Mechanisms of long-distance mRNA movement 2 · 95 species/genotype was used as a scion and another...

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Short title: Mechanisms of long-distance mRNA movement 1

2

*Corresponding Authors: 3

Cankui Zhang 4

Department of Agronomy 5

Purdue University 6

West Lafayette, IN 47907 7

Phone: +1 765-496-6889 8

Email: [email protected] 9

Zhangjun Fei 10

Boyce Thompson Institute 11

Cornell University 12

Ithaca, NY 14853, USA 13

Phone: +1 607-254-3234 14


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Plant Physiology Preview. Published on May 2, 2018, as DOI:10.1104/pp.17.01836

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Article title: Elucidation of the mechanisms of long-distance mRNA movement in a Nicotiana 17

benthamiana/tomato heterograft system 18

19

Chao Xia1,2,3†

, Yi Zheng4†

, Jing Huang1, Xiangjun Zhou

1, Rui Li

5, Manrong Zha

1, Shujuan 20

Wang1, Zhiqiang Huang

6, Hai Lan

2,3, Robert Turgeon

7, Zhangjun Fei

4,8*, and Cankui Zhang

1,9* 21

22

1Department of Agronomy, Purdue University, West Lafayette, IN, 47907, USA 23

2Maize Research Institute, Sichuan Agricultural University, Chengdu, Sichuan 611130, China 24

3Key Laboratory of Biology and Genetic Improvement of Maize in Southwest Region, Ministry 25

of Agriculture, China 26

4Boyce Thompson Institute, Cornell University, Ithaca, NY 14853, USA 27

5College of Agronomy, Sichuan Agricultural University, Chengdu, Sichuan 611130, China 28

6Biost Technology Co., Ltd, Beijing 102206, China 29

7Plant Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY 30

14853, USA 31

8USDA-ARS Robert W. Holley Center for Agriculture and Health, Ithaca, NY 14853, USA 32

9Purdue Center for Plant Biology, Purdue University, West Lafayette, IN, 47907, USA 33

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One-sentence summary: Messenger RNA is degraded as it moves through the tomato phloem 35

and the mobility of a transcript cannot be reliably predicted based on its abundance in the 36

Nicotiana benthamiana leaf or on whether it harbors a tRNA-like structural motif. 37

Author Contributions: C.Z., R.T., C.X., and X.Z. conceived and designed the experiments; 38

C.X., J.H., M.Z., and S.W. performed N. benthamiana/tomato grafting in hydroponic 39

experiments; C.X. and R.L. performed transgenic potato grafting experiments; C.X. performed 40



3

long-stem grafting, split shoot grafting, and canola/Arabidopsis grafting; Z.Y., Z.F., C.X., and 41

Z.H. devised and implemented the bioinformatics methodology and analysis; C.X. and C.Z. 42

wrote the manuscript; C.Z., Z.F., R.T., and H.L. revised and finalized the manuscript. 43

Funding Information: This work was supported by funds from Purdue University as part of 44

AgSEED Crossroads funding to support Indiana’s Agriculture and Rural Development (to C. Z.), 45

National Key Research and Development Project of China (2016YFD0101206), and the US 46

National Science Foundation (IOS-1339287 and IOS-1539831). 47

†These authors contributed equally to the article. 48

The author responsible for distribution of materials integral to the findings presented in this 49

article in accordance with the Journal policy described in the Instructions for Authors 50

(http://www.plantphysiol.org) is: Cankui Zhang ([email protected]). 51

*Corresponding Authors: 52

Cankui Zhang 53


Zhangjun Fei 55


57


mailto:[email protected]




4

ABSTRACT 58

Recent heterograft analyses showed that large-scale mRNA movement takes place in the phloem, 59

but the number of mobile transcripts reported varies widely. However, our knowledge of the 60

mechanisms underlying large-scale mRNA movement remains limited. In this study, using a 61

Nicotiana benthamiana/tomato (Solanum lycopersicum) heterograft system and a transgenic 62

approach involving potato (Solanum tuberosum), we found that: 1) the overall mRNA abundance 63

in the leaf is not a good indicator of transcript mobility to the root; 2) increasing the expression 64

levels of non-mobile mRNAs in the companion cells does not promote their mobility; 3) mobile 65

mRNAs undergo degradation during their movement; and 4) some mRNAs arriving in roots 66

move back to shoots. These results indicate that mRNA movement has both regulated and 67

unregulated components. The cellular origins of mobile mRNAs may differ between herbaceous 68

and woody species. Taken together, these findings suggest that the long-distance movement of 69

mRNAs is a complex process and elucidating the physiological roles associated with this 70

movement is challenging but remains an important task for future research. 71

72

Keywords: heterograft, phloem, mobile mRNA, long-distance, mRNA degradation, mRNA 73

cycling, TLS motif, RNA-Seq 74

75



5

INTRODUCTION 76

Higher plants have evolved a communication system that enables the coordination of 77

developmental and environmental cues between different organs (Spiegelman et al., 2013; 78

Turnbull and Lopez‐Cobollo, 2013). This communication is achieved by long-distance signaling 79

that takes place in the vasculature tissue (Banerjee et al., 2006). Phloem, one of the major 80

components in the vasculature system, has long been recognized as a tissue that transports 81

carbohydrates and amino acids. In recent years, it has been found that this tissue is also a conduit 82

for signals, e.g., mRNAs, small RNAs, proteins, small peptides, and hormones (Turgeon and 83

Wolf, 2009). 84

Although mRNAs have been traditionally viewed as local intermediate components between the 85

genomic DNA and the protein in a cell, a handful of classical studies have shown that some 86

mRNAs are able to traffic from source to sink tissues via the phloem and exert important 87

physiological functions in the distal recipient organs. For example, the development of sink 88

tissues, such as young leaves (Kim et al., 2001), tubers (Banerjee et al., 2006), and roots 89

(Notaguchi et al., 2012), are partially controlled by the long-distance mobile mRNAs generated 90

in the source tissues. 91

A recent study on the interaction between the parasitic Cuscuta pentagona and its host indicated 92

that a large amount of bidirectional mRNA exchange occurred via the vasculature between the 93

two species (Kim et al., 2014). In recent years, a few heterograft systems, in which one 94

species/genotype was used as a scion and another as a rootstock, were used to demonstrate that 95

large-scale migration of mRNAs occurs from leaf to root, or vice versa. Notaguchi et al. (2015) 96

determined that 138 transcripts moved from the rootstock of Arabidopsis thaliana to the 97

Nicotiana benthamiana scion via the phloem. Using two different ecotypes of Arabidopsis, 98

Thieme et al. (2015) determined that 2,006 mRNAs could move from the shoot to the root, or 99

vice versa, under either normal or mineral-deficient conditions. In a grapevine (Vitis vinifera) 100

heterograft system, a total of 3,333 mRNAs were found to be transmissible (Yang et al., 2015). 101

In another heterograft system, an analysis of the response to early phosphate deficiency revealed 102

that 3,546 mRNAs moved from cucumber (Cucumis sativus) source leaves to watermelon 103

(Citrullus lanatus) sink tissues via the phloem (Zhang et al., 2016). 104



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This variability, with over an order of magnitude differences in the number of mRNAs 105

transported, suggests a great deal of species specificity and that not all the mobile mRNAs are 106

functional. Zhang et al. (2016) discovered that among the large number of mobile mRNAs 107

identified in the Arabidopsis heterografts, 11.4% of them harbored a tRNA-like structure (TLS). 108

Further experimental evidence supported the hypothesis that not only does this motif impart 109

stability and mobility to mRNAs, but also that mRNAs with this structure can be translated into 110

proteins after transport (Zhang et al., 2016). However, how this mechanism can be applied to 111

other plant heterograft systems remains unknown. A computational analysis conducted by 112

Calderwood et al. (2016) on the same set of mobile mRNAs suggested that most of the identified 113

mRNA species are mobile as a consequence of local abundance in companion cells. Similar 114

correlation between abundance and long-distance mobility has been noted by other researchers as 115

well (Kim et al., 2014; Yang et al., 2015). The extent to which this correlation, drawn from either 116

mathematical modeling methods or computational analysis, applies to natural plant systems 117

needs further experimental verification. 118

In this study, we developed a heterograft system using Nicotiana benthamiana and tomato 119

(Solanum lycopersicum) to investigate shoot-to-root mRNA movement. Compared to most 120

published heterograft systems, the phylogenetic distance between these two species is relatively 121

large, which allowed for more accurate distinction of scion mRNAs from those in the rootstock. 122

In addition, the ease of transformation of the two partners is advantageous in future molecular 123

and physiological studies. We used this system to test if: 1) the abundance of mRNAs in the leaf 124

is a determining factor for mRNA mobility; 2) the movement of mRNAs is a regulated or 125

unregulated process; 3) mobile mRNAs undergo degradation during their movement from shoots 126

to roots; and 4) shoot-to-root-to-shoot cycling movement occurs. In addition, a transgenic 127

approach involving potato (Solanum tuberosum) was used to test the relationship between the 128

abundance of companion cell transcripts and their shoot-to-root mobility. 129

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RESULTS 131

mRNA migration from shoot to root 132

A heterograft system, in which N. benthamiana was used as the scion and tomato as the 133

rootstock, was established to identify the shoot-to-root long-distance movement of mRNAs 134

through the phloem (Fig. 1A). We compared the morphology of leaves and roots in both the 135

heterografts and the non-grafted counterparts. No visible phenotypic differences were observed, 136

indicating that the heterografts had largely maintained the endogenous physiology of the non-137

grafted plants (data not shown). 138

A total of 183 N. benthamiana mRNAs were determined to move into the tomato root in 139

heterografts grown in a hydroponic system (Supplementary Table 1). Gene ontology (GO) 140

analysis of these mobile mRNAs indicated that certain biological processes, e.g., translation 141

(19.1%), transport (14.2%), and biosynthetic process (14.8%), were over-represented. Within the 142

cellular component category, ribosome (15.3%), membrane (28.4%), and intracellular (14.8%) 143

were over-represented. Moreover, nucleotide binding (20.8%), transporter activity (16.9%), and 144

RNA binding (7.1%) were over-represented in the molecular function category (Fig. 1B and 145

Supplementary Table 2). 146

Orthologues of some of the mRNAs identified from this work were also reported in previous 147

studies in which traditional phloem collection methods were used (Ivashikina et al., 2003; 148

Doering-Saad et al., 2006; Omid et al., 2007; Deeken et al., 2008; Kanehira et al., 2010). For 149

example, IAA1, the mRNA encoding an auxin-responsive protein, was identified as mobile in our 150

system. A previous analysis discovered a member of the Aux/IAA family encoding a 151

transcriptional regulator in auxin signaling in the phloem sap of melon (Cucumis melo) (Omid et 152

al., 2007). IAA18 and IAA28, two additional auxin signaling-related transcripts, were found to be 153

expressed in the vasculature tissue of mature Arabidopsis leaves, and transported to the root tip 154

to regulate lateral root formation (Notaguchi et al., 2012). In addition, a number of mRNAs 155

encoding essential translation machinery components, e.g., ribosomal protein, elongation factor, 156

and eukaryotic translation initiation factor, were found to be mobile. Previous proteome studies 157

have discovered that many proteins related to translation exist in the phloem (Lin et al., 2009; 158



8

Ma et al., 2010; Ham and Lucas, 2014) even though the translational machinery is absent in 159

sieve elements. 160

Abundance of mRNA is not associated with mobility 161

To determine whether more abundant leaf mRNAs are prone to move, we collected mature 162

leaves from the N. benthamiana scions in the N. benthamiana/tomato heterograft and sequenced 163

the mRNAs. The abundances of the transcripts in leaves corresponding to the 183 mobile 164

mRNAs were compared with the abundances of the same 183 mRNAs in the heterograft roots. 165

No correlation (r2 = 0.0037) was found between the shoot-to-root mobility of the mRNAs and 166

their abundances in the leaves, the origin of these mobile mRNAs (Fig. 2A and Supplementary 167

Table 3). Further detailed analysis showed that none of the 100 most abundant leaf mRNAs 168

moved from shoots to roots; among the 183 mobile mRNAs, only 3 transcripts were ranked 169

among the 183 most abundant leaf mRNAs (Fig. 2B). On the contrary, some mRNAs with low 170

abundance in the leaf were able to move to the rootstock. The abundances of approximately half 171

(91 out of 183) of the mobile mRNAs were ranked lower than 30,000th

among the entire leaf 172

transcriptome. For example, the abundance of Niben101Scf00291g02025.1, a mRNA ranked the 173

8th

most mobile, was ranked 30,982th

in abundance in the leaf; Niben101Scf05425g00016.1 was 174

ranked 16th

in the mobile list but the 33,512th

most abundant in the leaf transcriptome. Although 175

most of the shoot-to-root mobile mRNAs had higher abundances in the scion than in the 176

rootstock, it is noteworthy that the abundances of 27 mobile mRNAs were higher in the rootstock 177

than in the leaf. For example, Niben101Scf01796g01005.1, an mRNA that was ranked the 17th

178

most mobile, had a reads per kilobase of exon per million fragments mapped (RPKM) value of 179

1.14 in the rootstock but only 0.20 in the leaf (the 40,445th

most abundant in the leaf 180

transcriptome) (Supplementary Table 4). 181

Overexpressing phloem immobile mRNAs in the companion cells does not promote 182

mobility 183

The lack of correlation between the mobility of mRNAs and their abundances in the leaf 184

indicated that using whole leaf tissues is not informative enough to predict the mobility of 185

mRNAs. One possibility is that only cells directly connected to the sieve tubes act as sources of 186

mobile mRNAs. In apoplastic loading species, such as N. benthamiana, the phloem is isolated 187



9

from surrounding cells and it is generally believed that the components moving in the sieve tubes 188

originate in the associated companion cells (King and Zeevaart, 1974; Stadler et al., 2005). Using 189

a simple computational model, Calderwood et al. analyzed a series of mobile RNA datasets 190

associated with Arabidopsis and postulated that mRNAs with higher abundance in the 191

companion cells are more prone to move (Mustroph et al., 2009; Calderwood et al., 2016). To 192

test this hypothesis, we investigated whether increasing the abundance of a phloem-immobile 193

mRNA will make it mobile. We overexpressed the Arabidopsis dual-affinity nitrate transporter 194

gene (AtCHL1) and the Arabidopsis ammonium transporter gene (AtAMT1;2) in the phloem of 195

potato driven by the strong companion-cell-specific sucrose transporter 2 (SUC2) promoter. 196

Neither of the homologous mRNA transcripts of these two genes were detected to be mobile in 197

our heterograft system. In addition, the phloem immobility of homologues of these two 198

transcripts in previously published heterograft systems was further confirmed by exploring the 199

PlaMoM database (Guan et al., 2016). Previous analysi had shown that the size of the shoot-to-200

root mobile mRNAs can be as large as 4 kb (Notaguchi et al., 2015; Thieme et al., 2015; Zhang 201

et al., 2016). Therefore, the length, i.e., 1,545 bp and 1,773 bp, respectively, of AtAMT1;2 and 202

AtCHL1, should not pose a negative effect to the movement of the individual mRNAs from the 203

companion cell to the sieve tube. Multiple transgenic lines were generated and the transgenic 204

potato plant with the highest expression of either AtCHL1 or AtAMT1;2 in the companion cells 205

was used as the scion that was grafted onto the wild-type potato rootstock (Fig. 3A and 206

Supplementary Fig. 1). The lack of amplification via PCR of these genes in the rootstock of the 207

heterografts indicated that the increased abundances of these phloem-immobile mRNAs 208

transcribed in the companion cells did not promote shoot-to-root movement (Fig. 3B). 209

Mobile mRNAs differentially accumulate along the movement path 210

In addition to the cell specificity that might confer the mobility of an mRNA, transport from 211

shoot to root could depend on other factors, such as sequence structure and half-life (Calderwood 212

et al., 2016; Zhang et al., 2016). In the Arabidopsis/Cuscuta system, three host-born mRNAs 213

were chosen as representatives to investigate the fate of mobile mRNAs once entering the 214

parasitic plant. It was found that the accumulation patterns, i.e., increased or decreased 215

abundance, of these mobile mRNAs differed during their transport path (LeBlanc et al., 2013). 216

To understand whether mobile mRNAs accumulate differently once passing the graft joint on a 217



10

more global scale, N. benthamiana scions were grafted onto the tops of 2.5-m tall tomato plants 218

(Fig. 4A and B). RNAs were extracted from three locations, high stem (10-20 cm below the 219

grafting joint), low stem (120-130 cm below the grafting joint) and root, and sequenced. The 220

analysis revealed that a total of 1,096 mRNAs from the N. benthamiana scion passed the grafting 221

joint and moved downward to the tomato rootstock. However, 78% (854 transcripts) of the 222

mobile mRNAs did not arrive in the root. The total number of mobile mRNAs decreased from 223

the “high stem” (723) to the “low stem” (663) and the root (242) (Fig. 4C and Supplementary 224

Table 5, 6, and 7). Although the abundance of most mRNAs decreased during the shoot-to-root 225

transport, 10 mRNAs showed higher abundance in the root than in the “high stem” and “low 226

stem” (Fig. 4D, Table 1 and Supplementary Table 8). It is noteworthy that two of these root-227

accumulated mobile mRNAs were annotated as casein kinase I, which has been reported to be 228

involved in plant hormonal metabolism and establishment of root architecture (Liu et al., 2003). 229

Another interesting observation is that some of the mobile mRNAs identified in “low stem” or 230

root were not detected in tissues located above it. For example, 325 mRNAs detected in the “low 231

stem” were not detectable in the “high stem” site; similarly, 36 mRNAs detected in root were not 232

detectable in either location in the stem. A similar phenomenon was observed in the Arabidopsis 233

heterograft, where some of the rootstock mRNAs identified in the scion flowers were not 234

detectable in the inflorescence stem, a tissue mediating the mRNA transport (Thieme et al., 235

2015). One possible explanation for this is that the abundances of these mobile mRNAs are so 236

low that they cannot be readily detected in those tissues using the RNA-Seq analyses. 237

mRNAs move from scion to rootstock to scion 238

In addition to the shoot-to-root movement of mRNAs (Thieme et al., 2015; Yang et al., 2015; 239

Zhang et al., 2016), Arabidopsis and grapevine heterograft systems indicate that mRNAs 240

transcribed in roots can also move from roots to shoots (Thieme et al., 2015; Yang et al., 2015). 241

In these previous studies, two separate groups of mRNAs, originating either from leaves or roots, 242

were demonstrated to be mobile. We asked whether mRNAs in the rootstock that had arrived 243

from the scion can be transported back to the shoot. In contrast to previous analysis, our interest 244

was only focused on the same set of mRNAs that are transcribed in the leaf. To test this, we 245

developed a system in which potato and N. benthamiana were individually grafted onto two 246

separate stems emerging from the same tomato rootstock (Fig. 5A). The potato scion was first 247



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grafted onto one of the two stems on the tomato rootstock (Fig. 5B). Once the first heterograft 248

was established and the potato scion was actively growing, the young sink leaves on the potato 249

shoot were removed and a N. benthamiana scion was grafted onto the second stem of the tomato 250

rootstock (Fig. 5C). Since only mature source leaves of the potato scion remained, N. 251

benthamiana mRNAs identified in the potato leaves would have to be imported either via the 252

phloem, against source-to-sink bulk flow, or via the non-vasculature cell-to-cell based rootstock-253

to-scion transport approach mediated by plasmodesmata (Lucas et al., 1995). A total of 58 N. 254

benthamiana mobile mRNAs were detected in the mature leaves of the potato scions 255

(Supplementary Table 9). 256

Functional analysis of the 58 scion-to-rootstock-to-scion mobile mRNAs revealed that diverse 257

biological processes were over-represented including those related to translation, transport, and 258

biosynthetic processes (Supplementary Table 10). Within the cellular component category, 259

intracellular, membrane, and thylakoid were over-represented. Moreover, structural molecule 260

activity, transporter activity, and hydrolase activity were over-represented in the molecular 261

function category. 262

Mobile mRNAs are highly system specific 263

Although large-scale movement of mRNAs has been demonstrated, it is not clear how many of 264

the mobile sequences are functional. If the mRNAs do play physiological roles, one would 265

predict sequence conservation between different systems. Identification of the “core” mRNAs 266

shared by these heterograft systems and functional characterization of these mRNAs will shed 267

light on their physiological roles. However, most species involved in these previous systems are 268

not easy to transform, which is a pre-requisite for future in-depth functional analyses of the 269

mobile mRNAs. To address this issue, we developed another heterograft system using canola 270

(Brassica napus) and Arabidopsis, both of which are transformable, as scion and rootstock, 271

respectively (Fig. 6A). Although canola and Arabidopsis are both Brassicaceae species, there is 272

considerable variation in their genome sequences, which facilitates accurate identification of 273

species-specific mRNAs. Surprisingly, RNA-Seq analysis of the Arabidopsis roots only led to 274

the identification of 23 shoot-to-root mobile mRNAs derived from canola (Supplementary Table 275

11). In previous heterograft studies, 1,698, 1,963, and 1,593 shoot-to-root mobile mRNAs were 276



12

detected in Arabidopsis, grapevine, and cucumber systems, respectively. In our N. 277

benthamiana/tomato system, 1,163 mRNAs, when counts from all experimental systems were 278

combined, were detected to be mobile from shoot to root (Supplementary Table 12). 279

To explore whether growth condition and physiological status can cause the movement of 280

different sets of mRNAs, we compared the 183 mobile mRNAs identified in the “regular stem” 281

N. benthamiana/tomato heterograft grown in a hydroponic condition to the 242 mobile mRNAs 282

identified in the “long stem” N. benthamiana/tomato heterograft grown in soil. Forty-one and 283

100 mRNAs were found to be “short stem + hydroponic-” and “long stem + soil-” specific, 284

respectively (Supplementary Table 13). The large difference in the number and identity of 285

mobile mRNAs was also observed in the Cuscuta system, where a total of 9,518 or 347 host 286

mRNAs were detected in Cuscuta when the host species was either Arabidopsis or tomato, 287

respectively (Kim et al., 2014). Together, these findings suggest that the movement of mobile 288

mRNAs could be determined by the species involved in the systems as well as other factors such 289

as the growth environment. 290

To detect whether a “core” group of shoot-to-root mobile mRNAs exists in various systems, we 291

compared the identified mobile mRNAs from the N. benthamiana/tomato heterografts with those 292

identified in Arabidopsis, grape, and cucumber heterograft systems (Thieme et al., 2015; Yang et 293

al., 2015; Zhang et al., 2016). Through orthology analysis, we found that only one mobile 294

mRNA, chlorophyll a/b binding protein 8 (Niben101Scf01328g01012), was shared among these 295

four systems (Fig. 6B). A physiological role for the chlorophyll a/b binding protein in the stem 296

and root has not been reported, although previous localization studies have shown that this gene 297

is lowly expressed in the stem and root (Sakamoto et al., 1991; Tada et al., Song et al., 2007). 298

Future functional study specifically targeted to the movement of this transcript will provide more 299

insight into the regulation of the transport of this transcript. A similar analysis was carried out 300

with the canola/Arabidopsis heterograft system and those in Arabidopsis, grape, and cucumber, 301

and no mRNA was found to be shared (Fig. 6C). 302

Harboring TLS motif does not necessarily lead to high mobility 303

Recently, Zhang et al. demonstrated that a 70-73-nt long transfer RNA (tRNA)-like structure 304

(TLS) motif confers shoot-to-root or root-to-shoot mobility of mRNAs and that approximately 305



13

11.4% and 7.5% of the mobile mRNAs identified from the Arabidopsis Col/Arabidopsis PED 306

and the grapevine heterografts, respectively, harbor this motif (Zhang et al., 2016). We used 307

TLSfinder in the PlaMoM database to scan the mobile transcripts identified in the N. 308

benthamiana/tomato system (Guan et al., 2016). Among the 1,163 mobile mRNAs, 126 (10.8%) 309

harbor at least one TLS motif in the coding sequence or untranslated region, which was 310

significantly enriched (p < 0.05, hypergeometric test) when compared to the genome background 311

(5,066 TLS-containing genes out of 57,140 total genes; 8.9%). We then asked to what extent this 312

positive relationship is reflected in individual mRNAs. To our surprise, among the top 100 most 313

abundant mRNAs in leaves of our N. benthamiana/tomato heterograft system, 18 harbored the 314

TLS motif but none of them were mobile; among the top 2,000 most abundant mRNAs, 174 315

harbored the TLS motif but only 11 were mobile. In addition, in the long-stem N. 316

benthamiana/tomato heterograft system, we found that the majority of the mobile mRNAs 317

harboring the TLS motif did not arrive in the tomato root. Only 23 of the 122 mobile transcripts 318

having this motif that successfully passed the graft junction were detected in the roots. It is 319

important to note that our discovery on the lack of correlation between mobility and the 320

harboring of the TLS motif does not negate the importance of this motif because it is possible 321

that under certain circumstances, e.g., low minerals, some of the immobile mRNAs containing 322

this motif could become mobile (Thieme et al., 2015; Zhang et al., 2016). 323

324



14

DISCUSSION 325

Previous studies using EDTA-facilitated exudation, laser capture micro-dissection (LMC), 326

fluorescence-activated cell sorting (FACS), or cucurbit exudation identified large numbers of 327

mRNAs in the phloem translocation stream (Ivashikina et al., 2003; Doering-Saad et al., 2006; 328

Omid et al., 2007; Deeken et al., 2008; Kanehira et al., 2010). However, the authenticity of these 329

mRNAs was often questioned (Turgeon and Wolf, 2009; Liu et al., 2012; Zhang et al., 2012; 330

Zhang et al., 2014). Recent studies using different heterograft systems strongly suggest the 331

existence of large-scale, long-distance movement of mRNAs via the phloem (Notaguchi et al., 332

2015; Thieme et al., 2015; Yang et al., 2015; Zhang et al., 2016). In addition, several earlier 333

studies on the interaction of the host plants Arabidopsis and tomato with the parasite Cuscuta 334

pentagona have demonstrated that large numbers of host plant mRNAs move to the parasitic 335

species via the phloem (LeBlanc et al., 2013; Kim et al., 2014). These discoveries collectively 336

indicate that movement of mRNAs via the phloem is a common physiological process. In this 337

study, we established a N. benthamiana/tomato heterograft system to identify shoot-to-root 338

phloem-mobile mRNAs. The relatively large differences in genome sequence between the two 339

species allowed confident and exhaustive identification of mobile mRNAs. In addition, we took 340

advantage of this system to study the accumulation pattern of shoot-born mRNAs during their 341

movement to the root. 342

Regulated and unregulated movement of mRNAs 343

It has been demonstrated that some phloem-mobile mRNAs play physiological roles in recipient 344

sink organs such as young leaves, roots, and tubers (Kim et al., 2001; Banerjee et al., 2006; 345

Notaguchi et al., 2012). However, the identification of large numbers of mobile mRNAs 346

(hundreds to thousands) from recent plant-parasitic or heterograft experimental systems and high 347

variation across different systems have raised concerns as to the percentage of these mobile 348

mRNAs associated with physiological functions. Is mRNA transport a regulated physiological 349

and developmental process or due primarily to the leakage of leaf mRNAs into the sieve tubes? 350

In the grapevine study, the number of mobile mRNAs identified from the field-grown 351

heterografts was much smaller than that in the in vitro-grown grafts (Yang et al., 2015). One 352

explanation is that more mobile mRNAs were degraded before reaching the recipient organs in 353

the field-grown grafts due to the longer distance than in the in vitro-grown grafts (Yang et al., 354



15

2015). Similar tendencies for RNA movement were reported for both the Arabidopsis grafts and 355

the parasitic plant and its host plant (LeBlanc et al., 2013; Kim et al., 2014; Thieme et al., 2015). 356

Our long-stem N. benthamiana/tomato experiments showed that a total of 1,096 mRNAs passed 357

the graft joint, but 854 of them disappeared, including some of those with the TLS motif, during 358

their movement from shoot-to-root. The disappearance of mRNAs during their movement can be 359

attributed to two reasons. One is that companion cells along the transport phloem in the stem 360

could specifically arrest certain types of mRNAs from the sieve tube for translation or 361

degradation. The other is that there is an RNase in the sieve tube which can degrade mRNAs 362

lacking protection. Although it is generally believed that the phloem is devoid of RNase and 363

therefore RNA degradation is unlikely (Morris, 2018), the small molecular weights (e.g., 25-29 364

kDa; Bariola et al., 1999) of some of the RNase enzymes are certainly an advantage for their 365

movement from the companion cell to the sieve element. Previous studies have shown that the 366

size exclusion limit between companion cells and sieve elements is large enough to allow the 367

transit of a 67-kDa green fluorescent protein (GFP) in Arabidopsis (Stadler et al., 2005). The 368

lack of detection of the RNase activity in the phloem may be due to inadequate sensitivity of the 369

chemical kits used for the assay (Sasaki et al., 1998; Doering‐Saad et al., 2002). It is reasonable 370

to assume that the movement of mRNAs undergoing degradation in the phloem is not regulated, 371

and therefore it is less likely that there are physiological functions associated with them. 372

However, evidence of a regulated process for mRNA movement exists. It was demonstrated that 373

the long-distance trafficking of StBEL5 in potato is regulated and plays a physiological role in 374

tuberization (Banerjee et al., 2006). A recent study by Zhang et al. (2016) demonstrated that a 375

TLS motif confers mobility for mRNAs. In the grapevine study, some mRNAs were transmitted 376

at rates higher than random transmission (Yang et al., 2015). In our N. benthamiana/tomato 377

grafts, a number of mRNAs had higher abundances in the rootstock than in the leaf, which is the 378

origin of the synthesis of these mobile mRNAs (Table 1; Supplemental Table 4). A mRNA 379

encoding casein kinase I was discovered to be mobile and accumulated in both the regular and 380

the “long-stem” N. benthamiana/tomato heterografts. In rice (Oryza sativa), casein kinase I is 381

involved in auxin metabolism and root development. Arabidopsis plants with downregulated 382

casein kinase I have fewer lateral and adventitious roots as well as shortened primary roots (Liu 383

et al., 2003). It is intriguing to study whether the long-distance movement of the casein kinase 384



16

mRNA plays a role in the establishment of root architecture. Transcript abundance in the 385

companion cells was proposed as one of the mechanisms related to mRNA mobility 386

(Calderwood et al., 2016). However, concerns associated with the mathematical model used to 387

draw the conclusion have been raised (Morris, 2018). Our transgenic potato experiment showed 388

that the abundance itself is not enough to lead to the movement of a mRNA because 389

overexpressing two phloem-immobile mRNAs, AtCHL1 or AtAMT1;2, in the companion cells 390

did not promote their shoot-to-root movements (Fig. 3A and B). This result is in agreement with 391

a recent study in which the overexpression of GFP in the companion cells did not lead to 392

movement of the transcript from the leaf to the root (Paultre et al., 2016). It is important to note 393

that the result from the transgenic potato experiment does not negate the importance of transcript 394

abundance and cell specificity to phloem mobility. They rather indicate that other unidentified 395

regulatory mechanisms, e.g., motif structure, length, interaction with RNA binding proteins or 396

the plasmodesmata between the companion cell and sieve element, etc., in addition to transcript 397

abundance, may also be involved in conferring mobility. 398

Cell origin: apoplastic and symplastic loading species may differ 399

When we compared transcript abundance in the entire leaf versus phloem mobility in the N. 400

benthamiana/tomato heterografts we did not observe any correlation (Fig. 2A), indicating that 401

more abundant transcripts in the leaf do not necessarily lead to higher probability of shoot-to-402

root movement. This lack of correlation is in conflict with the grapevine graft system in which 403

17 of the highly abundant 33 leaf mRNAs were mobile (Yang et al., 2015). This large difference 404

between the two systems led us to hypothesize whether leaf ultrastructure could play a role in 405

this physiological process. N. benthamiana, the scion in our heterograft system, is an apoplastic 406

loading species. The phloem companion cell-sieve element (CC-SE) complex is almost entirely 407

isolated from its surrounding cell types, including the mesophyll, while in grapevine, a woody 408

species and a symplastic loader, the plasmodesmatal connections between the mesophyll cells 409

and the CC-SE complex are very abundant. Therefore, when mRNAs extracted from the entire 410

leaf are used for abundance analysis, the most abundant mRNAs in an apoplastic loader may not 411

have the highest mobility unless they are transcribed in the phloem companion cells. Transcripts 412

generated in the mesophyll cells cannot move to the CC-SE due to the lack of plasmodesmata 413

between them. In contrast, in a symplastic loading species, such as grapevine, mRNAs can 414



17

potentially move directly to the translocation stream sieve element from surrounding cells such 415

as mesophyll. To explore the origin of the mobile mRNAs identified from our heterograft system 416

in which the scion, N. benthamiana, is an apoplastic species, we compared the 1,163 mobile 417

mRNAs derived from the three types of N. benthamiana/tomato heterografts (Supplementary 418

Table 12) to the phloem mRNAs identified with either phloem sap collection or the laser capture 419

microdissection (LCM) method (Ivashikina et al., 2003; Doering-Saad et al., 2006; Omid et al., 420

2007; Deeken et al., 2008; Kanehira et al., 2010). A total of 128 mobile mRNAs were found to 421

be detected in previous studies. A hypergeometric test showed that these mobile mRNAs were 422

over-represented in the mRNAs identified from previous studies (p < 0.05; Supplementary Table 423

14). Previous studies have shown that mRNAs can move from cell to cell via the plasmodesmata 424

(Lucas et al., 1995; Roberts and Oparka, 2003). Hence, the abundance of mRNAs in the leaf 425

could be a better indicator of mRNA mobility in symplastic loading species than in apoplastic 426

species. This hypothesis could also be used to explain why a large number of transcripts 427

harboring the TLS motif in the leaf of the N. benthamiana/tomato heterograft did not move to the 428

root. It is highly possible that this motif could confer mobility only when the mRNAs are 429

transcribed in the companion cells. 430

Scion-to-rootstock-to-scion mRNA cycling 431

While the xylem mainly serves to conduct water and minerals from roots to shoots, the phloem 432

serves as a conduit to transport carbohydrates, amino acids, and a number of signaling molecules. 433

Previous studies in different heterograft systems indicate that mRNAs not only move from 434

shoots to roots via the phloem, but also move from roots to shoots (Thieme et al., 2015; Yang et 435

al., 2015). It has been suggested that the root-to-shoot movement of mobile mRNAs can take 436

place either in the phloem against the source to sink bulk flow or via the cell-to-cell-based root-437

to-shoot transport system (Thieme et al., 2015; Ham and Lucas, 2017). The attentions of these 438

prior studies were either on shoot- or root-derived mRNAs. To find out whether root-arriving, 439

shoot-born mRNAs can move back to the shoot, we designed a “split shoot” system involving 440

tripartite grafting. To our surprise, 58 N. benthamiana mRNAs were found in the potato shoot. 441

To fulfill this scion-to-rootstock-to-scion movement of mRNAs, the scion-to-rootstock mobile 442

mRNAs from N. benthamiana need to be unloaded from the phloem to the apoplast/xylem area 443

in tomato and then are loaded to either an adjacent shoot-ward transport phloem or to other root 444



18

cells, as discussed above, before the rootstock-to-scion movement takes place. How the scion-to-445

rootstock-transmitted mRNAs are released from the phloem to the apoplast/xylem area and 446

exchanged to other cells is a fascinating question to be addressed in the future. It has been known 447

for a long time that the exchange of carbon containing compounds and minerals between the 448

apoplast/xylem and phloem happens in plants, and membrane transporters play important roles in 449

this process (van Bel, 1990; Zhang and Turgeon, 2009; White, 2012). However, there are no 450

mRNA transporters that have been discovered to efflux mRNAs. An alternative explanation is 451

that the scion-to-rootstock-arriving mRNAs are initially unloaded from the phloem in the stele 452

region via plasmodesmata, as indicated by a recent study in which the shoot-to-root-arriving 453

proteins can be unloaded symplastically (Paultre et al., 2016), and then by an unknown 454

mechanism, the unloaded mRNAs are transferred to cells, e.g., phloem and/or cortical, and move 455

to the shoot. 456

Conclusions 457

Heterografting is a powerful system to identify long-distance transport of mobile mRNAs. 458

However, the large variation in the number and identity of the mobile mRNAs derived from 459

different systems indicates that a more general understanding of the mechanisms of the 460

movement of these transcripts is needed before large-scale functional characterizations on 461

individual mRNAs is pursued. Endogenous physiological difference among plant species may be 462

one of the reasons for the large diversity of identified mobile mRNAs. Different heterograft 463

combinations and the degree of the distortion associated with the involved species may be 464

another reason leading to the large variation of identified mobile transcripts. Identifying the core 465

mobile mRNAs across species and dissecting the physiological functions associated with them 466

are challenging but remain an important task for future research. 467

468



19

MATERIALS AND METHODS 469

Plant materials and growth conditions 470

Seedlings of Nicotiana benthamiana, tomato (Solanum lycopersicum cv. Heinz 1706-BG), and 471

potato (Solanum tuberosum L. cv. Désirée) were grown in Propagation mix (Sun Gro 472

Horticulture, Agawam, MA) in a greenhouse with a day/night temperature of 28°C /25°C and a 473

light intensity of approximately 400-600 µmol m-2

s-1

on a 14-h:10-h light regime. Canola 474

(Brassica napus cv. Westar) and Arabidopsis (Arabidopsis thaliana ecotype Columbia) were 475

grown in a growth chamber with a day/night temperature of 26oC/23

oC and a light intensity of 476

250 µmol m-2

s-1

on a 12-h:12-h light regime. 477

Grafting and tissue sampling 478

To produce heterografts between N. benthamiana and tomato, 3-week-old tomato and N. 479

benthamiana seedlings were used as rootstock and scion, respectively. A “V”-shaped wedge of 480

an N. benthamiana stem was inserted into a slit in a tomato stem. Both the scion and the graft 481

joint were kept in a transparent plastic bag and the heterografts were placed beneath a bench with 482

dim light. After one week, the plastic bag was gradually opened over a period of 3 days and the 483

established heterografts were transferred to full-strength hydroponic growth solution and grown 484

in a growth chamber with a day/night temperature of 28°C /25°C and a light intensity of 400-600 485

µmol m-2

s-1

on a 14-h:10-h regime. At this stage, visible flower buds from the N. benthamiana 486

scion were pinched off to avoid contaminating the tomato root tissue with pollen. 487

To overexpress non-mobile mRNAs in the phloem companion cells of potato, two representative 488

Arabidopsis genes, nitrate transporter 1 (AtCHL1) and ammonium transporter 1;2 (AtAMT1;2), 489

were cloned and individually fused behind the promoter of the Arabidopsis sucrose transporter 2 490

(AtSUC2), a phloem companion-cell-specific gene. Primers flanked with restriction sites used to 491

amplify both promoters and genes are listed in Supplementary Table 15. pRI 101-AN was used 492

as the binary vector. Transgenic potato plants were produced by Agrobacterium-mediated 493

transformation following the protocol described in Zhou et al. (Zhou et al., 2017). Grafting 494

transgenic potato onto wild-type potato followed the same procedure described above. These 495

plants were grown in a greenhouse under the aforementioned conditions. 496



20

To study whether the accumulation pattern of mobile mRNAs differs during their movement, the 497

shoot tips of 2.5-m-tall (5-month-old) tomato plants were severed and N. benthamiana scions 498

were grafted onto the tops of these tomato plants. The established heterografts were allowed to 499

grow for 6 weeks in a greenhouse in the conditions described above. 500

To study whether scion-to-rootstock mobile mRNAs can move back to the scion after they arrive 501

in the root, tomato seedlings were trained to have two major stems during their first 3 weeks of 502

growth. A potato scion was grafted on one of the two stems to form the first heterograft. After 3 503

weeks, the young sink leaves on the actively growing potato scion were pinched off and a N. 504

benthamiana scion was grafted onto the second stem of the tomato to create a “split-shoot” plant. 505

These tripartite heterografts were grown in the same greenhouse in the conditions described 506

above for another 3 weeks before the mature leaves on the potato scion were harvested. 507

To produce the canola/Arabidopsis heterograft, shoots of 2-week-old canola plants were grafted 508

onto the severed inflorescence stems of 4-week-old Arabidopsis. The procedure was similar to 509

that used for the N. benthamiana/tomato system. The heterografts were allowed to grow for 6 510

weeks in a chamber with a day/night temperature of 26°C /23°C and a light intensity of 250 µmol 511

m-2

s-1

in a 12-h:12-h regime to produce several actively growing mature canola leaves. At 5 512

days prior to harvesting the Arabidopsis roots, the Arabidopsis leaves were covered by aluminum 513

foil to facilitate the source-to-sink bulk flow from the canola leaves to the Arabidopsis roots. 514

RNA isolation and RT-PCR 515

Total RNA was isolated from tissues using the E.Z.N.A. Total RNA Kit I (Omega Bio-tek, 516

Norcross, GA) following the manufacturer's instructions. One microgram of total RNA was 517

treated with RQ1 DNase (Promega, Madison, WI) for 30 min to remove genomic DNA, and then 518

converted into cDNA using iScript Reverse Transcription Supermix (Bio-Rad, Hercules, CA). 519

Gene-specific primers used in RT-PCR are listed in Table S15. Ex Taq DNA Polymerase 520

(Takara Bio USA, Mountain View, CA) was used to amplify the PCR products. The PCR cycle 521

consisted of 95°C for 3 min, followed by 40 cycles of 95°C for 30 s, 60°C for 30 s, and 72°C for 522

30 s. 523

RNA sequencing and RNA-Seq data processing 524



21

Strand-specific RNA-Seq libraries were constructed from 4 μg total RNA using the Illumina 525

TruSeq Stranded mRNA Library Prep Kit (Illumina, San Diego, CA) following the 526

manufacturer’s protocol. Three independent biological replicates for either leaf or root from the 527

different heterograft combinations described above were prepared and sequenced on an Illumina 528

NextSeq 500 system at the Genomics Resources Core Facility of Weill Cornell Medical College. 529

Libraries from different species were sequenced on different lanes of NextSeq 500 to avoid cross 530

contaminations between samples. 531

Raw RNA-Seq reads were first processed to trim the adaptor and low-quality sequences using 532

Trimmomatic (Bolger et al., 2014) and trimmed reads shorter than 40 bp were discarded. The 533

remaining high-quality reads were first aligned to a ribosomal RNA (rRNA) database using 534

Bowtie (Langmead et al., 2009), allowing up to three mismatches. These rRNA-mapped reads 535

were excluded from subsequent analyses. The remaining cleaned RNA-Seq reads were mapped 536

to the corresponding genomes using HISAT (Kim et al., 2015). Following alignments, raw 537

counts for each gene model were derived and then normalized using the RPKM (reads per 538

kilobase of exon per million fragments mapped) method (Mortazavi et al., 2008). 539

Graft-transmissible mRNA identification 540

To identify mRNAs transmitted from the N. benthamiana scion to the tomato rootstock, the 541

cleaned reads from the tomato rootstock were first mapped to the tomato genome (Tomato 542

Genome, 2012) using HISAT allowing up to two edit distances. The unmapped reads were 543

compared with the RNA-Seq reads from the non-grafted tomato plants, and those having perfect 544

matches were discarded. The remaining reads were further mapped to the N. benthamiana 545

genome (Bombarely et al., 2012) using HISAT, allowing up to one edit distance. Reads mapped 546

to the N. benthamiana genome were regarded as transmitted. The graft-transmissible mRNAs 547

were identified if the corresponding reads were detected in at least two out of the three biological 548

replicates. Similar procedures were followed to identify mobile mRNAs for the tripartite N. 549

benthamiana/tomato/potato system and the canola/Arabidopsis system. GO terms enriched in the 550

mobile mRNAs were identified using GO::TermFinder (Boyle et al., 2004). 551

Differential accumulation analysis in long-stem N. benthamiana/tomato heterografts 552



22

Plant tissues from “high stem” (a region approximately 10-20 cm below the grafting joint), “low 553

stem” (a region approximately 120-130 cm below the grafting joint) and root were collected for 554

RNA-Seq analysis. Identification of the mobile mRNAs followed the same procedure as 555

described above. Raw counts were then fed to edgeR (Robinson et al., 2010) to identify 556

differentially accumulated genes. The Benjamini and Hochberg method (Benjamini and 557

Hochberg, 1995) was used to adjust raw P-values with a confidence threshold of false discovery 558

rate (FDR) <0.01. The abundance of each mRNA in “high stem”, “low stem”, and root was 559

divided by that in the root to obtain relative fold changes along the movement path. 560

TLS structure analysis 561

tRNA-like structures (TLS) for either the entire N. benthamiana leaf transcriptome or all of the 562

identified mobile mRNAs were scanned using TLSfinder in the PlaMoM database (Guan et al., 563

2016) with default parameter settings. 564

Orthology analysis 565

Complete proteome sequences of N. benthamiana were compared to those of Arabidopsis, 566

grapevine, and cucumber using BLASTP with an e-value cutoff of 1e-05

. Orthologous pairs 567

between N. benthamiana and Arabidopsis, grapevine, or cucumber were identified based on the 568

reciprocal best hits of BLASTP. The orthologous pairs that shared the same N. benthamiana 569

genes were identified as those present in all four species. The same procedure was used to 570

identify orthologous pairs between canola and Arabidopsis, grapevine, or cucumber. Mobile 571

mRNAs identified from the different heterograft systems and presented in the four-way 572

orthology were used for the comparisons. 573

Accession Numbers 574

The sequence data were deposited in the NCBI sequence read archive (SRA) under the accession 575

number SRP111187. 576

SUPPLEMENTARY MATERIALS 577

The following materials are available in the online version of this article. 578



23

Supplementary Figure 1. Companion cell-specific overexpression of two phloem immobile 579

mRNAs in potato. 580

Supplementary Table 1. N. benthamiana mRNAs detected in the tomato root samples in the N. 581

benthamiana/tomato heterografts 582

Supplementary Table 2. Enrichment of GO slim terms in the 183 mobile mRNAs detected from 583

the N. benthamiana/tomato hetergrafts 584

Supplementary Table 3. Expression of genes in the leaf of N. benthamiana collected from the N. 585


Supplementary Table 4. Abundance of mobile mRNAs in the scion or rootstock in the N. 587


Supplementary Table 5. Mobile mRNAs detected from the root samples of tomato in the long-589

stem N. benthamiana/tomato heterografts 590

Supplementary Table 6. Mobile mRNAs detected from the "low stem" region of the tomato 591

rootstock in the long-stem N. benthamiana/tomato heterografts 592

Supplementary Table 7. Mobile mRNAs detected from the "high stem" region of the tomato 593

rootstock in the N. benthamiana/tomato heterografts 594

Supplementary Table 8. Differentially expressed mobile mRNAs detected in the "high-stem", 595

"low-stem", and root regions in the "long-stem" N. benthamiana/tomato heterografts 596

Supplementary Table 9. Mobile mRNAs detected from mature potato leaves in the split-shoot 597

grafting system 598

Supplementary Table 10. GO terms enriched in the shoot-to-root-to-shoot mobile mRNAs 599

Supplementary Table 11. Mobile mRNAs detected in the Arabidopsis root collected from the 600

canola/Arabidopsis heterografts 601

Supplementary Table 12. A combined list of shoot-to-root mobile mRNAs in the different 602

heterograft systems 603



24

Supplementary Table 13. Mobile mRNAs identified in the roots from different N. 604


Supplementary Table 14. Comparison of the 1,163 mobile mRNAs identified from the three N. 606

benthamiana/tomato heterografts with phloem mRNAs identified from previous studies 607

Supplementary Table 15. Primers used in this study 608

609



25

ACKNOWLEDGEMENTS 610

We are grateful to the Tomato Genetics Resource Center at the University of California, Davis, 611

for providing the tomato seeds and the Plant Gene Resources of Canada (PGRC) for supplying 612

the Brassica napus, Westar seeds. 613

614

Table 1. Top 10 most highly accumulated mobile mRNAs in the roots of long-stem heterografts 615

mRNA accessions Annotation

Niben101Scf36076g00002.1 Elongation factor 1-alpha 1

Niben101Scf00987g00004.1 Casein kinase I

Niben101Scf02525g03015.1 Casein kinase I

Niben101Scf05201g02004.1 Magnesium transporter NIPA2

Niben101Scf11383g00015.1 40S ribosomal protein S24-2

Niben101Scf05618g04003.1 tRNA (guanine(26)-N(2))-dimethyltransferase

Niben101Scf09409g02014.1 Choline/ethanolaminephosphotransferase 1

Niben101Scf08309g01008.1 Homogentisate 1,2-dioxygenase

Niben101Scf02597g00003.1 30S ribosomal protein S8

Niben101Scf16439g00004.1 30S ribosomal protein S8

616

617



26

Figure legends 618

Figure 1. Shoot-to-root mobile mRNAs identified from the N. benthamiana/tomato heterografts 619

grown in a hydroponic condition. A. Representative heterograft established between N. 620

benthamiana and tomato. The white box indicates the graft union (GU). Image to the right shows 621

an enlargement of the region boxed in the left image. Bar: 2cm. B. GO terms enriched in the 183 622

mobile mRNAs. Columns indicate the percentages of genes that were enriched in the GO terms. 623

“All genes” refers to the whole genome background. 624

Figure 2. Correlation analysis of the abundances of leaf mRNAs and their mobility. Expression 625

levels of the graft-transmissible mRNAs in leaf and root tissues were ranked by mean RPKM 626

values derived from heterografts (n=3) grown with full-strength nutrients. A. Correlation of 627

abundances for the 183 mobile mRNAs in the scion and rootstock. Red dashed is the trend line. 628

B. Venn diagram showing the number of mobile mRNAs among the most abundant 100 or 183 629

mRNAs in the scion. Blue color represents the number of the most abundant mRNAs in the N. 630

benthamiana scion. Red color represents the number of the mobile mRNAs in the tomato 631

rootstock. 632

Figure 3. Mobility of non-mobile mRNAs overexpressed in transgenic potato phloem 633

companion cells. A. Representative SUC2prom::AtCHL1 transgenic potato/WT potato 634

heterograft. White box indicates the graft union (GU). Image to the right shows an enlargement 635

of the region boxed in the left image. Bar: 2cm. B. RT-PCR analysis of AtAMT1;2 and AtCHL1 636

in transgenic potato grafts. Both AtAMT1;2 and AtCHL1 are phloem immobile mRNAs. 637

Transgenic potato plants with overexpressed AtAMT1;2 or AtCHL1 was grafted onto WT and the 638

expression of these genes in the rootstock was compared with that in the homografts in which the 639

scion and the rootstock were the same genotype (WT or transgenic). For the transgenic/WT 640

grafts, three shoots excised from the same transgenic potato plant with either overexpressed 641

AtAMT1;2 or AtCHL1 were grafted on the tomato rootstock, respectively. 642

Figure 4. Differentially accumulated mobile mRNAs along the movement path in a “long-stem” 643

heterograft. A. Representative long-stem heterograft. An actively growing N. benthamiana scion 644

grafted on the top of a 2.5-m-tall tomato rootstock. B. Magnification of the dashed box in (A). 645

GU: graft union. C. Venn diagram indicating the number of mobile mRNAs identified at 646



27

different locations on the tomato rootstock. D. Heatmap showing the abundance profiles of the 647

39 differentially accumulated mobile mRNAs. Colors indicate different log2 (fold change) 648

values, which are related to the mRNA abundance in the root (=0 in the heat map). Left dashed 649

box indicates the 29 mRNAs decreased in abundance during the transport. Right dashed box 650

indicates the 10 mobile mRNAs over-accumulated in the heterograft root. 651

Figure 5. Scion-to-rootstock-to-scion mRNA cycling revealed by a split-shoot heterograft 652

system. A. Representative “split-shoot” heterograft in which the scion on the right is N. 653

benthamiana, the scion on the left is potato, and the rootstock is tomato. The white boxes 654

indicate the graft union (GU). B. Close-up view of the heterograft union between potato and 655

tomato. C. Close-up view of the heterograft union between N. benthamiana and tomato. Bar: 2 656

cm. 657

Figure 6. Heterograft established between canola and Arabidopsis and comparison of mobile 658

mRNAs identified from different heterograft systems. A. Representative canola/Arabidopsis 659

heterograft grown in a hydroponic solution. White box indicates the graft union (GU). Bar: 2cm. 660

B. Venn diagram of orthologous mobile mRNAs identified in the N. benthamiana/tomato system 661

and other heterograft systems. C. Venn diagram of orthologous mobile mRNAs identified in the 662

canola/Arabidopsis system and other heterograft systems. Mobile mRNAs having orthologs in 663

the proteomes of the other three systems based on reciprocal BLASTP hits were included in the 664

comparison. 665

666

667



28

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2

Figure 1. Shoot-to-root mobile mRNAs identified from the N. benthamiana/tomato heterografts

grown in a hydroponic condition. A. Representative heterograft established between N.

benthamiana and tomato. The white box indicates the graft union (GU). Image to the right shows

an enlargement of the region boxed in the left image. Bar: 2cm. B. GO terms enriched in the 183

mobile mRNAs. Columns indicate the percentages of genes that were enriched in the GO terms.

“All genes” refers to the whole genome background.



1

Figure 2. Correlation analysis of the abundances of leaf mRNAs and their mobility. Expression

levels of the graft-transmissible mRNAs in leaf and root tissues were ranked by mean RPKM

values derived from heterografts (n=3) grown with full-strength nutrients. A. Correlation of

abundances for the 183 mobile mRNAs in the scion and rootstock. Red dashed is the trend line.

B. Venn diagram showing the number of mobile mRNAs among the most abundant 100 or 183

mRNAs in the scion. Blue color represents the number of the most abundant mRNAs in the N.

benthamiana scion. Red color represents the number of the mobile mRNAs in the tomato

rootstock.



1

Figure 3. Mobility of non-mobile mRNAs overexpressed in transgenic potato phloem

companion cells. A. Representative SUC2prom::AtCHL1 transgenic potato/WT potato

heterograft. White box indicates the graft union (GU). Image to the right shows an enlargement

of the region boxed in the left image. Bar: 2cm. B. RT-PCR analysis of AtAMT1;2 and AtCHL1

in transgenic potato grafts. Both AtAMT1;2 and AtCHL1 are phloem immobile mRNAs.

Transgenic potato plants with overexpressed AtAMT1;2 or AtCHL1 was grafted onto WT and the

expression of these genes in the rootstock was compared with that in the homografts in which the

scion and the rootstock were the same genotype (WT or transgenic). For the transgenic/WT



2

grafts, three shoots excised from the same transgenic potato plant with either overexpressed

AtAMT1;2 or AtCHL1 were grafted on the tomato rootstock, respectively.



1

Figure 4. Differentially accumulated mobile mRNAs along the movement path in a “long-stem”

heterograft. A. Representative long-stem heterograft. An actively growing N. benthamiana scion

grafted on the top of a 2.5-m-tall tomato rootstock. B. Magnification of the dashed box in (A).

GU: graft union. C. Venn diagram indicating the number of mobile mRNAs identified at

different locations on the tomato rootstock. D. Heatmap showing the abundance profiles of the

39 differentially accumulated mobile mRNAs. Colors indicate different log2 (fold change)

values, which are related to the mRNA abundance in the root (=0 in the heat map). Left dashed

box indicates the 29 mRNAs decreased in abundance during the transport. Right dashed box

indicates the 10 mobile mRNAs over-accumulated in the heterograft root.



1

Figure 5. Scion-to-rootstock-to-scion mRNA cycling revealed by a split-shoot heterograft

system. A. Representative “split-shoot” heterograft in which the scion on the right is N.

benthamiana, the scion on the left is potato, and the rootstock is tomato. The white boxes

indicate the graft union (GU). B. Close-up view of the heterograft union between potato and

tomato. C. Close-up view of the heterograft union between N. benthamiana and tomato. Bar: 2

cm.



1

Figure 6. Heterograft established between canola and Arabidopsis and comparison of mobile

mRNAs identified from different heterograft systems. A. Representative canola/Arabidopsis



2

heterograft grown in a hydroponic solution. White box indicates the graft union (GU). Bar: 2cm.

B. Venn diagram of orthologous mobile mRNAs identified in the N. benthamiana/tomato system

and other heterograft systems. C. Venn diagram of orthologous mobile mRNAs identified in the

canola/Arabidopsis system and other heterograft systems. Mobile mRNAs having orthologs in

the proteomes of the other three systems based on reciprocal BLASTP hits were included in the

comparison.



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Ivashikina N, Deeken R, Ache P, Kranz E, Pommerrenig B, Sauer N, Hedrich R (2003) Isolation of AtSUC2 promoter–GFP-markedcompanion cells for patch–clamp studies and expression profiling. Plant J 36: 931–945


Kanehira A, YamadaeIwaya T, Tsuwamoto R, Kasai A, Nakazono M, Harada T (2010) Apple phloem cells contain some mRNAstransported over long distances. Tree Genet Genomes 6: 635–642


Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12: 357-360Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Kim G, LeBlanc ML, Wafula EK, Depamphilis CW, Westwood JH (2014) Genomic-scale exchange of mRNA between a parasitic plant andits hosts. Science 345: 808-811


Kim M, Canio W, Kessler S, Sinha N (2001) Developmental changes due to long-distance movement of a homeobox fusion transcript intomato. Science 293: 287-289


King R, Zeevaart J (1974) Enhancement of phloem exudation from cut petioles by chelating agents. Plant Physiol 53: 96-103Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the humangenome. Genome Biol 10: R25


LeBlanc M, Kim G, Patel B, Stromberg V, Westwood J (2013) Quantification of tomato and Arabidopsis mobile RNAs trafficking into theparasitic plant Cuscuta pentagona. New Phytol 200: 1225-1233


Lin MK, Lee YJ, Lough TJ, Phinney BS, Lucas WJ (2009) Analysis of the pumpkin phloem proteome provides insights into angiospermsieve tube function. Mol Cell Proteomics 8: 343-356


Liu DD, Chao WM, Turgeon R (2012) Transport of sucrose, not hexose, in the phloem. J Exp Bot 63: 4315-4320Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Liu W, Xu Z-H, Luo D, Xue H-W (2003) Roles of OsCKI1, a rice casein kinase I, in root development and plant hormone sensitivity. PlantJ 36: 189-202


Lucas WJ, Bouché-Pillon S, Jackson DP, Nguyen L (1995) Selective trafficking of KNOTTED1 homeodomain protein and its mRNAthrough plasmodesmata. Science 270: 1980


Ma Y, Miura E, Ham BK, Cheng HW, Lee YJ, Lucas WJ (2010) Pumpkin eIF5A isoforms interact with components of the translationalmachinery in the cucurbit sieve tube system. Plant J 64: 536-550 www.plantphysiol.orgon July 29, 2018 - Published by Downloaded from


http://www.ncbi.nlm.nih.gov/pubmed?term=Ham BK%2C Lucas WJ %282017%29 Phloem%2DMobile RNAs as Systemic Signaling Agents%2E Annu Rev Plant Biol 68%3A 173%2D195&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ham BK, Lucas WJ (2017) Phloem-Mobile RNAs as Systemic Signaling Agents. Annu Rev Plant Biol 68: 173-195

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

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http://www.ncbi.nlm.nih.gov/pubmed?term=Ivashikina N%2C Deeken R%2C Ache P%2C Kranz E%2C Pommerrenig B%2C Sauer N%2C Hedrich R %282003%29 Isolation of AtSUC2 promoter�??GFP%2Dmarked companion cells for patch�??clamp studies and expression profiling%2E Plant J 36%3A 931�??945&dopt=abstract

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http://search.crossref.org/?page=1&rows=2&q=Kanehira A, YamadaeIwaya T, Tsuwamoto R, Kasai A, Nakazono M, Harada T (2010) Apple phloem cells contain some mRNAs transported over long distances. Tree Genet Genomes 6: 635?642

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http://www.ncbi.nlm.nih.gov/pubmed?term=Kim D%2C Langmead B%2C Salzberg SL %282015%29 HISAT%3A a fast spliced aligner with low memory requirements%2E Nat Methods 12%3A 357%2D360&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12: 357-360

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

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http://www.ncbi.nlm.nih.gov/pubmed?term=Kim G%2C LeBlanc ML%2C Wafula EK%2C Depamphilis CW%2C Westwood JH %282014%29 Genomic%2Dscale exchange of mRNA between a parasitic plant and its hosts%2E Science 345%3A 808%2D811&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kim G, LeBlanc ML, Wafula EK, Depamphilis CW, Westwood JH (2014) Genomic-scale exchange of mRNA between a parasitic plant and its hosts. Science 345: 808-811


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http://www.ncbi.nlm.nih.gov/pubmed?term=Kim M%2C Canio W%2C Kessler S%2C Sinha N %282001%29 Developmental changes due to long%2Ddistance movement of a homeobox fusion transcript in tomato%2E Science 293%3A 287%2D289&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kim M, Canio W, Kessler S, Sinha N (2001) Developmental changes due to long-distance movement of a homeobox fusion transcript in tomato. Science 293: 287-289


http://scholar.google.com/scholar?as_q=Developmental changes due to long-distance movement of a homeobox fusion transcript in tomato&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=King R%2C Zeevaart J %281974%29 Enhancement of phloem exudation from cut petioles by chelating agents%2E Plant Physiol 53%3A 96%2D103&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=King R, Zeevaart J (1974) Enhancement of phloem exudation from cut petioles by chelating agents. Plant Physiol 53: 96-103

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http://www.ncbi.nlm.nih.gov/pubmed?term=Langmead B%2C Trapnell C%2C Pop M%2C Salzberg SL %282009%29 Ultrafast and memory%2Defficient alignment of short DNA sequences to the human genome%2E Genome Biol 10%3A R25&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=LeBlanc M%2C Kim G%2C Patel B%2C Stromberg V%2C Westwood J %282013%29 Quantification of tomato and Arabidopsis mobile RNAs trafficking into the parasitic plant Cuscuta pentagona%2E New Phytol 200%3A 1225%2D1233&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=LeBlanc M, Kim G, Patel B, Stromberg V, Westwood J (2013) Quantification of tomato and Arabidopsis mobile RNAs trafficking into the parasitic plant Cuscuta pentagona. New Phytol 200: 1225-1233

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http://www.ncbi.nlm.nih.gov/pubmed?term=Lin MK%2C Lee YJ%2C Lough TJ%2C Phinney BS%2C Lucas WJ %282009%29 Analysis of the pumpkin phloem proteome provides insights into angiosperm sieve tube function%2E Mol Cell Proteomics 8%3A 343%2D356&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Lin MK, Lee YJ, Lough TJ, Phinney BS, Lucas WJ (2009) Analysis of the pumpkin phloem proteome provides insights into angiosperm sieve tube function. Mol Cell Proteomics 8: 343-356

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http://www.ncbi.nlm.nih.gov/pubmed?term=Liu DD%2C Chao WM%2C Turgeon R %282012%29 Transport of sucrose%2C not hexose%2C in the phloem%2E J Exp Bot 63%3A 4315%2D4320&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Liu W%2C Xu Z%2DH%2C Luo D%2C Xue H%2DW %282003%29 Roles of OsCKI1%2C a rice casein kinase I%2C in root development and plant hormone sensitivity%2E Plant J 36%3A 189%2D202&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Lucas WJ%2C Bouch�%2DPillon S%2C Jackson DP%2C Nguyen L %281995%29 Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata%2E Science 270%3A 1980&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Morris RJ %282018%29 On the selectivity%2C specificity and signalling potential of the long%2Ddistance movement of messenger RNA%2E Curr Opin Plant Biol 43%3A 1%2D7&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Morris RJ (2018) On the selectivity, specificity and signalling potential of the long-distance movement of messenger RNA. Curr Opin Plant Biol 43: 1-7

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

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http://scholar.google.com/scholar?as_q=On the selectivity, specificity and signalling potential of the long-distance movement of messenger RNA&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Morris&as_ylo=2018&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Mortazavi A%2C Williams BA%2C McCue K%2C Schaeffer L%2C Wold B %282008%29 Mapping and quantifying mammalian transcriptomes by RNA%2DSeq%2E Nat Methods 5%3A 621%2D628&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Mustroph A%2C Zanetti ME%2C Jang CJ%2C Holtan HE%2C Repetti PP%2C Galbraith DW%2C Girke T%2C Bailey%2DSerres J %282009%29 Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis%2E Proc Natl Acad Sci USA 106%3A 18843%2D18848&dopt=abstract

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Thieme CJ, Rojas-Triana M, Stecyk E, Schudoma C, Zhang W, Yang L, Minambres M, Walther D, Schulze WX, Paz-Ares J, Scheible WR,Kragler F (2015) Endogenous Arabidopsis messenger RNAs transported to distant tissues. Nat Plants 1: 15025


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Turnbull CG, Lopez‐Cobollo RM (2013) Heavy traffic in the fast lane: long‐distance signalling by macromolecules. New Phytol 198: 33-51


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Yang Y, Mao L, Jittayasothorn Y, Kang Y, Jiao C, Fei Z, Zhong GY (2015) Messenger RNA exchange between scions and rootstocks ingrafted grapevines. BMC Plant Biol 15: 251


Zhang C, Turgeon R (2009) Downregulating the sucrose transporter VpSUT1 in Verbascum phoeniceum does not inhibit phloemloading. Proc Natl Acad Sci USA 106: 18849-18854


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

http://scholar.google.com/scholar?as_q=Messenger RNA exchange between scions and rootstocks in grafted grapevines.&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=Messenger RNA exchange between scions and rootstocks in grafted grapevines.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yang&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang C%2C Turgeon R %282009%29 Downregulating the sucrose transporter VpSUT1 in Verbascum phoeniceum does not inhibit phloem loading%2E Proc Natl Acad Sci USA 106%3A 18849%2D18854&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang C, Turgeon R (2009) Downregulating the sucrose transporter VpSUT1 in Verbascum phoeniceum does not inhibit phloem loading. Proc Natl Acad Sci USA 106: 18849-18854

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

http://scholar.google.com/scholar?as_q=Downregulating the sucrose transporter VpSUT1 in Verbascum phoeniceum does not inhibit phloem loading&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=Downregulating the sucrose transporter VpSUT1 in Verbascum phoeniceum does not inhibit phloem loading&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang C%2C Han L%2C Slewinski TL%2C Sun J%2C Zhang J%2C Wang Z%2DY%2C Turgeon R %282014%29 Symplastic phloem loading in poplar%2E Plant Physiol 166%3A 306%2D313&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang C, Han L, Slewinski TL, Sun J, Zhang J, Wang Z-Y, Turgeon R (2014) Symplastic phloem loading in poplar. Plant Physiol 166: 306-313


http://scholar.google.com/scholar?as_q=Symplastic phloem loading in poplar&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=Symplastic phloem loading in poplar&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang C%2C Yu X%2C Ayre BG%2C Turgeon R %282012%29 The origin and composition of cucurbit �??phloem�?� exudate%2E Plant Physiol 158%3A 1873%2D1882&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang C, Yu X, Ayre BG, Turgeon R (2012) The origin and composition of cucurbit ?phloem? exudate. Plant Physiol 158: 1873-1882


http://scholar.google.com/scholar?as_q=The origin and composition of cucurbit â�?�?phloemâ�?� exudate&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The origin and composition of cucurbit â�?�?phloemâ�?� exudate&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang W%2C Thieme CJ%2C Kollwig G%2C Apelt F%2C Yang 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&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang W, Thieme CJ, Kollwig G, Apelt F, Yang L, Winter N, Andresen N, Walther D, Kragler F (2016) tRNA-Related Sequences Trigger Systemic mRNA Transport in Plants. Plant Cell 28: 1237-1249


Google Scholar: Author Only Title Only Author and Title

Zhang Z, Zheng Y, Ham BK, Chen J, Yoshida A, Kochian LV, Fei Z, Lucas WJ (2016) Vascular-mediated signalling involved in earlyphosphate stress response in plants. Nat Plants 2: 16033


Zhou X, Zha M, Huang J, Li L, Imran M, Zhang C (2017) StMYB44 negatively regulates phosphate transport by suppressing expressionof PHOSPHATE1 in potato. J Exp Bot 68: 1265-1281




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=Zhang Z%2C Zheng Y%2C Ham BK%2C Chen J%2C Yoshida A%2C Kochian LV%2C Fei Z%2C Lucas WJ %282016%29 Vascular%2Dmediated signalling involved in early phosphate stress response in plants%2E Nat Plants 2%3A 16033&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang Z, Zheng Y, Ham BK, Chen J, Yoshida A, Kochian LV, Fei Z, Lucas WJ (2016) Vascular-mediated signalling involved in early phosphate stress response in plants. Nat Plants 2: 16033


http://scholar.google.com/scholar?as_q=Vascular-mediated signalling involved in early phosphate stress response 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=Vascular-mediated signalling involved in early phosphate stress response 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=Zhou X%2C Zha M%2C Huang J%2C Li L%2C Imran M%2C Zhang C %282017%29 StMYB44 negatively regulates phosphate transport by suppressing expression of PHOSPHATE1 in potato%2E J Exp Bot 68%3A 1265%2D1281&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhou X, Zha M, Huang J, Li L, Imran M, Zhang C (2017) StMYB44 negatively regulates phosphate transport by suppressing expression of PHOSPHATE1 in potato. J Exp Bot 68: 1265-1281

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

http://scholar.google.com/scholar?as_q=StMYB44 negatively regulates phosphate transport by suppressing expression of PHOSPHATE1 in potato&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=StMYB44 negatively regulates phosphate transport by suppressing expression of PHOSPHATE1 in potato&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhou&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1


Mechanisms of long-distance mRNA movement 2 · 95 species/genotype was used as a scion and another...

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Transcript of Mechanisms of long-distance mRNA movement 2 · 95 species/genotype was used as a scion and another...