Regulation of Hormonal Control, Cell Reprogramming and ... · 43 Body regeneration through formation of new organs is a major question in developmental ... We identified four developmental

1

REGULATION OF HORMONAL CONTROL, CELL REPROGRAMING AND 1

PATTERNING DURING DE NOVO ROOT ORGANOGENESIS 2

Estefano Bustillo-Avendaño#, 1, Sergio Ibáñez#, 2, Oscar Sanz1, Jessica Aline Sousa Barros2, 3, 3

Inmaculada Gude1, Juan Perianez-Rodriguez1, José Luis Micol2, Juan Carlos Del Pozo1, Miguel 4

Angel Moreno-Risueno+$, 1, José Manuel Pérez-Pérez+$, 2 5

6 1Centro de Biotecnología y Genómica de Plantas (Universidad Politécnica de Madrid – Instituto 7

Nacional de Investigación y Tecnología Agraria y Alimentaria), Madrid, Spain 8 2Instituto de Bioingeniería, Universidad Miguel Hernández, 03202 Elche, Spain 9 3Current address: Departamento de Biologia Vegetal, Universidade Federal de Viçosa, 36570-10

900 Viçosa, Minas Gerais, Brazil 11

12

#: Co-first author 13

+: Co-senior author 14 $: Corresponding authors: M.A. Moreno-Risueno (e-mail: [email protected]) and 15

J.M. Pérez-Pérez (e-mail: [email protected]) 16

17

Short title: De novo root regeneration in Arabidopsis leaves 18

One-sentence summary: Distinctive developmental stages lead to de novo root organogenesis 19

in leaves guide genetically dissection of the primary developmental pathways 20

Keywords: regeneration; cell reprogramming; hormonal signaling; de novo organ formation; 21

adventitious rooting; root patterning 22

23

Word count breakdown: Abstract, 195; Introduction, 908; Results, 3749; Discussion, 2210; 24

Materials and methods, 1420; Acknowledgements, 34; References, 2844; Figure legends, 1042 25

Figures: 8 Supplemental figures: 826

Plant Physiology Preview. Published on December 12, 2017, as DOI:10.1104/pp.17.00980

Copyright 2017 by the American Society of Plant Biologists

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2

FOOTNOTES 27

List of author contributions: Conceptualization and Supervision: J.M.P.-P. and M.A.M.-R.; 28

Methodology, J.M.P.-P., M.A.M.-R., E.B.-A., and S.I.; Investigation, E.B.-A., S.I., O.S., J.A.S.B., 29

I.G., and J.P.; Formal Analysis: E.B.-A. and S.I.; Writing – Original Draft, J.M.P.-P., M.A.M.-R., 30

E.B.-A. and S.I.; Writing – Review & Editing, . J.M.P.-P., M.A.M.-R., J.L.M., and J.C.P.; Funding 31

Acquisition, J.M.P.-P. and M.A.M.-R.; Resources, . J.M.P.-P., M.A.M.-R., J.L.M., and J.C.P. 32

33

Funding information: This work was supported by grants from Ministerio de Economía y 34

Competitividad (MINECO) of Spain, ERDF and FP7 Funds of the European Commission, 35

BFU2013-41160-P, BFU2016-80315-P and PCIG11-GA-2012-322082 to M.A.M.-R., AGL2012-36

33610 and BIO2015-64255-R to J.M.P.-P. and BIO2014-52091-R to J.C.P. M.A.M.-R. was 37

supported by a Ramon y Cajal contract from MICINN. 38

39

Corresponding authors e-mail: M.A. Moreno-Risueno (e-mail: [email protected]) 40

and J.M. Pérez-Pérez (e-mail: [email protected]) 41



3

ABSTRACT 42

Body regeneration through formation of new organs is a major question in developmental 43

biology. We investigated de novo root formation using whole leaves of Arabidopsis thaliana. Our 44

results show that local cytokinin biosynthesis and auxin biosynthesis in the leaf blade followed 45

by auxin long-distance transport to the petiole leads to proliferation of J0121-marked xylem-46

associated tissues and others through signaling of INDOLE-3-ACETIC ACID INDUCIBLE28 47

(IAA28), CRANE (IAA18), WOODEN LEG, and ARABIDOPSIS RESPONSE REGULATORS1 48

(ARR1), ARR10 and ARR12. Vasculature proliferation also involves the cell cycle regulator KIP-49

RELATED PROTEIN2 and ABERRANT LATERAL ROOT FORMATION4 resulting in a mass of 50

cells with rooting competence that resembles callus formation. Endogenous callus formation 51

precedes specification of postembryonic root founder cells, from which roots are initiated 52

through the activity of SHORT-ROOT (SHR), PLETHORA1 (PLT1) and PLT2. Primordia 53

initiation is blocked in shr plt1 plt2 mutant. Stem cell regulators SCHIZORIZA, JACKDAW, 54

BLUEJAY and SCARECROW also participate in root initiation and are required to pattern the 55

new organ, as mutants show disorganized and reduced number of layers and tissue initials 56

resulting in reduced rooting. Our work provides an organ regeneration model through de novo 57

root formation, stating key stages and the primary pathways involved. 58



4

INTRODUCTION 59

Plants have striking regeneration capacities, and can produce new organs from postembryonic 60

tissues (Hartmann et al., 2010; Chen et al., 2014; Liu et al., 2014) as well as reconstitute 61

damaged organs upon wounding (Xu et al., 2006; Heyman et al., 2013; Perianez-Rodriguez et 62

al., 2014; Melnyk et al., 2015; Efroni et al., 2016). Intriguingly, root regeneration upon stem cell 63

damage recruits embryonic pathways (Hayashi et al., 2006; Efroni et al., 2016), while in 64

contrast, postembryonic formation of whole new organs, such as lateral roots, appears to use 65

specific postembryonic pathways (Lavenus et al., 2013). 66

Crosstalk between auxin and cytokinin signaling is required for many aspects of plant 67

development and regeneration (El-Showk et al., 2013) although how their synergistic interaction 68

is implemented at the molecular level has not been clarified (Skoog and Miller, 1957; Chandler 69

and Werr, 2015). Exogenous in vitro supplementation of these two hormones results in 70

continuous cell proliferation, to form a characteristic structure termed callus. Callus emerges as 71

a common regenerative mechanism for almost all plant organs through in vitro culture (Atta et 72

al., 2009; Sugimoto et al., 2010). There is increasing evidence that callus formation requires 73

hormone-mediated activation of a lateral and meristematic root development program in 74

pericycle-like cells defined by expression of the J0121 marker (Sugimoto et al., 2010). 75

Accordingly, many regulators of lateral root development, such as AUXIN RESPONSE 76

FACTOR7 (ARF7), ARF19, LATERAL ORGAN BOUNDARIES DOMAIN16 (LBD16), LBD17, 77

LBD18 and LBD29, are required for hormone-induced callus formation (reviewed in Ikeuchi et 78

al., 2013). 79

Many species can regenerate new organs from explants (e.g. roots from leaves) without 80

exogenous supplementation of hormones (Bellini et al., 2014). Making roots de novo requires 81

generating the different tissues and cell types of the new organ. All roots have the same tissues, 82

although the number of layers and cells types of these may vary (Kuroha et al., 2006; Lucas et 83

al., 2011). Tissues are continuously formed by asymmetric division of initial cells, which are 84

stem cells, followed by proliferative divisions of their daughter meristematic cells. Stem cell 85

activity is maintained by quiescent center (QC) (van den Berg et al., 1997; Drisch and Stahl, 86

2015) and auxin activity (Della Rovere et al., 2013). Auxin accumulation in the QC area triggers 87



5

a dose-dependent and slow response that activates PLETHORA (PLT) factors. PLT proteins 88

form a gradient in the root meristem which is required to position the QC, maintain stem cell 89

activity and trigger proliferation of meristematic cells (Aida et al., 2004; Mahonen et al., 2014). 90

Position and activity of the QC also requires radial information delivered by the mobile factor 91

SHORT-ROOT and its downstream target SCARECROW (Sabatini et al., 2003; Levesque et al., 92

2006; Moubayidin et al., 2016). In addition, WUSCHEL-RELATED HOMEOBOX5 (WOX5) is 93

confined by auxin signaling into the QC and represses differentiation of the stem cell niche, 94

primarily from the QC (Sarkar et al., 2007; Forzani et al., 2014; Pi et al., 2015; Zhang et al., 95

2015). Tissue formation in the primary root meristem also requires lineage specific factors that 96

function as cell fate determinants and as tissue endogenous signaling factors to incorporate 97

positional information into patterning (Moreno-Risueno et al., 2015). However, little is known 98

about how tissues are formed de novo. 99

Recently, a hormone-free method to study de novo root organogenesis in excised leaf 100

blades has been described (Chen et al., 2014). YUCCA-mediated auxin biosynthesis was 101

shown to be ubiquitously enhanced in the leaf mesophyll and indirectly contribute to auxin 102

accumulation near the excision site to trigger localized auxin signalling in the vasculature (Liu et 103

al., 2014; Chen et al., 2016). Formation of new roots involves formation of competent cells 104

through auxin-induced expression of WOX11 transcription factor, which has been defined as a 105

first-step for cell fate transition during de novo organ regeneration (Liu et al., 2014). WOX11 and 106

its homolog WOX12 can in addition promote callus formation and upregulate the callus 107

formation factors LBD16 and LDB29 (Fan et al., 2012; Liu et al., 2014), suggesting that de novo 108

root formation might share similar regulatory mechanisms with callus formation. Subsequently in 109

leaf blade rooting, WOX11 and WOX12 activate WOX5 and WOX7 factors, which are 110

expressed in dividing cells forming root primordia, while WOX11/12 expression quickly 111

decreases in dividing cells (Liu et al., 2014; Hu and Xu, 2016). Activation and maintenance of 112

WOX5/7 expression also requires auxin signalling in an unknown pathway different from 113

WOX11/12. Mutants in these WOX factors reduce the number of roots regenerated per leaf 114

blades and affect rooting rate of leaf blades. As a considerably high percentage of leaf blades 115

still root in these mutants, additional regulation must exist. 116



6

We have performed an extensive study to further understanding root regeneration from 117

aerial organs. Whole leaves of many species can regenerate entire functional plants in 118

hormone-free medium, and thus we used whole leaves with petioles of Arabidopsis thaliana 119

instead of excised leaf blades. We identified four developmental stages: 1) proliferation of some 120

xylem-associated tissues to form an endogenous callus; 2) specification of root founder cells 121

within the callus; 3) root primordia initiation from founder cells and patterning and 4) root 122

meristem activation and emergence. We have also characterized a number of factors regulating 123

these developmental stages. Some auxin and cytokinin signaling factors appear as critical for 124

endogenous callus initiation and formation while some stem cell regulators control initiation and 125

patterning of newly formed organs. These results define key stages and regulators required for 126

leaf rooting establishing a developmental framework for de novo organ formation in plants. 127

128



7

129



8

RESULTS 130

Vasculature-associated cell proliferation is required for de novo organ regeneration in 131

Arabidopsis 132

We found that excised whole leaves of Arabidopsis can root without hormone supplementation, 133

similarly to leaf blades as previously described (Chen et al., 2014) and at similar percentages 134

(Fig. S1A-B). Because some species can regenerate entire functional plants from whole leaves 135

without the aid of external hormones, we performed our studies using whole leaves. As de novo 136

formed roots emerged from the petiole base of whole leaves (Fig. 1A), petioles were 137

microscopically observed (Fig. 1B). All petioles showed the same morphological changes during 138

de novo organ regeneration. Although asynchrony was observed in the regeneration process, 139

by day 10 after excision (dae) most leaves (85-100%) had regenerated at least one root. At 2 140

dae cells adjacent to xylem started to proliferate, forming stratified layers from 3 dae onwards 141

(Fig. 1C-E) that pushed away xylem conducts and displaced the collenchyma. Vasculature 142

proliferation and subsequent formation of primordia caused the proximal petiole to thicken (Fig. 143

S1C). First primordia were visible at 4 dae, and located at external layers of proliferating 144

vasculature (Fig. 1F). At 5 dae root primordia showed a layered pattern (Fig. 1G). Eventually, 145

newly formed roots with well-organized meristems emerged through petiole tissues from 7 dae 146

onwards (Fig. 1H). 147

Pericycle-like cells (those expressing the J0121 reporter) have been associated to 148

regenerative and morphogenic processes as the source of reprogrammable cells (Sugimoto et 149

al., 2010; Chen et al., 2014). Sections of petioles at the time of excision revealed that the root-150

pericycle line J0661-GFP marks cells around xylem and procambium cells (Figure 1I-J), while 151

the J0121-GFP line (Fig. 1L-M) was restricted to a layer around xylem vessels, being excluded 152

from procambium. Number of cells marked with J0661 and J0121increased quickly during first 153

days of regeneration (Fig. 1K, N-P). We observed that all proliferating cells were marked with 154

J0661-GFP while some proliferating cells in the J0121 line did not have the GFP (Fig.1 K, O-P) 155

indicating that cell proliferation associated to the J0661 reporter. Although it cannot be ruled out 156

that J0661-GFP is activated in proliferating cells, it is possible that xylem and procambium 157

proliferate as part of the reprogramming process. In addition, we observed that primordia at 158



9

early stages of development were marked with J0121-GFP (Fig. 1P), establishing an 159



10

association between de novo primordia formation and J0121 identity, similarly to other 160

developmental or regenerative processes such as callus or lateral root formation (Dubrovsky el 161

al., 2006; Sugimoto et al., 2010). 162

We next studied mutants defective in cell cycle progression, at the G1/S transition, such 163

as the KIP-RELATED PROTEIN2 (KRP2) overexpressor, and at the G2/M transition, such as 164

cyclinB1;1 (cycb1;1) and cycb1;2 mutants and a dominant negative form of the CDKB1;1 kinase 165

(CDKB1;1 DN161). Percentage of petioles showing vasculature-associated proliferation was 166

reduced in Pro35S:KRP2 and CDKB1;1 DN161 lines (Fig. 1Q), while only size of proliferating 167

mass of cells was reduced in rest of lines. In addition, Pro35S:KRP2 blocked de novo organ 168

regeneration, while cycb1;1 and CDKB1;1 DN161 showed a significant reduction in the number 169

of petioles regenerating roots (Fig. 1R). We also chemically inactivated the G1/S transition by 170

incubating leaves with either 2.5 or 5 mM hydroxyurea (HU). We observed a significant 171

decrease in rate of petioles showing vascular-associated proliferation and subsequent new root 172

formation by the HU treatment (Fig. 1Q-R and Fig. S2A-B). HU treatment did not associate with 173

increased cell death around the vasculature near the leaf excision site upon trypan blue staining 174

(Fig. S2C). All together, these results indicate that cell division activation of vasculature cells is 175

the first and required stage for de novo organogenesis during rooting of leaves. 176

177

Cytokinin biosynthesis and response during de novo root regeneration 178

As we had found an association between de novo root regeneration and J0661 and J0121 179

identities, and callus originates from J0121-marked cells after hormonal induction (Sugimoto et 180

al., 2010), we hypothesized that vasculature proliferation required for leaf rooting could be a 181

type of callus. Cytokinin and auxin signalling are required for callus formation and regeneration, 182

and thus we tested if these two hormones were involved in the developmental pathway leading 183

to de novo organ regeneration from leaves. 184

First, we investigated cytokinin biosynthesis and signalling (Zürcher and Müller, 2016). 185

We found enriched expression of ProIPT3:GUS in petioles right after excision (Fig. 2A). 186

ProIPT5:GUS was highly expressed in vascular-associated cells in the petiole base at 2 dae (Fig. 187

2B), while ProLOG4:GUS, which was originally expressed in leaf vasculature at 0 dae, increased 188



11

expression at the petiole base over time (Fig. 2C, arrowhead). Cytokinin signalling, as reported 189

by ProARR5:GUS (D'Agostino et al., 2000), was restricted to a subset of vascular-associated cells 190

near the petiole base at 2 dae, which associated with proliferation of vasculature, to decrease at 191

later time points (Fig. 2D) and it did not show expression during de novo primordia formation. 192

Consistent with ARR5 reporting primary cytokinin response during petiole vasculature 193

proliferation (D'Agostino et al., 2000), incubation of leaf explants with synthetic cytokinin 6-194

benzylaminopurine (6-BAP) increased ProARR5:GUS expression in the petiole vasculature and 195

basal region (Fig. 2E). 196



12

Next, we studied the ability of several cytokinin signalling mutant combinations in 197

ARABIDOPSIS HISTIDINE KINASE4 (AHK4), ARABIDOPSIS HISTIDINE 198

PHOSPHOTRANSFER PROTEIN1 (AHP1) to AHP5 and ARR1, ARR10 and ARR12 genes in 199

regulating both vasculature proliferation and de novo root regeneration. We quantified petioles 200

regenerating as petioles showing vasculature proliferation/thickening, root primordia formation 201

or visible roots. Leaf petioles of wooden leg (wol, a dominant negative mutant in AHK4 202

receptor), and ahp1 ahp2 ahp3 and arr1 arr10 arr12 loss-of-function mutants displayed lower 203

regeneration percentage at 7 dae (Fig. 2F). Interestingly, wol, ahp1 ahp2 ahp3 and arr1 arr10 204

arr12 mutants were also defective in hormone-induced callus formation from different tissue 205

explants, such as leaves, cotyledons and roots (Fig. S3), indicating that specific cytokinin 206

signalling is required for both callus formation and vasculature proliferation in leaf petioles. 207

Despite cytokinin signalling was required for vasculature proliferation in petioles during rooting, 208

for those leaf petioles of cytokinin signalling mutants which regenerated, we detected higher 209

number of roots (which we categorized by frequencies in numbers of roots and designated as 210

rooting capacity) (Fig. 2F). Higher auxin-to-cytokinin ratios have been shown to induce 211

specification and growth of new root primordia (Müller and Sheen, 2008). Thus, we wondered if 212

we could alter new primordia initiation by altering hormone ratios. Cytokinin treatment increased 213

vascular proliferation on a concentration- and time-dependent manner (Fig. S2D-E). We 214

observed that regeneration deficiencies of most cytokinin signalling mutants could be 215

compensated by low levels of exogenous auxin (Fig. 2G) that also increased vasculature 216

proliferation at expenses of reducing rooting capacity in the ahp1 ahp2 ahp3 mutant (Fig. 2G). 217

All together, these results indicate a dual role for cytokinin first as a positive activator of 218

vasculature cell division, and second as a negative regulator of root primordia initiation. 219

220

Specific auxin signalling factors regulate de novo root regeneration 221

Next we investigated auxin signalling during rooting of leaves using the DR5 reporter line 222

(Ulmasov et al., 1997). ProDR5:GUS was expressed in vascular-associated cells at the proximal 223

region of the petiole, as early as 12 hours after excision (hae), to increase quickly to 1 dae, 224

remaining high during proliferative stages and decreasing over time coincident with deceleration 225



13

of vasculature growth (Fig. 3A-B). We observed high localized expression of ProDR5:GUS in 226

clusters of cells at the time of primordia initiation and formation. Consistent with a regulatory role 227

of auxin in rooting, local IAA application significantly increased root formation, along with 228

expansion of ProDR5:GUS expression domain (Fig. 3A, C). In addition, the auxin-overproducing 229

mutant superroot2 (sur2) (Barlier et al., 2000) also showed increased number of de novo 230

formed roots at 7 dae, similarly to auxin treated petioles (Fig. 3C). 231

Auxin signalling is regulated by INDOLE-3-ACETIC ACID INDUCIBLE (IAA) co-factors 232

acting in combination with AUXIN RESPONSE FACTOR (ARF) transcriptional partners (Li et 233



14

al., 2016). We reasoned that IAA factors regulating postembryonic (lateral) root formation (Goh 234

et al., 2012) could be involved in de novo organ formation. We assessed the mutants auxin 235

resistant2-1 (axr2-1), solitary-root-1 (slr-1), crane-2, iaa28-1, and the double mutant non-236

phototrophic hypocotyl4-1 (nhp4-1) arf19-1 (see Materials and Methods); which are, 237

respectively, gain-of-function mutants for the factors IAA7, IAA14, IAA18, IAA28 and a double 238

loss-of-function mutant for ARF7 and ARF19. crane-2 reduced de novo root regeneration, with 239

approximately 40% of petioles not showing any sign of vasculature proliferation or de novo root 240

formation (Fig. 3D). In addition, slr-1 and iaa28-1 showed reduced rooting capacity although all 241

petioles showed some vasculature proliferation (Fig. 3E). When we quantified vasculature 242

proliferation area of petioles regenerating we observed a reduction for iaa28-1 and crane-2 but 243

not for slr-1 (Fig. 3F). These results indicate that the auxin signalling module mediated by 244

IAA18 is required for de novo root regeneration at stages of vascular proliferation, that of IAA28 245

for vascular proliferation and root initiation, while IAA14 appears to be only required for de novo 246

root initiation. 247

We also investigated if these mutants were affected in hormone-induced callus formation. 248

We found that only crane-2 showed reduction in all explants assayed after hormonal incubation, 249

while axr2-1 intriguingly showed an increase for callus formed from root explants (Fig. S4A-C). 250

These results indicate that vasculature proliferation during rooting and hormone-induced callus 251

use the auxin signaling pathway mediated by IAA18. Our previous results also showed that 252

cytokinin signaling required for vasculature proliferation during de novo organogenesis was also 253

required for hormone-induced callus formation suggesting that vasculature proliferation is a type 254

of callus. We investigated ABERRANT LATERAL ROOT FORMATION4 (ALF4) during leaf 255

rooting, as alf4-1 mutants have been previously linked to callus formation (Sugimoto et al., 256

2010) and vascular connection during graft establishment (Melnyk et al., 2015). We observed 257

that during de novo root formation vasculature proliferation is reduced by 2.5 fold in alf4-1 258

mutants which is accompanied by 15 fold decrease in de novo formed root and primordia (Fig. 259

S5). Based on these results, we designated vasculature proliferation developmental stage as 260

endogenous callus formation. 261

262



15

Auxin signalling factors are required for de novo organ regeneration in leaf blades 263

In contrast to endogenous callus formation observed in petioles of whole leaves during rooting, 264

limited vasculature proliferation was observed during rooting of leaf blades (Liu et al., 2014). We 265

wondered to what extent auxin and cytokinin signaling factors regulating proliferation at the 266

petiole base would be involved in rooting of leaf blades. When we assessed rooting capacity in 267

leaf blades of these mutants, we observed that crane-2 and iaa28-1 displayed a reduction in 268

rooting capacity while slr-1 presented moderate although non-significant reductions (Fig. S6A). 269

wol and arr1 arr10 arr12 mutants were similarly affected as slr-1, while no change was detected 270

for ahp1 ahp2 ahp3 and ahp2 ahp4 ahp5 mutants (Fig. S6B). As IAA18 and IAA28 are required 271

for endogenous callus formation during whole leaf rooting and are shared with leaf blade 272

rooting, it is possible that de novo root regeneration in leaf blades could also involve an 273

endogenous callus developmental program. 274

275

Local auxin accumulation at the petiole base is dependent on polar auxin transport 276

As localized auxin signalling was required for whole leaf rooting we wondered about the source 277

of auxin. YUCCA-mediated auxin biosynthesis was shown to be ubiquitously enhanced in the 278

mesophyll of leaf blades shortly after wounding (Chen et al., 2016). During rooting of whole 279

leaves, we detected ProYUC9:GUS enriched expression in leaf mesophyll cells at 12 hae, which 280

progressively decreased at later time points (Fig. S7A). ProYUC8:GUS expression was induced in 281

proliferating vascular-associated cells at the petioles base 2 dae (Fig. S7B). These results 282

indicate two possible sources of auxin during first stages of regeneration, one from the leaf 283

blade, and the other from the proliferating vasculature itself. To determine if there was 284

differential contribution of these two auxin sources, we removed the leaf blade and found a 285

significant decrease in regeneration and rooting capacity, which in most cases stopped at the 286

endogenous callus stage (Fig. 4A). Local auxin response (ProDR5:GUS expression) in petioles 287

without leaf blade was low or undetectable (Fig. 4B). We also locally inhibited polar auxin 288

transport through application of N-1-naphthylphthalamic acid (NPA) at the blade-petiole 289

junction, resulting in almost complete block of auxin response and subsequent regenerative 290

response (Fig. 4C-D). 291



16

We next characterized PIN-FORMED (PIN) expression. ProPIN4:GUS was ubiquitously 292

expressed in the leaf vasculature at the time of excision; however at 1 dae it was only 293

expressed at the base of the petiole and in endogenous callus at 3 dae (Fig. 4E). 294

ProPIN3:PIN3:GFP expression in the petiole at the time of excision was polarized towards the 295



17

base in epidermal cell membranes and both laterally- and basally-localized in some vascular-296

associated cell membranes (Fig. 4F, arrowheads). From 12 hae to 1 dae, we found enriched 297

expression of ProPIN3:PIN3:GFP in a subset of vascular-associated cells at the petiole base 298

region (Fig. 4G). Interestingly, PIN3-GFP protein in cells proximal to the excision was oriented 299

towards the apex (upper left direction in Fig. 4G, arrowheads) while its orientation changed to 300

the base in cells at the distal position from the excision. 301

We also investigated rooting in mutants of genes affected in auxin influx (AUX1) or auxin 302

efflux (PIN1, PIN2, PIN3 and PIN7), which have been described to have low auxin transport 303

rates (Petrasek et al., 2006). Consistent with our previous observations the regenerative 304

potential of leaves of pin1, pin2 pin3, pin2 pin3 pin7 and aux1 mutants was reduced (Fig. 4H). 305

GNOM loss-of-function mutants have altered polar auxin transport by interfering with PIN 306

internalization (Kleine-Vehn et al., 2009). When we studied the GNOM mutant fewer (fwr) 307

(Okumura et al., 2013), we observed significant differences in regeneration and rooting capacity 308

(Fig. 4H). fwr is a weak gnom allele but it is possible that several auxin transporters are 309

simultaneously affected, which could explain why there is also a reduction in rooting capacity 310

while no reduction was observed for single auxin transporter mutants. 311

312

Postembryonic root founder cells establish on endogenous callus prior primordia 313

formation 314

WOUND INDUCED DEDIFFERENTIATION1 (WIND1) is rapidly induced at the wound site to 315

promote callus formation through the ARR-dependent signaling pathway (Iwase et al. 2011). 316

From 1 to 4 dae, we found ProWIND1:GUS expression in vascular cells at the petiole near the 317

excision site, while expression was downregulated in new root primordia and no expression was 318

detected at the time of root emergence by 6 dae (Fig. 5A). Postembryonic development involves 319

specification of organ founder cells (Chandler, 2011). Thus, we hypothesized that root founder 320

cells (RFCs) could be specified within the endogenous callus to de novo form a root. It has been 321

proposed that RFCs during de novo root formation in leaf blades could be marked by 322

ProWOX11:GUS expression (Liu et al., 2014; Hu and Xu, 2016). We observed discrete 323

ProWOX11:GUS signals early detected, at 1 dae, in a few xylem-associated cells at the petiole 324



18

base (Fig. 5B). From 1 dae onwards, during callus formation, high ProWOX11:GUS expression 325

was observed in many cells within this domain, but not simultaneously in all proliferating cells. 326

Later on, ProWOX11:GUS expression was observed near the central zone of the endogenous 327

callus but excluded from the dome-shape root primordia. WOX11 expression thus appears to 328



19

associate with endogenous callus formation while not all marked cells resulted in primordia 329

initiation. We wondered whether cell division of vascular-associated cells was downstream of 330

the WOX11 signal. ProWOX11:GUS expression was increased in vasculature of petioles of 331

excised leaves incubated with the G1/S cell cycle inhibitor hydroxyurea, even when little 332

vasculature proliferation was observed (Fig. 5E-F). 333

ProSKPB2s:GUS expression has been shown to mark RFCs and their progeny during early 334

stages of lateral root formation (Manzano et al., 2012). We detected ProSKPB2s:GUS expression 335

at 3 dae restricted to few cells within the endogenous callus (Fig. 5C). From 4 to 5 dae, we 336

observed marker expression in developing root primordia while its expression disappeared from 337

functional primordia during the emerging process, remaining in some cells of the endogenous 338

callus (Fig. 5C). Interestingly, RFCs did not appear to be specified simultaneously, supporting 339

our initial observations about asynchrony in the regeneration process. In order to follow 340

primordia formation we used ProWOX5:GUS. WOX5 is expressed early during lateral root 341

primordia formation (Tian et al., 2014; Goh et al., 2016), and also following root primordia 342

initiation during de novo organogenesis (Liu et al., 2014; Hu and Xu, 2016). Expression of 343

ProWOX5:GUS was first detected at 4 dae in clusters of cells within the endogenous callus (Fig. 344

5D), similarly to ProSKPB2s:GUS after root primordia initiation. At 6 dae ProWOX5:GUS expression 345

was enriched at root meristem tip, coinciding with meristem activation and growth prior 346

emergence. Interestingly, we did not detect ProWOX5:GUS in the endogenous callus (Fig. 5D), 347

although WOX5 expression has been associated to hormone-induced callus (Sugimoto et al., 348

2010), suggesting specific regulation. 349

Cell division is required for primordia initiation and formation, and petioles of leaves 350

treated with the cell cycle inhibitor HU which started to form an endogenous callus remained 351

almost blocked at this stage (Fig. 5G). We wondered if general regulators of cell cycle 352

progression would be involved in de novo primordia formation. Our results indicate that rooting 353

capacity is compromised in cycb1;1, cycb1;2 and CDKB1;1 DN161 mutants. Accordingly, 354

overexpression of the cell cycle inhibitor KRP2 blocked progression to root initiation and 355

formation, along with reduction in callus formation by 60% previously shown in Fig. 1Q. Taken 356

together, our results indicate that WIND1 and WOX11 expression associates with vasculature 357



20

proliferation leading to endogenous callus formation at the petiole base, while ProSKPB2s:GUS is 358

restricted to a few RFCs within the callus that quickly acquire WOX5 expression associated to 359

cell division, in turn mediated by CYCB1;1, CYCB1;2, CDKB1;1 and KRP2, to initiate de novo 360

root primordia regeneration (Fig. 5G). 361

362

SHORT-ROOT, PLETHORA1 and PLETHORA2 are required for de novo initiation of roots 363

We investigated whether factors specifying stem cell fate or their activity, such as PLETHORA 364

(PLT), JACKDAW (JKD), BLUEJAY (BLJ), SCARECROW (SCR), SHORT-ROOT (SHR), 365

SCHIZORIZA (SCZ) and WOX5 were required during de novo root regeneration. In addition to 366

single loss-of-function mutants, double plt1-4 plt2-2 and triple blj-1 jkd-4 scr-4, we generated 367

and tested the double mutant jkd-4 scz-1. We found significant differences in percentage of 368

leaves rooting and in rooting capacity for shr-2 and plt1-4 plt2-2 (Fig. 6A-B). In addition, scr-4, 369

blj-1 jkd-4 scr-4, scz-1 and jkd-4 scz-1 were impaired in rooting capacity. These phenotypes 370

suggested impairment in de novo root initiation or primordia formation. As in shr-2 and plt1-4 371

plt2-2 many leaves failed to regenerate any root, we generated shr-2 plt1-4 plt2-2. Notably, 372

leaves of shr-2 plt1-4 plt2-2 were not capable of rooting (Fig. 6A-C). 373

Petioles of shr-2 plt1-4 plt2-2 were observed through confocal microscopy at 6, 10 and 20 374

dae. We did not observed any primordia at 6 dae in shr-2 plt1-4 plt2-2, while most control 375

leaves had one or more primordia (Fig. 6D). Inspection at later days indicated that most leaves 376

(97%, n=90) of shr-2 plt1-4 plt2-2 did not form any primordia up to 20 dae. The few primordia 377

found (3%, n=90) remained blocked or developed aberrant shapes with presence of mature 378

xylem indicating premature differentiation. These primordia did not emerge through petiole 379

tissues. We observed endogenous callus formation, which maintained growth over time up to 20 380

dae in all observed petioles of shr-2 plt1-4 plt2-2. These results indicate that the combined 381

activity of SHR and PLT1 and PLT2 is required to de novo initiate root primordia. In addition, 382

these factors maintain proliferative activity in the forming primordia, as when these factors are 383

removed primordia differentiate. 384

385



21

JACKDAW, BLUEJAY, SCARECROW AND SCHIZORIZA are required for de novo 386

formation of root primordia 387



22

We observed formation of root primordia in petioles of jkd-4 scz-1 and blj-1 jkd-4 scr-4 through 388

confocal microscopy. We observed abnormal formative divisions in jkd-4 scz-1 primordia at 5 389

dae, which did not organize properly in layers or rows as compare to control roots (Fig. 6E). At 6 390

dae we observed reduced and disorganized number of cell rows in jkd-4 scz-1 and blj-1 jkd-4 391

scr-4 primordia. While endodermis, cortex and middle cortex could be identified in control roots 392

at this developmental stage based on position, corresponding rows in jkd-4 scz-1 and blj-1 jkd-4 393

scr-4 could not be identified (Fig. 6E). These results suggest that cell lineages or positional 394

identity could not be correctly established in these mutants during de novo root formation. 395

396

JACKDAW, BLUEJAY, SCARECROW, SHORT-ROOT AND SCHIZORIZA regulate 397

patterning of de novo formed roots and of lateral roots 398

Primordia formation occurred incorrectly in blj-1 jkd-4 scr-4 and jkd-4 scz-1, and therefore 399

patterning of these de novo formed roots could be compromised after emergence. Longitudinal- 400

and cross sections of de novo root meristems were examined through confocal microscopy after 401

emergence at 10 dae (encompassing roots at 1-3 days post emergence, dpe). de novo wild-402

type roots showed ground tissue with middle cortex formation, a layer located between 403

endodermis and cortex and associated to postembryonic development (Paquette and Benfey, 404

2005), while de novo roots of shr-2, scr-4, blj-1 jkd-4 scr-4 and jkd-4 scz-1 had a single layer of 405

ground tissue which we denoted as mutant (m) layer (Fig. 7A and Fig S8A-B). In addition, 406

number of cell rows making the ground tissue, which indicates number of tissue initials was 407

reduced in de novo emerged roots of blj-1 jkd-4 scr-4 and jkd-4 scz-1 as compared to wild-type 408

roots (Fig 7E and Fig. S8C). As a result, the stele region in these mutants was not delimited by 409

a closed ring of ground tissue as in wild-type roots as shown in cross sections (Fig 7B). In 410

addition, shr-2, scr-4, blj-1 jkd-4 scr-4 and jkd4 scz-1 mutants also had a smaller stele region 411

(Fig. 7B-C and Fig. S8D-E). 412

Lateral roots are organs formed postembryonically the same as de novo formed roots. 413

We decided to investigate if stem cell regulators regulating de novo root formation could also 414

regulate lateral root formation. We quantified lateral root capacity. In this assay the root tip is cut 415

to induce growth of lateral roots as described previously (Van Norman et al., 2014). We 416



23

confirmed there were not unemerged primordia under the microscope. We observed reduced 417

lateral root capacity in shr-2 plt1-4 plt2-2, blj-1 jkd-4 scr-4 and jkd-4 scz-1 mutant combinations 418

indicating defects in founder cell specification or lateral root initiation (Fig. 7D), similarly to 419

defects observed in these mutants during de novo root formation. We also observed patterning 420



24

defects in emerged lateral roots of these mutants, which showed a single mutant layer of 421

ground tissue and reduced number of cell rows as compared to wild type lateral roots (Fig. 7E). 422

In addition, we observed signs of premature differentiation in shr-2 plt1-4 plt2-2, with presence 423

of mature xylem in the meristem similarly to de novo formed roots. 424

425



25

426



26

DISCUSSION 427

Plants have the remarkable ability to regenerate a new entire individual, specific organs or their 428

tissues from explants or even few cells (Birnbaum and Sánchez Alvarado, 2008; Della Rovere 429

et al., 2016). Plant regeneration through de novo organogenesis can be achieved through 430

hormonal induction, directly or indirectly (Ikeuchi et al., 2013), but also in hormone free medium. 431

The molecular pathways involved (Ikeuchi et al., 2016; Kareem et al., 2016) and the relationship 432

between hormonal-induced and endogenous programmes are not well understood. Moreover 433

callus formation, which is a prerequisite for hormonal-induced regeneration, does not appear to 434

occur during endogenous organogenesis, although both processes share regulation (Sugimoto 435

et al., 2010; Liu et al., 2014; Perianez-Rodriguez et al., 2014; Ramirez-Parra et al., 2017). Using 436

a simple method to study de novo root organogenesis without hormone supplementation (Chen 437

et al., 2014; Liu et al., 2014) but applied to whole leaves (Fig. 8A) we found that formation of an 438

endogenous callus is a required step for de novo root organogenesis, and thus we established 439

a direct connection between both regenerative processes. Our research has also identified the 440

distinctive and required developmental stages leading to novo root organogenesis (Fig. 8B): 1) 441

vasculature proliferation and endogenous callus formation, 2) specification of root founder cells, 442

3) root primordia initiation and patterning, and 4) root meristem activation and emergence. 443

Furthermore, we have genetically dissected the primary developmental pathways involved in its 444

regulation and identified some of the key regulators involved (Fig. 8C). 445

446

Vasculature proliferation and endogenous callus formation 447

Vasculature division is the first morphological change we detect and by chemically or genetically 448

inhibiting vasculature proliferation we affected de novo root organogenesis. We also observed 449

that root primordia originated from vasculature. Pericycle-like cells, particularly those expressing 450

the J0121 marker, have been associated to regenerative and morphogenic processes as the 451

source of reprogrammable cells (Sugimoto et al., 2010; Chen et al., 2014). When we assessed 452

the J0661 and J0121 pericycle markers we observed that vasculature proliferation associated to 453

J0661 identity while some proliferating cells were devoid of J0121 expression. Intriguingly, 454

J0661 marks cells around xylem and procambium in petioles while J0121 only marks cells in 455



27

contact to xylem. Proliferation competence, therefore, appears to involve different cell types. 456

Closer examination showed that all primordia expressed J0121 marker which indicates that 457

regeneration competence associates with J0121 identity and shows parallelisms with callus and 458

lateral root formation. Cell lineage tracing using clonal markers and live imaging could dissect 459

the exact source of reprogrammable cells during de novo root regeneration from whole leaves. 460

We also found that proliferating vascular cells express WOUND INDUCED 461

DEDIFFERENTIATION1 (WIND1), a positive regulator of wound-induced callus formation 462



28

(Iwase et al., 2011), suggesting together with J0121 analysis that these proliferating tissues 463

could be a type of callus. Callus formation requires confluence of auxin and cytokinin responses 464

in the same set of cells (Gordon et al., 2007). In agreement with this idea, our results show 465

specific expression of auxin and cytokinin signalling reporters ProDR5:GUS and ProARR5:GUS, 466

respectively, in the vasculature. These results also indicate that specific regulation was required 467

to induce auxin and cytokinin signalling at the petiole base. In contrast to early notions that 468

cytokinins are produced only in roots, it is now recognised that they are synthesized throughout 469

the plant (Zürcher and Müller, 2016). Our results are consistent with 470

ISOPENTENYLTRANSFERASE3 (IPT3), IPT5 and LONELY GUY4 locally mediating cytokinin 471

biosynthesis at the petiole base to contribute to vascular proliferation during root regeneration. 472

Thus, cytokinin signalling mutants displayed reduced regeneration potential as well as defective 473

hormone-induced callus formation. Interestingly, the triple cytokinin signaling mutant ahp2 ahp4 474

ahp5 is affected in hormone-induced callus formation but not in vasculature proliferation during 475

rooting, indicating the existence of specific genetic differences between hormone-induced callus 476

formation and de novo root formation. 477

ProDR5:GUS expression in the proximal petiole vasculature could be indicative of auxin 478

accumulation. A study in leaf blades has shown that YUCCA1 (YUC1) and YUC4 appear to 479

mediate synthesis of auxin in mesophyll cells (Chen et al., 2016). If this occurred in our system, 480

auxin would need in addition to be transported to cells near the wound to induce de novo root 481

organogenesis. We observed that YUC9 expression was induced in the leaf blade mesophyll 482

but not in the petiole (Fig. 8A), suggesting a predominant function of the leaf blade mesophyll as 483

source of auxin for regeneration. We confirmed this by removing leaf blades which resulted in 484

inhibition of regeneration. YUC9 expression has been shown to respond to methyl-jasmonate 485

(MeJA) treatment in a COI1-dependent manner (Hentrich et al., 2013). As excision of whole 486

leaves or leaf blades involves wounding and therefore MeJA production, MeJA might activate 487

YUC9 expression to rapid increase auxin levels in leaf blades, likely in combination with YUC1 488

and YUC4 activity. We also found that YUC8 was specifically upregulated in the vascular region 489

of the petiole associated with proliferation, and thus, it is possible that YUC8 might have a 490



29

specific role in maintaining auxin levels during vasculature proliferation or at later regenerative 491

steps. 492

Our results indicate that a long distance basipetal transport system concentrates auxin 493

generated in the leaf blade mesophyll towards defined vascular cells at the petiole base. We 494

showed that genetic and localized chemical inhibition of auxin transport significantly affected 495

regeneration. Despite of known redundancy among auxin transporters (Blilou et al., 2005; Péret 496

et al., 2012) we detected phenotypes in single mutants suggesting spatial 497

compartmentalization. Supporting this idea, PIN-FORMED3 (PIN3) was expressed in the petiole 498

vasculature while PIN4 was later restricted to the proliferating vascular region. In contrast, more 499

de-localized auxin transport is involved in rooting of leaf blades (Liu et al., 2014; Chen et al., 500

2016). As we observed predominant expression of ProDR5:GUS in the proximal petiole 501

vasculature, it is possible that auxin would need to be retained in this area. Our data suggest a 502

model in which subcellular PIN3 localization shifts from basal to apical membranes in vascular 503

cells near the wound to redirect auxin flow backwards and thus maintaining high auxin levels in 504

the proximal petiole vasculature. Interestingly, an auxin-dependent switch in PIN3 polarization 505

contributing to auxin-flow reversal is involved in the shoot gravitropic response (Rakusová et al., 506

2016), where basal-to-apical shift in PIN localization has been described to depend on 507

phosphorylation (Dai et al., 2012). It is thus tempting to speculate that auxin-dependent 508

phosphorylation of PIN3 would be involved in maintaining high auxin levels in the petiole base 509

vasculature during root regeneration. 510

The aberrant lateral root formation4 (alf4) mutant (DiDonato et al., 2004) has been linked 511

to hormone-induced callus formation (Sugimoto et al., 2010) but not to wound-induced callus 512

formation during graft stablishment (Melnyk et al., 2015). We observed reduced vasculature 513

proliferation along with great reduction in de novo root formation from whole leaves in alf4-1 514

mutants. As vasculature proliferation during de novo root formation associates to J0121- and 515

WIND1-marked cells, requires auxin and cytokinin signalling and involves ALF4, we propose it 516

is a type of callus, and therefore we refer to it as “endogenous callus” to differentiate it from 517

callus obtained by exogenous hormone supplementation. In our model, time-dependent auxin 518

accumulation in a subset of vascular cells activates proliferation, while cytokinins might regulate 519



30

the expression of genes that are directly involved in callus formation (such as WIND1 or ALF4) 520

or that are downstream targets of the auxin signal involved in callus formation (LATERAL 521

ORGAN BOUNDARIES DOMAIN factors) (Schaller et al., 2015). Particularly, we found that 522

INDOLE-3-ACETIC ACID INDUCIBLE18 (IAA18) and IAA28 are both involved in endogenous 523

callus formation, although only mutations in IAA18 affect whole regeneration response, while 524

ARABIDOPSIS HISTIDINE PHOSPHOTRANSFER PROTEIN1 (AHP1) to AHP3 and 525

ARABIDOPSIS RESPONSE REGULATOR1 (ARR1), ARR10 and ARR12 were involved in 526

vasculature proliferation and regeneration response. 527

528

Specification of root founder cells 529

Hormone-induced callus is organized in layers showing root tissue identities that resemble a 530

root meristem and therefore a new organ could be theoretically initiated through a differentiation 531

process (Sugimoto et al., 20010). WUSCHEL-RELATED HOMEOBOX11 (WOX11) expression 532

has been associated to first cell-fate transition from regeneration-competent cells to root 533

founder cells during leaf blade rooting (Liu et al., 2014; Hu and Xu, 2016). WOX11 activates 534

WOX5 during root formation in leaf blades; however we did not find WOX5 expression in 535

endogenous callus during de novo regeneration from whole leaves, suggesting that WOX11 536

could be involved in an earlier step in the reprograming process. On the other hand, specific 537

expression associated to root founder cell specification (SKP2B) revealed the establishment of 538

a cell lineage capable of forming a new root. These results indicate that additional 539

reprogramming processes are required. 540

PLETHORA1 (PLT1) and PLT2 have been recently shown to be required to establish 541

pluripotency during de novo shoot regeneration (Kareem et al., 2015). Our results show that 542

during de novo root formation PLT1 and PLT2, in combination with SHORT-ROOT (SHR), could 543

also be involved in specification of root founder cells, which are pluripotent. In addition, 544

persistent expression of PLT1, PLT2 and SHR appears to be necessary during subsequent 545

formative stages to maintain primordia growth, as the very primordia found in shr-2 plt1-4 plt2-2 546

quickly differentiate. In contrast, in the de novo shoot regeneration system transient induction of 547

PLT2 has been shown to be sufficient to specify shoot progenitors, while subsequent 548



31

expression of other regulators is required to accomplish de novo shoot formation from these 549

progenitors (Kareem et al., 2015). 550

551

Root primordia initiation and patterning 552

Multiple INDOLE-3-ACETIC ACID INDUCIBLE (IAA)-ARF modules cooperatively regulate 553

lateral root formation (Goh et al., 2012). We observed that factors regulating auxin signaling, 554

such as SOLITARY ROOT (IAA14) could be also involved in de novo root initiation, as we 555

detected decreased root capacity for slr-1, which could be indicative of fewer primordia 556

initiation. In addition, the IAA28 module, which is upstream of lateral root founder cell 557

specification (De Rybel et al., 2010), also regulates de novo root founder cell specification or 558

initiation, although further experiments could dissect more precisely at which stage IAA28 is 559

involved. Our results show that factors primarily involved in formation of lateral roots are also 560

affected in rooting of leaves, suggesting the existence of partially overlapping auxin signalling 561

modules during postembryonic root development. Conversely, cytokinin mutants (ahp1 ahp2 562

ahp3 and arr1 arr10 arr12) showed increased rooting capacity and thus, a repressor role in de 563

novo root initiation can be assigned for these factors, likely in an analogue manner as their role 564

during lateral root initiation (Lavenus et al., 2013; Chang et al., 2015). In agreement with this 565

model, we restored regeneration potential of cytokinin signalling mutants by a moderate 566

increase in auxin levels. 567

PLT1 and PLT2 expression is considered to be a slow read-out of auxin response and 568

prolonged auxin treatment results in PLT1 and PLT2 activation and the de novo specification of 569

WOX5-marked stem cells (Mahonen et al., 2014). We found severe impairment in de novo 570

primordia initiation in shr-2 plt1-4 plt2-2 and WOX5 expression during de novo primordia 571

formation requires auxin input through an unknown pathway (Hu and Xu, 2016). Therefore, it is 572

possible that PLT1 and PLT2 are required for specification of WOX5-marked cells downstream 573

of auxin during de novo organ initiation, which could occur in combination with activity of WOX5 574

transcription factor itself and/or SHORT-ROOT (SHR), in turn acting in an auxin-independent 575

pathway. Further experiments will be required to dissect the molecular pathway including PLTs, 576

SHR and WOX5. 577



32

We have also identified specific factors involved in formation of de novo root primordia. 578

We have found that the stem cell regulators BLUEJAY (BLJ), JACKDAW (JKD), SCARECROW 579

(SCR), SHR and SCHIZORIZA (SCZ) regulate ground tissue patterning and vasculature 580

formation prior emergence at the step of dome-shape primordia. Subsequently, more developed 581

primordia are not properly organized in cell layers or rows and by the time of emergence, these 582

defects persist and aggravate. Our results indicate that ground tissue patterning appears to be 583

regulated in newly formed roots at two levels. First, we observed impairment in asymmetric 584

divisions specifying cortex, middle cortex and endodermis in mutants of SHR and SCR, 585

although still a few asymmetric divisions were observed. In agreement, shr mutants have been 586

shown to form endodermis in anchor roots (Lucas et al., 2011), which are a type of adventitious 587

roots. Furthermore, we observed that ground tissue asymmetric divisions were absent in mutant 588

combinations of scr-4 with bjl-1 and jkd-4 and in double mutants jkd-4 scz-1. Interestingly, when 589

we studied if these mutant combinations had defects in lateral roots, which are also organs 590

formed postembryonically, we also observed absence of ground tissue asymmetric divisions 591

suggesting a conserved developmental program for endodermis and cortex specification. 592

Secondly, we observed that SCR, JKD, BLJ and SCZ could function as ground tissue lineage 593

determinants during de novo root organogenesis. The combined action of BLJ, JKD and SCR is 594

required to maintain postembryonically the ground tissue lineage and lacking these three factors 595

results in missing ground tissue initials (hence fewer ground tissue cell rows are observed in 596

cross sections) (Moreno-Risueno et al., 2015). We observed that de novo formed roots in blj-1 597

jkd-4 scr-4 and jkd-4 scz-1 mutants were missing ground tissue cell rows shortly after 598

emergence, which indicates incorrect specification of ground tissue initials during primordia 599

formation or later on in the course of development.. It, thus, possible SCZ, SHR, PLT1 and 600

PLT2 function as lineage or cell fate determinants during postembryonic development, and 601

particularly during de novo organogenesis. 602



33

MATERIALS AND METHODS 603

Growth conditions 604

Seeds were surfaced-sterilized in 10% (m/v) NaClO and rinsed with sterile water before being 605

transferred to 120×120×10 mm Petri dishes containing 65 mL of one-half-Murashige and Skoog 606

(MS) medium with 1% sucrose and 10 g/L Plant Agar (Duchefa). After two days of stratification 607

at 4°C in darkness, plates were transferred to Panasonic MLR-352-PE growth chamber at 22°C, 608

16/8 photoperiod or continuous light (50 µmol·m-2·s-1). Twelve days after germination, the first 609

pair of leaves was excised across the junction of the petiole with the stem and transferred to 610

Gamborg B5 medium with 2.5% sucrose, 10 g/L Difco Agar (BD) or 3 g/L Gelrite (Sigma) and 611

Gamborg B5 vitamin mixture (Duchefa). Leaves after excision were grown in darkness at 22°C, 612

routinely for 10 days, or for number of days indicated in corresponding experiment. 613

614

Hormonal and inhibition treatments 615

For exogenous hormone treatment, filter-sterilized indole-3-acetic acid (IAA), 6-616

benzylaminopurine (6-BAP) or thidiazuron (TDZ) stock solutions were added to warm growth 617

medium before pouring into plates to provide a final concentration of 1 μM IAA,, 5 μM 6-BAP or 618

4 μM TDZ respectively. N-1-naphthylphtalamic acid (NPA) was applied locally by preparing a 619

lanoline solution containing 1% w/w NPA. For cell cycle arrest, leaf explants were incubated 620

with growth medium supplemented with 0.5, 2.5 or 5 mM hydroxyurea (Sigma). 621

622

Plant material 623

Columbia-0 (Col-0), Landsberg erecta (Ler), and Wassilewskija-2 (Ws-2) accessions were used 624

as a genetic background as corresponding. The reporter lines ProIPT3:GUS, ProIPT5:GUS 625

(Miyawaki et al., 2004), ProLOG4:GUS s (Kuroha et al., 2009), obtained from RIKEN, and 626

ProARR5:GUS (D'Agostino et al., 2000) were used for tracing cytokinin biosynthesis and signaling 627

during rooting. ProYUC8:GUS, ProYUC9:GUS (Hentrich et al., 2013) and ProDR5:GUS (Ulmasov et 628

al., 1997) were used to investigate auxin biosynthesis and signaling; ProPIN3:PIN3:GFP (Xu et 629

al., 2006) and ProPIN4:GUS (Friml et al., 2004) for auxin transport. To trace the molecular 630

mechanisms during de novo root formation we used: ProWIND1:GUS (Iwase et al., 2011) 631



34

ProWOX11:GUS (Liu et al., 2014), ProWOX5:GUS (Sarkar et al., 2007) and ProSKP2Bs:GUS version 632

(Manzano et al., 2012), which corresponds to a promoter deletion containing 0.5 Kb upstream 633

from the ATG. J0121 and J0661 lines (Laplaze et al., 2005) were used to locate pericycle-like 634

cells during rooting. The following mutant lines were used: wol-1 (Scheres et al., 1995), ahp1 635

ahp2 ahp3 (Hutchison et al., 2006), ahp2 ahp4 ahp5, arr1 arr10 arr12 (Mason et al., 2005), 636

aux1-22 (Bennett et al., 1996), axr2-1 (Timpte et al., 1994), slr-1 (Fukaki et al., 2005), crane-2 637

(Uehara et al., 2008), sur2-1 (Delarue et al., 1998) and iaa28-1 (Rogg et al., 2001) obtained 638

from NASC; pin1, pin2 pin3, pin2 pin3 pin7 (Blilou et al., 2005); fwr (Okumura et al., 2013); 639

cyclinb1;1 (cycb1;1) and cycb1;2 (Nowack et al., 2012) and CDKB1;1 DN161 and Pro35S:KRP2 640

(Boudolf et al., 2004; Verkest et al., 2005). We also used the following stem cell niche mutants, 641

blj-1 jkd-4 scr-4 (Moreno-Risueno et al., 2015), scr-4 (Fukaki et al., 1996), shr-2 ProSHR:SHR:GR 642

(Levesque et al., 2006), plt1-4 plt2-2 (Aida et al., 2004), jkd-4 (Welch et al., 2007), scz-1 643

(Mylona et al., 2002), wox5-1 (Sarkar et al., 2007), and jkd-4 scz-1 and shr-2 plt1-4 plt2-2 644

ProSHR:SHR:GR (generated in this study). 645

646

Genotyping 647

The triple mutant shr-2 plt1-4 plt2-2 ProSHR:SHR:GR was generated by crossing shr-2 648

ProSHR:SHR:GR and plt1-4 plt2-2. F2 seedlings were grown and pre-selected on one-half-MS 649

medium with 10 µM dexamethasone followed by DNA extraction and genotyping by PCR to 650

finally obtain homozygous lines. The oligonucleotides used for genotyping shr-2, while 651

discriminating ProSHR:SHR:GR, were: F 5´-CCAATACCATCCCGCCAC-3´ and R 5´-652

TGAACCGGTCATGCGGTTG-3´; for plt1-4: F 5´-AGACGGCCACGCCAAGAC-3´ and R 653

5´CTAGTATCACGACATTATTTGC-3´; for plt-2-2: F 5´-ACCTACAGTCGTCACTTGTGC-3´ and 654

R 5´-ACTCTTGTCTCGTCATGTTTTTC-3´. T-DNA insertions of PLT1 and PLT2 were amplified 655

using LB 5´-CATTTTATAATAACGCTGCGGACATCTAC-3´ and respective reverse primer. 656

Double mutant jkd-4 scz-1 was generated by crossing jkd-4 and scz-1. DNA extraction from F2 657

seedlings was used for genotyping by PCR. The oligonucleotides used for genotyping jkd-4 658

were: F 5´-GGATGAAAGCAATGCAAAACA-3´ and R 5´-AATGTCGGGATGATGAACTCC-3´. 659

The T-DNA insertion in the jkd-4 line was genotyped using respective forward primer and RB 5´-660



35

TCAAACAGGATTTTCGCCTGCT-3´. For scz-1 genotyping, a SCZ fragment was amplified 661

using F 5’-CGAAGGTCAAGGCAAAGCTG-3’ and R 5´-GAGCAACAGGCTTGACATGG-662

3´primers, followed by digestion with NlaIII restriction enzyme. Upon digestion, SCZ fragment 663

from scz-1 renders a band of 900 bp, while the wild-type fragment is cut by the enzyme 664

resulting in two fragments of 530 and 360 bp. 665

666

Cell death, GUS staining and microscopy analysis 667

In leaf tissues, dying cells were visualized by lactophenol-trypan blue staining as described in 668

Pavet et al. (2005). For GUS staining, leaf explants were incubated at 37 °C for variable times 669

(4-24 h) in multi-well plates in the presence of the GUS staining solution as described in Perez-670

Perez et al. (2010) or Manzano et al. (2012). To bleach chlorophyll two different methods were 671

used indistinctly with similar results. First method: samples were dehydrated after GUS staining 672

using increasing ethanol concentrations (15, 50, 70, 96 and 100%) 15 minutes in each one, and 673

kept overnight in 100% ethanol. Next, samples were rehydrated following the same ethanol 674

concentration series to 15% ethanol and mounted in 15% glycerol. Second method: samples 675

were fixed in 96% ethanol for 48 h and washed with 0.1 M phosphate buffer (pH 6.8) before 676

being transferred them to clearing solution (80 g chloral hydrate and 30 mL distilled water). Leaf 677

explants were mounted on slides using a mixture of 80 g chloral hydrate, 20 mL distilled water 678

and 10 mL glycerol. After GUS staining, pictures were taken in a Leica DM 2000 with a DCF300 679

camera, or in a bright field Olympus AX70 microscope equipped with an Olympus PM-C35DX 680

microphotography system. The area of proliferating tissues (callus or vasculature) was manually 681

drawn from microscopic images using a Wacon Bamboo tablet and areas or diameters of their 682

best-fitting ellipses were measured with ImageJ (v1.50) software. 683

684

Microscopy analysis 685

Leaf petioles (for studying developmental stages during rooting) and mature embryos, were 686

stained using aniline blue staining method as described in (Bougourd et al., 2000). Processed 687

samples were observed by Leica TCS SP8 laser scanning confocal microscope (Heerbrugg, 688

Switzerland) with the settings described in Bougourd et al. (2000). J0121 fluorescent reporter 689



36

line was processed prior imaging as indicated in Kurihara et al. (2015). Cross sections (10 µm 690

of thickness) of J0121 petioles were obtained using Vibratome 1000 Plus when indicated. Other 691

fluorescent reporter lines were incubated on methanol:acetone solution for 20 min at −20°C , 692

and immediately transferred to 0.1 M phosphate buffer (pH 6.8). Imaging was performed by 693

confocal microscopy using a Nikon Digital Eclipse C1 equipped with the EZ-C1 control software 694

(Nikon Instruments) or a Leica TCS SP8 laser scanning microscope. GFP was excited with an 695

Argon laser at 488 nm and emission was collected at 505-530 nm, while YFP was excited at 696

514 nm and emission collected at 535-560 nm. To exclude auto-fluorescence contamination, 697

sample emission was collected at 605-675 nm prior excitation with He-Ne laser at 543 nm, and 698

used as a reference for background. Root samples for radial and longitudinal analyses in 699

patterning studies were fluorescently stained with 10 mM propidium iodide (Sigma), and imaged 700

using standard settings on a Leica TCS SP8 confocal. 701

702

Quantification and statistical analysis 703

Regeneration percentage was scored as the number of leaf explants that showed swelling of 704

petioles, proliferation of vascular-associated cells and/or outgrowth of roots at the proximal 705

region of the petiole, at 7 days after excision (dae) or as indicated in corresponding 706

experiments. Rooting percentage was scored as the number of leaf explants showing roots at 707

10 dae or as indicated. Proliferation of vascular-associated cells and number of de novo formed 708

roots were scored on individual leaf samples and used to estimate rooting capacity categories 709

at indicated days in corresponding experiments. Ten dae de novo formed roots were used for 710

establishing differences in tissue patterning using number of cortical cells. Number of cortical 711

cells was quantified using confocal cross sections taken at the site of lateral root cap ending. To 712

determine lateral root capacity, root meristems of 4 days post-imbibition seedlings were 713

removed and number of lateral roots quantified 3 days later. Roots were observed at the 714

microscope to confirm there were not unemerged primordia. Data values referred to % rooting, 715

% regeneration, number of cortical cells, lateral root capacity and vasculature or callus area 716

were statistically analyzed by univariate General Linear Model (GLM) and ANOVA with DMS 717

Post-Hoc test, using IBM SPSS Statistics 21 software. For rooting capacity, Chi-square test was 718



37

performed to assay if there were differences in distribution frequency between lines, analyzed 719

two by two, using STATGRAPHICS Centurion XVI.I software. Significant differences were 720

collected with 5% level of significance (p-value˂0.05). 721

722

ACKNOWLEDGEMENTS 723

We are especially indebted to M.A. Fernández-López for her expert technical assistance. We 724

thank Dr. M. Pernas for providing scz-1 mutant and advice about its genotyping, and two 725

anonymous reviewers for their useful suggestions. 726

727

Figure S1. Rooting of whole leaves and leaf blades of Arabidopsis wild-type 728

accessions. 729

Figure S2. Vascular proliferation and callus formation during rooting of whole leaves. 730

Figure S3. AHK4, AHP1, AHP2, AHP3, AHP4, AHP5 and ARR1, ARR10 and ARR12 731

cytokinin signaling factors regulate hormone-induced callus formation. 732

Figure S4. IAA7/AXR2 and IAA18 auxin signaling factors regulate hormone-induced 733

callus formation. 734

Figure S5. ALF4 is required for vasculature proliferation and de novo root formation. 735

Figure S6. IAA7/AXR2, CRANE/IAA18 and IAA28 signaling factors regulate de novo 736

root formation in leaf blades. 737

Figure S7. The YUC8 and YUC9 auxin biosynthesis genes are induced in excised 738

leaves. 739

Figure S8. SCARECROW and SHORT-ROOT regulate ground tissue patterning of de 740

novo formed roots. 741

742

743

FIGURE LEGENDS 744

Figure 1. Developmental stages during rooting of Arabidopsis leaves. (A) Whole leaf 745

rooting procedure. (B-H) Confocal microscopy pictures of petioles showing (C-E) proliferation of 746



38

vasculature cells, (F, G) initiation and formation of primordia, and (H) de novo root emergence. 747

(I-K) J0661-GFP line in sections of petioles at (I, J) excision time or (K) 5 days after excision 748

(dae). (L-P) J0121-GFP line in sections of petioles at (L, M) excision time, (N, O) 2 dae and (P). 749

5 dae. (J, M, O) Transversal sections of petioles at the base. va, vasculature; co, collenchyma; 750

xy, xylem; pc, proliferating cells; RP, root primordium; AR, adventitious root; ph, phloem; pr, 751

procambium. Scale bar: 25 µm. (Q-R) Leaves of wild type and cell-cycle mutants, or upon 752

treatment with hydroxyurea (HU), were assessed for (Q) vasculature proliferation and (R) 753

rooting at 7dae. Asterisks: statistically significant (p-value <0.05) by General Linear Model 754

(GLM) and DMS Post-Hoc test 755

756

Figure 2. Cytokinin acts locally during de novo root regeneration. (A-C) Expression of (A) 757

ProIPT3:GUS, (B) ProIPT5:GUS, (C) ProLOG4:GUS and (D-E) ProARR5:GUS in petioles at indicated 758

days after excision (dae). (E) Leaves were incubated with 5 µM 6-benzylaminopurine (6-BAP). 759

(F) Mutants impaired in cytokinin signalling show defective regeneration (which accounts for 760

petioles with vasculature proliferation, primordia and roots; yellow barplots) and rooting capacity 761

(multi-coloured barplots show frequencies of vasculature proliferation and of roots or primordia, 762

indistinctly) at 7 dae. (G) Cytokinin signalling mutant leaf explants incubated with 1 µM indol-3-763

acetic acid (IAA) and measured for root regeneration responses as in (F). Scale bars: (A-C) 0.5 764

mm, (D-E) 0.25 mm. Asterisks: p-value<0.05 by General Linear Model (GLM) followed by DMS 765

Post-Hoc or Chi-square test. 766

767

Figure 3. Distinctive auxin signaling pathways regulate de novo root regeneration. (A-B) 768

Auxin response reported by (A) ProDR5:GUS expression in Arabidopsis leaf petioles and (B) 769

quantification of GUS stained area; dae, days after excision. (C) ProDR5:GUS expression and de 770

novo formed roots (AR) in leaves supplemented with 1 µM IAA (left) and in the sur2-1 auxin 771

overproduction mutant (right). (D) Regeneration percentage and (E) rooting capacity at 7 days 772

after excision of auxin signaling mutants (nph4-1 arf19-1, axr2-1, slr-1, crane-2, and iaa28-1) 773

and auxin overproducer sur2-1. (F) Vasculature proliferation area on Arabidopsis leaves 774



39

cultivated for 14 days in hormone-free medium. Scale bars: 200 μm. Asterisks: p-value<0.05 by 775

General Linear Model (GLM) followed by DMS Post-Hoc or Chi-square test. 776

777

Figure 4. Polar auxin transport from the leaf blade to the petiole is required for rooting. 778

(A-B) Distal blade excision reduces (A) regeneration rate and rooting capacity at 7 days after 779

excision (dae and (B) ProDR5:GUS expression at 12 hours after excision (hae) and 3 dae. (C-D) 780

Local treatment at the blade-petiole junction with 1% N-1-naphthylphthalamic acid (NPA) 781

reduces (C) regeneration rate and rooting capacity at 7 dae, and (D) ProDR5:GUS expression. 782

(E-G) Expression of (E) ProPIN4:GUS and (F-G) ProPIN3:PIN3:GFP Arrowheads point to 783

membrane-localized PIN-GFP. Scale bars: (B, D, F, G) 0.2 and (E) 0.5 mm. (H) Regeneration 784

and rooting capacity in auxin transport mutants at 7 dae. Asterisks: p-value<0.05 by General 785

Linear Model (GLM) followed by DMS Post-Hoc or Chi-square test. 786

787

Figure 5. Root founder cells establish on endogenous callus prior de novo primordium 788

formation. (A-F) Expression of (A) ProWIND1:GUS, (B, E, F) ProWOX11:GUS, (C) ProSKP2Bs:GUS 789

and (D) ProWOX5:GUS in leaf petioles at indicated days after excision (dae). (E) Control 790

conditions or (F) upon 5 mM hydroxyurea (HU) treatment. GUS staining time in (E) was set for 791

no expression; xy, xylem; pc, proliferating cells; va, vasculature; RFC, root founder cell; RP, root 792

primordium; NR, de novo formed root. Scale bars: 200 µm. (G) Regeneration percentage and 793

rooting capacity at 7 dae of mutants impaired in cell cycle progression and hydroxyurea (HU)-794

treated Col-0 leaves. Asterisks: p-value<0.05 by General Linear Model (GLM) followed by DMS 795

Post-Hoc or Chi-square test. 796

797

Figure 6. SHORT-ROOT, PLETHORA1, PLETHORA2, JACKDAW, BLUEJAY, SCARECROW 798

and SCHIZORIZA are required for de novo root primordia initiation and formation. (A) 799

Rooting percentage and (B) rooting capacity at 10 days after excision (dae) for loss-of-function 800

mutants in stem cell regulators. Asterisks: p-value<0.05 by General Linear Model (GLM) 801

followed by DMS Post-Hoc or Chi-square test. (C) Triple shr-2 plt1-4 plt2-2 mutant does not 802

regenerate roots at 10 dae. (D) Confocal images of control and shr-2 plt1-4 plt2-2 during root 803



40

regeneration. Malformed primordia (3%, n=90) in shr-2 plt1-4 plt2-2 do not emerge through 804

petiole tissues. (E) Confocal images of de novo root primordia of Wild type, jkd4-4 scz-1 and blj-805

1 jkd-4 scr-4 at 5 and 6 dae; co, collenchyma; AR, adventitious root; pc, proliferative cells; RP, 806

root primordium; xy, xylem; black dashed line corresponds to cells in the position of quiescent 807

center; white dashed line cells in the position of the ground tissue and in contact to quiescent 808

center; green asterisk: cortex ; turquoise asterisk: middle cortex; yellow asterisk: endodermis. 809

Scale bars: (C) 5 mm and (D-I) 50 µm. 810

811

Figure 7. JACKDAW, BLUEJAY, SCARECROW, SHORT-ROOT and SCHIZORIZA regulate 812

patterning of postembryonic roots. (A-B) Confocal (A) longitudinal and (B) transversal 813

sections of de novo formed roots at 10 days after excision (1-3 days post emergence). 814

Transversal sections were taken at end of lateral root cap. Dashed lines and asterisks: green, 815

cortex; turquoise, middle cortex; yellow, endodermis; brown, stele; white and m: mutant 816

undivided ground tissue; xy, xylem. (C) Number of cortical-like cell or undivided mutant cell rows 817

in control accessions, jkd-4 scz-1 and blj-1 jkd-4 scr-4. (D) Lateral root capacity in Col-0, shr-2 818

plt1-4 plt2-2, jkd-4 scz-1 and blj-1 jkd-4 scr-4 and at 4 days after seed imbibition. (E) Confocal 819

longitudinal sections of emerged lateral roots of Col-0, shr-2 plt1-4 plt2-2, jkd-4 scz-1 and blj-1 820

jkd-4 scr-4 at 7 days after seed imbibition. Scale bars: 50 μm. Asterisks: p-value<0.05 by 821

General Linear Model (GLM) and DMS Post-Hoc test. 822

823

Figure 8. Model of de novo root regeneration in Arabidopsis leaves. (A) Auxin is 824

transported to the petiole base and acts in combination with locally-produced cytokinin to induce 825

endogenous callus formation; LOG4, IPT3, IPT5: cytokinin biosynthesis; ARR5: cytokinin 826

response; YUCCA8/9: auxin synthesis; PIN1/2/3/7, AUX1: auxin transport; DR5: auxin 827

response. (B) Stages of de novo formation of roots based on morphological changes and 828

expression of markers. (C) Regulation of distinctive stages of de novo organogenesis based on 829

mutant phenotypes. Regulation or functions which could not be directly assigned are indicated 830

as hypothetical. 831

832



41

833



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Barlier I, Kowalczyk M, Marchant A, Ljung K, Bhalerao R, Bennett M, Sandberg G, Bellini C (2000) The SUR2 gene of Arabidopsisthaliana encodes the cytochrome P450 CYP83B1, a modulator of auxin homeostasis. Proc Natl Acad Sci USA 97: 14819-14824.


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http://www.ncbi.nlm.nih.gov/pubmed?term=Aida M%2C Beis D%2C Heidstra R%2C Willemsen V%2C Blilou I%2C Galinha C%2C Nussaume L%2C Noh YS%2C Amasino R%2C Scheres B %282004%29 The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche%2E Cell 119%3A 109%2D120&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh YS, Amasino R, Scheres B (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119: 109-120

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

http://scholar.google.com/scholar?as_q=The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche&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 PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Aida&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Atta R%2C Laurens L%2C Boucheron%2DDubuisson E%2C Guivarc%27h A%2C Carnero E%2C Giraudat%2DPautot V%2C Rech P%2C Chriqui D %282009%29 Pluripotency of Arabidopsis xylem pericycle underlies shoot regeneration from root and hypocotyl explants grown in vitro%2E Plant J 57%3A 626%2D644%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Atta R, Laurens L, Boucheron-Dubuisson E, Guivarc'h A, Carnero E, Giraudat-Pautot V, Rech P, Chriqui D (2009) Pluripotency of Arabidopsis xylem pericycle underlies shoot regeneration from root and hypocotyl explants grown in vitro. Plant J 57: 626-644.

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

http://scholar.google.com/scholar?as_q=Pluripotency of Arabidopsis xylem pericycle underlies shoot regeneration from root and hypocotyl explants grown in vitro&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=Pluripotency of Arabidopsis xylem pericycle underlies shoot regeneration from root and hypocotyl explants grown in vitro&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Atta&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Barlier I%2C Kowalczyk M%2C Marchant A%2C Ljung K%2C Bhalerao R%2C Bennett M%2C Sandberg G%2C Bellini C %282000%29 The SUR2 gene of Arabidopsis thaliana encodes the cytochrome P450 CYP83B1%2C a modulator of auxin homeostasis%2E Proc Natl Acad Sci USA 97%3A 14819%2D14824%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Barlier I, Kowalczyk M, Marchant A, Ljung K, Bhalerao R, Bennett M, Sandberg G, Bellini C (2000) The SUR2 gene of Arabidopsis thaliana encodes the cytochrome P450 CYP83B1, a modulator of auxin homeostasis. Proc Natl Acad Sci USA 97: 14819-14824.

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

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http://www.ncbi.nlm.nih.gov/pubmed?term=Bellini C%2C Pacurar DI%2C Perrone I %282014%29 Adventitious roots and lateral roots%3A similarities and differences%2E Annu Rev Plant Biol 65%3A 639%2D666%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Bellini C, Pacurar DI, Perrone I (2014) Adventitious roots and lateral roots: similarities and differences. Annu Rev Plant Biol 65: 639-666.

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

http://scholar.google.com/scholar?as_q=Adventitious roots and lateral roots: similarities and differences&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=Bennett MJ%2C Marchant A%2C Green HG%2C May ST%2C Ward SP%2C Millner PA%2C Walker AR%2C Schulz B%2C Feldmann KA %281996%29 Arabidopsis AUX1 gene%3A a permease%2Dlike regulator of root gravitropism%2E Science 273%3A 948%2D950%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Bennett MJ, Marchant A, Green HG, May ST, Ward SP, Millner PA, Walker AR, Schulz B, Feldmann KA (1996) Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273: 948-950.

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

http://scholar.google.com/scholar?as_q=Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism&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=Birnbaum KD%2C S�nchez Alvarado A %282008%29 Slicing across kingdoms%3A regeneration in plants and animals%2E Cell 132%3A 697%2D710%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Birnbaum KD, S�nchez Alvarado A (2008) Slicing across kingdoms: regeneration in plants and animals. Cell 132: 697-710.

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

http://scholar.google.com/scholar?as_q=Slicing across kingdoms: regeneration in plants and animals&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=Slicing across kingdoms: regeneration in plants and animals&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Birnbaum&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Blilou I%2C Xu J%2C Wildwater M%2C Willemsen V%2C Paponov I%2C Friml J%2C Heidstra R%2C Aida M%2C Palme K%2C Scheres B %282005%29 The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots%2E Nature 433%3A 39%2D44%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433: 39-44.

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

http://scholar.google.com/scholar?as_q=The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots&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 PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Blilou&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Boudolf V%2C Vlieghe K%2C Beemster GT%2C Magyar Z%2C Acosta JAT%2C Maes S%2C Van Der Schueren E%2C Inz� D%2C De Veylder L %282004%29 The plant%2Dspecific cyclin%2Ddependent kinase CDKB1%3B1 and transcription factor E2Fa%2DDPa control the balance of mitotically dividing and endoreduplicating cells in Arabidopsis%2E Plant Cell 16%3A 2683%2D2692%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Boudolf V, Vlieghe K, Beemster GT, Magyar Z, Acosta JAT, Maes S, Van Der Schueren E, Inz� D, De Veylder L (2004) The plant-specific cyclin-dependent kinase CDKB1;1 and transcription factor E2Fa-DPa control the balance of mitotically dividing and endoreduplicating cells in Arabidopsis. Plant Cell 16: 2683-2692.

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Della Rovere F, Fattorini L, Ronzan M, Falasca G, Altamura MM (2016) The quiescent center and the stem cell niche in the adventitiousroots of Arabidopsis thaliana. Plant Signal Behav 11: e1176660.


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Dubrovsky JG, Gambetta GA, Hernández-Barrera A, Shishkova S, González I (2006) Lateral root initiation in Arabidopsis:developmental window, spatial patterning, density and predictability. Ann Bot 97: 903-915.


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http://www.ncbi.nlm.nih.gov/pubmed?term=De Rybel B%2C Vassileva V%2C Parizot B%2C Demeulenaere M%2C Grunewald W%2C Audenaert D%2C Van Campenhout J%2C Overvoorde P%2C Jansen L%2C Vanneste S%2C et al%2E %282010%29 A novel aux%2FIAA28 signaling cascade activates GATA23%2Ddependent specification of lateral root founder cell identity%2E Curr Biol 20%3A 1697%2D1706%2E&dopt=abstract

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Forzani C, Aichinger E, Sornay E, Willemsen V, Laux T, Dewitte W, Murray J (2014) WOX5 suppresses CYCLIN D activity to establishquiescence at the center of the root stem cell niche. Curr Biol 24: 1939-1944.


Friml J, Yang X, Michniewicz M, Weijers D, Quint A, Tietz O, Benjamins R, Ouwerkerk PB, Ljung K, Sandberg G, et al. (2004) A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306: 862-865.


Fukaki H, Fujisawa H, Tasaka M (1996) SGR1, SGR2, SGR3: novel genetic loci involved in shoot gravitropism in Arabidopsis thaliana.Plant Physiol 110: 945-955.


Fukaki H, Nakao Y, Okushima Y, Theologis A, Tasaka M (2005) Tissue-specific expression of stabilized SOLITARY-ROOT/IAA14 alterslateral root development in Arabidopsis. Plant J 44: 382-395.


Goh T, Kasahara H, Mimura T, Kamiya Y, Fukaki H (2012) Multiple AUX/IAA-ARF modules regulate lateral root formation: the role ofArabidopsis SHY2/IAA3-mediated auxin signalling. Philos Trans R Soc Lond B-Biol Sci 367: 1461-1468.


Goh T, Toyokura K, Wells DM, Swarup K, Yamamoto M, Mimura T, Weijers D, Fukaki H, Laplaze L, Bennett MJ, et al. (2016) Quiescentcenter initiation in the Arabidopsis lateral root primordia is dependent on the SCARECROW transcription factor. Development 143:3363-3371.


Gordon SP, Heisler MG, Reddy GV, Ohno C, Das P, Meyerowitz EM (2007) Pattern formation during de novo assembly of theArabidopsis shoot meristem. Development 134: 3539-3548.


Hartmann HT, Kester DE, Davies FT, Geneve R (2010) Hartmann and Kester's plant propagation: principles and practices (8th edn.).Englewood Cliffs, NJ, USA: Prentice-Hall.


Hayashi K, Hashimoto K, Kusaka N, Yamazoe A, Fukaki H, Tasaka M, Nozaki H (2006) Caged gene-inducer spatially and temporallycontrols gene expression and plant development in transgenic Arabidopsis plant. Bioorg Med Chem Lett 16: 2470-2474.


Hentrich M, Bottcher C, Duchting P, Cheng Y, Zhao Y, Berkowitz O, Masle J, Medina J, Pollmann S (2013) The jasmonic acid signalingpathway is linked to auxin homeostasis through the modulation of YUCCA8 and YUCCA9 gene expression. Plant J 74: 626-637.


Heyman J, Cools T, Vandenbussche F, Heyndrickx KS, Van Leene J, Vercauteren I, Vanderauwera S, Vandepoele K, De Jaeger G, VanDer Straeten D, et al. (2013) ERF115 controls root quiescent center cell division and stem cell replenishment. Science 342: 860-863.


Hu X, Xu L (2016) Transcription factors WOX11/12 directly activate WOX5/7 to promote root primordia initiation and organogenesis.Plant Physiol 172: 2363-2373.

Pubmed: Author and Title www.plantphysiol.orgon July 11, 2018 - Published by Downloaded from Copyright © 2017 American Society of Plant Biologists. All rights reserved.

http://www.ncbi.nlm.nih.gov/pubmed?term=Fan M%2C Xu C%2C Xu K%2C Hu Y %282012%29 LATERAL ORGAN BOUNDARIES DOMAIN transcription factors direct callus formation in Arabidopsis regeneration%2E Cell Res 22%3A 1169%2D1180%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Fan M, Xu C, Xu K, Hu Y (2012) LATERAL ORGAN BOUNDARIES DOMAIN transcription factors direct callus formation in Arabidopsis regeneration. Cell Res 22: 1169-1180.

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http://www.ncbi.nlm.nih.gov/pubmed?term=Forzani C%2C Aichinger E%2C Sornay E%2C Willemsen V%2C Laux T%2C Dewitte W%2C Murray J %282014%29 WOX5 suppresses CYCLIN D activity to establish quiescence at the center of the root stem cell niche%2E Curr Biol 24%3A 1939%2D1944%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Forzani C, Aichinger E, Sornay E, Willemsen V, Laux T, Dewitte W, Murray J (2014) WOX5 suppresses CYCLIN D activity to establish quiescence at the center of the root stem cell niche. Curr Biol 24: 1939-1944.

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

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http://www.ncbi.nlm.nih.gov/pubmed?term=Friml J%2C Yang X%2C Michniewicz M%2C Weijers D%2C Quint A%2C Tietz O%2C Benjamins R%2C Ouwerkerk PB%2C Ljung K%2C Sandberg G%2C et al%2E %282004%29 A PINOID%2Ddependent binary switch in apical%2Dbasal PIN polar targeting directs auxin efflux%2E Science 306%3A 862%2D865%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Friml J, Yang X, Michniewicz M, Weijers D, Quint A, Tietz O, Benjamins R, Ouwerkerk PB, Ljung K, Sandberg G, et al. (2004) A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306: 862-865.

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http://www.ncbi.nlm.nih.gov/pubmed?term=Fukaki H%2C Fujisawa H%2C Tasaka M %281996%29 SGR1%2C SGR2%2C SGR3%3A novel genetic loci involved in shoot gravitropism in Arabidopsis thaliana%2E Plant Physiol 110%3A 945%2D955%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Fukaki H, Fujisawa H, Tasaka M (1996) SGR1, SGR2, SGR3: novel genetic loci involved in shoot gravitropism in Arabidopsis thaliana. Plant Physiol 110: 945-955.

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http://www.ncbi.nlm.nih.gov/pubmed?term=Fukaki H%2C Nakao Y%2C Okushima Y%2C Theologis A%2C Tasaka M %282005%29 Tissue%2Dspecific expression of stabilized SOLITARY%2DROOT%2FIAA14 alters lateral root development in Arabidopsis%2E Plant J 44%3A 382%2D395%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Fukaki H, Nakao Y, Okushima Y, Theologis A, Tasaka M (2005) Tissue-specific expression of stabilized SOLITARY-ROOT/IAA14 alters lateral root development in Arabidopsis. Plant J 44: 382-395.

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http://www.ncbi.nlm.nih.gov/pubmed?term=Goh T%2C Kasahara H%2C Mimura T%2C Kamiya Y%2C Fukaki H %282012%29 Multiple AUX%2FIAA%2DARF modules regulate lateral root formation%3A the role of Arabidopsis SHY2%2FIAA3%2Dmediated auxin signalling%2E Philos Trans R Soc Lond B%2DBiol Sci 367%3A 1461%2D1468%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Goh T, Kasahara H, Mimura T, Kamiya Y, Fukaki H (2012) Multiple AUX/IAA-ARF modules regulate lateral root formation: the role of Arabidopsis SHY2/IAA3-mediated auxin signalling. Philos Trans R Soc Lond B-Biol Sci 367: 1461-1468.

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http://www.ncbi.nlm.nih.gov/pubmed?term=Goh T%2C Toyokura K%2C Wells DM%2C Swarup K%2C Yamamoto M%2C Mimura T%2C Weijers D%2C Fukaki H%2C Laplaze L%2C Bennett MJ%2C et al%2E %282016%29 Quiescent center initiation in the Arabidopsis lateral root primordia is dependent on the SCARECROW transcription factor%2E Development 143%3A 3363%2D3371%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Goh T, Toyokura K, Wells DM, Swarup K, Yamamoto M, Mimura T, Weijers D, Fukaki H, Laplaze L, Bennett MJ, et al. (2016) Quiescent center initiation in the Arabidopsis lateral root primordia is dependent on the SCARECROW transcription factor. Development 143: 3363-3371.

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http://www.ncbi.nlm.nih.gov/pubmed?term=Gordon SP%2C Heisler MG%2C Reddy GV%2C Ohno C%2C Das P%2C Meyerowitz EM %282007%29 Pattern formation during de novo assembly of the Arabidopsis shoot meristem%2E Development 134%3A 3539%2D3548%2E&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Hartmann HT%2C Kester DE%2C Davies FT%2C Geneve R %282010%29 Hartmann and Kester%27s plant propagation%3A principles and practices %288th edn%2E%29%2E Englewood Cliffs%2C NJ%2C USA%3A Prentice%2DHall%2E&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Hayashi K%2C Hashimoto K%2C Kusaka N%2C Yamazoe A%2C Fukaki H%2C Tasaka M%2C Nozaki H %282006%29 Caged gene%2Dinducer spatially and temporally controls gene expression and plant development in transgenic Arabidopsis plant%2E Bioorg Med Chem Lett 16%3A 2470%2D2474%2E&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Heyman J%2C Cools T%2C Vandenbussche F%2C Heyndrickx KS%2C Van Leene J%2C Vercauteren I%2C Vanderauwera S%2C Vandepoele K%2C De Jaeger G%2C Van Der Straeten D%2C et al%2E %282013%29 ERF115 controls root quiescent center cell division and stem cell replenishment%2E Science 342%3A 860%2D863%2E&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Hu X%2C Xu L %282016%29 Transcription factors WOX11%2F12 directly activate WOX5%2F7 to promote root primordia initiation and organogenesis%2E Plant Physiol 172%3A 2363%2D2373%2E&dopt=abstract


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Ikeuchi M, Ogawa Y, Iwase A, Sugimoto K (2016) Plant regeneration: cellular origins and molecular mechanisms. Development 143:1442-1451


Ikeuchi M, Sugimoto K, Iwase A (2013) Plant callus: mechanisms of induction and repression. Plant Cell 25: 3159-3173Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

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Kareem A, Durgaprasad K, Sugimoto K, Du Y, Pulianmackal AJ, Trivedi ZB, Abhayadev PV, Pinon V, Meyerowitz EM, Scheres B, PrasadK (2015) PLETHORA genes control regeneration by a two-step mechanism. Curr Biol 25: 1017-1030


Kareem A, Radhakrishnan D, Sondhi Y, Aiyaz M, Roy MV, Sugimoto K, Prasad K (2016) De novo assembly of plant body plan: a stepahead of Deadpool. Regeneration (Oxf) 3: 182-197


Kleine-Vehn J, Huang F, Naramoto S, Zhang J, Michniewicz M, Offringa R, Friml J (2009) PIN Auxin efflux carrier polarity is regulated byPINOID kinase-mediated recruitment into GNOM-independent trafficking in Arabidopsis. Plant Cell 21: 3839-3849


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Kuroha T, Tokunaga H, Kojima M, Ueda N, Ishida T, Nagawa S, Fukuda H, Sugimoto K, Sakakibara H (2009) Functional analyses ofLONELY GUY cytokinin-activating enzymes reveal the importance of the direct activation pathway in Arabidopsis. Plant Cell 21: 3152-3169


Kuroha T, Ueguchi C, Sakakibara H, Satoh S (2006) Cytokinin receptors are required for normal development of auxin-transportingvascular tissues in the hypocotyl but not in adventitious roots. Plant Cell Physiol 47: 234-243


Laplaze L, Parizot B, Baker A, Ricaud L, Martinière A, Auguy F, Franche C, Nussaume L, Bogusz D, Haseloff, J (2005) GAL4-GFPenhancer trap lines for genetic manipulation of lateral root development in Arabidopsis thaliana. J Exp Bot 56: 2433-2442


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http://search.crossref.org/?page=1&rows=2&q=Hu X, Xu L (2016) Transcription factors WOX11/12 directly activate WOX5/7 to promote root primordia initiation and organogenesis. Plant Physiol 172: 2363-2373.

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

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http://www.ncbi.nlm.nih.gov/pubmed?term=Hutchison CE%2C Li J%2C Argueso C%2C Gonzalez M%2C Lee E%2C Lewis MW%2C Maxwell BB%2C Perdue TD%2C Schaller GE%2C Alonso JM%2C et al%2E %282006%29 The Arabidopsis Histidine Phosphotransfer Proteins are redundant positive regulators of cytokinin signaling%2E Plant Cell 18%3A 3073%2D3087&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Hutchison CE, Li J, Argueso C, Gonzalez M, Lee E, Lewis MW, Maxwell BB, Perdue TD, Schaller GE, Alonso JM, et al. (2006) The Arabidopsis Histidine Phosphotransfer Proteins are redundant positive regulators of cytokinin signaling. Plant Cell 18: 3073-3087

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http://www.ncbi.nlm.nih.gov/pubmed?term=Ikeuchi M%2C Ogawa Y%2C Iwase A%2C Sugimoto K %282016%29 Plant regeneration%3A cellular origins and molecular mechanisms%2E Development 143%3A 1442%2D1451&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Ramirez%2DParra E%2C Perianez%2DRodriguez J%2C Navarro%2DNeila S%2C Gude I%2C Moreno%2DRisueno MA%2C Del Pozo JC %282017%29 The transcription factor OBP4 controls root growth and promotes callus formation%2E New Phytol 213%3A 1787%2D1801&dopt=abstract

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Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres B, Heidstra R, Laux T (2007) Conserved factorsregulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446: 811-814


Schaller GE, Bishopp A, Kieber JJ (2015) The yin-yang of hormones: cytokinin and auxin interactions in plant development. Plant Cell27: 44-63


Scheres B, Di Laurenzio L, Willemsen V, Hauser MT, Janmaat K, Weisbeek P, Benfey PN (1995) Mutations affecting the radialorganisation of the Arabidopsis root display specific defects throughout the embryonic axis. Development 121: 53-62


Skoog F, Miller CO (1957) Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp Soc Exp Biol 11:118-130


Sugimoto K, Jiao Y, Meyerowitz EM (2010) Arabidopsis regeneration from multiple tissues occurs via a root development pathway. DevCell 18: 463-471


Tian H, Jia Y, Niu T, Yu Q, Ding Z (2014) The key players of the primary root growth and development also function in lateral roots inArabidopsis. Plant Cell Rep 33: 745-753


Timpte C, Wilson AK, Estelle M (1994) The axr2-1 mutation of Arabidopsis thaliana is a gain-of-function mutation that disrupts an earlystep in auxin response. Genetics 138: 1239-1249


Uehara T, Okushima Y, Mimura T, Tasaka M, Fukaki H (2008) Domain II mutations in CRANE/IAA18 suppress lateral root formation andaffect shoot development in Arabidopsis thaliana. Plant Cell Physiol 49: 1025-1038


Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural andhighly active synthetic auxin response elements. Plant Cell 9: 1963-1971


van den Berg C, Willemsen V, Hendriks G, Weisbeek P, Scheres B (1997) Short-range control of cell differentiation in the Arabidopsisroot meristem. Nature 390: 287-289


Van Norman JM, Zhang J, Cazzonelli CI, Pogson BJ, Harrison PJ, Bugg TD, Chan KX, Thompson AJ, Benfey PN (2014) Periodic rootbranching in Arabidopsis requires synthesis of an uncharacterized carotenoid derivative. Proc Natl Acad Sci USA 111: E1300-E1309


Verkest A, Manes CO, Vercruysse S, Maes S, Van Der Schueren E, Beeckman T, Genschik P, Kuiper M, Inzé D, De Veylder L (2005) Thecyclin-dependent kinase inhibitor KRP2 controls the onset of the endoreduplication cycle during Arabidopsis leaf developmentthrough Inhibition of mitotic CDKA;1 kinase complexes. Plant Cell 17: 1723-1736



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Welch D, Hassan H, Blilou I, Immink R, Heidstra R, Scheres B (2007) Arabidopsis JACKDAW and MAGPIE zinc finger proteins delimitasymmetric cell division and stabilize tissue boundaries by restricting SHORT-ROOT action. Genes Dev 21: 2196-2204


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http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang Y%2C Jiao Y%2C Liu Z%2C Zhu YX %282015%29 ROW1 maintains quiescent centre identity by confining WOX5 expression to specific cells%2E Nat Commun 6%3A 6003&dopt=abstract

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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=ROW1 maintains quiescent centre identity by confining WOX5 expression to specific cells.&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=ROW1 maintains quiescent centre identity by confining WOX5 expression to specific cells.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Z�rcher E%2C M�ller B %282016%29 Cytokinin synthesis%2C signaling%2C and function %2D Advances and new insights%2E Int Rev Cell Mol Biol 324%3A 1%2D38&dopt=abstract

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