1 Running head: A salivary effector in rice brown ... · 134 The brown planthopper (BPH,...

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Running head: A salivary effector in rice brown planthopper 1

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Correspondence: Yonggen Lou 4

State Key Laboratory of Rice Biology 5

Institute of Insect Science 6

Zhejiang University 7

Hangzhou 310058 8

China 9

Tel.: 0086 571 88982622 10

Email: [email protected] 11

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Plant Physiology Preview. Published on January 26, 2017, as DOI:10.1104/pp.16.01493

Copyright 2017 by the American Society of Plant Biologists

www.plantphysiol.orgon August 7, 2019 - Published by Downloaded from Copyright © 2017 American Society of Plant Biologists. All rights reserved.

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A salivary endo-β-1,4-glucanase acts as an effector that enables the 30

brown planthopper to feed on rice 31

Rui Ji, Wenfeng Ye, Hongdan Chen, Jiamei Zeng, Heng Li, Haixin Yu, Jiancai Li, 32

Yonggen Lou* 33

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State Key Laboratory of Rice Biology, Institute of Insect Science, Zhejiang University, 35

Hangzhou, Zhejiang, China 36

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Summary 43

A salivary endo-β-1,4-glucanase in the rice brown plant hopper Nilaparvata lugens facilitates access 44

to the phloem by degrading celluloses in plant cell walls. 45

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Footnotes: 55

Author contributions 56



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Y.L. conceived the original research plans and supervised the experiments; Y.L., R.J. 57

and W.Y. designed the experiments and analyzed the data; R.J., W.Y., H.C., J.Z., H.L., 58

H.Y. and J.L. performed the experiments; Y.L. and R.J. wrote the manuscript; all authors 59

reviewed the manuscript. 60

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Funding information: The study was jointly sponsored by Projects of International 62

Cooperation and Exchanges of National Natural Science Foundation of China 63

(31520103912), the Special Fund for Agro-scientific Research in the Public Interest 64

(201403030), the Special Fund for Agro-scientific Research in the Public Interest of 65

Zhejiang (2014C22004) and the earmarked fund for China Agriculture Research System 66

(CARS-01-21). 67

Corresponding author: Yonggen Lou ([email protected]) 68

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The author responsible for distribution of materials integral to the findings presented in 70

this article in accordance with the policy described in the Instructions for Authors 71

(www.plantphysiol.org) is: Yonggen Lou ([email protected]). 72

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Abstract 75

The rice brown planthopper (BPH) Nilaparvata lugens (Stål) is one of the most 76

destructive insect pests on rice in Asia. After landing on plants, BPH rapidly accesses 77

plant phloem and sucks the phloem sap through unknown mechanisms. We discovered a 78

salivary endo-β-1,4-glucanase (NlEG1) which has endoglucanase activity with a 79

maximal activity at pH 6 at 37˚C and is secreted into rice plants by BPH. NlEG1 is 80

highly expressed in the salivary glands and midgut. Silencing NlEG1 decreases the 81

capacity of BPH to reach the phloem and reduces its food intake, mass, survival, and 82

fecundity on rice plants. By contrast, NlEG1 silencing had only a small effect on the 83

survival rate of BPH raised on artificial diet. Moreover, NlEG1 secreted by BPH did not 84

elicit the production of defense-related signal molecules -- salicylic acid, jasmonic acid 85

(JA), and jasmonoyl-isoleucine (JA-Ile) -- in rice, although wounding plus the 86

application of the recombination protein NlEG1 did slightly enhance the levels of JA 87

and JA-Ile in plants compared to in the corresponding controls. The data suggest that 88

NlEG1 enables the BPH’s stylet to reach the phloem by degrading celluloses in plant 89

cell walls (PCWs), thereby functioning as an effector that overcomes the PCW defense 90

in rice. 91

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INTRODUCTION 94

To protect themselves from attack by herbivores, plants have developed a set of 95

resistance mechanisms, including constitutive and induced defenses (Felton and 96

Tumlinson, 2008; Erb et al., 2012; Stam et al., 2014; Schuman and Baldwin, 2016). 97

Constitutive defenses are physical and chemical defensive traits that plants express 98

regardless of the presence of herbivores. By contrast, induced defenses are activated 99

only when plants are infested by herbivores (Wu and Baldwin, 2010). Defense induction 100

starts with the recognition of specific herbivore-associated molecular patterns and is 101

followed by the activation of a complex signaling network, such as mitogen-activated 102

protein kinase cascades, and jasmonic acid (JA), jasmonoyl-isoleucine (JA-Ile), salicylic 103

acid (SA), and ethylene signaling pathways; the expression of defense-related genes; 104

and the production of defensive chemicals (Erb et al., 2012; Stam et al., 2014; Schuman 105

and Baldwin, 2016). 106

In response, herbivores have evolved the capacity to suppress and circumvent these 107

plant defenses through the release of effectors (Elzinga and Jander, 2013). Plant cell 108

walls (PCWs), for instance, are thick, rigid structures that mainly consist of a 109

pectin-embedded network of cellulose and hemicellulose (Calderón-Cortés et al., 2012); 110

these structures not only act as physical defenses against herbivores by enhancing the 111

mechanical hardness of plant tissues, but they also reduce the digestibility of food for 112

herbivores (Santiago et al., 2013), thereby functioning as the first layer of defense 113

against herbivores. Herbivores can secrete salivary PCW-degrading enzymes such as 114

cellulases (consisting of endo-β-1,4-glucanases and β-glucosidases) and pectinases to 115

degrade PCWs (Backus et al., 2012; Calderón-Cortés et al., 2012). Herbivores can also 116

secrete other effectors to overcome plant defenses. C002, for instance, is a salivary 117

protein identified from the salivary glands of the pea aphid Acyrthosiphon pisum; this 118

protein is essential for sustained phloem feeding (Mutti et al., 2008). Expressing C002 119

from the green peach aphid Myzus persicae in Nicotiana benthamiana increased aphid 120

reproduction on these plants, whereas reducing C002 expression in aphids by 121

plant-mediated RNA interference reduced aphid fecundity (Bos et al., 2010; Pitino et al., 122

2011). Other salivary proteins, such as glucose oxidase from corn earworm Helicoverpa 123



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zea (Musser et al., 2002), calcium-binding proteins from the vetch aphid Megoura 124

viciae (Will et al., 2007), Mp10 and Mp55 from the green peach aphid (Bos et al., 2010; 125

Elzinga et al., 2014), structural sheath proteins from the grain aphid Sitobion avenae 126

(Abdellatef et al., 2015), Me10 and Me23 from the potato aphid Macrosiphum 127

euphorbiae (Atamian et al., 2013), and Armet from the pea aphid (Wang et al., 2015) 128

have also been found to increase herbivore performance. Thus, herbivore effectors play 129

a central role in overcoming plant defenses and helping the herbivore establish a 130

population on host plants. However, the mechanisms underlying the effector-mediated 131

promotion of herbivore abilities to overcome plant defenses remain mostly unknown 132

(Elzinga and Jander, 2013). 133

The brown planthopper (BPH, Nilaparvata lugens (Stål)), one of the most destructive 134

insect pests of the rice plant (Oryza sativa L.) in Asia, causes substantial losses in rice 135

yield every year (Heong et al., 2014). As a piercing-sucking insect, BPH secretes two 136

primary kinds of saliva during feeding: coagulable and watery. Coagulable saliva forms 137

salivary sheaths around the insect’s stylets which help to stabilize and protect the stylets 138

and may suppress plant defense responses to components of the watery saliva (Miles, 139

1999; Abdellatef et al., 2015). Watery saliva, which contains a mixture of amino acids, 140

proteins, and digestive enzymes, assists in the digestion of plant material and helps 141

suppress plant defense responses (Miles, 1968; Miles, 1999; Harmel et al., 2008; 142

Carolan et al., 2009; Hogenhout and Bos, 2011; Nicholson et al., 2012; Elzinga and 143

Jander, 2013). Thus, BPH saliva plays an important role in BPH feeding. The 144

morphology, transcriptomes and secreted proteins of BPH salivary glands have been 145

analyzed and identified (Sogawa, 1968; Konishi et al., 2009; Ji et al., 2013). Moreover, 146

several BPH salivary proteins, such as a catalase-like protein Kat-1, NlShp, salivap-3, 147

and annexin-like5, have been reported to be secreted into rice and play an important role 148

in salivary sheath formation and/or BPH feeding (Petrova and Smith, 2014; Huang et al., 149

2015; Huang et al., 2016). However, whether other salivary proteins are also involved in 150

BPH feeding and how these proteins regulate BPH feeding remain unclear. 151

By screening 352 reported genes encoding putative secreted proteins of salivary 152

gland of BPH (Ji et al., 2013), we identified a BPH gene NlEG1 which encodes a 153



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putative endo-β-1,4-glucanase. Given the role of salivary cellulases in degrading PCWs 154

stated above, we thought that NlEG1 may play a role in BPH feeding by influencing the 155

formation of the salivary sheaths and/or the defense in rice. Therefore, we chose NlEG1 156

and explored its role in rice-BPH interactions. Through a combination of molecular 157

biology and behavioral experiments, we show that NlEG1 is an effector that enables 158

BPH to feed on rice plants and simultaneously circumvents plant defenses. 159

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RESULTS 161

Isolation and characterization of NlEG1 162

Based on the data from BPH salivary gland transcriptomes (Ji et al., 2013), the full 163

length of cDNA of the gene NlEG1 (1454 bp), including an open reading frame (ORF) 164

of 1386 bp, was obtained by reverse transcription--polymerase chain reaction (RT-PCR) 165

(Fig. 1, GenBank: KM459012). Its deduced amino acid sequence revealed that NlEG1 166

encodes a protein of 461 amino acids with a calculated relative molecular mass of 52.2 167

kDa. The protein possesses an extracellular signal peptide and has no transmembrane 168

domains, suggesting a putative secreted protein. Moreover, two potential 169

O-glycosylation sites and two N-glycosylation sites were identified (Fig. 1). Protein 170

alignment followed by phylogenetic tree analysis revealed that NlEG1 is homologous to 171

insect endo-β-1,4-glucanases and belongs to the glycosyl hydrolase family 9 (GHF 9); 172

this family is characterized by catalytic domains, including catalytic nucleophile (77Asp), 173

a probable secondary nucleophile (80Asp) and proton acceptor (435Glu), and two 174

signature motifs (Nakashima et al., 2002; Kim et al., 2008; Willis et al., 2011) (Fig. 1; 175

Supplemental Figs. S1 and S2). NlEG1 shares the highest homology (72%) with the 176

endo-β-1,4-glucanase from Isoptera (Zootermopsis nevadensis KDR16731.1) and 177

Phthiraptera (Pediculus humanus corporis XP_002426465.1), followed by that from 178

Hemiptera (A. pisum XP_001944774.2) (71%) and Hymenoptera (Apis florea 179

XP_003690676.1) (69%). 180

To confirm that NlEG1 has endoglucanase activity, the recombination protein 181

NlEG1 was produced in Pichia pastoris (Fig. 2A). The mass of the recombination 182



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protein NlEG1 was about 60 kDa (Fig. 2A). Enzyme activity assays demonstrated that 183

NlEG1 acted hydrolytically on carboxymethyl cellulose (CMC) and showed the highest 184

activity at pH 6 at 37℃ (Fig. 2, B and C). Moreover, NlEG1 also acted hydrolytically 185

on filter paper and cellulose from rice plants (0.55 and 0.79 U/mg at pH 6 at 37℃, 186

respectively) but had no activity on crystalline cellulose (Avicel), curdlan, laminarin 187

and xylan. The catalytic activity of NlEG1 against CMC showed a Michaelis constant 188

(Km) of 6.72 mg/ml with a maximal reaction rate (Vmax) of 9.91 U/mg. QRT-PCR 189

analysis revealed that NlEG1 was expressed in most life stages of BPH (Fig. 2D) and 190

highly expressed in the salivary gland, midgut, fat body, and ovary (Fig. 2E). 191

NlEG1 is secreted into rice during BPH feeding 192

To explore whether BPH excretes NlEG1 through salivation during feeding, rice stems 193

were individually infested with 200 fourth- and fifth-instar nymphs for 24 h, after which 194

the outer three leaf sheaths were harvested and the proteins extracted. Western blot 195

analysis was performed using polyclonal anti-NlEG1 rabbit anti-bodies. As shown in 196

Figure 3A (lane 2), a band of about 50 kDa was detected in plants attacked by BPH. The 197

same band was also detected in extracts from BPH salivary glands (Fig. 3A, lane 1). On 198

the other hand, the band of NlEG1 was not detected in control plants (non-infested 199

plants) (Fig. 3A, lane 3). The results indicate that NlEG1 is transferred from BPH 200

salivary glands to the plant during feeding. A band of about 38 kDa was also detected in 201

extracts of the salivary glands (Fig. 3A, lane 1) but could not be detected in the plant 202

extracts either before or after BPH feeding (Fig. 3A, lanes 2 and 3). It appears that the 203

rabbit used for raising antibodies against the protein NlEG1 polypeptide also contained 204

antibodies that matched another salivary gland protein of 38kDa. These results show 205

that NlEG1 accumulates in rice plants after BPH feeding and is therefore likely excreted 206

into the plant by the herbivore. 207

Silencing NlEG1 impairs BPH feeding and fecundity 208

To explore the function of NlEG1, we used RNA interference (RNAi) as described in 209

Liu et al. (2010). Injection with dsRNA of NlEG1 decreased the transcript levels of 210

NlEG1 in the whole body, salivary gland, midgut, fat body, and ovary of BPH by 211

81%-95% over a period of 6 days (2-8 d post injection; Fig. 3, B and C). Silencing also 212



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reduced the abundance of the protein in the salivary glands and the enzyme activity of 213

NlEG1 (Fig. 3D). Silencing NlEG1 did not influence the body length and pronotum 214

width of BPH nymphs (Fig. 4A; Supplemental Fig. S3). However, the mass of 215

NlEG1-silenced nymphs and the number of eggs in the ovaries of NlEG1-silenced 216

female adults were reduced by about 21% and 54-57%, respectively, although eggs were 217

normal (Fig. 4, B-D). 218

To study the effect of NlEG1 on BPH feeding, we used the electrical penetration 219

graph (EPG) technique, a powerful method used to profile the feeding behavior of 220

piercing-sucking insects (Seo et al., 2009; Cao et al., 2013). Five main phases of feeding 221

can be distinguished by EPG: non-penetration, the pathway phase (including penetration 222

initiation, salivation and stylet movement, and extracellular activity near the phloem), 223

intracellular activity in the phloem, phloem sap ingestion, and the xylem phase. 224

Representative EPG traces from BPH, including the different phases, are shown in Fig. 225

5A (upper panel). NlEG1 silencing significantly increased the non-penetration (Fig. 5A, 226

NP) and the pathway phase (Fig. 5A, PP) time. On the other hand, the phloem 227

intracellular activity and ingestion phases were significantly reduced (Fig. 5A, N4-a, 228

and N4-b). Eleven of the 15 tested NlEG1 silenced individuals did not reach the phloem 229

during the 6 h trial period, whereas all control individuals did. The few silenced 230

individuals that reached the phloem still spent significantly less time ingesting phloem 231

sap than did controls (Fig. 5A, N4-b’). Silencing NlEG1 also significantly and 232

consistently reduced the amount of secreted honeydew, which is an indicator of the 233

amount of food intake (Fig. 5B). Moreover, in accord with the result on the number of 234

eggs in the ovaries, the number of eggs laid by NlEG1-silenced female adults was 235

decreased by 50% (Fig. 5D). Collectively, these results show that NlEG1 is required for 236

cell wall penetration and feeding as well as fecundity. 237

NlEG1 is indispensable for BPH survival on rice 238

To further test whether the presence of NlEG1 influences BPH survival rates on rice and 239

whether this influence is related to the effect of NlEG1 on the ability of BPH to reach 240

the phloem, we compared the performance of BPH nymphs on different food matrices. 241



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NlEG1 silencing generally reduced the survival rate (Fig. 6), and the effect was most 242

pronounced on rice plants: Three days after dsRNA injection, the survival rate of BPH 243

on rice dropped significantly and was 23% 7 days post-injection (Fig. 6A). In contrast, 244

the survival rate of BPH nymphs with silenced NlEG1 was much higher in insects 245

raised on artificial diet than in those raised on rice; moreover, the survival rate of BPH 246

nymphs with knocked-down NlEG1 raised on artificial diet was only slightly reduced 247

compared to that of control BPH nymphs 7 days after the start of the experiment (Fig. 248

6B). Compared with that of BPH nymphs with silenced NlEG1 raised on artificial diet, 249

the corrected survival rate of BPH nymphs with silenced NlEG1 raised on rice was 250

significantly lower 4-7 days after injection (Fig. 6C). These results demonstrate that 251

NlEG1 contributes to the survival rate of BPH nymphs raised on rice. 252

NlEG1 secreted by BPH does not induce defense responses in rice 253

Plant hormones – namely, JA, JA-Ile and SA -- play major roles in rice defense against 254

herbivores (Zhou et al., 2009; Lu et al., 2011; Lu et al., 2015). To determine if the 255

salivary protein NlEG1 influences the production of these phytohormones and thus 256

modulates defense responses in rice, we investigated the levels of SA, JA and JA-Ile in 257

rice after the plant was either infested by fifth-instar BPH nymphs whose ability to 258

produce NlEG1 had been silenced or treated with the recombination protein NlEG1. The 259

results showed that BPH nymph feeding did not induce, or very weakly induced, the 260

production of SA, JA and JA-Ile from 8 to 48h after feeding (Fig. 7A-C). Silencing 261

NlEG1 did not alter the effect of BPH nymph feeding on SA, JA, and JA-Ile levels in 262

plants: levels of these signals in all of the three treatments -- feeding by nymphs, by 263

nymphs with injected dsRNA of GFP or by nymphs with knocked-down NlEG1 -- and 264

in controls were similar (Fig. 7A-C). However, compared to plants that were treated 265

with wounding plus the purified elution products from the empty vector, plants treated 266

with wounding plus the application of the recombination protein NlEG1 showed slightly 267

higher levels of JA (8h and 24h after treatment) and JA-Ile (24h after treatment) but not 268

SA (Fig. 7D-F). These findings indicate that the NlEG1 secreted by BPH nymphs 269

during feeding did not elicit JA- and JA-Ile-mediated defense responses in rice, 270

although the recombination protein NlEG1 did slightly induce the production of these 271



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signals in plants that had been mechanically wounded. 272

DISCUSSION 273

Our experiments demonstrate that NlEG1 acts as an herbivore effector that enables 274

BPH to overcome the defense of PCWs of rice plants. NlEG1 has endo-β-1,4-glucanase 275

activity but no exoglucanase activity (Fig. 2, B and C) and is injected into rice during 276

BPH feeding (Fig. 3A). Knocking down NlEG1, which significantly reduced the 277

transcript and protein levels as well as enzyme activity of NlEG1 (Fig. 3B-D), caused 278

BPH to spend more time in non-penetration and the pathway phase, and less time 279

feeding on phloem (Fig. 5A); this in turn decreased the amount of food intake, nymph 280

mass, survival rate and fecundity of BPH fed on rice (Figs. 4-6). By contrast, NlEG1 281

silencing did not affect the early ability of BPH to feed on artificial diet without 282

cellulose and rigid PCWs, that is, for the first 6 days. These results suggest that NlEG1 283

aids phloem access through cell wall penetration by degrading PCW celluloses. 284

Endo-β-1,4-glucanases play an important role in degrading PCWs by randomly 285

cleaving amorphous sites of cellulose chains. Thus far, endogenous 286

endo-β-1,4-glucanases have been reported in 16 insect orders; most belong to the GHF 287

9 and are mainly expressed in the salivary glands and midguts (Calderón-Cortés et al., 288

2012). NlEG1 is also classified as a GHF 9 protein, and is most highly expressed in the 289

midgut and salivary glands of BPH (Fig. 2E and Supplemental Fig. S1), an expression 290

pattern that fits its biological functions well. Interestingly, NlEG1 was also found to be 291

highly expressed in the fat bodies and ovaries of BPH (Fig. 2E), with highest expression 292

levels in female adults (Fig. 2D). This suggests that NlEG1 may have other biological 293

functions. NlEG1 produced in the ovaries may, for instance, be secreted into the plants 294

by the ovipositor of the female adult to soften plant tissues and assist egg deposition; 295

such was found to be the case in Deraeocoris nebulosus, which uses salivary pectinases 296

to soften plant materials before oviposition (Boyd et al., 2002). Our silencing 297

experiments also illustrate that the gene is directly required for egg production in the 298

ovaries (Fig. 4, B and C). NlEG1 expression in the fat body might be related to the 299

detoxification of plant defense chemicals, as has been reported for some 300

PCW-degrading enzymes in insects (Calderón-Cortés et al., 2012). Further research will 301



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be necessary to elucidate these roles in NlEG1. 302

Using the P. pastoris expression system, we obtained the purified recombinant 303

NlEG1 with an estimated relative molecular mass of about 60 kDa by SDS-PAGE (Fig. 304

2A); this observed mass was about 10 kDa bigger than the predicted mass of mature 305

NlEG1, 49.6kDa. This inconsistency can be explained by the 36 additional amino acids 306

from the expression vector (which caused the mass of the recombinant protein to 307

increase to 53.9 kDa) and the mobility retardation due to the His-tag consisting of six 308

histidine residues in the recombinant NlEG1. That the molecular mass of a His-tag 309

fusion protein determined by SDS-PAGE is greater than expected has been reported by 310

many researchers (Niu and Guiltinan, 1994; Qiu et al., 2010; Yin et al., 2013; Wang et 311

al., 2016); and the His-tag is known to decrease the mobility of a His-tag fusion protein 312

(Tang et al., 2000). In a specific enzyme activity assay, we found that NlEG1 acted 313

hydrolytically on CMC, filter paper and rice cellulose, but not on crystalline cellulose, 314

glucose polymers with β-1,3 or β-1,6 linkages and xylose polymers, suggesting a similar 315

substrate specificity of NlEG1 to insect GHF9 endo-β-1,4-glucanases, such as rCfEG5 316

and rCfEG3a from Coptotermes formosanus (Zhang et al., 2009; Zhang et al., 2011). 317

Using CMC as a substrate, the Km value of NlEG1 (6.72 mg/ml) was similar to the 318

values of other purified GHF 9 enzymes from termites – for example, rCfEG5 (2 319

mg/ml), rCfEG3a (4.67 mg/ml) and RsEG (15 mg/ml) from Reticulitermes speratus; 320

however, the Vmax of NlEG1 (9.91 U/mg) was much lower than the Vmax of the three 321

enzymes stated as above (548, 590 and 89 U/mg, respectively) (Ni et al., 2010; Zhang et 322

al., 2011). This difference may reflect the various efficiency levels among insect species 323

in degrading celluloses (Oppert et al., 2010; Zhang et al., 2011). As a piercing-sucking 324

herbivore, BPH might not have to possess cellulase activity at levels comparable to 325

those of wood-feeding herbivores, such as termites. We also investigated the optimal 326

temperature and pH condition of NlEG1. The result showed that the pH optimum of 327

NlEG1 was 6, which was consistent with the pH optimum of cellulases reported in most 328

insects that had an optimal pH between 4 and 6 (Tokuda et al., 1997; Willis et al., 2011). 329

The optimal temperature of NlEG1 was 37°C, near the lower limit value of the range of 330

the optimal temperature (37-65°C) reported in insect endo-β-1,4-glucanases (Tokuda et 331



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al., 1997). This difference may reflect the adaptation of NlEG1 to the environmental 332

conditions in which BPH lives. 333

It has been reported that cellulases and/or their degraded cell wall fragments, such as 334

oligosaccharides, can induce plant defense responses (Martinez et al., 2001). Similarly, 335

here we found that wounding plus the application of the recombination protein NlEG1 336

elicited slightly higher levels of JA and JA-Ile in rice than did wounding plus the 337

addition of the purified elution products from the empty vector (Fig. 7D-F). However, 338

levels of JA, JA-Ile and SA in plants infested by BPH nymphs whose NlEG1 had been 339

knocked down were similar to levels in plants infested by control BPH nymphs and in 340

control plants (Fig. 7A-C), suggesting that NlEG1 secreted by BPH did not induce these 341

signal-mediated defense responses in rice. This discrepancy is probably related to the 342

feeding behavior of BPH, namely, its use of a stylet to penetrate intercellular spaces, 343

allowing it to suck phloem sap (Seo et al., 2009); this behavior causes little tissue 344

damage and circumvents plant defenses. Moreover, the salivary sheath and some 345

components of the watery saliva secreted and/or formed during the piercing-sucking 346

insect feeding can also reduce the chance that plants will produce defensive responses 347

(Miles, 1968; Miles, 1999). These reasons may also explain why BPH nymph feeding 348

had little induction on the production of JA, JA-Ile and SA in rice (Fig. 7A-C). Whether 349

NlEG1 elicits the biosynthesis of other defense-related signals, such as ethylene, and 350

thus also acts as a plant defense elicitor needs to be elucidated. However, our present 351

experiments show that the benefit of NlEG1 as an effector outweighs its potential costs 352

as an elicitor. 353

CONCLUSIONS 354

In summary, our study shows that NlEG1, a salivary endo-β-1,4-glucanase of BPH, is 355

an effector that enables BPH to feed on rice by degrading PCW celluloses and, 356

simultaneously, to circumvent JA- and JA-Ile-mediated defense responses in rice. The 357

finding reveals the molecular basis of how piercing-sucking insects overcome 358

PCW-based resistance traits in plants and provides a plausible mechanism that helps to 359

explain the extraordinary success and impact of BPH as a rice pest since the green 360

revolution started in the 1960s; that revolution resulted in extensive plantations of 361



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semi-dwarf rice varieties whose GA pathways had been impaired, varieties that have 362

lower levels of lignin and cellulose than those with normal GA pathways (Okuno et al., 363

2014; Huang et al., 2015). 364

MATERIALS AND METHODS 365

Plant growth and insect rearing 366

Mudgo, a rice variety containing the resistance gene Bph1, was used for experiments. 367

Plants were grown as described by Lu et al. (2011), and 35- to 40-day-old plants 368

individually planted in 500-ml hydroponic plastic pots were used. Colonies of BPH 369

were originally provided by the Chinese National Rice Research Institute (Hangzhou, 370

China), and maintained on Mudgo at 27 ± 1°C and 70 ± 10% relative humidity under a 371

14/10 h light/dark photoperiod. 372

Cloning, sequence alignment and phylogenetic analysis of NlEG1 373

The full-length cDNA of NlEG1 was obtained by RT-PCR from total RNA isolated 374

from salivary glands of adult BPH females. The primers (Supplemental Table S1) were 375

designed based on the consensus sequence of endo-β-1,4-glucanase genes in insects and 376

transcriptome data of BPH salivary glands and whole bodies (Xue et al., 2010; Ji et al., 377

2013). PCR-amplified fragments were cloned into the pMD19-T vector (TaKaRa, Otsu, 378

Japan) and sequenced. The NlEG1 sequence was translated and analyzed with the 379

compute pI/MW tool to predict the isoelectric point (pI) and molecular weight of the 380

predicted protein (http://expasy.org/tools). NetOGlyc 4.0 381

(http://www.cbs.dtu.dk/services/NetOGlyc/) and NetNGlyc 1.0 382

(http://www.cbs.dtu.dk/services/NetNGlyc) were used to predict O- and N-glycosylation 383

sites, respectively. Predictions of signal peptide and transmembrane domain were made 384

using SignalP 4.1 (http://www.cbs.dtu.dk/services/SignalP/) and TMHMM 2.0 385

(http://www.cbs.dtu.dk/services/TMHMM/), respectively. Amino acid sequences of 386

insect endo-β-1,4-glucanase sequences downloaded from NCBI (National Center for 387

Biotechnology Information, http://www.ncbi.nlm.nih.gov) were aligned using ClustalX2. 388

Phylogenetic relationships were determined using MEGA 5.0 with the neighbor-joining 389

method. 390

RNA preparation and quantitative real-time PCR (qRT-PCR) 391



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Total RNA was extracted from the following materials: 1) whole bodies of BPH at 392

different developmental stages (from first- to fifth-instar nymphs, newly emerged 393

brachypterous male and female adults); 2) specific tissue of BPH: salivary glands, 394

thorax muscles, integuments, midguts, ovaries, legs, and fat bodies that had been 395

dissected from newly emerged brachypterous female adults. Total RNA was isolated 396

using the SV Total RNA Isolation System (Promega, Fitchburg, MA, USA), according 397

to the manufacturer’s instructions. One microgram of each total RNA sample was 398

reverse-transcribed using the PrimeScript RT–PCR Kit (TaKaRa). The qRT-PCR 399

reactions were performed on a CFX96TM Real-Time System (Bio-Rad, Hercules, USA) 400

using SsoFastTM probes supermix (Bio-Rad). A linear standard curve, threshold cycle 401

number versus log (designated transcript level), was constructed using a series dilutions 402

of a specific cDNA standard and the relative levels of the transcript of the target gene in 403

all unknown samples were determined according to the standard curve. A BPH actin 404

gene (GenBank: EU179848) was used as an internal standard to normalize cDNA 405

concentrations. The primers and probes used for qRT-PCR for all tested genes are 406

provided in Supplemental Table S1. Three to four independent biological replicates 407

were analyzed in each experiment. 408

Expression of NlEG1 in Pichia pastoris 409

The full-length ORF of NlEG1 was PCR-amplified using a pair of primers 410

(Supplemental Table S1) and cloned into the Pichia expression vector pPICZα A 411

(Invitrogen, Carlsbad, CA, USA). The recombinant vector NlEG1:pPICZɑ A and empty 412

vector pPICZɑ A (as a control) were transformed into Pichia pastoris strain KM71 413

(Invitrogen). Expression was induced by adding 100% methanol to a final concentration 414

of 1%. The expressed products from the empty vector and recombinant vector were 415

purified by using Ni-NTA columns and following the instructions of Ni-NTA Superflow 416

Cartridge Handbook (Qiagen, Valencia, USA), and the purified products were 417

concentrated with a YM-10 Microcon centrifugal filter device (Millipore, Billerica, MA, 418

USA) to remove imidazole. The final purified concentrated products from P. pastoris 419

cells with the empty vector and recombinant vector were mixed with 2×SDS loading 420

buffer, respectively, separated by SDS/PAGE on a 12% gradient gel, and stained with 421



16

0.025% Coomassie blue R-250 in water. The predicted mass of the mature recombinant 422

protein NlEG1, including 6 C-terminal His-tags, is 53.9 kDa. 423

Polyclonal antibody preparation and western blot analysis 424

Based on the Optimum AntigenTM design tool, a polypeptide (WRGDSSLNDRGLKGC) 425

of NlEG1 was selected as the antigen to produce the rabbit polyclonal antibodies, and 426

the polyclonal antibodies were purified by GenScriptTM (GenScript, Nanjing, China). 427

The following protein samples used for western blot analysis were prepared: 1) Proteins 428

extracted from salivary glands of BPH. The salivary glands of one hundred newly 429

emerged adult females were collected and homogenized in 1 ml PBS. The extract was 430

centrifuged at 12,000ⅹg for 5 min at 4 ℃, and the supernatant was collected as 431

samples. 2) Proteins from rice leaf sheaths, infested by BPH or not. Rice stems were 432

individually confined within glass cylinders (diameter 4.00 cm, height 8.00 cm, with 48 433

small holes, diameter 0.800 mm) in which 200 fourth- or fifth-instar nymphs were 434

released, and 24 h later, the herbivore was removed. Plants in empty glass cylinders 435

were used as controls. For each rice stem, the outer three leaf sheaths were harvested, 436

and the entire leaf sheaths (0.900 g) from 3 rice stems were merged and homogenized in 437

4 ml PBS in liquid nitrogen. The extract was centrifuged at 12,000ⅹg for 5 min at 4°C, 438

and the supernatant was collected and concentrated to 200 µL by using a YM-3 439

Microcon centrifugal filter device (Millipore, Billerica, MA, USA). SDS/PAGE loading 440

buffer (2ⅹ ) was added to samples, and these samples were then subjected to 441

SDS/PAGE on a 12% gradient gel and transferred onto a PVDF membrane. Nonspecific 442

binding sites were blocked with 5% instant nonfat dry milk, and membranes were 443

incubated with the purified polyclonal antibody. The antigen–antibody complexes were 444

visualized with horseradish peroxidase-conjugated goat anti-rabbit IgG (Multisciences, 445

Hangzhou, China) at a dilution of 1:5,000 at 37℃ for 1h followed by extensive 446

washing for 30 minutes with frequent changes of TBST and detected by FluorChem 447

FC2 (Alpha Innotech, San Leandro, CA, USA). 448

Endo-β-1,4-glucanase activity assay 449

The endo-β-1,4-glucanase activity of the protein samples was determined, using CMC 450

as a substrate, by a reducing sugar releasing assay as described previously with some 451



17

modifications (Li et al., 1998). Briefly, 400 μL of 1.00% CMC-Na solution in 50.0 mM 452

sodium acetate buffer (pH 6.0) mixed with 15 μL of the sample was incubated at certain 453

temperatures (see below) for 30 min. We first used this method to investigate the 454

optimal pH and temperature condition of NlEG1 produced from P. pastoris. For the 455

optimum temperature, the enzyme activity was measured at 28°C, 37°C and 50°C at pH 456

6.0, and for the optimum pH, the activity was determined at 37℃ at pH 5.0, 6.0 and 7.0 457

(adjusted by 50.0 mM sodium acetate buffer solution). Based on these experimental 458

data, we found that NlEG1 has its highest activity at 37°C at pH 6.0. Thus, we 459

investigated the enzyme activity of the proteins extracted from newly emerged adult 460

females 3 days after injection at 37°C at pH 6.0. For the extraction of BPH proteins, 461

newly emerged BPH female adults were homogenized in 50.0 mM sodium acetate 462

buffer (pH 6.0) on ice, and then the solution was centrifuged at 12,000 rpm for 20 min 463

at 4 °C. The supernatant (proteins) was collected as samples. Endo-β-1,4-glucanase 464

activity was defined as units per mg of protein, where one unit of enzyme activity was 465

defined as the amount of enzyme that produced 1µmol of reducing sugars (glucose 466

equivalent) per min. The concentration of the proteins was measured in triplicate by 467

using Bio-Rad Bradford Protein Assay (Bio-Rad). 468

Specific enzymatic activity and kinetics of NlEG1 469

Using the reducing sugar assay, the specific enzyme activity of NlEG1 was measured. 470

Six substrates were used in the assay, including Whatman No. 1 filter paper (Whatman 471

Ltd, Maidstone, UK), cellulose extracted from rice plants using the method as described 472

by (Rosa et al., 2012), Avicel (PH101-type crystalline cellulose; Sigma-Aldrich, St 473

Louis, MO, USA), curdlan (β-1,3-glucan; Sigma-Aldrich), laminarin 474

(β-1,3:β-1,6-glucan; Sigma-Aldrich) and xylan (poly β-1,4-xylopyranose; 475

Sigma-Aldrich). An aliquot of 400 μL of 1% substrate solution in 50 mM sodium 476

acetate buffer (pH 6.0) was mixed with 10 μL NlEG1 (500 ng), and then the mixture 477

was incubated for 1h at 37°C. 478

The enzyme kinetics of NlEG1 was measured using serial concentrations of CMC 479

(from 1 to 10 mg/ml) in 50.0 mM sodium acetate buffer (pH 6.0). An aliquot of 20 μL 480

of NlEG1 (1000 ng) was added into 400 μL of CMC solution, and then the mixture was 481



18

incubated for 5 min at 37°C. Lineweaver–Burk plots were drawn using Microsoft Excel 482

2010, and Km and Vmax were determined. 483

RNAi experiment 484

A 215 bp fragment of NlEG1 and a 657 bp fragment of control gene GFP were 485

amplified by RT-PCR with primers including a T7 promoter sequence (Supplemental 486

Table S1). The PCR products were used to synthesize dsRNA in vitro by using the 487

MEGAscript RNAi kit (Ambion, Austin, TX, USA). Third- or fifth-instar nymphs (see 488

details in different experiments) were injected as described previously (Liu et al., 2010). 489

Each nymph was injected with about 0.100 μg dsRNA of NlEG1 or GFP (control), or 490

not injected (control). To determine the efficiency of gene silencing after dsRNA 491

injection, the levels of NlEG1 transcripts in the whole body, salivary gland, midgut, 492

ovary, and fat body of the insect that had been injected with NlEG1 or GFP dsRNA, or 493

not injected, were investigated at 2, 4, 6, and 8 days after injection. 494

BPH bioassays 495

To measure survival rates of BPH, third-instar nymphs injected with NlEG1 or GFP 496

dsRNA, or kept non-injected, were allowed to feed on rice plants or artificial diet. The 497

treated insects were first kept on rice seedlings at 27 ± 1°C with 70 ± 10% RH and a 498

14:10 h (light/dark) photoperiod to recover for 1 day, and then the healthy ones were 499

used for the following bioassay: Stems of rice plants (one plant per pot) were 500

individually confined within glass cylinders as stated above into which 15 third-instar 501

BPH nymphs were released. In the artificial diet experiment, 15 third-instar BPH 502

nymphs were introduced into individual feeding chambers (9 cm long and 2 cm in 503

diameter) as described previously (Fu et al., 2001). The number of surviving BPH 504

nymphs in each cylinder or feeding chamber was recorded every day. The survival rates 505

of each BPH treatment and the corrected survival rates of BPH nymphs with injected 506

NlEG1 dsRNA, using BPH nymphs with injected GFP dsRNA as controls, on rice or 507

artificial diet were calculated. The experiment was repeated four times. 508

To investigate the influence of NlEG1-knockdown on the growth phenotype of BPH 509

nymphs, third-instar nymphs injected with NlEG1 or GFP dsRNA were allowed to feed 510

on rice plants. Six days later, the body length and pronotum width of BPH nymphs 511



19

(using MshotDigital Imaging System) as well as nymph mass (to an accuracy of 0.1 mg) 512

were measured. Photographs of nymphs were also taken under a light stereomicroscope 513

(Olympus SZX7, Tokyo, Japan). The measurement for body length and pronotum width 514

was repeated 11 times. The mass measurement was replicated five times; each time the 515

total mass of 20 nymphs was measured and the average individual mass was calculated. 516

To assess the effect of the knock-down of NlEG1 on BPH feeding, a brachypterous 517

female adult at 3 (newly emerged) and 5 days after the injection of NlEG1 or GFP 518

dsRNA, or no injection (fifth-instar nymphs were injected), was placed into a small 519

parafilm bag (6.00×5.00 cm), which was then fixed on the stem of a rice plant. The 520

amount of honeydew excreted by a female adult was weighed (to an accuracy of 0.100 521

mg) at 24 h after the start of the experiment. The experiment was replicated 15 times. 522

The effect of NlEG1-knockdown on the fecundity of BPH female adults was also 523

investigated. Stems of rice plants (one plant per pot) were individually confined within 524

the glass cylinders into which were released one newly emerged BPH female adult, 2 525

days after the injection of NlEG1 or GFP dsRNA or no injection (fifth-instar nymphs 526

were injected), and one newly emerged BPH male adult without treatment. Eleven days 527

later, the insect was removed and the number of eggs laid by female adults in each rice 528

plant was counted under a microscope. The number of eggs in the ovary of each female 529

adult from the three treatment groups, at 3, 6, and 9 days after eclosion, was also 530

counted under a microscope. The experiment was repeated 11-15 times. 531

EPG recording of BPH feeding behavior 532

The feeding behavior of BPH was recorded on a direct current-EPG system 533

(Wageningen Agricultural University, Wageningen, The Netherlands). The method was 534

the same as described by Cao et al. (2013). All experiments were carried out at 26± 1℃ 535

and 70± 10% RH under continuous light conditions. The feeding behavior of individual 536

newly emerged adult females, 4 days after the injection of NlEG1 or GFP dsRNA, or 537

not injected (fifth-instar nymphs were injected), on rice was monitored for 6 h. For each 538

treatment (group), 15-19 replications were recorded. The signals recorded were 539

analyzed using the PROBE V. 3.4 software (Wageningen Agricultural University). The 540

output signals from EPG recordings were classified into five typical waveforms 541



20

associated with the stylet penetration behavior of BPH (Seo et al., 2009; Cao et al., 542

2013), including NP for non-penetration, PP (N1+ N2 + N3) for the pathway phase 543

(including penetration initiation, salivation and stylet movement, and extracellular 544

activity near the phloem), N4-a for an intracellular activity in the phloem, N4-b for 545

phloem sap ingestion, and N5 for the xylem phase (Fig. 5A). The durations of each 546

sequential waveform event for each insect were measured, and the average waveform 547

duration per insect (in minutes) for each waveform was calculated for each treatment 548

(Cao et al., 2013). Another variable used in this experiment was the duration of N4-a’, 549

N4-b’, and N5’, meaning the duration excluding the numerical value of zero in N4-a, 550

N4-b, and N5, respectively. 551

JA, JA-Ile, and SA Analysis 552

Potted plants (one per pot) were randomly assigned to the following treatments: 1) 553

infestation by different BPH nymph groups. Plant stems were individually confined in 554

glass cylinders into which 25 fifth-instar nymphs that had been injected with NlEG1 or 555

GFP dsRNA, or kept non-injected for 3 days, were released. 2) NlEG1 treatment. Plants 556

were individually pierced 200 times on the lower part of the stems (about 2 cm) with a 557

#00 insect pin and treated with 20µL of either the recombinant protein NlEG1 (32.7 558

ng/µL), the purified products of the empty vector (Vector), or water (W), or they were 559

kept non-manipulated (control). The outer three leaf sheaths of stems were harvested at 560

different time points (see details in Fig. 7) after the start of the treatment. Samples were 561

ground in liquid nitrogen, and SA, JA, and JA-Ile were extracted with ethyl acetate 562

spiked with labeled internal standards (2D4-SA, 2D6-JA, and 2D6-JA-Ile), then analyzed 563

with HPLC/mass spectrometry/mass spectrometry system following the method as 564

described in Lu et al. (2015). 565

Data analysis 566

Differences in BPH performance, expression levels of the gene and JA, JA-Ile and SA 567

levels between treatments were determined by analysis of variance (ANOVA) (Student’s 568

t-tests for comparing two treatments). All tests were carried out with Statistica 569

(Statistica, SAS, Institute Inc., Cary, NC, USA, http:// www.sas.com/). 570

Supplemental Materials 571



21

The following supplemental materials are available. 572

Supplemental Figure S1. Protein alignment of GHF 9 enzymes from insects. 573

Supplemental Figure S2. Phylogenetic tree for amino acid sequences of NlEG1 and 574

reported insect endogenous endo-β-1,4-glucanases. 575

Supplemental Figure S3. The growth phenotype of BPH nymphs 6 days after they had 576

been injected with either GFP (left) or NlEG1 (right) dsRNA. Representative 577

photographs are shown. 578

Supplemental Table S1. Primers and probes used for qRT-PCR and PCR. 579

580

ACKNOWLEDGMENTS 581

We thank Jian Xue for providing the BPH transcriptome data; Meng Ye, Tingting Cao, 582

Zhen Zhang, Qiyao Chai and Meng Zou for invaluable assistance with the experiment; 583

Ian T. Baldwin and Matthias Erb for insightful discussions, and Matthias Erb and Emily 584

Wheeler for editorial assistance. 585

586

Figure legends 587

Figure 1. Nucleotide sequence of NlEG1 and its deduced amino acid sequence. 588

The arrow indicates the signal peptide cleavage site. Predicted N-glycosylation and 589

O-glycosylation sites are underlined in black and highlighted in gray, respectively. 590

Square region denotes proton–donor catalytic region. The catalytic nucleophile, 591

probable secondary nucleophile, and proton acceptor (Glu) of the conserved catalytic 592

domain for GHF 9 members are represented as black diamond, gray diamond, and black 593

circle regions, respectively. Two GHF 9 signature motifs are underlined in bold gray. 594

Figure 2. Molecular characterization of NlEG1. 595

A, Expression and purification of NlEG1. Samples for western blot (lanes 1 and 2) and 596

SDS-PAGE analysis (lanes 3-6) were as follows: concentrated supernatant from Pichia 597

pastoris with the empty vector pPICZɑ A (lanes 1 and 4; control); concentrated 598

supernatant from P. pastoris with the recombinant vector NlEG1:pPICZɑ A (lanes 2 599

and 3); purified recombinant protein NlEG1 (lane 5); protein maker (lane 6). The black 600



22

arrow represents the target band. Rabbit anti-NLEG1 polyclonal antibodies were used to 601

develop the western blot. 602

B and C, Mean enzyme activity (+SE, n = 3) of the purified recombinant protein NlEG1 603

on carboxymethyl cellulose at different temperatures at pH 6 (B) and at 37℃ at 604

different pH levels (C). 605

D and E, Mean transcript levels (+SE, n = 3) of NlEG1 in whole bodies at various 606

developmental stages (D) and in different tissues (E). Sg, salivary gland; Tm, thorax 607

muscle; In, integument; Mg, midgut; Ov, ovary; Lg, leg; Fb, fat body; FA, female adults; 608

MA, male adults. 609

Figure 3. NlEG1 in rice and its silencing efficiency by RNAi. 610

A, Detection of protein NlEG1 in rice infested by BPH nymphs. Protein samples for 611

western blot analysis were as follows: the extract from the salivary glands (lane 1); the 612

extracts from rice plants that were infested by nymphs (lane 2) or kept non-infested 613

(lane 3). The black arrow represents the target band. 614

B and C, Mean transcript levels (+SE, n = 3) of NlEG1 in whole bodies on different 615

days (B) and in different tissues of newly emerged brachypterous female adults 3 days 616

(C) after they (fifth-instar nymphs) had been injected with dsRNA of NlEG1 (dsNlEG1) 617

or GFP (dsGFP), or kept non-injected (control). Sg, salivary gland; Mg, midgut; Ov, 618

ovary; Fb, fat body. 619

D, Mean endo-β-1,4-glucanase activities (+SE, n = 4) in the whole body 3 days after the 620

insects received the same treatments as above. Insert: western blot analysis for NlEG1 621

in the salivary glands of BPH received the same treatments as above. 622

Letters indicate significant differences among different treatments (p<0.05, Duncan’s 623

multiple range test). 624

Figure 4. Growth phenotypes of BPH nymphs that were injected with dsRNA of NlEG1 625

or GFP, or kept non-injected. 626

A and B, Mean body length and pronotum width (+SE, n=11; A) as well as individual 627

mass (+SE, n=5; B) of BPH nymphs 6 days after they had been injected with dsRNA of 628

NlEG1 (dsNlEG1) or GFP (dsGFP). Asterisks indicate significant differences between 629

treatments (*, p < 0.05; Student’s t-test). 630



23

C, Mean number of eggs (+SE, n=11-15) in the ovary of a female adult that had been 631

injected with dsRNA of NlEG1 (dsNlEG1) or GFP (dsGFP), or kept non-injected 632

(control) at the fifth-instar nymph stage. Letters indicate significant differences among 633

different treatments (p<0.05, Duncan’s multiple range test). 634

D, Photographs of ovaries of female adults at 3 and 6 days after eclosion that received 635

the same treatments as in C, showing that knocking down NlEG1 reduces the number of 636

eggs in the ovaries of female adults but does not result in deformities. The bar 637

represents 500µm. 638

Figure 5. Knocking down NlEG1 reduces the feeding and fecundity of female BPH 639

adults. 640

A, Overall typical view of EPG waveforms generated by the feeding behavior of BPH 641

on rice (upper panel) and mean duration (+SE, n=15-19) spent at different feeding 642

phases of female adults (under panel) that had been injected with dsRNA of NlEG1 643

(dsNlEG1) or GFP (dsGFP), or kept non-injected (control) at the fifth-instar nymph 644

stage. NP: non-penetration; PP: the pathway phase (N1+ N2 + N3), including 645

penetration initiation (N1), salivation and stylet movement (N2), and extracellular 646

activity near the phloem (N3); N4-a: intracellular activity in the phloem region; N4-b: 647

phloem sap ingestion; N5: the xylem phase. N4-a’, N4-b’, and N5’ indicate mean 648

duration (+SE, n=4-19), excluding the numerical value of zero in N4-a, N4-b, and N5 649

respectively. EPGs were recorded for 6h per insect. 650

B, Mean amount of honeydew per day (+SE, n=15) secreted by a female BPH adult that 651

received the same treatments as above. FA, female adult. 652

C, A gravid female adult of BPH on rice, showing its feeding, excreted honeydew, and 653

laying eggs. 654

D, Mean number of eggs (+SE, n=11-15) laid by a female adult on plants that received 655

the same treatments as above. 656

Letters indicate significant differences among different treatments (p<0.05, Duncan’s 657

multiple range test). 658

Figure 6. Knocking down NlEG1 decreases survival rates among BPH nymphs. 659

A and B, Mean survival rates (+SE, n=4) of BPH nymphs which had been injected with 660



24

dsRNA of NlEG1 (dsNlEG1) or GFP (dsGFP), or kept non-injected (control) at 661

third-instar nymph stage, feeding on rice (A) or AD (artificial diet, B). Letters indicate 662

significant differences among different treatments (p<0.05, Duncan’s multiple range 663

test). 664

C, Mean corrected survival rates (+SE, n=4) of BPH nymphs with injected NlEG1 665

dsRNA, using BPH nymphs with injected GFP dsRNA as controls, feeding on rice or 666

AD. Asterisks indicate significant differences between treatments (**, p < 0.01; 667

Student’s t-test). 668

Figure 7. NlEG1 secreted by BPH doesn’t affect levels of SA, JA, and JA-Ile in rice. 669

A, B, and C, Mean levels (+SE, n = 5) of SA (A), JA (B), and JA-Ile (C) in rice plants at 670

8 and 24h after they were kept non-manipulated (control) or were individually infested 671

by 25 fifth-instar nymphs, which had been injected 3 days earlier with dsRNA of NlEG1 672

(dsNlEG1) or GFP (dsGFP), or kept non-injected (BPH). Insert: mean levels (+SE, n = 673

5) of SA, JA, and JA-Ile in rice plants 48h after they received same treatments as stated 674

above. This experiment was not done at the same time as did the above experiment. 675

D, E, and F, Mean levels (+SE, n = 5) of SA (D), JA (E) and JA-Ile (F) in rice plants at 3, 676

8 and 24h after they were kept non-manipulated (control) or were individually treated 677

with wounding plus 20μl of either the purified recombinant protein NlEG1 (NlEG1), the 678

purified products of the empty vector (Vector), or water (W). 679

FW, Fresh weight. Letters indicate significant differences among different treatments 680

(p<0.05, Duncan’s multiple range test). 681

682

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827 828



Figure 1. Nucleotide sequence of NlEG1 and its deduced amino acid sequence.

The arrow indicates the signal peptide cleavage site. Predicted N-glycosylation and O-glycosylation

sites are underlined in black and highlighted in gray, respectively. Square region denotes proton–donor

catalytic region. The catalytic nucleophile, probable secondary nucleophile, and proton acceptor (Glu)

of the conserved catalytic domain for GHF 9 members are represented as black diamond, gray diamond,

and black circle regions, respectively. Two GHF 9 signature motifs are underlined in bold gray.



Figure 2. Molecular characterization of NlEG1.

A, Expression and purification of NlEG1. Samples for western blot (lanes 1 and 2) and SDS-PAGE

analysis (lanes 3-6) were as follows: concentrated supernatant from Pichia pastoris with the empty

vector pPICZɑ A (lanes 1 and 4; control); concentrated supernatant from P. pastoris with the

recombinant vector NlEG1:pPICZɑ A (lanes 2 and 3); purified recombinant protein NlEG1 (lane 5);

protein maker (lane 6). The black arrow represents the target band. Rabbit anti-NLEG1 polyclonal

antibodies were used to develop the western blot.

B and C, Mean enzyme activity (+SE, n = 3) of the purified recombinant protein NlEG1 on

carboxymethyl cellulose at different temperatures at pH 6 (B) and at 37℃ at different pH levels (C).



D and E, Mean transcript levels (+SE, n = 3) of NlEG1 in whole bodies at various developmental

stages (D) and in different tissues (E). Sg, salivary gland; Tm, thorax muscle; In, integument; Mg,

midgut; Ov, ovary; Lg, leg; Fb, fat body; FA, female adults; MA, male adults.



Figure 3 NlEG1 in rice and its silencing efficiency by RNAi.

A, Detection of protein NlEG1 in rice infested by BPH nymphs. Protein samples for western blot

analysis were as follows: the extract from the salivary glands (lane 1); the extracts from rice plants that

were infested by nymphs (lane 2) or kept non-infested (lane 3). The black arrow represents the target

band.

B and C, Mean transcript levels (+SE, n = 3) of NlEG1 in whole bodies on different days (B) and in

different tissues of newly emerged brachypterous female adults 3 days (C) after they (fifth-instar

nymphs) had been injected with dsRNA of NlEG1 (dsNlEG1) or GFP (dsGFP), or kept non-injected

(control). Sg, salivary gland; Mg, midgut; Ov, ovary; Fb, fat body.

D, Mean endo-β-1,4-glucanase activities (+SE, n = 4) in the whole body 3 days after the insects

received the same treatments as above. Insert: western blot analysis for NlEG1 in the salivary glands of

BPH received the same treatments as above.

Letters indicate significant differences among different treatments (p<0.05, Duncan’s multiple range

test).



Figure 4. Growth phenotypes of BPH nymphs that were injected with dsRNA of NlEG1 or GFP, or

kept non-injected.

A and B, Mean body length and pronotum width (+SE, n=11; A) as well as individual mass (+SE, n=5;

B) of BPH nymphs 6 days after they had been injected with dsRNA of NlEG1 (dsNlEG1) or GFP

(dsGFP). Asterisks indicate significant differences between treatments (*, p < 0.05; Student’s t-test).

C, Mean number of eggs (+SE, n=11-15) in the ovary of a female adult that had been injected with

dsRNA of NlEG1 (dsNlEG1) or GFP (dsGFP), or kept non-injected (control) at the fifth-instar nymph

stage. Letters indicate significant differences among different treatments (p<0.05, Duncan’s multiple

range test).

D, Photographs of ovaries of female adults at 3 and 6 days after eclosion that received the same

treatments as in C, showing that knocking down NlEG1 reduces the number of eggs in the ovaries of

female adults but does not result in deformities. The bar represents 500µm.



Figure 5 Knocking down NlEG1 reduces the feeding and fecundity of female BPH adults.

A, Overall typical view of EPG waveforms generated by the feeding behavior of BPH on rice (upper

panel) and mean duration (+SE, n=15-19) spent at different feeding phases of female adults (under

panel) that had been injected with dsRNA of NlEG1 (dsNlEG1) or GFP (dsGFP), or kept non-injected

(control) at the fifth-instar nymph stage. NP: non-penetration; PP: the pathway phase (N1+ N2 + N3),

including penetration initiation (N1), salivation and stylet movement (N2), and extracellular activity

near the phloem (N3); N4-a: intracellular activity in the phloem region; N4-b: phloem sap ingestion;

N5: the xylem phase. N4-a’, N4-b’, and N5’ indicate mean duration (+SE, n=4-19), excluding the

numerical value of zero in N4-a, N4-b, and N5 respectively. EPGs were recorded for 6h per insect.

B, Mean amount of honeydew per day (+SE, n=15) secreted by a female BPH adult that received the

same treatments as above. FA, female adult.

C, A gravid female adult of BPH on rice, showing its feeding, excreted honeydew, and laying eggs.

D, Mean number of eggs (+SE, n=11-15) laid by a female adult on plants that received the same

treatments as above.



Letters indicate significant differences among different treatments (p<0.05, Duncan’s multiple range

test).



Figure 6. Knocking down NlEG1 decreases survival rates among BPH nymphs.

A and B, Mean survival rates (+SE, n=4) of BPH nymphs which had been injected with dsRNA of

NlEG1 (dsNlEG1) or GFP (dsGFP), or kept non-injected (control) at third-instar nymph stage, feeding

on rice (A) or AD (artificial diet, B). Letters indicate significant differences among different treatments

(p<0.05, Duncan’s multiple range test).

C, Mean corrected survival rates (+SE, n=4) of BPH nymphs with injected NlEG1 dsRNA, using BPH

nymphs with injected GFP dsRNA as controls, feeding on rice or AD. Asterisks indicate significant

differences between treatments (**, p < 0.01; Student’s t-test).



Figure 7. NlEG1 secreted by BPH doesn’t affect levels of SA, JA, and JA-Ile in rice.

A, B, and C, Mean levels (+SE, n = 5) of SA (A), JA (B), and JA-Ile (C) in rice plants at 8 and 24h

after they were kept non-manipulated (control) or were individually infested by 25 fifth-instar nymphs,

which had been injected 3 days earlier with dsRNA of NlEG1 (dsNlEG1) or GFP (dsGFP), or kept

non-injected (BPH). Insert: mean levels (+SE, n = 5) of SA, JA, and JA-Ile in rice plants 48h after they

received same treatments as stated above. This experiment was not done at the same time as did the

above experiment.



D, E, and F, Mean levels (+SE, n = 5) of SA (D), JA (E) and JA-Ile (F) in rice plants at 3, 8 and 24h

after they were kept non-manipulated (control) or were individually treated with wounding plus 20μl of

either the purified recombinant protein NlEG1 (NlEG1), the purified products of the empty vector

(Vector), or water (W).

FW, Fresh weight. Letters indicate significant differences among different treatments (p<0.05,

Duncan’s multiple range test).



Parsed CitationsAbdellatef E, Will T, Koch A, Imani J, Vilcinskas A, Kogel KH (2015) Silencing the expression of the salivary sheath protein causestransgenerational feeding suppression in the aphid Sitobion avenae. Plant Biotechnol J 13: 849-857

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Atamian HS, Chaudhary R, Cin VD, Bao E, Girke T, Kaloshian I (2013) In planta expression or delivery of potato aphid Macrosiphumeuphorbiae effectors Me10 and Me23 enhances aphid fecundity. Mol Plant-Microbe Interact 26: 67-74


Backus EA, Andrews KB, Shugart HJ, Greve LC, Labavitch JM, Alhaddad H (2012) Salivary enzymes are injected into xylem by theglassy-winged sharpshooter, a vector of Xylella fastidiosa. J Insect Physiol 58: 949-959


Bos JI, Prince D, Pitino M, Maffei ME, Win J, Hogenhout SA (2010) A functional genomics approach identifies candidate effectorsfrom the aphid species Myzus persicae (green peach aphid). PLoS Genet 6: e1001216


Boyd DW, Cohen AC, Alverson DR (2002) Digestive enzymes and stylet morphology of Deraeocoris nebulosus (Hemiptera:Miridae), a predacious plant bug. Ann Entomol Soc Am 95: 395-401


Calderón-Cortés N, Quesada M, Watanabe H, Cano-Camacho H, Oyama K (2012) Endogenous plant cell wall digestion: a keymechanism in insect evolution. Annu Rev Ecol Evol Syst 43: 45-71


Cao TT, Lü J, Lou YG, Cheng JA (2013) Feeding-induced interactions between two rice planthoppers, Nilaparvata lugens andSogatella furcifera (Hemiptera: Delphacidae): effects on feeding and honeydew excretion. Environ Entomol 42: 1281-1291


Carolan JC, Fitzroy CI, Ashton PD, Douglas AE, Wilkinson TL (2009) The secreted salivary proteome of the pea aphidAcyrthosiphon pisum characterised by mass spectrometry. Proteomics 9: 2457-2467


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Harmel N, Létocart E, Cherqui A, Giordanengo P, Mazzucchelli G, Guillonneau F, De Pauw E, Haubruge E, Francis F (2008)Identification of aphid salivary proteins: a proteomic investigation of Myzus persicae. Insect Mol Biol 17: 165-174 www.plantphysiol.orgon August 7, 2019 - Published by Downloaded from

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http://www.ncbi.nlm.nih.gov/pubmed?term=Backus EA%2C Andrews KB%2C Shugart HJ%2C Greve LC%2C Labavitch JM%2C Alhaddad H %282012%29 Salivary enzymes are injected into xylem by the glassy%2Dwinged sharpshooter%2C a vector of Xylella fastidiosa%2E J Insect Physiol 58%3A 949%2D959&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Boyd DW%2C Cohen AC%2C Alverson DR %282002%29 Digestive enzymes and stylet morphology of Deraeocoris nebulosus %28Hemiptera%3A Miridae%29%2C a predacious plant bug%2E Ann Entomol Soc Am 95%3A 395%2D401&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Cao TT%2C L� J%2C Lou YG%2C Cheng JA %282013%29 Feeding%2Dinduced interactions between two rice planthoppers%2C Nilaparvata lugens and Sogatella furcifera %28Hemiptera%3A Delphacidae%29%3A effects on feeding and honeydew excretion%2E Environ Entomol 42%3A 1281%2D1291&dopt=abstract

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Musser RO, Hum-Musser SM, Eichenseer H, Peiffer M, Ervin G, Murphy JB, Felton GW (2002) Herbivory: caterpillar saliva beatsplant defences. Nature 416: 599-600


Mutti NS, Louis J, Pappan LK, Pappan K, Begum K, Chen MS, Park Y, Dittmer N, Marshall J, Reese JC (2008) A protein from thesalivary glands of the pea aphid, Acyrthosiphon pisum, is essential in feeding on a host plant. Proc Natl Acad Sci USA 105: 9965-9969


Nakashima K, Watanabe H, Saitoh H, Tokuda G, Azuma JI (2002) Dual cellulose-digesting system of the wood-feeding termite,Coptotermes formosanus Shiraki. Insect Biochem Mol Biol 32: 777-784


Ni JF, Takehara M, Watanabe H (2010) Identification of activity related amino acid mutations of a GH9 termite cellulase. BioresourTechnol 101: 6438-6443


Nicholson SJ, Hartson SD, Puterka GJ (2012) Proteomic analysis of secreted saliva from Russian Wheat Aphid (Diuraphis noxiaKurd.) biotypes that differ in virulence to wheat. J proteomics 75: 2252-2268


Niu X, Guiltinan MJ (1994) DNA binding specificity of the wheat bZIP protein EmBP-1. Nucl Acids Res 22: 4969-4978Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Okuno A, Hirano K, Asano K, Takase W, Masuda R, Morinaka Y, Ueguchi-Tanaka M, Kitano H, Matsuoka M (2014) New approach toincreasing rice lodging resistance and biomass yield through the use of high gibberellin producing varieties. PloS one 9: e86870


Oppert C, Klingeman WE, Willis JD, Oppert B, Jurat-Fuentes JL (2010) Prospecting for cellulolytic activity in insect digestive fluids.Biochem Physiol B 155: 145-154


Petrova A, Smith C (2014) Immunodetection of a brown planthopper (Nilaparvata lugens Stål) salivary catalase-like protein intotissues of rice, Oryza sativa. Insect Mol Biol 23: 13-25


Pitino M, Coleman AD, Maffei ME, Ridout CJ, Hogenhout SA (2011) Silencing of aphid genes by dsRNA feeding from plants. PloSone 6: e25709


Qiu L, Wang Y, Wang J, Zhang F, Ma J (2010) Expression of biologically active recombinant antifreeze protein His-MpAFP149 fromthe desert beetle (Microdera punctipennis dzungarica) in Escherichia coli. Mol Biol Rep 37: 1725-1732


Rosa SML, Rehman N, Miranda MIGD, Nachtigall SMB, Bica CID (2012) Chlorine-free extraction of cellulose from rice husk andwhisker isolation. Carbohyd Polym 87: 1131-1138


Santiago R, Barrosrios J, Malvar RA (2013) Impact of Cell Wall Composition on Maize Resistance to Pests and Diseases. Int J MolSci 14: 6960-6980

Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title www.plantphysiol.orgon August 7, 2019 - Published by Downloaded from


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http://search.crossref.org/?page=1&rows=2&q=Musser RO, Hum-Musser SM, Eichenseer H, Peiffer M, Ervin G, Murphy JB, Felton GW (2002) Herbivory: caterpillar saliva beats plant defences. Nature 416: 599-600

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http://scholar.google.com/scholar?as_q=Herbivory: caterpillar saliva beats plant defences&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=Mutti NS%2C Louis J%2C Pappan LK%2C Pappan K%2C Begum K%2C Chen MS%2C Park Y%2C Dittmer N%2C Marshall J%2C Reese JC %282008%29 A protein from the salivary glands of the pea aphid%2C Acyrthosiphon pisum%2C is essential in feeding on a host plant%2E Proc Natl Acad Sci USA 105%3A 9965%2D9969&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Mutti NS, Louis J, Pappan LK, Pappan K, Begum K, Chen MS, Park Y, Dittmer N, Marshall J, Reese JC (2008) A protein from the salivary glands of the pea aphid, Acyrthosiphon pisum, is essential in feeding on a host plant. Proc Natl Acad Sci USA 105: 9965-9969

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http://search.crossref.org/?page=1&rows=2&q=Nakashima K, Watanabe H, Saitoh H, Tokuda G, Azuma JI (2002) Dual cellulose-digesting system of the wood-feeding termite, Coptotermes formosanus Shiraki. Insect Biochem Mol Biol 32: 777-784

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http://search.crossref.org/?page=1&rows=2&q=Ni JF, Takehara M, Watanabe H (2010) Identification of activity related amino acid mutations of a GH9 termite cellulase. Bioresour Technol 101: 6438-6443

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http://search.crossref.org/?page=1&rows=2&q=Nicholson SJ, Hartson SD, Puterka GJ (2012) Proteomic analysis of secreted saliva from Russian Wheat Aphid (Diuraphis noxia Kurd.) biotypes that differ in virulence to wheat. J proteomics 75: 2252-2268

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http://search.crossref.org/?page=1&rows=2&q=Pitino M, Coleman AD, Maffei ME, Ridout CJ, Hogenhout SA (2011) Silencing of aphid genes by dsRNA feeding from plants. PloS one 6: e25709

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http://search.crossref.org/?page=1&rows=2&q=Qiu L, Wang Y, Wang J, Zhang F, Ma J (2010) Expression of biologically active recombinant antifreeze protein His-MpAFP149 from the desert beetle (Microdera punctipennis dzungarica) in Escherichia coli. Mol Biol Rep 37: 1725-1732

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http://search.crossref.org/?page=1&rows=2&q=Rosa SML, Rehman N, Miranda MIGD, Nachtigall SMB, Bica CID (2012) Chlorine-free extraction of cellulose from rice husk and whisker isolation. Carbohyd Polym 87: 1131-1138

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http://www.ncbi.nlm.nih.gov/pubmed?term=Santiago R%2C Barrosrios J%2C Malvar RA %282013%29 Impact of Cell Wall Composition on Maize Resistance to Pests and Diseases%2E Int J Mol Sci 14%3A 6960%2D6980&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Santiago R, Barrosrios J, Malvar RA (2013) Impact of Cell Wall Composition on Maize Resistance to Pests and Diseases. Int J Mol Sci 14: 6960-6980

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Schuman MC, Baldwin IT (2016) The layers of plant responses to insect herbivores. Annu Rev Entomol 61: 373-394Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Seo BY, Kwon YH, Jung JK, Kim GH (2009) Electrical penetration graphic waveforms in relation to the actual positions of the stylettips of Nilaparvata lugens in rice tissue. J Asia-Pacif Entomol 12: 89-95


Sogawa K (1968) Studies on the salivary glands of rice plant leafhoppers: III. Salivary phenolase. Appl Entomol Zool 3: 13-25Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Stam JM, Kroes A, Li Y, Gols R, van Loon JJ, Poelman EH, Dicke M (2014) Plant interactions with multiple insect herbivores: fromcommunity to genes. Plant Biol 65: 689


Tang W, Zhang J, Wang Z, Hong M (2000) The cause of deviation made in determining the molecular weight of His-tag fusionproteins by SDS-PAGE. Acta Photophysiologica Sinica 26: 64-68


Tokuda G, Watanabe H, Matsumoto T, Noda H (1997) Cellulose digestion in the wood-eating higher termite, Nasutitermestakasagoensis (Shiraki): distribution of cellulases and properties of endo-ß-1, 4-gIucanase. Zool Sci 14: 83-93


Wang W, Dai H, Zhang Y, Chandrasekar R, Luo L, Hiromasa Y, Sheng C, Peng G, Chen S, Tomich JM (2015) Armet is an effectorprotein mediating aphid-plant interactions. FASEB J 29: 2032-2045


Wang W, Li M, Lin H, Wang J, Mao X (2016) The Vibrio parahaemolyticus -infecting bacteriophage qdvp001: genome sequence andendolysin with a modular structure. Arch Virol: 1-8


Will T, Tjallingii WF, Thönnessen A, van Bel AJ (2007) Molecular sabotage of plant defense by aphid saliva. Proc Natl Acad Sci USA104: 10536-10541


Willis JD, Oppert B, Oppert C, Klingeman WE, Jurat-Fuentes JL (2011) Identification, cloning, and expression of a GHF9 cellulasefrom Tribolium castaneum (Coleoptera: Tenebrionidae). J Insect Physiol 57: 300-306


Wu J, Baldwin IT (2010) New insights into plant responses to the attack from insect herbivores. Annu Rev Genet 44: 1-24Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Xue J, Bao YY, Li Bl, Cheng YB, Peng ZY, Liu H, Xu HJ, Zhu ZR, Lou YG, Cheng JA (2010) Transcriptome analysis of the brownplanthopper Nilaparvata lugens. PLoS One 5: e14233


Yin L, Wang Y, Yan M, Zhang X, Pan H, Xu X, Han Z (2013) Molecular cloning, polyclonal antibody preparation, and characterizationof a functional iron-related transcription factor IRO2 from Malus xiaojinensis. Plant Physiol Biochem 67C: 63-70


Zhang D, Lax AR, Bland JM, Allen AB (2011) Characterization of a new endogenous endo-ß-1, 4-glucanase of Formosansubterranean termite (Coptotermes formosanus). Insect Biochem Mol Biol 41: 211-218

Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title www.plantphysiol.orgon August 7, 2019 - Published by Downloaded from


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http://search.crossref.org/?page=1&rows=2&q=Stam JM, Kroes A, Li Y, Gols R, van Loon JJ, Poelman EH, Dicke M (2014) Plant interactions with multiple insect herbivores: from community to genes. Plant Biol 65: 689

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http://search.crossref.org/?page=1&rows=2&q=Tokuda G, Watanabe H, Matsumoto T, Noda H (1997) Cellulose digestion in the wood-eating higher termite, Nasutitermes takasagoensis (Shiraki): distribution of cellulases and properties of endo-�-1, 4-gIucanase. Zool Sci 14: 83-93

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http://search.crossref.org/?page=1&rows=2&q=Wang W, Dai H, Zhang Y, Chandrasekar R, Luo L, Hiromasa Y, Sheng C, Peng G, Chen S, Tomich JM (2015) Armet is an effector protein mediating aphid-plant interactions. FASEB J 29: 2032-2045

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http://search.crossref.org/?page=1&rows=2&q=Wang W, Li M, Lin H, Wang J, Mao X (2016) The Vibrio parahaemolyticus -infecting bacteriophage qdvp001: genome sequence and endolysin with a modular structure. Arch Virol: 1-8

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http://search.crossref.org/?page=1&rows=2&q=Willis JD, Oppert B, Oppert C, Klingeman WE, Jurat-Fuentes JL (2011) Identification, cloning, and expression of a GHF9 cellulase from Tribolium castaneum (Coleoptera: Tenebrionidae). J Insect Physiol 57: 300-306

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http://search.crossref.org/?page=1&rows=2&q=Wu J, Baldwin IT (2010) New insights into plant responses to the attack from insect herbivores. Annu Rev Genet 44: 1-24

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http://search.crossref.org/?page=1&rows=2&q=Xue J, Bao YY, Li Bl, Cheng YB, Peng ZY, Liu H, Xu HJ, Zhu ZR, Lou YG, Cheng JA (2010) Transcriptome analysis of the brown planthopper Nilaparvata lugens. PLoS One 5: e14233

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http://search.crossref.org/?page=1&rows=2&q=Yin L, Wang Y, Yan M, Zhang X, Pan H, Xu X, Han Z (2013) Molecular cloning, polyclonal antibody preparation, and characterization of a functional iron-related transcription factor IRO2 from Malus xiaojinensis. Plant Physiol Biochem 67C: 63-70

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


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http://search.crossref.org/?page=1&rows=2&q=Zhang D, Lax AR, Bland JM, Allen AB (2011) Characterization of a new endogenous endo-�-1, 4-glucanase of Formosan subterranean termite (Coptotermes formosanus). Insect Biochem Mol Biol 41: 211-218

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=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1


Zhang D, Lax AR, Raina AK, Bland JM (2009) Differential cellulolytic activity of native-form and C-terminal tagged-form cellulasederived from Coptotermes formosanus and expressed in E. coli. Insect Biochem Mol Biol 39: 516-522


Zhou G, Qi J, Ren N, Cheng J, Erb M, Mao B, Lou Y (2009) Silencing OsHI-LOX makes rice more susceptible to chewingherbivores, but enhances resistance to a phloem feeder. Plant J 60: 638-648



http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang D%2C Lax AR%2C Raina AK%2C Bland JM %282009%29 Differential cellulolytic activity of native%2Dform and C%2Dterminal tagged%2Dform cellulase derived from Coptotermes formosanus and expressed in E%2E coli%2E Insect Biochem Mol Biol 39%3A 516%2D522&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang D, Lax AR, Raina AK, Bland JM (2009) Differential cellulolytic activity of native-form and C-terminal tagged-form cellulase derived from Coptotermes formosanus and expressed in E. coli. Insect Biochem Mol Biol 39: 516-522

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=Differential cellulolytic activity of native-form and C-terminal tagged-form cellulase derived from Coptotermes formosanus and expressed in E&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=Differential cellulolytic activity of native-form and C-terminal tagged-form cellulase derived from Coptotermes formosanus and expressed in E&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

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http://search.crossref.org/?page=1&rows=2&q=Zhou G, Qi J, Ren N, Cheng J, Erb M, Mao B, Lou Y (2009) Silencing OsHI-LOX makes rice more susceptible to chewing herbivores, but enhances resistance to a phloem feeder. Plant J 60: 638-648

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

http://scholar.google.com/scholar?as_q=Silencing OsHI-LOX makes rice more susceptible to chewing herbivores, but enhances resistance to a phloem feeder&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=Silencing OsHI-LOX makes rice more susceptible to chewing herbivores, but enhances resistance to a phloem feeder&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhou&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1


1 Running head: A salivary effector in rice brown ... · 134 The brown planthopper (BPH,...

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