into either N. 233

tabacum or N. sylvestris. Similar to the Arabidopsis antiflorigen atc-2 mutant (Huang et 234

al., 2012), the N. tabacum transformants harboring amiR-CETs displayed an early 235

flowering phenotype under SD but not under LD conditions (Supplemental Fig. S5, A 236

and B), which indicates a conserved function of antiflorigen in day-neutral tobacco and 237

Arabidopsis. In LD-grown N. sylvestris, the amiR-CET transformants flowered slightly 238

earlier than wild-type N. sylvestris (Fig 3A). RT-qPCR analysis revealed a reduced level 239

of NsCET1, NsCET2, and NsCET10 mRNA in N. sylvestris 35S-amiR-CET transformants 240

(Fig. 3, B–D). When these transformants were grown under SD conditions, floral 241

induction was not observed in N. sylvestris 35S-amiR-CET transformants or wild-type N. 242

sylvestris (Fig. 3E), suggesting that knocking down the expression of CET genes in 243

obligate LD tobacco is not sufficient to induce flowering under non-floral induction 244

conditions. However, when N. sylvestris 35S-amiR-CET transformants were grown under 245

SD conditions with dim light during the dark period to induce a low-level expression of 246



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NsFT4 (Supplemental Fig. S5, C and D), the N. sylvestris 35S-amiR-CET transformants 247

flowered earlier than wild-type N. sylvestris plants (Fig. 3F), which is consistent with the 248

notion that the function of CETs is to modulate flowering by antagonizing the activity of 249

florigen. 250



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NsCET1 mRNA is mobile in Arabidopsis and tobacco heterografts 252

Given that the SUC2 promoter is a strong promoter expressed in most CCs, 253

including CCs near the shoot apex, to further verify that the late-flowering phenotype in 254

PSUC2-NsCET1 transformants is caused by long-distance signals associated with 255

NsCET1, we grafted wild-type tobacco scions onto PSUC2-NsCET1 transformant stocks. 256

Because N. sylvestris is a rosette-type plant, we used N. tabacum plants for grafting 257

experiments. In control experiments, with wild-type N. tabacum scions grafted onto wild-258

type stocks, floral initiation occurred after a mean of 28.4±3.8 leaves was produced on 259

scions (Fig. 4, A and B). However, when wild-type scions were grafted onto PSUC2-260

NsCET1 transformant stocks, floral initiation occurred after a mean of 45.6±3.7 leaves 261

was produced (Fig. 4, A and B). In addition, the internodes of wild-type scions were 262

shorter after grafting onto PSUC2-NsCET1 transformant stocks (Fig. 4, C and D). 263

Therefore, the late-flowering and short-internode phenotypes observed in PSUC2-264

NsCET1 transformants were graft-transmissible. 265

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To examine whether tobacco NsCET1 mRNA is a mobile mRNA, we first 267

used the Arabidopsis pin-fasten grafting method (Huang and Yu, 2015) to graft 10-day-268

old Arabidopsis wild-type scions onto Arabidopsis P35S-NsCET1 or PSUC2-NsCET1 269

transformant stocks. At 2 weeks after grafting, RT-qPCR analysis detected NsCET1 270

mRNA in wild-type scions grafted onto P35S-NsCET1 or PSUC2-NsCET1 transformant 271

stocks but not onto wild-type controls (Fig. 5, A and B), which indicates that 272

overexpressed NsCET1 mRNA was mobile in Arabidopsis. To investigate the long-273



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distance movement of NsCET1 mRNA in tobacco, we grafted tobacco wild-type scions 274

onto tobacco PSUC2-NsCET1 transformant stocks or control wild-type stocks. At 3 275

weeks after grafting, RT-PCR with NsCET1 transgene-specific primers resulted in PCR 276

products from wild-type scions grafted onto PSUC2-NsCET1 stocks but not from controls 277



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of wild-type scions grafted onto wild-type stocks. Further sequencing of amplified DNA 278

fragments confirmed the identity of PCR products (Supplemental Fig. S6), which 279

indicates that overexpressed NsCET1 mRNA is also mobile in tobacco. 280

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To further determine whether endogenous NsCET1 mRNA is a mobile 282

mRNA in tobacco, we performed hetero-species grafting experiments. The sequences of 283

the PEBP genes of tomato and tobacco exhibit significant variations, which allows for 284

differentiation of species-specific PEBP mRNA by RT-PCR and sequencing analysis. We 285

grafted wild-type tomato scions with N. sylvestris stocks (Fig. 6A). At 3 weeks after 286

grafting, RT-PCR with NsCET1 gene-specific primers resulted in PCR products from 5 287

independent tomato scions grafted onto N. sylvestris stocks but not from wild-type 288

tomato plants (Fig. 6B). The PCR products from tomato scions verified by sequencing 289

analysis showed that these products were indeed derived from tobacco NsCET1 mRNA 290

(Supplemental Fig. S7). In contrast, control RT-PCR experiments with primers for 291

tobacco PHLOEM PROTEIN 2A (PP2A), a previously shown non-mobile mRNA (Huang 292

and Yu, 2009), revealed no tobacco PP2A mRNA in wild-type tomato plants and tomato 293

scions grafted onto N. sylvestris stocks (Fig. 6B). These results indicate that endogenous 294

NsCET1 mRNA can move from tobacco stocks to tomato scions. 295

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The mRNA of MFT-like genes is mobile in tomato-tobacco heterografts 297

In angiosperms, phylogenetic analysis shows that FT- and TFL1-like genes 298

may arise from the ancestor in the MFT-like clade (Hedman et al., 2009; Karlgren et al., 299

2011). To investigate whether the mRNA movement of FT- and TFL1-like genes evolved 300

from mobile MFT-like genes, we examined the mRNA movement of the leaf-expressed 301

MFT-like genes in tomato-tobacco heterografting experiments. The literature and 302

database search identified two tobacco MFT-like genes, namely NsMFTL1 and NsMFTL2, 303

and two tomato MFT-like genes, namely SELF-PRUNING 2G (SP2G) and SELF-304



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PRUNING 3A (SP3A) (Supplemental Fig. S1A; Carmel-Goren et al., 2003). RT-PCR 305

analysis showed weak expression of NsMFTL1 and NsMFTL2 in leaves of N. sylvestris, 306

whereas SP2G but not SP3A was highly expressed in leaves of tomato (Supplemental Fig. 307

S8). To examine the movement of NsMFTL1 and NsMFTL2 mRNA, RT-PCR analysis 308



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was conducted to analyze tomato scions grafted onto N. sylvestris stocks and revealed 309

that NsMFTL2 but not NsMFTL1 mRNA was present in 1 of 5 independent tomato scions 310

grafted onto N. sylvestris stocks (Fig. 6C). In addition, RT-PCR with primers for different 311

tobacco PEBP genes detected NsFT2 and NsFT3 mRNA, which are two tobacco floral 312

inhibitors belonging to the FT-like clade (Harig et al., 2012), in tomato scions grafted 313

onto N. sylvestris stocks (Fig. 6C). These results suggest that in tobacco, a number of 314

members in FT-, TFL1- and MFT-like clades are mobile mRNAs. 315

316

To further verify mRNA movement of tomato PEBP genes, we grafted wild-317

type N. tabacum scions onto tomato stocks (Fig. 7A). At 3 weeks after heterografting, 318

RT-PCR analysis detected SP2G mRNA in tobacco scions grafted onto tomato stocks 319

(Fig. 7B), which suggests that the mRNA movement of MFT-like genes is conserved in 320

tomato and tobacco. In addition, RT-PCR with the primers for different tomato PEBP 321

genes detected SP3D, SP5G (FT-like clade), and SP9D (TFL1-like clade) mRNA in 322

tobacco scions (Fig. 7B). However, RT-PCR with primers for SP11A (FT-like clade) 323

detected SP11A mRNA in tomato stocks but not in tomato scions grafted onto tobacco 324

stocks (Fig. 7B), which suggests that the mRNA movement of PEBP genes is transcript-325

specific. Taken together, our results indicate that in tobacco and tomato, multiple FT-, 326

TFL1-, and MFT-like genes are mobile mRNAs. 327

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Discussion 330

The PEBP gene family is an evolutionarily conserved gene family. In many 331

plant species, the long-distance or cell-to-cell movement of different PEBP proteins in 332

FT- and TFL1-like clades has been well established (Conti and Bradley, 2007; Zeevaart, 333



22

2008; Turnbull, 2011). However, whether the mRNA of PEBP genes is mobile remained 334

controversial. Although previous Arabidopsis grafting experiments showed that the 335

mRNA of FT and ATC can move long distance from stocks to scions (Huang et al., 2012; 336

Lu et al., 2012), grafting experiments in tomato failed to detected the transport of 337

SINGLE FLOWER TRUSS (SFT) mRNA, which is a tomato FT ortholog (Lifschitz et al., 338

2006). Thus, questions remaining are whether the mRNA movement of PEBP genes 339

occurs in other plant species and how florigen and antiflorigen evolved to acquire RNA 340

mobility. In Arabidopsis, MFT is not directly involved in flowering control but rather is 341

involved in seed development (Xi et al., 2010). A specific expression pattern of MFT in 342

germinating seeds is inappropriate for examining the RNA long-distance movement. In 343

this study, we identified a tobacco antiflorigen NsCET1 and showed that NsCET1 mRNA 344

is mobile in Arabidopsis and tobacco (Fig. 5 and 6). Through the use of tobacco-tomato 345

heterografts, we showed that many PEBP genes, including the genes in FT-, TFL-, and 346

MFT-like clades, are mobile in tomato and tobacco (Fig. 6 and 7). The simplest 347

explanation for these findings is that RNA mobility in the PEBP gene family has the 348

same evolutionary lineage: the acquisition of mRNA mobility in FT- and TFL1-like 349

genes may have evolved before the split of FT/TFL1-like clades from the more ancient 350

MFT-like clade. Alternatively, individual PEBP genes in different clades may have 351

independently evolved to access the RNA mobility. Our recent RNA live-imaging 352

analysis showed that Arabidopsis FT and ATC mRNAs are selectively targeted to 353

plasmodesmata for cell-to-cell movement (Luo et al., 2018), suggesting that the same 354

mechanism may be used to direct the cell-to-cell movement of FT and ATC mRNA. This 355

result is consistent with the hypothesis that the RNA mobility in the PEBP gene family 356



23

may have evolved before the divergence of the FT/TFL1-like clade from the MFT-like 357

clade. However, more experiments are required to verify whether the RNA movement of 358

different PEBP genes is controlled by the same mechanism. 359

360

Whether the movement of mobile mRNAs is governed by specific or non-361

specific mechanisms is uncertain (Kehr and Kragler, 2018; Morris, 2018). The detection 362

of a significant number of mobile mRNAs in grafted plants (Thieme et al., 2015; Yang et 363

al., 2015) and phloem exudates (Guo et al., 2013) indicates weak selection in regulating 364

mRNA transport (Morris, 2018). A computational simulation indicated that the 365

movement of mobile mRNAs is nonspecific and correlated with transcript abundance 366

(Calderwood et al., 2016). In contrast, in Arabidopsis, grafting experiments with ectopic 367

expression of non-mobile mRNA such as GFP, Arabidopsis dual-affinity nitrate 368

transporter (CHL1), or Arabidopsis ammonium transporter (AMT1;2) showed that high 369

mRNA abundance in companion cells is not sufficient to trigger long-distance movement 370

of these mRNAs (Huang and Yu, 2009; Xia et al., 2018). In addition, the RNA sequences 371

involved in long-distance movement of Arabidopsis GA-INSENITIVE and FT have been 372

located (Huang and Yu, 2009; Lu et al., 2012). Recently, tRNA-like structures (TLSs) in 373

some phloem-mobile mRNAs were found necessary and sufficient to trigger RNA 374

movement (Zhang et al., 2016), which is consistent with the notion that the movement of 375

mobile mRNAs operates by specific mobile RNA motifs. In our grafting experiments, 376

tobacco NsCET1 mRNA could move long-distance in both tobacco and Arabidopsis (Fig. 377

5 and 6). In addition, endogenous NsCET1 mRNA could move across the graft union 378

from tobacco stocks to tomato scions (Fig. 6). These results suggest that the mechanism 379



24

by which NsCET1 mRNA moves long distance is likely conserved in these plants. Our 380

heterografting experiments failed to detect the translocated tomato SP11A mRNA in 381

tobacco scions grafted onto tomato stocks (Fig. 7), which suggests that the movement of 382

mobile mRNA is transcript-specific. Thus, the transport of mobile mRNA may be 383

controlled by a regulatory mechanism rather than non-specific diffusion. The cis-acting 384

elements required for Arabidopsis FT RNA movement were localized to nucleotides 1–385

102 on the FT coding sequence (Li et al., 2009; Lu et al., 2012). Given that the sequences 386

of NsCET1 and FT or other PEBP genes exhibit significant similarity, sequence 387

comparison and deletion analysis may provide information to understand whether 388

NsCET1 and FT or other PEBP genes share similar mobile RNA motifs. 389

390

Systemic spreading of many plant RNA viruses is mediated by movement 391

proteins (MPs). These virus-encoded RNA-binding proteins (RBPs) have been shown to 392

bind viral RNA for cell-to-cell movement through PD (Heinlein, 2015). To elucidate the 393

mechanisms underlying the long-distance transport of mobile mRNAs, the movement of 394

plant mobile mRNAs was proposed to be mediated by the interaction of systemic RBPs 395

and mobile RNA motifs (Lucas et al., 2001). The involvement of systemic RBPs in 396

delivery of plant phloem-mobile mRNAs was revealed by the identification of RBPs 397

from phloem exudates. The analysis of pumpkin phloem proteins that cross-react with 398

antiserum against the MP of red clover necrotic mosaic virus identified Cucurbita 399

maxima PHLOEM PROTEIN 16 (CmPP16), which acts as a paralog of viral MP in long-400

distance movement of phloem-mobile mRNA (Xoconostle-Cazares et al., 1999). In 401

pumpkin phloem sap, CmPP16 interacts with Cucurbita maxima PHLOEM RNA 402



25

BINDING PROTEIN 50 (CmRBP50), encoding a polypyrimidine track-binding (PTB) 403

protein, and other phloem proteins to form a protein complex that selectively binds with 404

PTB motifs containing phloem-mobile mRNAs (Ham et al., 2009; Li et al., 2011). In 405

agreement with these results, potato StPTB1 and StPTB6, two potato homologs of 406

CmRBP50, mediate tuber development by regulating long-distance movement of mobile 407

StBEL5 mRNA (Cho et al., 2015). Thus, the delivery of various mobile mRNAs may be 408

regulated by the interaction of systemic RBPs with distinct mobile RNA motifs, such as 409

PTB or TLS motifs (Zhang et al., 2016). The identification of the RBPs that involved in 410

long-distance trafficking of NsCETs or other mobile PEBP mRNAs may provide insights 411

into the mechanism of mRNA movement. 412

413

Several lines of evidence demonstrate that plant mobile mRNAs play 414

important roles in many developmental programs. This phloem-mediated RNA regulatory 415

network is involved in leaf development, tuber formation, flowering, and many other 416

developmental processes (Lucas et al., 1995; Kim et al., 2001; Haywood et al., 2005; 417

Banerjee et al., 2006; Lu et al., 2012; Huang et al., 2012). Grafting experiments of 418

tobacco (Lang et al., 1977), cucumber, squash (Satoh, 1996), and soybean (Cober and 419

Curtis, 2003) support the production of antiflorigen when plants are grown under non-420

floral induction conditions. Although previous grafting experiments with early- or late-421

flowering mutants also suggested the presence of graft-transmissible floral inhibitors in 422

pea (Paton and Barber, 1955), the effect is now more likely attributed to the lack of 423

florigen in these mutants (Weller et al., 2009). Recently, an analysis of Arabidopsis and 424

Chrysanthemum revealed that TFL1-like genes act non-cell-autonomously to inhibit 425



26

flowering (Huang et al., 2012; Higuchi et al., 2013), which agrees with our finding that 426

NsCET1 is an antiflorigen in tobacco. In tobacco, the PEBP genes in both FT- and TFL-427

like clades may act as floral inhibitors. At least three FT-like floral inhibitors, specifically 428

NtFT1, NtFT2, and NtFT3, are expressed in CCs (Harig et al., 2012). In addition, our 429

heterografting experiments indicated that NsFT2 and NsFT3 are mobile mRNA (Fig. 6C), 430

which suggests that NtFT1, NtFT2, and NtFT3 are probably also mobile in tobacco. Thus, 431

multiple members in both FT- and TFL-like clades of the tobacco PEBP gene family may 432

act redundantly to contribute to antiflorigen activity. 433

434

Floral inhibition of antiflorigen is mediated by antagonizing florigen activity 435

(Huang et al., 2012). In rice, florigen Hd3a may recruit 14-3-3 proteins and FD to form 436

florigen activation complexes and induce the expression of downstream floral identity 437

genes (Taoka et al., 2011). Analysis of Arabidopsis antiflorigen demonstrated that ATC 438

can physically interact with FD to downregulate similar floral identity genes (Huang et al., 439

2012). Similar to ATC, tobacco CET1 also interacted with FD in our BiFC assays (Fig. 440

2D). Therefore, antiflorigen may function to interfere in the binding of FD with florigen 441

to form a florigen activation complex. However, in addition to displaying a late-flowering 442

phenotype, CET1-overexpressed transformants also displayed other developmental 443

alterations, including abnormal floral organs with leafy-like bracts (Supplemental Fig. S1) 444

and shortened internodes (Supplemental Fig. S2). These phenotypes may not be simply 445

attributed to the defective functions of FT or FD. Thus, in addition to antagonizing the 446

activity of florigen, antiflorigen may also act independently of florigen to participate in 447

other developmental regulation. In agreement with this notion, the interaction between 448



27

Arabidopsis FT and BRANCHED1 is independent of FD (Niwa et al., 2013). Whether 449

antiflorigen can interact with other factors remains to be investigated. 450

451

Material and Methods 452

Plant growth condition 453

A. thaliana seeds were obtained from the Arabidopsis Biological Resource Center 454

(ABRC, Ohio, USA) and grown in growth chambers under LD (16 h light/8 h dark) or 455

SD (8 h light/16 h dark) conditions, with a 22°C/20°C day/night cycle and white 456

fluorescent light (light intensity 100 μmol m-2 s-1). Tomato, Nicotiana tabacum cv 457

Turkish, and N. sylvestris were grown in a growth chamber with a 25°C/22°C day/night 458

cycle and light intensity 200 μmol m-2 s-1. To induce low-level expression of the tobacco 459

florigen NsFT4, tobacco plants were grown under SD conditions but with dim light (10 460

μmole m-2 s-1) during the dark period. 461

462

Plasmid construction 463

Full-length cDNA of tobacco NsCET1, NsCET2, or NsCET10 was amplified by RACE 464

RT-PCR with gene-specific primers (Sequences are in Supplemental Table S1). The 465

cDNA was driven by a CaMV35S or Arabidopsis SUC2 promoter and transferred into 466

Agrobacterium tumefaciens strain AGL1. The amiR-CETs were designed by using 467

WMD3 Web MicroRNA Designer (http://wmd3.weigelworld.org/cgi-bin/webapp.cgi; 468

Schwab et al., 2006) and confirmed by sequencing. The resulting amiR-CETs constructs 469

were driven by a CaMV35S promoter and transferred into A. tumefaciens strain AGL1 for 470

plant transformation. 471



28

Tobacco NsCET1 5.5K promoter was amplified by PCR with forward (5′-472

AAGTGAAGTCGACTAATTCTTTTATATG-3′) and reverse primers (5′-473

CTTCACCCTTTTGTTTCTTCTTCTTTTTGG-3′). The 5.5K promoter was fused with a 474

β-glucuronidase (GUS) reporter gene in pCAMBIA1390 for plant transformation. 475

476

Arabidopsis and tobacco transformation 477

Arabidopsis transformation was performed by the floral dip method. The T1 478

transformants were selected on MS medium containing 40 μg ml-1 hygromycin. At 10 479

days after selection, resulting transformants were selected and transferred to soil for 480

further analysis. For transformation of tobacco (N. tabacum cv. Turkish), tobacco seeds 481

were surface-sterilized and germinated on MS30 medium (MS medium containing 30 g/L 482

sucrose) in growth chambers with 25°C LD conditions for 1 month until plants produced 483

5–6 fully expanded leaves. The midrib of developed leaves was removed, and the 484

remaining blades were cut into 1.0-cm2 pieces and placed on plates with shooting 485

medium I (SM I; MS30 medium containing 1 mg/L BAP and 0.1 mg/L NAA) at 25°C for 486

2 days. Explants were then co-cultured with overnight agrobacterium cultures (diluted to 487

OD600= 0.8–1.0 in SM I solution) for 20 min and blotted dry on sterilized 3M filter paper, 488

then transferred to SM I agar plates at 25°C under dark conditions for 2 days. The 489

explants were transferred to shooting medium II (SM II; MS30 medium containing 1 490

mg/L BAP, 0.1 mg/L NAA, 200 mg/L cefotaxime, and 30 mg/L hygromycin) and 491

incubated in growth chambers under LD conditions to produce callus. Every 2 weeks, 492

calli were subcultured on a new SM II agar plate until new shoots developed. The well-493

developed shoots were transferred to rooting medium (MS30 medium containing 200 494



29

mg/L cefotaxime and 30 mg/L hygromycin) until roots were well developed. The 495

successful transformants were transferred to soil. N. sylvestris transformation followed 496

the N. tabacum transformation procedures, except the hormone concentration in SM II 497

medium was reduced to 0.5 mg/L BAP and 0.05 mg/L NAA. 498

499

Bimolecular Fluorescence Complementation (BiFC) Analyses 500

The cDNA of NsCET1 or NsCET2 was cloned into VenusN binary vector HygII-501

VYNE(R), and FD was cloned into the SCFP3AC vector KanII-SCYCE(R), under control 502

of a CaMV35S promoter (Waadt et al., 2008). The successful constructs were introduced 503

into A. tumefaciens strain AGL1. For BiFC analysis, Agrobacterium strains carrying 504

individual BiFC constructs were cultured in LB media containing 50 μg ml-1 kanamycin, 505

10 mM MES, pH 5.7, and 20 μM acetosyringone at 28°C overnight. The bacteria were 506

pelleted and diluted in infiltration solution (10 mM MgCl2, 10 mM MES, pH 5.7, 200 μM 507

acetosyringone) to OD600 = 1.0. The bacteria solution was incubated at room temperature 508

for 1 h. Co-infiltration was conducted with a 1:1 mix of HygII-VYNE(R)-CET and 509

KanII-SCYCE(R)-FD strains. The mixed solution was infiltrated into the leaves of 3-510

week-old Nicotiana benthamiana using syringes. Three days after infiltration, tissue was 511

visualized under a confocal laser-scanning microscope (Zeiss LSM 510 Meta). 512

513

Histochemical analysis 514

The 40-day-old Nicotiana sylvestris transformants carrying NsCET1pro-GUS were 515

incubated with GUS staining solution (50 mM sodium phosphate pH 7.0, 10 mM EDTA, 516

0.5 mM potassium ferricyanide, 0.5 mM potassium ferrocyanide, 1 mM X-Gluc, 0.01% 517



30

Triton X-100) at 37°C for 16 hrs. Plants were treated with 95% ethanol to remove 518

chlorophyll and photographed under a Leica Z16 Apo microscope. 519

520

Grafting experiments 521

Arabidopsis grafting was performed by pin-fasten grafting as previously described 522

(Huang and Yu, 2015). At 2 weeks after grafting, the mature leaves of the stocks and the 523

tissues from 0.2 cm above the graft union of the scions were collected for RNA extraction. 524

For tobacco grafting experiments, we used a simple cleft grafting approach. The 525

wild-type or PSUC2-NsCET1 transformant of N. tabacum cv. Turkish were grown in a 526

growth chamber for 2 months. At this stage, plants usually produced 10–15 leaves. The 527

wild-type scions were cut from 10–12 cm below the apex. Mature leaves on the scions 528

were removed and the base of scions was cut into a wedge shape to insert into the slit 529

made by a vertical cut on apex-removed stocks. The graft junctions were secured with 530

parafilm and sealed in a Ziploc bag to retain humidity for 1 week. The mature leaves of 531

the scions on successfully grafted plants were regularly removed to ensure sink strength. 532

For tomato and N. sylvestris heterografting, 1-month-old wild-type tomato were 533

used as scions to graft with wild-type N. sylvestris tobacco plants stocks. The N. 534

sylvestris plants with 4–5 expanding leaves were cut from the base of hypocotyls and 535

shaped into a wedge cut, then inserted into slits made on the stem of tomato plants. The 536

mature leaves of tomato were removed to ensure phloem transport from N. sylvestris to 537

tomato. The graft junctions were secured with parafilm and sealed in a Ziploc bag. 538

Successfully grafted plants were grown in growth chambers with regular removal of 539

mature leaves of tomato scions to ensure sink strength. At 3 weeks after grafting, the 540



31

mature leaves of N. sylvestris stocks and the apex of tomato scions, which contains shoot 541

meristem and young primordia, were collected for RNA extraction. 542

N. tabacum and tomato heterografting was made by the simple cleft grafting 543

method conducted with 1-month-old wild-type N. tabacum cv. Turkish scions and tomato 544

stocks. The N. tabacum scions were cut from 6 cm below the apex and shaped into a 545

wedge to insert into the vertical cut of the apex-removed tomato stocks. The graft 546

junctions were secured with parafilm and sealed in a Ziploc bag to retain humidity for 1 547

week. The mature leaves of the scions on successfully grafted plants were regularly 548

removed to ensure sink strength. 549

550

RNA extraction and RT-PCR or RT-qPCR analysis 551

Total RNA was extracted by using Trizol reagent according to user’s manual with 552

modifications (Invitrogen, CA). In brief, 0.4 g of ground tissues were mixed with 1 ml 553

Trizol reagent and centrifuged at 4°C for 10 min at full speed to remove cell debrides. 554

The solution was extracted with chloroform and phenol/chloroform and subjected to 555

ethanol precipitation. RNA was vacuum dried and dissolved in DEPC-treated dH2O. 556

For RT-PCR analysis, 5 μg of total RNA was used in reverse transcription reactions 557

performed with oligo(dT)20 and SuperScript III reverse transcriptase (Invitrogen). One 558

microliter of cDNA was used for the PCR reaction with the following conditions: 1 min 559

at 94°C for 1 cycle; 30 sec at 94°C, 30 sec at 60°C, 1min at 68°C for 35 cycles, and 10 560

min at 68°C for 1 cycle. An aliquot (5 μl) of PCR products was separated on agarose gels. 561

For nested PCR, the PCR products were diluted 1:50 and subjected to a second round of 562

PCR with nested primers. 563



32

For RT-qPCR analysis, RNA was treated with DNase I to remove potential DNA 564

contamination. An amount of 5 μg total RNA was used to synthesize first-strand cDNA 565

using Superscript III reverse transcriptase (Invitrogen, CA) in a reaction volume of 20 μl. 566

cDNA was diluted to 10 ng/μl with RNase-free water. An aliquot of 5 μl diluted cDNA 567

and 200-nM gene-specific primers were used for real-time PCR with the Applied 568

Biosystems StepOnePlus Real-Time PCR System (Applied Biosystems). PCR was run at 569

95°C for 10 min, then 40 cycles of 95°C for 15 sec, and 60°C for 1 min, with triplicates 570

technical replicates included for each sample. The expression of β-tubulin (TUB) was a 571

normalization control. The sequences of primers are in Supplemental Tables S1 and S2. 572

573

Accession Numbers 574

Sequence data from this article can be found in the GenBank/EMBL data libraries under 575

accession numbers: NsCET1 (LOC104248269), NsCET2 (LOC104226905), NsCET5 576

(LOC104217580), NsCET9 (LOC104239376), NsCET10 (LOC104229471), NsFTL5 577

(LOC104234573), NsFTL6 (LOC104235396), NsFTL7 (LOC104225910), NsMFTL1 578

(LOC104210644), NsMFTL1 (LOC104210681), NsFT2 (XM_009770669), NsFT3 579

(XM_009773706), SP2G (AY186734), SP3D (AY186735), SP5G (XM_004239797), 580

SP9D (AY186738), SP11A (XM_004250027). 581

582

Supplemental Data 583

The following supplemental materials are available. 584

Supplemental Figure S1. Tobacco NsCET1, NsCET2, and NsCET10 act as floral 585

inhibitors in Arabidopsis. 586



33

Supplemental Figure S2. N. tabacum cv. Turkish PSUC2-NsCET1 transformants 587

displayed phenotypes of short internodes and wild-type floral organs. 588

Supplemental Figure S3. Gene expression of N. sylvestris NsCET2 and NsCET10 under 589

LD or SD conditions. 590

Supplemental Figure S4. GUS activity of NsCET1 promoters in tobacco and 591

Arabidopsis. 592

Supplemental Figure S5. Suppression of CETs expression in day-neutral tobacco 593

promotes flowering under SD conditions. 594

Supplemental Figure S6. Long-distance movement of tobacco NsCET1 RNA in tobacco 595

PSUC2-NsCET1 transformants. 596

Supplemental Figure S7. Sequencing analysis of mobile tobacco NsCET1 mRNA in 597

tobacco-tomato heterografts. 598

Supplemental Figure S8. Expression pattern of MFT-like genes in tomato and tobacco. 599

Supplemental Table S1. Primers used in identification of tobacco CET genes and RT-600

qPCR analysis. 601

Supplemental Table S2. Primers used in RT-PCR analysis. 602

603

Acknowledgements 604

We thank the Arabidopsis Biological Resource Stock Center (ABRC) for providing 605

Arabidopsis seeds and Dr. Jörg Kudla for providing the BiFC vectors. This work was 606

supported by grants from the Academia Sinica, Taiwan. 607

608



34

Table I. Flowering time of Arabidopsis transformants expressing tobacco 609

CENTRORADIALIS-like (CET) transgenes 610

Plant line Flowering time (no. of rosette leaves)

Col 8.6±0.7

35S-NsCET1 16.8±1.7

SUC2-NsCET1 22.4±2.9

35S-NsCET2 11.9±1.0

SUC2-NsCET2 14.0±1.7

35S-NsCET10 11.3±0.9

SUC2-NsCET10 11.1±0.7

Data are means±SD. 611

612

Figure Legends 613

Figure 1. Tobacco NsCET1 acts act non-cell-autonomously to inhibit flowering 614

A, Flowering time of wild-type Nicotiana sylvestris plant and Nicotiana sylvestris 615

transformants harboring P35S-NsCET1 or PSUC2-NsCET1 transgenes under LD 616

conditions. The black circles represent the leaf number of 3 transformants that did not 617

flower at 5 months after transfer from rooting medium. Flowering time is represented by 618

the number of leaves during flowering (*=p<0.05; **=p<0.01, unpaired Student’s t-test). 619

B, Flowering time of wild-type N. tabacum cv. Turkish and N. tabacum transformants 620

harboring P35S-NsCET1 or PSUC2-NsCET1 transgenes under LD conditions. The black 621

circles represent the leaf number of 2 transformants that did not flower at 5 months after 622

transfer from rooting medium. (*=p<0.05, unpaired Student’s t-test). C, Wild-type N. 623



35

sylvestris (left) and N. sylvestris P35S-NsCET1 transformants (right) under LD conditions. 624

D, Wild-type N. tabacum cv. Turkish (left) and N. tabacum PSUC2-NsCET1 625

transformants (right) under LD conditions. 626

627

Figure 2. Expression pattern of NsCET1 in N. sylvestris 628

A, RT-qPCR analysis of NsCET1 mRNA level in N. sylvestris under long-day (LD) or 629

short-day (SD) conditions. The relative expression of NsCET1 was normalized to β-630

tubulin expression. B and C, Histochemical staining of leaf (B) and apex (C, indicated by 631

an arrow) tissue of N. sylvestris transformants carrying a 5.5-kb fragment of NsCET1 632

promoter fused with a GUS reporter gene. Scale bars=0.5 mm. D, Bimolecular 633

fluorescence complementation (BiFC) assay of interaction between NsCET1 and FD. 634

VYNE(R)-CET1 and SCYCE(R)-FD were co-infiltrated in leaves of Nicotiana 635

benthamiana by agro-infiltration. Scale bars=50 μm. E and F, Histochemical staining of 636

roots of root (E) and root tip (F) tissue of N. sylvestris CET1pro-GUS transformants. 637

Scale bars=0.2 mm. 638

639

Figure 3. Knockdown of NsCET expression promotes flowering in tobacco 640

A, Flowering time of wild-type N. sylvestris (Syl, white circle) and N. sylvestris P35S-641

amiR-CET transformants (amiR, black circle) under LD conditions. Each spot represents 642

the leaf number of individual wild-type or transformants during flowering (**=p<0.01, 643

unpaired Student’s t-test). B–D, RT-qPCR analysis of NsCET1 (B), NsCET2 (C), and 644

NsCET10 (D) mRNA level in mature leaves of wild-type N. sylvestris (Syl) and 3 645

representative N. sylvestris P35S-amiR-CET T2 plants (T1-4. T1-5, and T1-9). The 646



36

relative expression of CETs was normalized to β-tubulin expression. E, Representative 647

images of wild-type N. sylvestris (Syl, left) and P35S-amiR-CET transformants (amiR, 648

right) grown under SD conditions for 6 months. F, Representative images of wild-type N. 649

sylvestris (Syl, left) and P35S-amiR-CET transformant (amiR, right) grown under SD 650

conditions but with dim light (10 μmole m-2 s-1) during the dark period. 651

652

Figure 4. Phenotypes of tobacco PSUC2-NsCET1 transformants are graft-653

transmissible 654

A, Wild-type N. tabacum cv Turkish scions grafted onto wild-type Turkish stocks 655

(WT/WT; left two plants) or onto PSUC2-NsCET1 transformant stocks (WT/CET1ox; 656

right two plants). The mature leaves were regularly removed from scions to enhance sink 657

strength. Note that the flowering time of the scions grafted onto PSUC2-NsCET1 658

transformant stocks (WT/CET1ox) was significantly delayed. B, Box whisker plot of 659

flowering time of wild-type scions grafted onto wild-type stocks (WT*/WT; yellow, n=7) 660

or PSUC2-NsCET1 transformant stocks (WT*/CET1ox; green, n=10). Flowering time 661

was presented as number of leaves of scions, which was calculated from the grafted 662

junction to the first floral bud. WT* indicates that samples were calculated from wild-663

type scions (****=p<0.0001, unpaired Student’s t-test). C, Internodes of wild-type scions 664

grafted onto wild-type stock (WT*/WT) or PSUC2-NsCET1 transformant stock 665

(WT*/CET1ox). The nodes are indicated by red asterisks. Scale bar=1 cm. D, Box-666

whisker plots of internode length of 5 representative scions grafted onto wild-type stocks 667

(WT*/WT; yellow, 1–5) or PSUC2-NsCET1 transformant stocks (WT*/CET1ox; green, 668



37

6–10). Horizontal lines are median; box edges are Q1–Q3; whiskers are highest and 669

lowest values (****=p<0.0001, unpaired Student’s t-test). 670

671

Figure 5. Long-distance movement of NsCET1 mRNA in Arabidopsis 672

A and B, RT-qPCR analysis of NsCET1 mRNA level in wild-type Arabidopsis scions 673

grafted onto Arabidopsis P35S-NsCET1 (A) or PSUC2-NsCET1 (B) transformant stocks. 674

RNA was extracted from mature leaves of wild-type (Col), P35S-NsCET1, or PSUC2-675

NsCET1 stocks or wild-type scions grafted onto P35S-NsCET1 or PSUC2-NsCET1 676

transformant stocks (SC1 and SC2). The relative mRNA level of NsCET1 was 677

normalized to ubiquitin-conjugating enzyme (UBC) expression. 678

679

Figure 6. Long-distance movement of tobacco NsCET1 mRNA in tomato-tobacco 680

heterografts 681

A, Representative images of tomato-tobacco heterografting experiments, depicting a 682

wild-type tomato scion grafted with a wild-type N. sylvestris stock. The grafting union 683

was secured by grafting clips (white arrow). Mature leaves of tomato recipient were 684

removed to enhance the sink strength. B and C, RT-PCR analysis of various mRNA in 685

mature leaves of wild-type N. sylvestris (Tob), wild-type tomato (Tom), or tomato scions 686

(indicated by stars) grafted onto tobacco stocks (Tom*/Tob, 1–5). PCR (B) was 687

performed with gene-specific primers for tobacco NsCET1 (upper panel), tobacco 688

NsPP2A (middle panel) and loading controls of tobacco ACTIN2 (NsACT2, the first lane 689

in lower panel), or tomato IMPORTINα (SIKAPα, lanes 2–6 in lower panel). Nested RT-690

PCR (C) was performed for tobacco NsMFTL2 (upper panel), tobacco NsFT2 (middle 691



38

panel), and tobacco NsFT3 (lower panel). The position of the 0.25- and 1-kb DNA 692

marker (lower and upper black lines, respectively) is indicated in each panel. 693

694

Figure 7. Long-distance movement of tomato PEBP genes mRNA in tobacco-tomato 695

heterografting experiments 696

A, Representative images of tobacco-tomato heterografting experiments, depicting a 697

wild-type tobacco scion grafted with a wild-type tomato stock. The grafting union was 698

secured by parafilm (white arrow). Mature leaves of tobacco scions were removed to 699

enhance the sink strength. B, RT-PCR analysis of mRNA from wild-type tomato (Tom), 700

wild-type tobacco (Tob), or tobacco scions (indicated by stars) grafted onto tomato stocks 701

(Tob*/Tom). PCR was performed with gene-specific primers for tomato SP2G (MFT-like 702

clade); SP3D, SP5G and SP11A (FT-like clade); SP9D (TFL-like clade); and loading 703

controls of tomato, IMPORTINα (SIKAPα, the first lane), or tobacco ACTIN2 (NtACT2, 704

lane 2 and 3). 705

706

707



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http://scholar.google.com/scholar?as_q=Phloem long-distance delivery of FLOWERING LOCUS T to the apex&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yoo&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zeevaart JAD %281976%29 Physiology of flower formation%2E Annu Rev Plant Physiol 27%3A 321%2D348%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Physiology of flower formation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zeevaart&as_ylo=1976&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zeevaart JAD %282008%29 Leaf%2Dproduced floral signals%2E Curr Opin Plant Biol 11%3A 541%2D547%2E&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang W%2C Thieme CJ%2C Kollwig G%2C Apelt F%2C Yamg L%2C Winter N%2C Andresen N%2C Walther D%2C Kragler F %282016%29 tRNA%2Drelated sequences trigger systemic mRNA transport in plants%2E Plant Cell 28%3A 1237%2D1249%2E&dopt=abstract

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http://scholar.google.com/scholar?as_q=tRNA-related sequences trigger systemic mRNA transport in 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

http://scholar.google.com/scholar?as_q=tRNA-related sequences trigger systemic mRNA transport in plants&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhu Y%2C Liu L%2C Shen L%2C Yu H %282016%29 NaKR1 regulates long%2Ddistance movement of FLOWERING LOCUS T in Arabidopsis%2E Nature Plant 2%3A 16075%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=NaKR1 regulates long-distance movement of FLOWERING LOCUS T in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=NaKR1 regulates long-distance movement of FLOWERING LOCUS T in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhu&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1


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