Regulation of strigolactone biosynthesis by gibberellin ... · PDF file2 Regulation of strigolactone biosynthesis by gibberellin signaling ... 108 step in GA signaling ... One approache

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Title 1

Regulation of strigolactone biosynthesis by gibberellin signaling 2

3

Corresponding author 4

Tadao Asami 5

Department of Applied Biological Chemistry, The University of Tokyo, 1-1-1 6

Yayoi, Bunkyo, Tokyo 113-8657, Japan 7

Phone, +81-3-5841-5157 8

FAX, +81-3-5841-8025 9

E-mail address: [email protected] 10

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Authors 12

Shinsaku Ito1,2,*, Daichi Yamagami2,*, Mikihisa Umehara3, Atsushi Hanada4, 13

Satoko Yoshida5,6, Yasuyuki Sasaki1, Shunsuke Yajima1, Junko Kyozuka7, 14

Miyako Ueguchi-Tanaka8, Makoto Matsuoka8, Ken Shirasu5, Shinjiro 15

Yamaguchi4, Tadao Asami2,9,10 16

17

Author addresses 18

1 Department of Bioscience, Faculty of Applied Bioscience, Tokyo University 19

of Agriculture, 1-1-1 Sakuragaoka, Setagaya, Tokyo 156-8502, Japan 20

2 Department of Applied Biological Chemistry, The University of Tokyo, 1-1-1 21

Yayoi, Bunkyo, Tokyo 113-8657, Japan 22

3 Department of Applied Biosciences, Faculty of Life Sciences, Toyo 23

Plant Physiology Preview. Published on April 12, 2017, as DOI:10.1104/pp.17.00301

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University, Ora-gun, Gunma 374-0193, Japan 24

4 Graduate School of Life Sciences, Tohoku University, Katahira 2-1-1, 25

Aoba-ku, Sendai 980-8577, Japan 26

5 RIKEN Center for Sustainable Resource Science, 1-7-22 Suehirocho, 27

Tsurumi, Yokohama 230-0045, Japan 28

6 Graduate School of Biological Sciences, Nara Institute of Science and 29

Technology, 8916-5 Takayama-cho, Ikoma, Nara, 630-0192, Japan 30

7 Department of Agricultural and Environmental Biology, The University of 31

Tokyo, 1-1-1 Yayoi, Bunkyo, Tokyo 113-8657 Japan 32

8 Bioscience and Biotechnology Center, Nagoya University, Nagoya 464-8601, 33

Japan 34

9 JST, CREST, Saitama, Japan 35

10 Department of Biochemistry, King Abdulaziz University, Jeddah, Saudi 36

Arabia 37

*These authors contributed equally to this work. 38

39

Author Contributions 40

S.I. and D.Y. performed and analyzed most of the experiments; S.I., M.U. and 41

A.H. carried out LC-MS/MS analysis; Sa.Y. and K.S. designed and performed 42

Striga infection assay; Y.S, Shu.Y, J.K., M.UT., M.M., K.S. and Shi.Y. 43

contributed to the experiment design. T.A. directed the project and designed 44

the experiments. S.I. and T.A. wrote the manuscript. 45

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3

Funding information 47

This work was supported in part by grants from the Core Research for Evolutional 48

Science and Technology (CREST) (T. A.) and The Science and Technology 49

Research Promotion Program for Agriculture, Fisheries and Food Industry (T. 50

A.). 51

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4

Abstract 53

Strigolactones (SLs) are a class of plant hormones that regulate diverse 54

physiological processes, including shoot branching and root development. 55

They also act as rhizosphere signaling molecules to stimulate the 56

germination of root parasitic weeds and the branching of arbuscular 57

mycorrhizal fungi. Although various types of cross-talk between SLs and 58

other hormones have been reported in physiological analyses, the cross-talk 59

between gibberellin (GA) and SLs is poorly understood. We screened for 60

chemicals that regulate the level of SLs in rice and identified GA as a novel 61

SL-regulating molecule. The regulation of SL biosynthesis by GA is 62

dependent on the GA receptor GID1 and F-box protein GID2. GA treatment 63

also reduced the infection of rice plants by the parasitic plant Striga. These 64

data not only demonstrate the novel plant hormone cross-talk between SL 65

and GA, but also suggest that GA can be used to control parasitic weed 66

infections. 67

68

Keywords 69

Strigolactone, Root parasitic weed, Rice, Gibberellin, Hormone interaction 70

71

Abbreviations 72

SL, strigolactone; GA, gibberellin A; epi-5DS, 2′-epi-5-deoxystrigol; LC–73

MS/MS, liquid chromatography–tandem mass spectrometry 74

75



5

Introduction 76

Strigolactones (SLs) are a group of terpenoid lactones that regulate shoot 77

branching outgrowth and root development in various plant species 78

(Gomez-Roldan et al., 2008, Umehara et al., 2008, Koltai et al., 2011a, 79

Ruyter-Spira et al., 2011, Seto et al., 2012). SLs are also exuded from roots 80

into the rhizosphere as signaling molecules that stimulate the germination 81

of root parasitic weeds and the branching of arbuscular mycorrhizal fungi 82

(Cook et al., 1966, Akiyama et al., 2005). At present, two carotenoid cleavage 83

dioxygenases (D10 and D17), a carotenoid isomerase (D27), and 84

Os01g0700900 (Os0900) and Os01g0701400 (Os1400) are known to be 85

involved in the biosynthesis of SLs in rice (Lin et al., 2009, Cardoso et al., 86

2014, Zhang et al 2014, Seto et al., 2014, Abe et al., 2014). The activities of 87

SLs depend on D3 and D14: D3 encodes the F-box protein and D14 encodes 88

SL receptor, which act in SL signaling. D53, which encodes a substrate of the 89

SCFD3 complex, was recently reported to be a repressor of SL signaling in 90

rice, and the degradation of D53 protein by SL, in cooperation with D14 and 91

D3, is considered as a key event in SL signaling (Jiang et al., 2013, Zhou et 92

al., 2013, Yao et al., 2016, de Saint Germain et al., 2016). 93

Gibberellin A (GA) is a plant hormone that regulates many aspects 94

of plant growth and development during the life cycle of plants (Yamaguchi 95

et al. 2008). Plants defective in GA biosynthesis or signaling show 96

characteristic phenotypes, including dwarfism, small dark green leaves, 97

prolonged germination dormancy, root growth retardation, suppression of 98



6

flowering, reduced seed production, and male sterility (Yamaguchi et al. 99

2008). Several factors involved in GA perception have been identified. In rice, 100

GA binds to the GA receptor called ‘GID1’, and GA binding promotes the 101

interaction between GID1 and the transcriptional repressor DELLA protein, 102

called ‘SLR1’. GA-induced interaction of GID1 and SLR1 triggers the 103

ubiquitination of SLR1 by the GID2 F-box protein, one of the components of 104

an SCF-type E3 ubiquitin ligase that degrades SLR1 through the 26S 105

proteasomal pathway (Ueguchi-Tanaka et al., 2005, Sasaki et al., 2003). 106

GA-dependent loss of the repressor activity of DELLA is considered a key 107

step in GA signaling (Ueguchi-Tanaka et al., 2008). 108

Root parasitic weeds, such as Orobanche spp. and Striga spp., are 109

harmful plants in sub-Saharan Africa, the Middle East, and Asia which 110

maintain seed dormancy in the absence of host plant (Spallek et al., 2013). 111

The germination mechanisms of Orobanche and Striga spp. are very similar. 112

Both species require germination stimulants released from the host plant. 113

SLs are the major group of germination stimulants effective for almost all 114

Orobanche and Striga spp. It has been reported that around 300 million 115

people are affected economically by Striga spp. in Africa, with estimated 116

losses of $US 7 billions (Parker, 2009). Although many approaches to 117

controlling these parasitic weeds have been explored, their success has been 118

limited. One approache is the method called as suicidal germination that 119

induces the germination of the parasites’ seeds in the absence of the host 120

plants, because Striga and Orobanche spp. are obligate parasites. However, 121



7

this approach is not cost-effective for controlling these weeds expanded in 122

large area. 123

There is some cross-talk between SLs and various hormones. For 124

example, auxin which regulates shoot branching and root morphology, acts 125

both up- and downstream from SL signaling, in secondary growth and root 126

hair elongation, respectively (Agusti et al., 2011, Koltai et al., 2011a). SL also 127

inhibits auxin transport by reducing the accumulation of auxin efflux carrier 128

component 1 (PIN1) in xylem parenchyma cells (Crawford et al., 2010). 129

Ethylene also affects root hair elongation by exerting epistatic effects on SLs 130

(Kapulnik et al., 2011). Two reports have also directly demonstrated an 131

interaction between SL and hormonal signaling. Wang et al. showed an 132

interaction between the SL and brassinosteriod signaling pathways. BES1, 133

an important transcriptional regulator in the brassinosteroid signaling 134

pathway, interacts with MAX2, which is the ortholog of rice D3, and BES1 135

degradation is accelerated by SLs in Arabidopsis (Wang et al., 2013). 136

Nakamura et al. reported an SL-dependent interaction between D14 and 137

SLR1 in rice (Nakamura et al., 2013). This data suggests the existence of 138

cross-talk between the GA and SL signaling pathways. However, 139

contradicting result has been reported that SLs act independently of GAs in 140

stimulating internode elongation in the pea (de Saint Germain et al., 2013). 141

Therefore, there is as yet no physiological evidence of the existence of 142

cross-talk between the GA and SL signaling pathways, although Lo et al. 143

reported that GA deficiency promotes tiller bud elongation in rice (Lo et al., 144



8

2008). 145

To identify a novel regulator of SL biosynthesis that controls the 146

germination of root parasitic weeds in this study, we screened for chemicals 147

that regulate SL biosynthesis. We found that GA is a regulator of SL 148

biosynthesis, and that GA signaling controls the biosynthesis of SL by 149

regulating the expression of SL biosynthesis genes. Moreover, GA-treated 150

rice showed reduced Striga infection. Therefore, we demonstrate the 151

cross-talk between the GA and SL signaling pathways for the first time, and 152

also present new insight into the management of root parasitic weeds. 153

154

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9

Results 156

157

GAs regulate SL biosynthesis 158

159

Because root parasitic weeds such as Striga and Orobanche germinate in 160

response to SL in a concentration-dependent manner, low-SL-producing 161

plants can be resistant to infection by these weeds (Jamil et al., 2012). In an 162

attempt to find a novel SL biosynthesis regulator, we screened several 163

chemicals, including plant hormones, plant growth regulators, and triazole 164

derivatives previously constructed in our laboratory (Min et al., 1999, 165

Sekimata et al., 2001, 2002). To evaluate their ability to regulate SL 166

biosynthesis, we analyzed the levels of 2’-epi-5-deoxystriol (epi-5DS), an 167

endogenous SL in rice, in root exudates, using liquid chromatography–168

tandem mass spectroscopy (LC–MS/MS). Because the SL levels in the root 169

exudates of rice seedlings are elevated when inorganic phosphate is depleted 170

in the medium (Umehara et al., 2008), we examined the effects of these 171

chemical treatments on SL levels under phosphate-deficient conditions. With 172

screening, we identified a plant hormone, GA3, that strongly reduced the 173

levels of epi-5DS in the root exudates (Fig. 1A). Another SL (orobanchol) in 174

the root exudates was nearly undetectable in the GA3-treated rice (Fig. 1B). 175

The application of a GA biosynthesis inhibitor (1 µM uniconazole-P or 1 µM 176

paclobutrazol) also slightly increased the levels of epi-5DS (Fig. 1A). To 177

exclude the possibility that GA3 inhibits SL export and reduces the levels of 178



10

epi-5DS in root exudates, we analyzed the endogenous epi-5DS levels in rice 179

roots. Our data clearly indicate that GA3 strongly and dose-dependently 180

reduces the levels of epi-5DS in both roots and root exudates in a 181

concentration range of 0.1–10 nM (Fig. 1C). Moreover, the reduced levels of 182

epi-5DS in a GA3-treated Lotus japonicus root cell culture suggested that 183

GA3 also reduces the levels of SL in in vitro culture systems and other plant 184

species (Supplemental Fig. S1). 185

Many GAs are present in plants. In many cases, the intensity of GA 186



11

responses is dependent on GA-GID1 binding affinity (Ueguchi-Tanaka et al., 187

2005). To examine the effects of various GAs on SL production, we analyzed 188

the levels of epi-5DS in rice treated with active (GA1, GA3 and GA4) or 189

inactive (GA8) GAs. The effects of GAs on SL production were generally 190

consistent with the physiological activities of each GA (Fig. 1D; Nishijima et 191

al., 1994). These results indicate that bioactive GAs reduce SL production. 192

193

Regulation of SL biosynthesis via a GID-DELLA signaling pathway 194

195

To investigate the mechanism underlying the regulation of SL biosynthesis 196

by GA, the levels of epi-5DS were measured in the roots and root exudates of 197

mutants defective in GA biosynthesis or signaling, with LC–MS/MS (Fig. 2). 198

In the GA biosynthesis mutant, Tanginbozu, which shows a semidwarf 199

phenotype, elevated levels of epi-5DS were detected in the roots and root 200

exudates, and were suppressed after GA treatment (Fig. 2A). In 201

GA-insensitive mutants gid1-3 and gid2-2, the level of epi-5DS did not 202

change after GA treatment (Ueguchi-Tanaka et al., 2005, Sasaki et al., 2003). 203

The level of epi-5DS was also higher in the gid2-2 mutant than in wild-type 204

seedlings (Fig. 2B). SLR1 is a repressor of GA signaling and most GA-related 205

responses are induced by the degradation of SLR1. One SLR1 mutants, 206

slr1-5, is a constitutive GA response mutant. epi-5DS was undetectable in 207

the roots and root exudates of the slr1-5 mutant (Fig. 2C). These results 208

suggest that the regulation of SL production by GAs is caused by a 209



12

GID-DELLA signaling pathway. 210

SL biosynthesis is tightly controlled by endogenous SL levels 211

through the negative feedback regulation of D10 and D17 expression 212

(Umehara et al., 2008). To determine whether the regulation of SL 213

production by GAs depends on SL signaling, we tested the effects of GA on 214

SL levels in an SL signaling mutant. Although the epi-5DS levels were 215



13

higher in the loss of function mutants in SL signaling (d3-1 and d14-1) than 216

in the WT, presumably as a consequence of the feedback regulation of the SL 217

pathway, GA3 reduced the levels of epi-5DS in both roots and root exudates 218

(Fig. 3). These results indicate that the pathway through which GA3 219

regulates SL biosynthesis is independent of D3 and D14. 220

We used a quantitative reverse transcription PCR (qRT–PCR) 221

analysis of the SL biosynthesis genes to clarify the mechanism underlying 222

the regulation of SL biosynthesis by GA signaling (Fig. 4A). SLs are 223



14

synthesized by OsD27, OsD10, OsD17, Os0900, and Os1400 in rice (Alder et 224

al., 2012, Zhang et al., 2014, Supplemental Fig. S2). Our qRT–PCR analysis 225



15

revealed that treatment with GA3 for 24 h reduced these transcript levels in 226

the WT roots (Fig. 4B). A time-course analysis of the SL biosynthesis genes 227

was performed in roots exposed to 50 nM GA3 for 0–24 h. All of the genes 228

tested here showed similar expression patterns (Fig. 4C). In the control roots, 229

the transcripts increased until 24 h, but remained low in the GA3-treated 230

roots. This result suggests two possibilities: one is that GA treatment 231

reduces transcript levels of SL biosynthesis genes, and the other is GA 232

suppresses the up-regulation of SL biosynthesis genes and maintains the 233

transcription at basal level. To clarify these hypotheses, we performed the 234

expression analysis of SL biosynthesis genes in the time course shown in 235

Supplemental Fig. S3A. The transcript levels of SL biosynthesis genes were 236

reduced by GA treatment (Supplemental Fig. S3B). This result indicates GA 237

down-regulates SL production through mediating the expression levels of SL 238

biosynthesis genes. Next, we estimated the effects of a protein synthesis 239

inhibitor, cycloheximide (CHX), on the regulation of SL biosynthesis by GA 240

signaling. As mentioned above, treatment with 50 nM GA3 reduced the 241

transcript levels of the SL biosynthesis genes. On the other hand, CHX 242

abolished the repression by GA on the transcript levels in comparison with 243

the control (Fig. 4C). These results imply that the regulation of SL levels by 244

GA signaling is attributable to the altered expression of the SL biosynthetic 245

genes via de novo protein synthesis. 246

247

Effects of SL treatment on GA deficient mutant 248



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249

GA-deficient mutants show increased tiller bud outgrowth and 250

dwarfism (Lo et al., 2008, Ito et al., 2010). To evaluate the effects of SL on 251

GA-deficient rice, we used the GA-deficient mutant Tanginbozu. Tanginbozu 252

displays dwarfism and greater tiller outgrowth in 5-week-old seedlings than 253

the WT (Ginbozu) (Supplemental Fig. S4), although the length of the second 254

tiller buds of Tanginbozu did not differ from that of Ginbozu in 2-week-old 255

seedlings (Fig. 5). The length of the second tiller was suppressed in Ginbozu 256

by the application of 2 µM GR24, a synthetic SL analog, whereas no response 257

was observed in the length of the second tiller bud of Tanginbozu. Plant 258

height did not differ between the control and the GR24-treated plants of 259

either Ginbozu or Tanginbozu. This result suggests that GA is required for 260

the regulation of tiller bud outgrowth by SL. 261

262

GA-treated rice is infected by fewer Striga plants 263

264

We have demonstrated that GA regulates SL biosynthesis. To explore the 265

effects of GA treatment on the interaction of plants with root parasitic weeds, 266

we performed Striga germination and infection assays. Consistent with the 267

results of the epi-5DS level in GA-treated rice, the root exudates of rice 268

seedlings treated with 50 nM GA contained less germination-stimulating 269

activity than those of the control plants (Fig. 6A). Moreover, fewer seeds 270

germinated in the vicinity of the roots of 100 nM GA-treated rice than in the 271



17

vicinity of the control roots (Fig. 6B). As a result of the reduced germination 272

frequency, statistically fewer Striga established parasitism on the 100 nM 273

GA-treated rice. When germinated Striga seeds that had been stimulated 274

with Strigol were incubated with 100 nM GA-treated rice, there was no 275

significant difference in the frequency of successful parasitism between the 276

control and 100 nM GA-treated rice plants (Fig. 6C). This result indicates 277

that GA treatment does not affect the infectious processes except for 278

germination process. 279

280

281



18

Discussion 282

SLs are important phytohormones required for plant growth and 283

development. Because SLs are known to be involved in the regulation of 284

diverse physiological phenomena, including shoot branching, root 285

development, and leaf senescence, they are thought to be involved in 286

physiological interactions with various hormones and environmental cues 287

(Crawford et al., 2010, Dun et al., 2012, Kapulnik et al., 2011, Ha et al., 2014, 288

de Jong et al., 2014, Mayzlish-Gati et al., 2012, Tsuchiya et al., 2010). 289

However, the physiological cross-talk between SL and GA has not been 290

determined, despite their molecular interaction, in which the putative SL 291

receptor, D14, interacts with the GA signaling repressor, SLR1 (Nakamura 292



19

et al., 2013). Here, we provide evidence of the interaction between these two 293

hormones, by showing that GA signaling regulates SL biosynthesis. 294

GA signaling negatively regulates the endogenous levels of SLs. 295

Importantly, the application of an inactive GA metabolite (GA8) to WT plants 296

or active GA to GA signaling mutants (gid1-3 and gid2-2) did not induce this 297

regulation, whereas the application of active GA to the WT and a GA 298

biosynthesis mutant (Tanginbozu) reduced their levels of SLs (Figs 1 and 2). 299

We also detected no SL in a constitutive GA response mutant (slr1-5). These 300

results indicate that the regulation of endogenous SL level by GA signaling 301

depends on the activity of the DELLA protein. The repressive activity of GA 302

on SL biosynthesis did not correlate with the binding activity of GA to GID1 303

(Fig. 1D; Ueguchi-Tanaka et al, 2005). GA4 shows the highest affinity for 304

GID1. However, whereas GA1 and GA4 are inactivated by GA 2-oxidase in 305

plants, GA3 is not oxidized by GA 2-oxidase (Nakayama et al., 1990). These 306

facts explain the inconsistency between the repressive activity on SL 307

biosynthesis and the binding activity on GID1. The increased levels of SL in 308

gid2-2 are similar to those in Tanginbozu, suggesting that a reduction in GA 309

signaling induces an increase in the level of SLs. Interestingly, however, the 310

level of SL was lower in the gid1-3 mutant than in the WT (Fig. 2A and B), 311

whereas both the gid1-3 and gid2-2 mutants were insensitive to GA and had 312

similar phenotypes. These data suggest that a GID1-independent GA 313

signaling pathway could be present, similar to the GID2-independent GA 314

signaling pathway reported by Ueguchi-Tanaka et al. (2008), although this 315



20

regulatory mechanism is still unclear. Alternatively, as GID1 and D14 316

competitively binds to SLR1, by the loss of function of GID1 binding to GA 317

D14 can become to dominantly bind to SLR1 and suppress SLR1 function. As 318

a result in gid1 mutant 5DS level decrease could be due to feedback 319

regulation similar to in slr1 mutant. 320

SL biosynthesis is positively and negatively regulated by various 321

hormones and environmental cues (Yoneyama et al., 2007a, Yoneyama et al., 322

2007b, Hayward et al., 2009, Koltai et al., 2011b, López-Ráez et al., 2010). 323

Phosphate is a negative regulator of SL biosynthesis and its regulatory 324

activity alters the expression of the SL biosynthetic genes (Umehara et al., 325

2010). A previous gene expression analysis indicated that phosphate 326

deficiency increased the transcription levels of D10, D17, D27, Os0900, 327

Os01g0701500, and Os02g0221900 (Umehara et al., 2010), whereas GA 328

signaling regulated the expression of the Os1400 gene, as well as D10, D17, 329

D27, and Os0900 (Fig. 2). These results suggest that GA signaling regulates 330

the expression of the SL biosynthesis genes through a different pathway 331

from phosphate signaling. However, CHX treatment reduced the 332

transcription level of Os1400, while the other SL biosynthesis genes (D10, 333

D17, D27 and Os0900) were hardly affected by CHX treatment, suggesting 334

that the regulatory mechanisms of Os1400 expression by GA signaling was 335

different from those of the other SL biosynthesis genes. 336

In the time-course experiment, the expression levels of SL 337

biosynthesis genes were increased at 24 h (Fig. 4C). We did not exchange 338



21

hydroponic culture media from day 7 to day 13 and transferred rice seedlings 339

into fresh media at day 13 (Fig. 4A). Removal of the accumulated SLs from 340

media might lead the up-regulation of SL biosynthesis genes. 341

Tanginbozu showed GR24 insensitive phenotype in tiller bud length 342

(Fig. 5). In Tanginbozu, endogenous level of epi-5DS was higher than that in 343

Ginbozu (Fig. 2A). In addition, d10-1 mutant is more sensitive to GR24 than 344

WT (Umahara et al., 2008). Therefore, the result that Tanginbozu displayed 345

GR24 insensitive phenotype, suggests the possibility that SL signal is 346

saturated with the accumulated SL in Tanginbozu. However, the 347

overexpression of GA 2-oxidase also positively regulated the number of tillers, 348

indicating the importance of GA signaling in shoot outgrowth in rice (Lo et 349

al., 2008). Further physiological studies may contribute to the elucidation of 350

the mechanism of shoot outgrowth. 351

In many parts of the world, Striga and Orobanche are serious 352

agricultural pests. Reducing SL biosynthesis is one way to control these 353

pests and low-SL-producing plants are actually resistant to root parasitic 354

weed infections (Jamil et al., 2012, Umehara et al., 2008). In this study, we 355

have shown that GA-treated rice was infected by fewer Striga plants than 356

the control rice, at least under experimental conditions. Therefore, 357

tissue-specific modification of GA signaling can be used to control root 358

parasitic weed infection. 359

360

Materials and methods 361



22

362

Plant material 363

364

The wild-type rice varieties used in this study were Shiokari (d3-1 and 365

d10-1) (Ishikawa et al., 2005), Nipponbare (d10-2) (Arite et al., 2007), 366

Taichung 65 (slr1-5, gid1-3, and gid2-2) (Ueguchi-Tanaka et al., 2008), and 367

Ginbozu (Tanginbozu) (Itoh et al., 2004). 368

369

Growth conditions 370

371

Rice seedlings were grown hydroponically as described previously (Umehara 372

et al., 2008). Surface-sterilized rice seeds were incubated in sterile water at 373

25 °C for 2 days in the dark. For the analysis of SL, germinated seeds were 374

transferred into hydroponic culture medium (Kamachi et al., 1991) solidified 375

with 0.7% agar and cultured at 25 °C for 6 days under fluorescent white light 376

with a photoperiod of 14 h light/10 h dark. Each seedling was transferred to 377

a glass vial containing 12 mL of sterilized hydroponic culture solution and 378

grown under the same conditions for 6 days. The seedlings were then 379

transferred to a new glass vial containing the culture solution, with or 380

without chemicals, for 1 day. For the tillering experiment, the germinated 381

seeds were transferred into hydroponic culture medium with 0.7% agar, with 382

or without chemicals, under the same conditions. Each seedling was 383

transferred to a new identical vial with or without chemicals. The 384



23

hydroponic solution was refreshed every 3 days. 385

386

LC–MS/MS analysis 387

388

The SL analysis was performed according to a previously described method 389

(Umehara et al., 2008). Briefly, the hydroponic culture medium was 390

extracted twice with ethyl acetate after the addition of d6-epi-5DS (200 pg) as 391

the internal standard. The organic layer was dried and dissolved in 1 mL of 392

ethyl acetate:n-hexane (15:85). The solutions were loaded onto a Sep-Pak 393

silica 1 mL cartridge (Waters, Milford, MA, USA), washed twice with the 394

same solution, eluted three times with ethyl acetate:n-hexane (35:65), and 395

concentrated in vacuo. The roots were homogenized in acetone containing 396

d6-epi-5DS. The filtrates were dried and dissolved in water. The solutions 397

were extracted twice with ethyl acetate, dried, and dissolved in 10% acetone. 398

The extracts were loaded onto Oasis HLB 3 mL cartridges (Waters), washed 399

twice with water, eluted twice with acetone, and dried in vacuo. The 400

concentrates were dissolved in 1 mL of ethyl acetate:n-hexane (15:85) and 401

loaded onto Sep-Pak silica 1 mL cartridges, washed, eluted, and 402

concentrated in the same way. 403

The SL-containing fractions were dissolved in 50% acetonitrile and 404

subjected to an LC–MS/MS analysis in a system consisting of a 405

quadruple/time-of-flight tandem mass spectrometer (Triple TOF 5600 406

system; AB Sciex, Framingham, MA, USA) and an ultra-high-performance 407



24

liquid chromatograph (Nexera; Shimadzu, Kyoto, Japan) equipped with a 408

reversed-phase column (Acquity UPLC BEH-C18, 2.1 × 50 mm, 1.7 μm; 409

Waters). The mobile phase was changed from 30% acetonitrile containing 410

0.05% acetic acid to 40% acetonitrile at 5 min and to 70% acetonitrile at 10 411

min after injection, at a flow rate of 0.2 mL/min. The parent ions (m/z) were 412

331.2 for unlabeled epi-5DS, 337.2 for labeled epi-5DS, and 347.2 for 413

orobanchol. The samples were quantified using fragment ions 234.13 for 414

epi-5DS and 240.13 for d6-epi-5DS. 415

416

Striga germination and infection assays 417

418

The Striga germination and infection assays were performed as described by 419

Sugimoto et al. (2008) and Umehara et al. (2008), respectively. For the 420

infection assay, 1-week-old rice seedlings were transferred to root-observing 421

rhizotron chambers (140 mm × 100 mm square petri dishes filled with 422

rockwool and nylon mesh) supplied with 50 mL of nutrient solution with low 423

phosphate (1mM NH4NO3, 0.06 mM NaH2PO4, 0.3 mM K2SO4, 0.3 mM CaCl2, 424

0.4 mM MgCl2, 45 µM Fe-EDTA with micro-nutrients) (Makino et al., 1983) 425

with or without GA3, and grown for 2 weeks in a greenhouse with a 12:12 h 426

photoperiod (170–450 µmol/m2/s) with a day/night temperature cycle of 427

28 °C/20 °C. The Striga seeds were preconditioned on moist glass-fiber filter 428

papers (GF/A; Whatman, United Kingdom) at 26 °C in the dark for 2 weeks, 429

and treated with or without 10 nM strigol for 5 h in the dark. After they were 430



25

rinsed with excess water, approximately 50 parasite seeds were carefully 431

placed along the rice roots and the rhizotrons were incubated under the 432

growth conditions described above. The germination, infection, and 433

developmental status of the Striga plants were evaluated after cocultivation 434

for 4 weeks (Yoshida et al., 2009). 435

436

Gene expression analysis 437

438

Total RNA was extracted from the roots using Plant RNA Purification 439

Reagents (Invitrogen, MA, USA). cDNA was synthesized with the 440

PrimeScript RT Reagent Kit with gDNA eraser (Takara Bio, Shiga, Japan). 441

qRT–PCR was performed on a Takara Thermal Cycler Dice Real Time 442

System using SYBR® Premix Ex Taq™ (Takara Bio). The specific primers 443

used for qRT–PCR are listed in the Supplemental Table. 444

445

SUPPLEMENTAL DATA 446

Supplemental Table. List of Primers 447

Supplemental Figure 1. Effect of GA3 on SL levels of lotus japonicas root 448

culture. 449

Supplemental Figure 2. SL biosynthesis pathway in rice. 450

Supplemental Figure 3. Effects of GA on transcript levels of SL biosynthesis 451

genes in roots. 452

Supplemental Figure 4. Tiller number and plant height of GA biosynthesis 453



26

mutant (Tanginbozu). 454

455

Figure Legends 456

457

Fig. 1 458

Effects of GA on SL levels in 2-week-old rice. 459

A, Epi-5DS levels in root exudate of rice treated with GA3 and a GA 460

biosynthesis inhibitor, detected with LC–MS/MS. B, Monitoring selected ions 461

for orobanchol. Upper and lower panels show the chromatograms for the 462

control and 10 nM GA3-treated root exudates, respectively. C, Epi-5DS levels 463

in root exudates (upper) and roots (lower) of GA3-treated rice, determined 464

with LC–MS/MS. D, Epi-5DS levels in root exudates (upper) and roots 465

(lower) of rice treated with various GAs, determined with LC–MS/MS. 466

Thirteen-day-old rice seedlings were treated for 1 day with chemicals. Data 467

are means ± SD (n = 3). Uni: 1 µM unicaonazole-P; Pac: 1 µM pacrobutrazol; 468

GA3: 10 nM GA3. 469

470

Fig. 2 471

Effects of GA on SL levels in GA biosynthesis and signaling mutants. 472

Epi-5DS levels in root exudates (upper) and roots (lower) of GA3-treated rice, 473

determined with LC–MS/MS. A, GA biosynthesis mutant (Tanginbozu), Gin: 474

Ginbozu, Tan: Tanginbozu, B, GA signaling mutants (gid1 and gid2). C, 475

Constitutive GA signaling mutant (slr1-5). Thirteen-day-old rice seedlings 476



27

were treated for 1 day with GA3. Data are means ± SD (n = 3). 477

478

Fig. 3 479

Effects of GA on SL levels in SL signaling mutants. 480

Epi-5DS levels in root exudates (upper) and roots (lower) of the d3-1 (left) 481

and d14-1 (right) mutants, determined with LC–MS/MS. Thirteen-day-old 482

rice seedlings were treated for 1 day with GA3. Data are means ± SD (n = 3). 483

484

Fig. 4 485

Effects of GA on transcript levels of SL biosynthesis genes in roots. 486

A, Schematic diagram showing the experimental conditions. Orange bar 487

indicates a hydroponic culture without phosphate. B, Transcript levels of SL 488

biosynthesis genes in GA-treated rice roots. C, Time course analysis of the 489

expression of SL biosynthesis genes after treatment with 50 nM GA3. D, 490

Effect of protein synthesis inhibitor (CHX) on the expression levels of SL 491

biosynthesis genes after treatment with 50 nM GA3. Thirteen-day-old rice 492

seedlings were transferred to new vials containg fresh media with or without 493

chemicals for 1 day (B and D) or the indicated times (C). Data are means ± 494

SD (n = 3). * and ** indicate signify differences from 0 nM GA3-treated 495

plants (t-test, P < 0.05 and P < 0.01, respectively) 496

497

Fig. 5 498

499



28

Effects of GR24 on tiller bud growth in GA biosynthesis mutant. 500

Second tiller length and plant height in 2-week-old rice. Data are means ± 501

SD (n = 6). White arrowheads indicate second tillers. Scale bar: 1 cm. 502

503

Fig. 6 504

Effects of GA on Striga germination and infection. 505

A, Striga germination rate after treatment with culture medium. DW: 506

distilled water; GR24: 1 µM GR24; CE: culture medium for 0 nM GA3-treated 507

rice; GE: culture medium for 100 nM GA3-treated rice. Data are means ± SD 508

(n = 3). B and C, Ratio of Striga plants at each developmental stage 3 week 509

after the inoculation of SL-treated (C) or untreated seeds (B). Concentrations 510

in B and C indicate the GA concentrations of GA-treated rice. Data are 511

means ± SD; B, n = 8–10; C, n = 2–3. D: died after penetration; LD: leaf 512

developed after the establishment of parasitism; SC: penetration successful 513

and seed coat remained attached; NG: no germination. * and ** indicate 514

significantly different from untreated rice (t-test, P < 0.05 and P < 0.01, 515

respectively). 516

517

518

519

520

521

522



29

523

524

525



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Agusti J, Herold S, Schwarz M, Sanchez P, Ljung K, Dun EA, Brewer PB, Beveridge CA, Sieberer T, Sehr EM, Greb T (2011)Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc Natl Acad Sci U S A 108:20242-20247


Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature435: 824-827


Alder A, Jamil M, Marzorati M, Bruno M, Vermathen M, Bigler P, Ghisla S, Bouwmeester H, Beyer P, Al-Babili S (2012) The pathfrom ß-carotene to carlactone, a strigolactone-like plant hormone. Science 335: 1348-1351


Arite T, Iwata H, Ohshima K, Maekawa M, Nakajima M, Kojima M, Sakakibara H, Kyozuka J (2007) DWARF10, an RMS1/MAX4/DAD1ortholog, controls lateral bud outgrowth in rice. Plant J 51: 1019-1029


Cardoso C, Zhang Y, Jamil M, Hepworth J, Charnikhova T, Dimkpa SO, Meharg C, Wright MH, Liu J, Meng X, Wang Y, Li J,McCouch SR, Leyser O, Price AH, Bouwmeester HJ, Ruyter-Spira C (2014) Natural variation of rice strigolactone biosynthesis isassociated with the deletion of two MAX1 orthologs. Proc Natl Acad Sci U S A 111: 2379-2384


Cook CE, Whichard LP, Turner B, Wall ME, Egley GH (1966) Germination of Witchweed (Striga lutea Lour.): Isolation and Propertiesof a Potent Stimulant. Science 154: 1189-1190


Crawford S, Shinohara N, Sieberer T, Williamson L, George G, Hepworth J, Müller D, Domagalska MA, Leyser O (2010)Strigolactones enhance competition between shoot branches by dampening auxin transport. Development 137: 2905-2913


de Jong M, George G, Ongaro V, Williamson L, Willetts B, Ljung K, McCulloch H, Leyser O (2014) Auxin and strigolactone signalingare required for modulation of Arabidopsis shoot branching by nitrogen supply. Plant Physiol 166: 384-395


de Saint Germain A, Clavé G, Badet-Denisot MA, Pillot JP, Cornu D, Le Caer JP, Burger M, Pelissier F, Retailleau P, Turnbull C,Bonhomme S, Chory J, Rameau C, Boyer FD (2016) An histidine covalent receptor and butenolide complex mediates strigolactoneperception. Nat Chem Biol 12: 787-794


de Saint Germain A, Ligerot Y, Dun EA, Pillot JP, Ross JJ, Beveridge CA, Rameau C (2013) Strigolactones stimulate internodeelongation independently of gibberellins. Plant Physiol 163: 1012-1025


Dun EA, de Saint Germain A, Rameau C, Beveridge CA (2012) Antagonistic action of strigolactone and cytokinin in bud outgrowthcontrol. Plant Physiol 158: 487-498


Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagès V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, www.plantphysiol.orgon May 15, 2018 - Published by Downloaded from

Copyright © 2017 American Society of Plant Biologists. All rights reserved.

http://www.ncbi.nlm.nih.gov/pubmed?term=Abe S%2C Sado A%2C Tanaka K%2C Kisugi T%2C Asami K%2C Ota S%2C Kim HI%2C Yoneyama K%2C Xie X%2C Ohnishi T%2C Seto Y%2C Yamaguchi S%2C Akiyama K%2C Nomura T %282014%29 Carlactone is converted to carlactonoic acid by MAX1 in Arabidopsis and its methyl ester can directly interact with AtD14 in vitro%2E Proc Natl Acad Sci U S A 111%3A 18084%2D18089&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Abe S, Sado A, Tanaka K, Kisugi T, Asami K, Ota S, Kim HI, Yoneyama K, Xie X, Ohnishi T, Seto Y, Yamaguchi S, Akiyama K, Nomura T (2014) Carlactone is converted to carlactonoic acid by MAX1 in Arabidopsis and its methyl ester can directly interact with AtD14 in vitro. Proc Natl Acad Sci U S A 111: 18084-18089

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

http://scholar.google.com/scholar?as_q=Carlactone is converted to carlactonoic acid by MAX1 in Arabidopsis and its methyl ester can directly interact with AtD14 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=Carlactone is converted to carlactonoic acid by MAX1 in Arabidopsis and its methyl ester can directly interact with AtD14 in vitro&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Abe&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Agusti J%2C Herold S%2C Schwarz M%2C Sanchez P%2C Ljung K%2C Dun EA%2C Brewer PB%2C Beveridge CA%2C Sieberer T%2C Sehr EM%2C Greb T %282011%29 Strigolactone signaling is required for auxin%2Ddependent stimulation of secondary growth in plants%2E Proc Natl Acad Sci U S A 108%3A 20242%2D20247&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Agusti J, Herold S, Schwarz M, Sanchez P, Ljung K, Dun EA, Brewer PB, Beveridge CA, Sieberer T, Sehr EM, Greb T (2011) Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc Natl Acad Sci U S A 108: 20242-20247

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

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http://www.ncbi.nlm.nih.gov/pubmed?term=Akiyama K%2C Matsuzaki K%2C Hayashi H %282005%29 Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi%2E Nature 435%3A 824%2D827&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435: 824-827

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http://scholar.google.com/scholar?as_q=Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Akiyama&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Alder A%2C Jamil M%2C Marzorati M%2C Bruno M%2C Vermathen M%2C Bigler P%2C Ghisla S%2C Bouwmeester H%2C Beyer P%2C Al%2DBabili S %282012%29 The path from �%2Dcarotene to carlactone%2C a strigolactone%2Dlike plant hormone%2E Science 335%3A 1348%2D1351&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Alder A, Jamil M, Marzorati M, Bruno M, Vermathen M, Bigler P, Ghisla S, Bouwmeester H, Beyer P, Al-Babili S (2012) The path from �-carotene to carlactone, a strigolactone-like plant hormone. Science 335: 1348-1351

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http://www.ncbi.nlm.nih.gov/pubmed?term=Arite T%2C Iwata H%2C Ohshima K%2C Maekawa M%2C Nakajima M%2C Kojima M%2C Sakakibara H%2C Kyozuka J %282007%29 DWARF10%2C an RMS1%2FMAX4%2FDAD1 ortholog%2C controls lateral bud outgrowth in rice%2E Plant J 51%3A 1019%2D1029&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Cardoso C%2C Zhang Y%2C Jamil M%2C Hepworth J%2C Charnikhova T%2C Dimkpa SO%2C Meharg C%2C Wright MH%2C Liu J%2C Meng X%2C Wang Y%2C Li J%2C McCouch SR%2C Leyser O%2C Price AH%2C Bouwmeester HJ%2C Ruyter%2DSpira C %282014%29 Natural variation of rice strigolactone biosynthesis is associated with the deletion of two MAX1 orthologs%2E Proc Natl Acad Sci U S A 111%3A 2379%2D2384&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Cardoso C, Zhang Y, Jamil M, Hepworth J, Charnikhova T, Dimkpa SO, Meharg C, Wright MH, Liu J, Meng X, Wang Y, Li J, McCouch SR, Leyser O, Price AH, Bouwmeester HJ, Ruyter-Spira C (2014) Natural variation of rice strigolactone biosynthesis is associated with the deletion of two MAX1 orthologs. Proc Natl Acad Sci U S A 111: 2379-2384

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http://www.ncbi.nlm.nih.gov/pubmed?term=Cook CE%2C Whichard LP%2C Turner B%2C Wall ME%2C Egley GH %281966%29 Germination of Witchweed %28Striga lutea Lour%2E%29%3A Isolation and Properties of a Potent Stimulant%2E Science 154%3A 1189%2D1190&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Cook CE, Whichard LP, Turner B, Wall ME, Egley GH (1966) Germination of Witchweed (Striga lutea Lour.): Isolation and Properties of a Potent Stimulant. Science 154: 1189-1190

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http://www.ncbi.nlm.nih.gov/pubmed?term=Crawford S%2C Shinohara N%2C Sieberer T%2C Williamson L%2C George G%2C Hepworth J%2C M�ller D%2C Domagalska MA%2C Leyser O %282010%29 Strigolactones enhance competition between shoot branches by dampening auxin transport%2E Development 137%3A 2905%2D2913&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Crawford S, Shinohara N, Sieberer T, Williamson L, George G, Hepworth J, M�ller D, Domagalska MA, Leyser O (2010) Strigolactones enhance competition between shoot branches by dampening auxin transport. Development 137: 2905-2913

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http://www.ncbi.nlm.nih.gov/pubmed?term=de Jong M%2C George G%2C Ongaro V%2C Williamson L%2C Willetts B%2C Ljung K%2C McCulloch H%2C Leyser O %282014%29 Auxin and strigolactone signaling are required for modulation of Arabidopsis shoot branching by nitrogen supply%2E Plant Physiol 166%3A 384%2D395&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=de Jong M, George G, Ongaro V, Williamson L, Willetts B, Ljung K, McCulloch H, Leyser O (2014) Auxin and strigolactone signaling are required for modulation of Arabidopsis shoot branching by nitrogen supply. Plant Physiol 166: 384-395

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http://www.ncbi.nlm.nih.gov/pubmed?term=de Saint Germain A%2C Clav� G%2C Badet%2DDenisot MA%2C Pillot JP%2C Cornu D%2C Le Caer JP%2C Burger M%2C Pelissier F%2C Retailleau P%2C Turnbull C%2C Bonhomme S%2C Chory J%2C Rameau C%2C Boyer FD %282016%29 An histidine covalent receptor and butenolide complex mediates strigolactone perception%2E Nat Chem Biol 12%3A 787%2D794&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=de Saint Germain A%2C Ligerot Y%2C Dun EA%2C Pillot JP%2C Ross JJ%2C Beveridge CA%2C Rameau C %282013%29 Strigolactones stimulate internode elongation independently of gibberellins%2E Plant Physiol 163%3A 1012%2D1025&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Dun EA%2C de Saint Germain A%2C Rameau C%2C Beveridge CA %282012%29 Antagonistic action of strigolactone and cytokinin in bud outgrowth control%2E Plant Physiol 158%3A 487%2D498&dopt=abstract

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