A mucin-like protein of planthopper is required for ... · insect pest of rice that causes extensive yield losses and economic damage to rice both . 142. directly (by feeding) and

1

Short title: Planthopper MLP induces plant immunity response 1

Correspondence: Guangcun He, National Key Laboratory of Hybrid Rice, College of 2

Life Sciences, Wuhan University, Wuhan 430072, China 3

E-mail: [email protected] 4

Tel: +86-27-68752384 5

6

A mucin-like protein of planthopper is required for feeding and induces immunity 7

response in plants 8

Xinxin Shangguan1, Jing Zhang

1, Bingfang Liu

1, Yan Zhao

1, Huiying Wang

1, 9

Zhizheng Wang1, Jianping Guo

1, Weiwei Rao

1, Shengli Jing

1, Wei Guan

1, Yinhua Ma

1, 10

Yan Wu1, Liang Hu

1, Rongzhi Chen

1, Bo Du

1, Lili Zhu

1, Dazhao Yu

2 & Guangcun 11

He1*

12

13

1State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, 14

430072 Wuhan, China; 2Institute for Plant Protection and Soil Sciences, Hubei 15

Academy of Agricultural Sciences, 430064 Wuhan, China. 16

17

One sentence Summary: A secreted mucin-like protein in the rice brown planthopper 18

(Nilaparvata lugens) enables insect feeding and induces plant immune responses. 19

20

Footnotes: 21

Author contributions: G.H. conceived the original research plans and supervised the 22

experiments. G.H. and X.S. designed the experiments. X.S. carried out most of the 23

experiments. J.Z., B.L., H.W., Z.W., S.J., W.G., R.C., B.D., L.Z., and D.Y. carried out 24

some of the experiments. G.H. and X.S. analyzed data and wrote the manuscript. 25

26

Funding information: This work was supported by grants from National Program on 27

Research & Development of Transgenic Plants Grants (2016ZX08009003-001-008), 28

National Natural Science Foundation of China (31630063, 31230060, 31401732), and 29

National Key Research and Development Program (2016YFD0100600, 30

2016YFD0100900). 31

32

Corresponding author: Guangcun He ([email protected]) 33

Plant Physiology Preview. Published on November 13, 2017, as DOI:10.1104/pp.17.00755

Copyright 2017 by the American Society of Plant Biologists

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2

Glossary 34

BPH: brown planthopper; 35

ET: ethylene; 36

GO: gene ontology; 37

COG: clusters of orthologous groups; 38

dsRNA: double-stranded RNA; 39

FDA: fluorescein diacetate; 40

GFP: green fluorescent protein; 41

HR: hypersensitive response; 42

IIM: Intestinal mucins; 43

LUC: luciferase; 44

JA: jasmonic acid; 45

MAPK: mitogen-activated protein kinase; 46

NlMLP: N. lugens-secreted mucin-like protein; 47

ORF: open reading frame; 48

PAMPs: pathogen-associated molecular patterns; 49

PRR: Pattern recognition receptor 50

PTI: PAMP-triggered immunity 51

RLUC: Renilla luciferase gene 52

RNAi: RNA interference; 53

qRT-PCR: quantitative reverse-transcription PCR; 54

SA: salicylic acid; 55

SEM: scanning electron microscopy; 56

SHP: structural sheath protein; 57

SIPK: SA-induced protein kinase; 58

Ubi: ubiquitin; 59

VIGS: virus-induced gene silencing; 60

WIPK: wounding-induced protein kinase 61

62

63

64



3

Abstract 65

The brown planthopper, Nilaparvata lugens (Stål), is a pest that threatens rice 66

production worldwide. While feeding on rice plants, planthoppers secrete saliva, which 67

plays crucial roles in nutrient ingestion and modulating plant defense responses, 68

although the specific functions of salivary proteins remain largely unknown. We 69

identified a N. lugens-secreted mucin-like protein (NlMLP) by transcriptome and 70

proteome analyses and characterized its function, both in brown planthopper and in 71

plants. NlMLP is highly expressed in salivary glands and is secreted into rice during 72

feeding. Inhibition of NlMLP expression in planthoppers disturbs the formation of 73

salivary sheaths, thereby reducing their performance. In plants, NlMLP induces cell 74

death, the expression of defense-related genes, and callose deposition. These defense 75

responses are related to Ca2+

mobilization and the MEK2 MAP kinase and JA 76

signaling pathways. The active region of NlMLP that elicits plant responses is located 77

in its C-terminus. Our work provides a detailed characterization of a salivary protein 78

from a piercing-sucking insect other than aphids. Our findings that the protein that 79

functions in plant immune responses offer new insights into the mechanism 80

underlying interactions between plants and herbivorous insects. 81



4

Introduction 82

Plants are subjected to attack by diverse herbivorous insects, which are generally 83

classified based on their feeding strategies as chewing or piercing-sucking insects. 84

Chewing insects, such as caterpillars and beetles, can cause serious mechanical damage 85

to plant tissues, whereas piercing-sucking insects feed on plants through specially 86

adapted mouthparts known as stylets and cause only limited physical damage to plant 87

tissues (Walling, 2000). Insects can also injure plants indirectly by transmitting viral, 88

bacterial, and fungal pathogens. Plants use sophisticated perception systems to detect 89

insect feeding through cues derived not only from damage caused by feeding 90

(Reymond et al., 2000), but also from insect saliva, oral secretions, eggs, volatiles, and 91

microbes associated with the insects (Reymond, 2013; Felton et al., 2014). 92

When phloem-feeding insects feed on plants, their stylets transiently puncture the 93

epidermis and penetrate plant cell walls. The insects then ingest the phloem sap. During 94

this process, insects secrete both gelling and watery saliva from their salivary glands 95

into plant cells. The secreted gelling saliva quickly solidifies and forms a continuous 96

salivary sheath in the plant encasing the full length of the stylet. The salivary sheath 97

provides mechanical stability, and protection for the insect against plant chemical 98

defenses. For example, inhibiting the expression of structural sheath protein (SHP), a 99

salivary protein secreted by Acyrthosiphon pisum aphids, reduces their reproduction by 100

disrupting salivary sheath formation and hence their feeding from host sieve tubes 101

(Will and Vilcinskas, 2015). Watery saliva contains digestive, and cell wall-degrading 102

enzymes. Plant immune responses to insect attack may be elicited or suppressed by 103

compounds in insect saliva (Miles, 1999; Felton et al., 2014). Broadly speaking, 104

effectors are proteins or other molecules produced by pathogens or insects that can alter 105

host structures and functions (Hogenhout et al., 2009). Several insect effectors with 106

diverse effects have been identified in aphids in recent years (Bos et al., 2010; Atamian 107

et al., 2013; Rodriguez et al., 2014; Naessens et al., 2015). For example, the 108

expression of aphid protein effector C002 in host plants increases the fecundity of green 109



5

peach aphid, while another effector, Mp10, reduces aphid fecundity (Bos et al., 2010). 110

Moreover, transient in planta expression of Mp10 activates jasmonic acid (JA) and 111

salicylic acid (SA) signaling pathways (Rodriguez et al., 2014) and triggers chlorosis 112

in Nicotiana benthamiana (Bos et al., 2010). Similarly, the expression of two candidate 113

effectors, Me10 and Me23, from the potato aphid in host N. benthamiana plants 114

increases aphid fecundity (Atamian et al., 2013), and MpMIF (a MIF cytokine secreted 115

in aphid watery saliva during feeding) plays an important role in aphid survival and can 116

affect both the SA and JA signaling pathways (Naessens et al., 2015). However, little is 117

known about effectors from piercing-sucking herbivores other than aphids and their 118

functions in host plants. 119

Plants have evolved sophisticated defense mechanisms to protect themselves from 120

insect herbivores, most of which are initiated by the recognition of their saliva or oral 121

secretions. The signals are transmitted within plants via transduction networks 122

including JA, ethylene (ET), SA, and hypersensitive response (HR) pathways. 123

Accordingly, infestation by piercing-sucking insects increases the production of JA, SA, 124

and ET in rice (Yuan et al., 2005; Du B et al., 2009; Hu et al., 2011). Key elements in 125

these signaling pathways include mitogen-activated protein kinase (MAPK) cascades, 126

which occur in all eukaryotes, are highly conserved, and modulate numerous cellular 127

responses to diverse cues (Wu et al., 2007). These responses include complex defense 128

responses against insects (Wu and Baldwin, 2010). For example, oral secretions from 129

the chewing insect tobacco hornworm (Manduca sexta) induce MAPK-activated 130

defense responses to herbivore attack in N. attenuata leaves (Wu et al., 2007). 131

Similarly, aphid resistance conferred by the Mi-1 gene in tomato (Solanum 132

lycopersicum) can be attenuated by virus-induced gene silencing (VIGS) of certain 133

MAPKs and MAPK kinases (Li et al., 2006). MAPK cascades also play important 134

roles in planthopper resistance gene-mediated immunity (Yuan et al., 2005). 135

Mechanisms for resistance to phloem-feeding insects include the induction of forisome 136

(sieve tube protein) dispersion, callose deposition, and thus, phloem plugging, which 137



6

prevent insects from continuously ingesting phloem sap from plants (Will et al., 2007; 138

Hao et al., 2008). 139

The brown planthopper (BPH), Nilaparvata lugens (Stål), is a severe herbivorous 140

insect pest of rice that causes extensive yield losses and economic damage to rice both 141

directly (by feeding) and indirectly (by transmitting viral diseases). During outbreaks, 142

planthoppers can completely destroy crops, an effect called “hopper burn” (Backus et 143

al., 2005). Like other piercing-sucking insects, BPHs secrete gelling and watery saliva. 144

Recently, genomic tools such as proteomics and transcriptomics have been used to 145

investigate BPH salivary glands and saliva at the molecular level (Konishi et al., 2009; 146

Ji et al., 2013; Huang et al., 2016; Liu et al., 2016). Two secretary proteins that 147

actively participate in salivary sheath formation were recently identified in BPHs 148

(Huang et al., 2015; Huang et al., 2016). Furthermore, several salivary proteins that 149

play important roles in interactions between BPH and rice was identified (Petrova and 150

Smith, 2014; Ji et al., 2017; Ye et al., 2017). However, the functions of the majority of 151

BPH-secreted proteins have not yet been experimentally determined. The biological 152

roles of specific BPH salivary protein effectors in rice-BPH interactions remain poorly 153

understood. 154

In an analysis of the BPH salivary gland transcriptome, we found a mucin-like 155

protein gene highly expressed in BPH salivary glands. Mucins are a family of high 156

molecular weight, heavily glycosylated proteins that mostly comprise tandem repeats 157

of identical or highly similar sequences rich in serine, threonine, and proline residues 158

(Verma and Davidson, 1994). Mucin-like proteins are widely distributed in 159

eukaryotes, bacteria, and viruses. Intestinal mucins (IIM) and salivary gland mucins 160

have been identified in insects. IIM is a major protein constituent of the peritrophic 161

membrane that facilitates the digestive process, as well as protecting invertebrate 162

digestive tracts from microbial infection (Wang and Granados, 1997). A mucin-like 163

protein that was identified in the salivary glands of Anopheles gambiae through 164

transcriptomic analysis might modulate parasite infectivity or help lubricate insect 165



7

mouthparts (Francischetti et al., 2002). A mucin-like protein in the salivary proteome 166

of BPH has been detected (Huang et al., 2016). However, the functions of mucin-like 167

proteins in insects are largely unknown. 168

Here, we identified this N. lugens-secreted mucin-like protein (abbreviated NlMLP) 169

as an insect cell death-inducing protein involved in plant-insect interactions. NlMLP 170

is required for salivary sheath formation and feeding of BPHs on their host plants. 171

NlMLP induces defense responses in plant cells, including cell death, the expression of 172

pathogen-responsive genes, and callose deposition. Finally, we found that the active 173

part of NlMLP is located at its C-terminal region. 174



8

RESULTS 175

NlMLP is highly expressed in N. lugens salivary glands and secreted into rice 176

tissues 177

Sequencing of a cDNA library produced from BPH salivary glands yielded 40,000,000 178

reads. After a series of assembly and alignment steps (Methods S1), 13,969 unigenes 179

were functionally annotated with gene descriptions. Assignment of clusters of 180

orthologous groups (COG) and gene ontology (GO) terms showed that the salivary 181

gland proteins are involved in basic processes such as transcription and translation, as 182

well functions including binding, catalytic activity, and secretion (Supplemental Fig. 183

S1 and S2). 184

Salivary proteins that are secreted outside of salivary gland cells to perform their 185

functions should contain a secretory signal peptide; 399 unigenes in the BPH salivary 186

gland transcriptome were predicted to encode proteins with signal peptides. Proteins 187

with more than one predicted transmembrane domain, which are likely anchored in cell 188

membranes of the salivary gland, were excluded. After these filtering steps, 256 189

potential secretory proteins were retained (Table S1). A gene (CL865) showing high 190

identity to the Laodelphax striatellus mucin-like protein was the most abundant in the 191

transcriptome. 192

We obtained a full-length cDNA for this gene, which contains a 2187 bp open 193

reading frame (ORF) and encodes a polypeptide of 728 amino acid residues (Fig. 1A). 194

We named this gene NlMLP (Nilaparvata lugens mucin-like protein) (accession 195

number AK348750). The first 19 amino acids comprise the signal peptide, with 196

cleavage predicted between residues 19 and 20. NlMLP is rich in serine (22.4%) 197

residues, 36% of which are predicted to be potential mucin type O-glycosylation sites. 198

Some repeated amino acid sequences, a typical feature of mucin-like proteins (Verma 199

& Davidson, 1994), were found. NlMLP protein has been detected in both gelling and 200

watery saliva (Huang et al., 2016; Liu et al., 2016). To investigate the functions of 201

NlMLP, we analyzed mRNA levels in BPHs at various developmental stages including 202



9

eggs, 1st to 5th instar BPHs, and female and male adults via quantitative 203

reverse-transcription PCR (qRT-PCR). NlMLP expression was higher in insects at 204

feeding stages (nymph or adult) than at the non-feeding stage (egg) (Fig. 1B). NlMLP 205

transcripts were detected at higher levels in the salivary gland than in the gut, fat body, 206

and remaining carcass (Fig. 1C). We also analyzed the expression of NlMLP in 207

salivary glands by mRNA in situ hybridization. Hybridization signals were detected in 208

the A-follicles of principal glands but not in the salivary ducts or accessory glands 209

(Fig. 1D). 210

To confirm that NlMLP was secreted into rice tissue during feeding, we extracted 211

proteins from the leaf sheaths of plants following BPH feeding and analyzed them by 212

mass spectrometry. Four NlMLP peptides were detected in BPH-infested rice leaf 213

sheaths but not in non-infested rice (Fig. 1A), indicating that NlMLP was secreted into 214

the rice plants. 215

To determine the cellular localization of NlMLP in plant cells when transiently 216

expressed, we conducted localization experiments using rice protoplasts and N. 217

benthamiana leaf cells. When the NlMLP-GFP fusion protein was transiently 218

expressed in rice protoplasts, GFP fluorescence was detected only in the cytoplasm, 219

while control GFP fluorescence was detected in both the cytoplasm and nucleus (Fig. 220

1E). When the NlMLP-YFP fusion protein was transiently expressed in N. 221

benthamiana leaves via agroinfiltration, NlMLP localized to the cytoplasm 222

(Supplemental Fig. S3). 223

224

NlMLP is required for the feeding of BPHs on rice plants and for insect 225

performance 226

To elucidate the role of NlMLP in BPH, we synthesized double-stranded RNA (dsRNA) 227

from NlMLP and injected it into 4th instar BPH nymphs to mediate RNA interference 228

(RNAi). This treatment had a very strong silencing effect, reducing NlMLP transcript 229

levels significantly (~95%) on the first day after treatment compared to the levels in 230



10

two control groups receiving either no injection or injection with dsGFP (P < 0.001 for 231

C and dsMLP from 1 to 6 days; P = 0.017 for dsGFP and dsMLP at 1 and 5 days; P = 232

0.016 for dsGFP and dsMLP at 2, 3 and 6 days; P = 0.015 for dsGFP and dsMLP at 4 233

days; Supplemental Fig. S4). The silencing was confirmed by RNA gel blot analysis 234

two days after injection (Supplemental Fig. S4). The treated BPH insects were allowed 235

to feed on TN1 rice plants. The survival rate of BPHs harboring a silenced NlMLP gene 236

was significantly lower (from 2 to 10 days following injection) than those of the two 237

control groups (P < 0.001 for C and dsMLP and P = 0.046 for dsGFP and dsMLP at 2 238

days; P < 0.001 for C and dsMLP and P = 0.001 for dsGFP and dsMLP at 10 days; 239

Fig. 2A). The cumulative mortality rate of BPHs injected with dsMLP, dsGFP, and 240

non-injected BPHs was 96%, 60%, and 52%, respectively, at 10 days after injection 241

(Fig. 2A). BPHs subjected to the NlMLP RNAi treatment also excreted significantly 242

less honeydew, a simple measurable indicator of BPH feeding activity, than the two 243

control groups (P < 0.001 for C and dsMLP; P = 0.003 for dsGFP and dsMLP; Fig. 244

2B), as well as having smaller weight gain values (P = 0.011 for C and dsMLP; P = 245

0.031 for dsGFP and dsMLP; Fig. 2C) and weight gain ratios (P = 0.023 for C and 246

dsMLP; P = 0.043 for dsGFP and dsMLP; Fig. 2D). Furthermore, silencing of NlMLP 247

reduced BPH virulence. Rice plants died in 7 days after infested by common BPH 248

insects or BPH insects injected with dsGFP, while those plants infested by BPH 249

insects injected with dsMLP still survived and grew normally (Supplemental Fig. S5). 250

These results indicate that silencing the NlMLP gene significantly reduced the feeding 251

and performance of BPHs on rice plants. 252

Feeding on rice plants expressing dsRNAs was previously shown to trigger RNA 253

interference of a target gene in BPH (Zha et al., 2011). We therefore transformed 254

BPH-susceptible rice plants with NlMLP-dsRNA and selected a T2 homozygous 255

dsMLP-transgenic line expressing NlMLP-dsRNA via qRT-PCR analysis 256

(Supplemental Fig. S6A). When 2nd instar BPHs were fed on dsMLP-transgenic plants, 257

their expression level of NlMLP was significantly (40%) lower than in BPHs fed on 258



11

wild-type plants at 7 and 9 days after the start of exposure (P = 0.042 at 7 days; P = 259

0.045 at 9 days; Supplemental Fig. S6B). BPH survival and weight gain were also 260

significantly lower in insects fed on dsMLP-transgenic plants than in those fed on 261

wild-type plants from 7 to 10 days (P = 0.049 at 7 days; P = 0.046 at 8 days; P = 0.005 262

at 9 days; P = 0.008 at 10 days; Fig. 2E) and after 10 days (P = 0.023; Fig. 2F), 263

respectively. These results clearly show that NlMLP protein is essential for BPH 264

feeding and performance. 265

266

NlMLP is necessary for salivary sheath formation 267

NlMLP was found in both gelling saliva and watery saliva (Huang et al., 2016). To 268

further investigate the effects of NlMLP on feeding, we focused on salivary sheath 269

formation. First, we fed BPHs on an artificial diet in Parafilm sachets for 2 days and 270

analyzed their salivary sheaths by fluorescence microscopy and scanning electron 271

microscopy observation. The fluorescence microscopy analysis revealed that BPHs 272

subjected to the NlMLP RNAi treatment produced salivary sheaths that were 273

significantly shorter and less branched than those produced by the control BPHs 274

receiving either no injection or injection with dsGFP (Fig. 3, A and B). Moreover, the 275

structure of the sheaths was incomplete or predominantly amorphous, or gelling saliva 276

deposits at their stylet penetration sites were minimal, whereas those secreted by 277

control BPHs had complete, typical structures (Fig. 3, C-E). Second, we collected 278

stems from rice plants after BPH feeding and sectioned them to observe salivary sheath 279

morphology in planta. Most salivary sheaths in rice stems produced by the control 280

BPHs reached the phloem (Fig. 3, F and G), whereas most salivary sheaths produced 281

by NlMLP-silenced BPHs were shorter and failed to reach the phloem, instead stopping 282

in the rice epidermis or xylem (Fig. 3H). Together, these observations indicate that 283

NlMLP is necessary for salivary sheath formation. Silencing of NlMLP in BPHs 284

resulted in imperfect, short salivary sheaths, thus affecting phloem feeding. 285

286



12

NlMLP induces plant cell death 287

The above findings clearly show that NlMLP is secreted into rice tissues (Fig. 1A) and 288

that it is localized to the cytoplasm of rice cells (Fig. 1E). To uncover the potential role 289

of NlMLP in the host plant, we transiently expressed NlMLP without the signal peptide 290

in rice protoplasts. We measured cell death, fluorescein diacetate (FDA) staining of the 291

protoplasts showed that the cell viability of protoplasts expressing NlMLP was 292

significantly lower than that of control protoplasts expressing GFP (P < 0.001; Fig. 4, 293

A and B). We also co-expressed NlMLP together with the luciferase (LUC) gene in rice 294

protoplasts. LUC activity was significantly lower in protoplasts co-expressing NlMLP 295

compared to the control co-expressing GFP (P < 0.001; Fig. 4C). Immunoblotting 296

confirmed that NlMLP and GFP were expressed properly in the rice protoplasts 297

(Supplemental Fig. S8A). These observations indicate that NlMLP expression triggers 298

cell death in rice protoplasts. To determine whether NlMLP-triggered cell death is 299

affected by the presence of BPH-resistance genes in rice, we performed similar LUC 300

assays after co-transfection of protoplasts with NlMLP and the genes Bph6, Bph9, and 301

Bph14. The LUC activity was still significantly lower in the presence of NlMLP than in 302

the GFP controls, regardless of the presence of resistance genes (P = 0.001 for Bph6; P 303

= 0.005 for Bph9; P = 0.004 for Bph14; Supplemental Fig. S7). Therefore, NlMLP 304

expression triggers cell death in rice protoplasts independently of these BPH-resistance 305

genes. 306

We further verified the ability of NlMLP to induce plant cell death by performing A. 307

tumefaciens-mediated expression of NlMLP in N. benthamiana leaves. INF1, an elicitin 308

secreted by Phytophthora infestans that induces HR cell death in Nicotiana plants 309

(Derevnina et al., 2016), was used as a positive control, while GFP was used as a 310

negative control. NlMLP, with or without YFP-HA tag, triggered marked cell death 311

(Fig. 4, D and E). Moreover, ion leakage was significantly higher from leaves 312

expressing NlMLP or INF1 than from the GFP-expressing controls (P = 0.002 for GFP 313

and INF1; P < 0.001 for GFP and NlMLP; Fig. 4F). Immunoblot analysis showed that 314



13

GFP, INF1, and NlMLP proteins accumulated to comparable degrees in N. 315

benthamiana leaves (Supplemental Fig. S8B). However, the cell death symptoms 316

caused by INF1 and NlMLP is different. Leaves infiltrated with INF1 strain appeared 317

chlorosis in 4 days, and became severe necrosis accompanied by brown or black color 318

after 5 days. On leaves infiltrated with NlMLP, white or grey-white necrotic spots 319

appeared in 4 days and became bigger around the infiltrated site as time goes on 320

(Supplemental Fig. S9). We further investigated the quantity of NlMLP required for 321

the cell death symptoms. We set up different concentrations (OD600=0.005, 0.01, 0.02, 322

0.03, 0.04, 0.05, 0.08, 0.1, 0.2 and 0.3) of NlMLP strains to infect N. benthamiana 323

leaves, and found that cell death was caused by NlMLP strains in OD=0.01 or over 324

but was not when the OD is 0.005 (Supplemental Fig. S10A). Immunoblot detected 325

NlMLP protein in the leaves infected by in leaves infected with strains in OD 0.01 or 326

over, but not in 0.005 (Supplemental Fig. S10B). 327

To further characterize the physiological properties of the cell death induced by 328

NlMLP, we examined the effects of treatments that inhibit various potential cell 329

death-associated processes in rice protoplasts and N. benthamiana leaves. The 330

application of LaCl3 blocked the induction of cell death by NlMLP, suggesting that the 331

cell-death process mediated by NlMLP is dependent on a calcium signaling pathway 332

(Boudsocq et al., 2010) (Table 1). There was no difference in cell viability between 333

protoplasts incubated in the light or dark, indicating that the cell death process induced 334

by NlMLP is light-independent (Asai et al., 2000). Bcl-xl is an anti-apoptotic protein 335

(Chen et al., 2012). The expression of Bcl-xl in N. benthamiana leaves suppressed cell 336

death induced by subsequent NlMLP expression (Table 1). Our results indicate that cell 337

death induced by NlMLP shares some common properties with cell death induced by 338

BAX and INF1. MAPK cascades play important roles in defense-related signal 339

transduction (Yang et al., 2001). MEK2 is a MAPK kinase that acts upstream of 340

SA-induced protein kinase (SIPK) and wounding-induced protein kinase (WIPK) and 341

controls multiple defense responses to pathogen invasion (Yang et al., 2001). When we 342



14

silenced MEK2 in N. benthamiana plants via VIGS (P = 0.006; Fig. 4I), 343

NlMLP-triggered cell death was significantly reduced in MEK2-silenced plants (Fig. 344

4H), but not in control plants (Fig. 4G). However, the presence of INF1, which triggers 345

cell death independently of MEK2 (Takahashi et al., 2007), clearly caused necrosis in 346

MEK2-silenced plants (Fig. 4H). Therefore, NlMLP-triggered cell death is associated 347

with MEK2-dependent MAPK cascades. 348

349

NlMLP triggers plant defense responses 350

Callose deposition is used as a marker for plant basal defense responses and participates 351

in plant defenses against phloem sap ingestion by insects (Hann and Rathjen, 2007; 352

Hao et al., 2008). Thus, to determine whether NlMLP activates defense responses in 353

planta, we expressed NlMLP in N. benthamiana leaves and investigated callose 354

deposition by aniline blue staining. Many more callose spots were present in 355

NlMLP-expressing leaves (47.0 per infiltration) than in GFP-expressing leaves (3.5 per 356

infiltration) (P = 0.001; Fig. 5A). Moreover, NlMLP induced transcriptional activation 357

of the pathogen resistance (PR) genes NbPR3 (P = 0.143 at 24h; P = 0.002 at 48h) and 358

NbPR4 (P = 0.002 at 24h; P = 0.002 at 48h), but not NbPR1 (P = 0.625 at 24h; P = 359

0.180 at 48h), within 48 h of infection (Fig. 5B). The upregulation of genes encoding 360

acidic NbPR1 protein is a characteristic feature of the activated SA-signaling pathway, 361

while the induction of genes encoding basic NbPR3 and NbPR4 proteins is associated 362

with JA-dependent defense responses (Zhang et al., 2012; Naessens et al., 2015). Thus, 363

NlMLP appears to induce defense responses mediated by the JA signaling pathway, 364

thereby promoting the production of PR proteins and the biosynthesis of cell 365

wall-reinforcing callose. 366

367

The functional motif is located in the C-terminus of NlMLP 368

NlMLP showed no sequence similarity to any known cell death-inducing effector. To 369

delineate the functional domains of NlMLP, we assayed the ability of N-terminal and 370



15

C-terminal deletion mutant proteins to trigger cell death in N. benthamiana leaves (Fig. 371

6). The N-terminal deletion mutant M428-728

strongly triggered cell death, but the 372

C-terminal deletion mutants M32-319

and M319-428

did not. Moreover, M428-674

triggered 373

cell death less strongly than did M428-728

, and the M674-728

mutant did not induce cell 374

death at all. These findings suggest that the 428-674 amino-acid fragment is required 375

for triggering cell death and that the 674-728 amino-acid fragment might promote this 376

effect. We also found that the 428-674 fragment was required for the expression of 377

NbPR4 (P = 0.001 for GFP and M1-728

; P = 0.002 for GFP and M32-728

; P = 0.008 for 378

GFP and M319-728

; P < 0.001 for GFP and M428-728

; P = 0.129 for GFP and M674-728

; P 379

= 0.007 for GFP and M428-674

; P = 0.209 for GFP and M319-428

; P = 0.656 for GFP and 380

M32-319

; Fig. 6). Immunoblot analysis showed that the mutant proteins accumulated to 381

comparable levels in N. benthamiana leaves (Supplemental Fig. S8C). 382



16

DISCUSSION 383

This is the first report of a planthopper salivary protein that plays important roles in 384

feeding and interactions with the host plant. We identified a N. lugens mucin-like 385

protein, NlMLP, which is highly expressed in the salivary glands of BPHs and secreted 386

into rice tissue during BPH feeding. NlMLP is necessary for the probing of rice plants 387

by BPHs to obtain phloem sap for insect survival. BPH feeding was inhibited and insect 388

performance was significantly reduced when NlMLP expression was knocked-down 389

(Fig. 2). Furthermore, the salivary sheaths produced by NlMLP-silenced BPHs were 390

shorter and less branched than those of control BPHs fed on both an artificial diet and 391

rice tissue. The sheaths had incomplete structures and were predominantly 392

amorphous. 393

Mucin-like proteins have been identified in various organisms; some mucins are 394

involved in controlling mineralization (Boskey, 2003) and are associated with 395

processes including nacre formation in mollusks (Marin et al., 2000), calcification in 396

echinoderms (Boskey, 2003), and bone formation in vertebrates (Midura and Hascall, 397

1996). Based on our current results, mucin appears to be an essential component of 398

the BPH salivary sheath. Notably, the mucin-like protein NlMLP is rich in serine, 399

which provides attachment sites for carbohydrate chains that participate in the 400

formation of large extracellular aggregates (Korayem et al., 2004), thus functioning in 401

the formation of salivary sheaths, which support stylet movements and exploration of 402

the host plant tissue. Therefore, reductions in the levels of NlMLP may prevent the 403

construction of complete sheaths. The immediate consequence of this reduction in 404

NlMLP-RNAi insects is that salivary sheaths formed in rice plants do not reach into the 405

sieve tube, which likely accounts for the reduction in phloem feeding and performance 406

of these insects on rice plants. 407

In aphids, the salivary protein SHP contributes to the solidification of gelling saliva 408

and sheath formation, partly through the formation of disulfide cystine bonds (Carolan 409

et al., 2009; Will and Vilcinskas, 2015). Mucins can form disulfide-dependent soluble 410



17

dimers and multimeric insoluble gels through cross-linking of cysteines (Axelsson et 411

al., 1998). Cysteine residues in NlMLP might behave in a similar fashion and strongly 412

contribute to the formation of the polymeric matrix during sheath hardening via the 413

formation of intermolecular disulfide bonds. NlMLP might also function in the growth 414

and development of BPHs. Silencing of NlMLP affected insect development, which in 415

turn reduced salivary sheath formation, feeding, and performance. 416

Plants usually detect molecules emitted by parasites to trigger defense responses. 417

When BPHs feed on phloem sap, their saliva is secreted into rice tissue, which contains 418

bioactive components involved in inducing the expression of defense genes. We 419

demonstrated that NlMLP is one such bioactive component. Mucin-like proteins have 420

also been detected in fungal pathogens. The surfaces of many parasites, including the 421

protozoan parasite Trypanosoma cruzi (Buscaglia et al., 2006), the fish pathogen T. 422

carassii (Lischke et al., 2000), and the potato pathogen Phytophthora infestans 423

(Gornhardt et al., 2000) are covered in mucins, which participate in interactions with 424

host cells during the invasion process (Buscaglia et al., 2006; Larousse et al., 2014). 425

Similarly, NlMLP is highly expressed in salivary glands and is secreted into the plant. 426

We found that NlMLP expression triggered cell death in rice protoplasts and N. 427

benthamiana leaves (Fig. 4), as well as plant immunity responses, including the 428

induction of PR gene expression and callose synthesis in leaves (Fig. 5). NlMLP 429

molecules on the surface of the salivary sheath, representing an essential component 430

of this structure, can be detected as signal of BPH feeding by host cells and evoke 431

defense responses. NlMLP in watery saliva may play the same role as well. Our 432

results indicate that the functional portion of NlMLP is located at its C-terminus. The 433

presence of a 428-674 amino-acid fragment was sufficient for triggering cell death and 434

inducing the expression of NbPR4. Mucin-like proteins are also detected in other 435

piercing-sucking insects such as leafhopper (Hattori et al., 2015) and several mosquito 436

species (Das et al., 2010). The wide taxonomic range of hosts in which NlMLP can 437

trigger cell death suggests that NlMLP may be recognized by a conserved protein found 438



18

in many plants. The plant receptor that recognizes NlMLP remains to be identified. 439

The defense reaction elicited by NlMLP shares common features with immune 440

responses which shown by well-known effectors and pathogen-associated molecular 441

patterns (PAMPs). NlMLP might be an elicitor that involved in the PTI process. It 442

may be recognized by plant PRRs which triggers plant defensive responses. NlMLP 443

triggers cell death, a common phenomenon in effector-triggered immune responses. 444

Ca2+

is a well-known secondary signal in eukaryotes. The early defense response to 445

BPH in rice involves Ca2+

influx, which is a common early plant response triggered 446

by insect feeding (Hao et al., 2008; Hogenhout and Bos, 2011; Bonaventure, 2012). 447

Our results indicate that the cell death process induced by NlMLP is dependent on 448

Ca2+

influx. Moreover, cell death induced by NlMLP is not dependent on light and is 449

suppressed by the anti-apoptotic protein Bcl-xl. NlMLP-triggered cell death requires 450

the MEK2 MAP kinase signal transduction pathway. MEK2 is a common component in 451

MAP kinase pathways required for HR followed by certain Avr-R interactions in 452

tomato and tobacco (Morris, 2001; Del Pozo et al., 2004; King et al., 2014). NbMEK2 453

is also required for cell death triggered by the Phytophthora sojae RxLR effector 454

Avh241 in N. benthamiana (Yu et al., 2012). Given the broad range of plants 455

responding to NlMLP and the dependence of these responses on the MEK2 pathway, 456

we speculate that plants respond to NlMLP may via a conserved upstream component 457

of plant signaling pathways. The expression of NlMLP induced the JA pathway marker 458

genes NbPR3 and NbPR4. NbPR3 is a chitinase gene associated with JA-dependent 459

defenses that is induced by elicitors (Naessens et al., 2015), while NbPR4 encodes a 460

hevein-like chitinase that is also primarily associated with JA responses (Kiba et al., 461

2014). The findings suggest that defense responses triggered by NlMLP are associated 462

with the JA signaling pathway. NlMLP expression in N. benthamiana leaves also 463

induced callose deposition. Callose deposition is a useful mechanism conferring plant 464

immunity to insects and pathogens (Luna et al., 2011). In the interaction of rice and 465

BPH, callose deposition on the sieve plates occludes sieve tubes, thereby directly 466



19

inhibiting continuous feeding by BPHs (Hao et al., 2008). 467

Nevertheless, BPH can successfully attack most rice cultivars and even results in 468

hopper burn. This success is thought because of the evolved ability of BPH to suppress 469

or counteract rice defense responses triggered by NlMLP and other elicitors (Walling, 470

2008 Kaloshian and Walling, 2016). Hemipterans saliva is a complex mixture of 471

biomolecules with potential roles in overcoming plant immune responses and enables 472

hemipterans to manipulate host responses to their advantage (Miles 1999; Kaloshian 473

and Walling, 2016). One example is that BPH can decompose the deposited callose and 474

unplug sieve tube occlusions by activating b-1,3-glucanase genes and thereby facilitate 475

the continuous phloem-feeding in rice plants (Hao et al., 2008). To date, some effectors, 476

including C002, Me10, Me23, Mp1, Mp2, and Mp55, have been identified by assays in 477

planta overexpression and RNAi in aphids. These effectors contribute to aphid survival 478

and suppressing host defense (Mutti et al., 2008; Bos et al., 2010; Atamian et al., 2013; 479

Pitino and Hogenhout, 2013; Elzinga et al., 2014). The effectors may target any 480

component in pattern-triggered immunity or host cell trafficking pathway (Derevnin et 481

al., 2016; Kaloshian and Walling, 2016; Rodriguez et al., 2017). It is likely that potent 482

effectors in BPH also target such cell processes in rice and enable BPH to successfully 483

feed on rice plants, which induces cascade reactions termed the BPH-feeding cascade, 484

and results in the death of susceptible rice varieties (Cheng et al., 2013). In contrast, in 485

resistant rice the resistance gene induces a strong defense response that inhibits insect 486

feeding, growth, and development, and enables the plant to grow normally. 487

In summary, our results indicate that NlMLP secreted by BPHs into rice plants plays 488

dual roles as a component in feeding sheath formation and activating plant defense 489

responses. The defense responses induced by NlMLP in plant cells are related to Ca2+

490

mobilization and the MEK2 MAP kinase and JA signaling pathways. Further studies 491

are needed to identify the target of NlMLP in rice cells and BPH effectors that suppress 492

rice defense responses to further explore the interaction mechanisms between plants 493

and planthoppers. 494



20

MATERIALS AND METHODS 495

Plant materials and insects 496

Wild-type and transgenic rice (Oryza sativa) plants were grown in the experimental 497

fields at Wuhan University Institute of Genetics, China under routine management 498

practices. Brown planthopper biotype 1 insect populations were reared on 499

one-month-old plants of the susceptible rice variety TN1 under controlled 500

environmental conditions (26 ± 0.5°C, 16 h light/8 h dark cycle). 501

502

Tanscriptome analysis of BPH salivary glands 503

BPH adult females were dipped in 70% ethanol for several seconds and washed in 504

0.85% NaCl solution. Salivary glands were dissected in phosphate buffer saline 505

solution (pH 7.4). This was accomplished by pulling the head off of the thorax with 506

forceps and carefully removing the salivary glands that emerged from the distal region 507

of the severed head. A total of 2,000 salivary glands were dissected and directly dipped 508

into 300 µL RNAiso Plus (Takara) for RNA preparation. The poly (A) RNA was 509

isolated, broken into smaller fragments (200-700 bp), and reverse-transcribed to 510

synthesize cDNA for Illumina HiSeq™ 2000 sequencing. After stringent quality 511

assessment and data filtering, 40,000,000 reads were selected as high-quality reads 512

(after removing adapters and low-quality regions) for further analysis. A set of 513

12,668,039 high-quality reads with an average length of 400 bp was assembled, 514

resulting in 59,510 contigs. The contigs were assembled into 31,645 unigenes, 515

consisting of 3960 clusters and 27,685 singletons. All unigene sequences were aligned 516

by Blastx to protein sequences in databases including nr, Swiss-Prot, KEGG, and COG, 517

followed by sequences in the non-redundant NCBI protein database (with e<10-5

in 518

both cases). 519

SignalP 3.0 was used to predict the presence of signal peptides. To predict 520

transmembrane domains, each amino acid sequence with a signal peptide was 521

submitted to the TMHMM Server v. 2.0. 522

523

Cloning and sequencing of NlMLP cDNA 524

The cDNA sequences of NlMLP were obtained from salivary-gland transcriptomes 525

of BPHs. To obtain the full-length sequence of each truncated sequence from BPHs, 5’ 526

and 3’ RACE amplification were performed using a 5’-Full RACE Kit and 3’-Full 527



21

RACE Core Set Ver. 2.0 (Takara) following the manufacturer’s instructions. For 528

5’-RACE, gene-specific primers were designed based on sequencing data, and an 529

external reverse primer (5’-RACE-EP) and a nested primer (5’-RACE-NP) were used. 530

For 3’-RACE, the cDNA was then amplified by nested PCR with the external forward 531

primer (3’-RACE-EP) and the nested forward primer (3’-RACE-NP) (Table S2) with 532

La Taq DNA polymerase (Takara). Purified PCR products were ligated to the 533

pMD18-T simple vector (Takara) and positive colonies were sequenced. 534

535

Proteomics analysis of rice leaf sheathes 536

The TN1 rice plants were grown in pots (8 cm in diameter and 15 cm in height). At the 537

fifth leaf stage, 2nd and 3rd-instar BPH nymphs were released onto the plants at 20 538

insects per plant. The leaf sheaths of BPH-infested plants and non-infested control 539

plants were collected after 72 h, immediately frozen in liquid nitrogen, and stored at 540

-80°C. Protein extraction and digestion, iTRAQ labeling, strong cation exchange 541

chromatography (SCX) fractionation, and LC−MS/MS proteomic analysis were 542

performed according to the manufacturer’s protocols using an iTRAQ Reagent 8 Plex 543

Kit (SCIEX). A TripleTOF 5600 (AB SCIEX, Concord, ON), fitted with a NanoSpray 544

III source (AB SCIEX, Concord, ON) and a pulled quartz tip as the emitter (New 545

Objectives, Woburn, MA), was used for MS/MS. Protein identification was performed 546

using Mascot 2.3.02 (Matrix Science, London, UK) against the transcriptomic database 547

of N. lugens salivary glands (containing 18,099 protein-coding sequences). 548

549

Expression analysis of NlMLP 550

The temporal and spatial expression patterns of NlMLP were investigated by 551

qRT-PCR as follows. For spatial expression pattern analysis, salivary glands, guts, fat 552

bodies, and carcasses (i.e., samples consisting of all parts remaining after the removal 553

of the salivary gland, gut, and fat body) were dissected from BPH adults under a 554

stereomicroscope. Total RNA was isolated from each type of tissue using RNAiso 555

Plus (Takara). For temporal expression pattern analysis, total RNA was isolated from 556

BPH at various developmental stages including eggs, 1st to 5th instar nymphs, female 557

adults, and male adults. First-strand NlMLP cDNA was obtained from all samples by 558


http://www.docin.com/p-464621855.html&s=B4F764A977E5BAD8859322088F0ED17F


22

reverse transcription using a PrimeScript RT Reagent Kit with gDNA Eraser (Takara) 559

according to the manufacturer’s instructions, followed by amplification by qRT-PCR 560

using a Bio-Rad CFX-96 Real-Time PCR system with an iTaq Universal SYBR 561

Green Supermix Kit (Bio-Rad, USA) and gene-specific primers qNlMLP-F and 562

qNlMLP-F (Table S2). As an endogenous control to normalize expression levels with 563

average threshold cycle (Ct) numbers, a partial fragment of the BPH actin gene was 564

amplified with primers qNlActin-F and qNlActin-R (Table S2). A relative quantitative 565

method (ΔΔCt) was applied to evaluate the variation in expression among samples. 566

567

Fluorescence in situ hybridization of BPH salivary glands. 568

The expression patterns of NlMLP within the salivary glands were examined by in 569

situ mRNA localization and confocal microscopy, as follows. BPHs were anesthetized 570

on ice and their salivary glands were dissected and fixed in 4% formaldehyde in PTw 571

(phosphate buffered saline + 0.1% Tween) overnight at 4°C. The fixed glands were 572

treated with 5 mg/mL Proteinase K for 10 minutes and subjected to various 573

hybridization steps (Villarroel et al., 2016). Briefly, the glands were prehybridized in 574

hybridization buffer for 1 h at 52°C, incubated in fresh hybridization buffer and probe 575

overnight at 52°C, and subjected to six 25 min washes at 52°C with wash buffer. After 576

washing at room temperature with PBTw, the glands were incubated for 3-5 h at 4°C in 577

the dark in a 1:200 dilution of anti-digoxigenin-fluorescein (Fab fragments, Roche) in 578

PBTw. The samples were then washed with PTw for 20 min and mounted in 70% 579

glycerol in PTw. Fluorescence images were obtained under an Olympus Fluoview 580

FV1000 confocal laser-scanning microscope (Olympus Corporation, Japan). 581

582

DsRNA synthesis and injection to trigger RNA interference (RNAi) in insects 583

The DNA template for NlMLP dsRNA (dsMLP) synthesis was obtained using primer 584

pair dsMLP-F and dsMLP-R. DsMLP was synthesized using a MEGAscript T7 High 585

Yield Transcription Kit (Ambion) according to the manufacturer’s instructions. The 586

amplified NlMLP fragment (500 bp) was confirmed by sequencing. The primers 587

dsGFP-F and dsGFP-R, which were designed based on the GFP (green fluorescent 588

protein) gene template, were used to synthesize dsGFP as a negative control in the 589

RNAi experiments. The dsRNA was purified by phenol chloroform extraction and 590



23

resuspended in nuclease-free water at a concentration of 5 µg/µL. 591

Fourth-instar nymphs were anesthetized with carbon dioxide for approximately 20 592

sec until they were unconscious and placed on 2% agarose plates with their abdomens 593

facing up. A 46 nL volume of dsMLP or dsGFP was injected into each insect at the 594

junction between the prothorax and mesothorax using a microprocessor-controlled 595

Nanoliter 2010 injector (World Precision Instruments, USA). The injected BPHs were 596

reared on rice cv. TN1 plants. 597

598

Bioassay of BPHs after dsRNA injection 599

The survival rates of BPHs injected with dsGFP or dsMLP and the non-injected 600

controls were determined as follows. Pots (diameter 7 cm, height 9 cm), each 601

containing a single one-month-old TN1 rice plant grown and maintained as described 602

above, were individually covered with plastic cages into which 10 injected BPH 603

nymphs were released. The number of surviving BPH nymphs on each plant was 604

recorded daily for 10 days. The experiment was repeated five times. 605

BPH growth rates were analyzed using newly emerged brachypterous females 606

(within one day of emergence), Parafilm sachets (2×2.5 cm), and one-month-old TN1 607

rice plants grown and maintained as described. After weighing the insects and sachets, 608

the insects were placed into the sachets, which were then attached to the plants (with 609

one BPH per sachet and one sachet per plant). After 72 h, each insect and Parafilm 610

sachet was re-weighed, and the changes in weight of the BPH and sachet were defined 611

as BPH weight gain and honeydew weight, respectively. The BPH weight gain ratio 612

was calculated as the change in weight relative to the initial weight. The experiment 613

was repeated 10 times per group, and the experiments were conducted five times. 614

615

Honeydew excretion on filter paper. 616

Honeydew excretion on filter paper was measured as previously described (Du B et 617

al., 2009). One-month-old rice cv. TN1 plants grown in pots (diameter 7 cm, height 9 618

cm, one plant per pot) as described were covered with an inverted transparent plastic 619

cup placed over filter paper resting on a plastic Petri dish. Two days after injection, 620

the BPHs were placed into the chamber. After 2 days of feeding, the filter paper was 621

collected and treated with 0.1% ninhydrin in acetone solution. After 30 min of oven 622

drying at 60°C, the honeydew stains appeared violet or purple due to their amino acid 623



24

content. The area of the ninhydrin-positive deposits was measured with Image J 624

software. The experiment was repeated three times. 625

626

Development of dsMLP-transgenic rice and the BPH bioassay 627

To constitutively express NlMLP-dsRNA in rice, a 500 bp template fragment (the same 628

as the target sequence used for micro-injection) and stuffer sequence fragment (a PDK 629

intron) were used to generate a hairpin RNAi construct as previously described (Zha et 630

al., 2011). The construct was inserted into binary vector pCXUN (accession no. 631

FJ905215) under the control of the plant ubiquitin (ubi) promoter. The construct was 632

transformed into rice cv. Kasalath (an indica rice variety susceptible to BPH and 633

amenable to gene transformation) using an Agrobacterium-mediated method. 634

Integration of the foreign DNA in T0 plants was confirmed by PCR and DNA gel blot 635

analysis. The plants were cultivated, and T2 seeds were collected for the bioassay. 636

The survival rates of BPHs on transgenic and WT plants (Kasalath) were determined 637

by releasing 20 2nd instar nymphs onto each plant. The number of surviving BPHs was 638

recorded daily for 10 days. The experiment was repeated five times. NlMLP 639

expression in BPHs was evaluated by qRT-PCR. BPH weight was measured on a 640

microbalance after 10 days of feeding. 641

642

Observation of salivary sheaths on Parafilm and in planta 643

To observe the morphology of the salivary sheaths, BPHs were fed on an artificial diet 644

(D-97) consisting of amino acids, vitamins, inorganic salts, and sucrose (Fu et al., 645

2001) using plastic cylinders (4.0 cm long and 2.5 cm in diameter) as feeding 646

chambers. Sachets formed from two layers of stretched Parafilm M (~4-times the 647

original area), each containing 200 µL portions of D-97, were placed at one end of the 648

chamber. The opposite end of the chamber was covered with a piece of nylon mesh 649

after the test insects had been introduced. Insects could feed by piercing through the 650

inner Parafilm layer of the diet sachets, leaving salivary sheaths in the sachets. To 651

assess the effects of dsRNA injection on salivary sheaths, two days after injection, 652

nymphs were individually placed in the chambers and allowed to feed for 48 h. The 653

inner Parafilm layers were then placed on a microscope slide and the salivary sheaths 654

were counted under a BX51 light microscope (Olympus). Sets of 10 655

dsNlMLP-injected, dsGFP-injected, and non-injected control BPHs were used per 656



25

experiment, and the experiment was repeated three times. 657

To obtain samples for scanning electron microscopy (SEM), the inner Parafilm 658

layer was placed on a microscope slide and salivary sheaths were identified under a 659

light microscope (Olympus BX51). Regions of interest were labeled and the Parafilm 660

was cut with a scalpel. The salivary sheaths from the Parafilm were attached to a 661

sample holder, coated with gold, and observed under an S-3400N SEM (Hitachi). Five 662

replicates were prepared per treatment, and 20 randomly chosen salivary sheaths were 663

observed. 664

The dsRNA-treated BPHs were reared on one-month-old TN1 rice seedlings for 48 h, 665

and the leaf sheaths were collected and used for paraffin sectioning. One-month-old 666

rice cv. TNI plants (grown and maintained as described) were infested with a set of 10 667

dsMLP-injected, dsGFP-injected, or non-injected BPHs. The leaf sheaths produced by 668

the insects were collected, fixed in 4% paraformaldehyde, dehydrated, embedded in 669

paraffin, and cut into 10 mm thick sections with a microtome. The sections were 670

mounted on microscope slides and stained with 0.25% Coomassie Blue staining 671

solution for 10 min. The slides were dewaxed, rehydrated, examined, and photographed 672

under a light microscope. 673

674

675

Viability assay using rice protoplasts 676

Rice (cv. 9311 an indica rice variety susceptible to BPH) protoplasts were isolated 677

from 10-day-old plants as previously described (Zhang et al., 2011). The cell viability 678

and luciferase assays were conducted using rice protoplasts as described (Zhao et al., 679

2016). Briefly, for the cell viability assay, protoplasts were transfected with the 680

indicated plasmids for 20 h and stained with 220 μg/mL FDA. For the luciferase 681

assays, protoplasts were co-transfected with the reporter Renilla luciferase gene 682

(RLUC) and another construct carrying GFP or NlMLP. Luciferase activity was 683

measured 40 h after transfection using a luciferase assay system (Promega). 684

685

A. tumefaciens infiltration assays of N. benthamiana leaves 686

A sequence of interest was amplified by PCR. The PCR products and the PUC19 vector 687

were both digested by Not I and Asc I and bound by DNA ligase to create entry vectors. 688



26

Using LR Clonase reaction enzyme mix (Invitrogen), the target sequence was 689

recombined into the destination vector pEarleyGate 101 (with the YFP-HA epitope tag) 690

or pEarleyGate 100 (with no epitope tag). Constructs were introduced into A. 691

tumefaciens strain GV3101 by electroporation. Recombinant strains were cultured in 692

Luria-Bertani medium supplemented with 50 µg/mL kanamycin and 50 μg/mL 693

rifampicin, harvested, washed three times in infiltration medium (10 mM MES pH 5.6, 694

10 mM MgCl2, 150 µM acetosyringone), and resuspended in infiltration medium to an 695

OD600 of 0.3. The resuspended recombinant strains were incubated for 2 h at room 696

temperature and infiltrated into the leaves of 4- to 6-week-old N. benthamiana plants 697

(grown in a greenhouse at 25: 20°C under a 16 h light: 8 h dark cycle) through a nick 698

created using a needleless syringe. Symptom development in N. benthamiana was 699

monitored visually 3-8 d after infiltration. To test the difference of cell death symptoms 700

caused by INF1 and NlMLP, 12 pieces of N. benthamiana leaves were injected. 701

Symptom development in N. benthamiana was continued monitored visually every day 702

after infiltration. Four independent biological replicates were conducted and got 703

similar results. 704

To test the induction of plant defense-related gene expression by NlMLP, RNA was 705

extracted from N. benthamiana leaves 48 h after infiltration. SYBR green qRT-PCR 706

assays were performed to determine gene expression levels as previously described. 707

Three independent biological replicates were conducted for each experiment. 708

Agroinfiltrated N. benthamiana leaves were harvested at 48 h post inoculation. Total 709

protein extracts were prepared by grinding 400 mg of leaf tissue in 1 mL extraction 710

buffer (20 mM Tris-Cl, 1% SDS, 5 mM EDTA) in the presence of 10 mM DTT. The 711

samples were shaken on a vortex for 30 s and centrifuged at 800 g for 10 min at 4°C. 712

The resulting supernatant was used for immunoblot analysis. 713

Cell death was assayed by measuring ion leakage from leaf discs. Four leaf discs of 714

equal dimension (10 mm) were placed into 5 mL of distilled water. The first set was 715

incubated at room temperature overnight and its conductivity (C1) recorded using a 716

conductivity meter (FiveGO-FG3). The second set was boiling and its conductivity (C2) 717

recorded after cooling. Relative electrolyte leakage [(C1/C2) x 100] was calculated. 718

The experiments were carried out four times. 719

Callose deposition in infiltrated leaf disks 48 h after infiltration was visualized after 720

aniline blue staining following published methods (Naessens et al., 2015). Briefly, 721



27

dissected leaf disks were destained by successive washes in 70%, 95%, and 100% 722

EtOH for two hours per wash, washed twice with ddH2O, and incubated in aniline blue 723

solution (70 mM KH2PO4, 0.05% [w/v] aniline blue, pH 9) for 1 h. Leaf discs were 724

mounted in 80% glycerol and observed under a fluorescence microscope (FV1000, 725

Olympus). After collecting callose images, fluorescence in the images was quantified 726

with ImageJ software. Each experiment was repeated three times independently. 727

728

Virus-induced gene silencing of MEK2 in N. benthamiana plants. 729

Silencing of NbMEK2 in N. benthamiana was performed by Potato virus X (PVX) 730

VIGS as described by Sharma et al. (2003). The NbMEK2 sequence (267 bp from the 3′ 731

terminus) was inserted into the PVX vector in the antisense direction to generate 732

PVX:MEK2. The construct containing the insert and the empty vector PVX were 733

transformed into A. tumefaciens strain GV3101. Bacterial suspensions were applied to 734

the undersides of N. benthamiana seedlings (~20 days) using a 1 mL needleless syringe. 735

The plants exhibited mild mosaic symptoms 3-4 weeks after inoculation. MEK2 gene 736

expression was measured by qRT-PCR, and plants in which silencing was established 737

were subjected to further analysis. 738

739

Cell death inhibition assays. 740

The effects of the calcium channel inhibitor LaCl3 and the human anti-apoptotic gene, 741

Bcl-xl, on cell death (under dark conditions) were determined as previously described4. 742

For the rice protoplast transient expression assay and agroinfiltration into N. 743

benthamiana leaves, rice protoplast or A. tumefaciens cultures were resuspended in 744

LaCl3 at a final concentration of 1 mM. Transient expression assays were performed 745

under dark conditions to determine whether cell death induced by NlMLP is light 746

dependent. Isolated protoplasts and N. benthamiana plants were incubated in the dark 747

for 30 minutes before transfection and maintained in the dark after transfection. Bcl-xl 748

was cloned into binary vector pGR107 and introduced into A. tumefaciens strain 749

GV3101. NlMLP or the cell death-inducing gene BAX or INF1 was expressed in N. 750

benthamiana leaves 24 h after introduction of the Bcl-xl expression vector or the empty 751

control vector via agroinfiltration. 752

753

Statistical analysis 754



28

Data were compared using a Student’s t-test or a Tukey honest significant difference 755

test using PASW Statistics v18.0. 756

757

Supplemental Materials 758

Supplemental Fig. S1 Clusters of orthologous group (COG) classification of 759

sequences in the BPH salivary gland transcriptome. 760

Supplemental Fig. S2 Gene ontology (GO) classification of sequences in the BPH 761

salivary gland transcriptome. 762

Supplemental Fig. S3 NlMLP is localized to the cytoplasm in plant cells. 763

Supplemental Fig. S4 Confirmation of the effect of RNA interference on NlMLP 764

expression in BPHs. 765

Supplemental Fig. S5 Virulence of BPHs on rice plants. 766

Supplemental Fig. S6 Relative expression of NlMLP in transgenic rice (A) and BPH 767

insects (B). 768

Supplemental Fig. S7 NlMLP induces cell death in rice irrespective of the presence of 769

BPH-resistance genes (Bph6, Bph9, and Bph14). 770

Supplemental Fig. S8 Immunoblot analysis of proteins in rice protoplasts and N. 771

benthamiana. 772

Supplemental Fig. S9 Symptoms of cell death caused by INF1 and NlMLP in N. 773

benthamiana leaves. 774

Supplemental Fig. S10 Quantitative estimate of NlMLP required for plant symptoms. 775

776

Table S2 List of PCR primers used in this study. 777

Table S3 List of qRT-PCR primers used in this study. 778

779

Supplemental Methods S1 Tanscriptome analysis of BPH salivary glands. 780

Supplemental Methods S2 Gene silencing analysis by qRT-PCR. 781

Supplemental Methods S3 Gene silencing analysis by RNA gel blotting. 782

Supplemental Methods S4 Virulence of BPHs on rice plants. 783



29

Supplemental Methods S5 Determining the quantity of NlMLP required for the cell 784

death symptoms. 785



30

Table 1. Results of inhibition assays of cell death in rice protoplasts and N. 786

benthamiana leaves. 787

788

Gene Treatment

LaCl3a Dark

b Bcl-xl

c

LUC activity

in RPd

Cell

death in

NBLe

LUC activity

in RP

Cell

death in

NBL

LUC

activity in

RP

Cell

death in

NBL

GFP 1.00± 0.19 0/8 1.00± 0.34 0/8 ND 0/8

NlMLP 0.74± 0.17 1/8 0.14± 0.02* 8/8 ND 0/8

BAX 0.66± 0.21 3/8 0.09± 0.02* 7/8 ND 0/8

INF1 0.92± 0.34 3/8 0.38± 0.11* 7/8 ND 6/8

a LaCl3 was applied to protoplasts immediately after transfection at a final 789

concentration of 1 mM. For agroinfiltration of N. benthamiana leaves, LaCl3 was 790

added to resuspended A. tumefaciens cultures at a final concentration of 1 mM. 791

b Rice protoplasts and N. benthamiana leaves were incubated in the dark for 30 minutes 792

before transfection and maintained in the dark after transfection. 793

c N. benthamiana leaves were pre-infiltrated with A. tumefaciens cells harboring the 794

Bcl-xl expression vector. 795

d LUC activity in rice protoplasts, data represent means ± SE of three repeats. 796

Asterisks after the number indicate significant differences compared with the 797

corresponding GFP (*, P < 0.05, Student's t-test). 798

e Number of cell death sites/ the total infiltrated leaves of N. benthamiana. 799

ND = not determined 800

801

Figure legends 802

Figure 1. Molecular characterization of NlMLP. 803

A, Amino acid sequence of NlMLP. The solid underline indicates the signal peptide 804

predicted by SignalP. The asterisk (*) indicates the stop codon. The shaded amino acid 805



31

residues indicate the peptides detected in BPH-infested rice tissue by LC-MS/MS 806

analyses. Ser is shown in red. The repeat region is boxed. 807

B and C, Expression patterns of NlMLP at different developmental stages (B) and in 808

different tissues (C). Relative levels of NlMLP expression at the indicated 809

developmental stages (1st to 5

th, 1

st to 5

th instar; F, female adult; M, male adult) and in 810

different tissues (salivary gland, gut, fat body, and remaining carcass) normalized 811

against β-actin gene expression, as determined by qRT-PCR. Data represent means ± 812

SE of three repeats. N = 30. Different letters above the bars indicate significant 813

differences, as determined by a Tukey honest significant difference test (P < 0.05). 814

D, mRNA in situ hybridization of NlMLP in salivary glands. Signals from 815

anti-DIG-FITC (shown in green) bound to a DIG-labeled antisense riboprobe used for 816

hybridization to NIMLP transcripts were detected by confocal laser-scanning 817

microscopy. PG, principal gland. AG, accessory gland. Scale bar = 100 μm. 818

E, NlMLP localizes to the cytoplasm of rice cells when transiently expressed. GFP or 819

NlMLP-GFP fusion protein was expressed in rice protoplasts by PEG-mediated 820

transformation. Confocal laser-scanning microscopy was used to investigate fusion 821

protein distribution 16 h after transformation. Scale bar = 5 μm. 822

823

Figure 2. Effects of NlMLP silencing on BPH feeding and performance. 824

A, The survival rates of BPH insects after injection were monitored daily. The survival 825

rates of BPHs injected with dsMLP was significantly reduced compared to BPHs with 826

no injection and those injected with dsGFP after 2 days of treatment (Student’s t-test). 827

C, BPHs with no injection; dsGFP, BPHs injected with GFP-dsRNA; dsMLP, BPHs 828

injected with NlMLP-dsRNA. The experiment was repeated five times, with 10 BPHs 829

per replicate. Data represent means ± SD of five repeats. 830

B, Honeydew excretion by BPH insects on filter paper. The intensity of the honeydew 831

color and area of the honeydew correspond to BPH feeding activity. The experiment 832

was repeated three times, with 10 filter papers per replicate. Data represent means ± SE 833



32

of three repeats. Different letters above the bars indicate significant differences, as 834

determined by a Tukey honest significant difference test (P < 0.05). 835

C and D, BPH weight gain (C) and BPH weight gain ratio (D) of BPHs after injection 836

with dsGFP or dsMLP. Data represent means ± SE of five independent experiments, 837

with 10 BPHs per replicate. Different letters above the bars indicate significant 838

differences, as determined by a Tukey honest significant difference test (P < 0.05). 839

E, Survival rates of BPH insects feeding on NlMLP-dsRNA-transgenic plants (SG33-2) 840

and WT plants. The experiment was repeated five times, with 20 BPHs per replicate. 841

Data represent means ± SD of five repeats. Asterisks above the columns indicate 842

significant differences compared with WT plants (*, P < 0.05; **, P < 0.01, Student's 843

t-test). 844

F, BPH weight after feeding for 10 days on NlMLP-dsRNA-transgenic plants (SG33-2) 845

and WT plants. The experiment was repeated five times, with 10 BPHs per replicate. 846

Data represent means ± SE of five repeats. Asterisks above the columns indicate 847

significant differences compared with WT plants (*, P < 0.05, Student’s t-test). 848

849

Figure 3. Effects of NlMLP silencing on salivary sheath formation. 850

A and B, Distribution of branch number (A) and length (B) of salivary sheaths formed 851

by BPHs on an artificial diet. BPH insects were fed with dietary sucrose for 48 h and the 852

salivary sheaths were collected and counted under a fluorescence microscope. C, 853

non-injected BPHs; dsGFP, BPHs injected with GFP-dsRNA; dsMLP, BPHs injected 854

with NlMLP-dsRNA. Data represent means ± SE of three repeats. Different letters 855

above the bars indicate significant differences, as determined by a Tukey honest 856

significant difference test (P < 0.05). 857

C, D and E, Scanning electron micrographs showing the morphology of salivary 858

sheaths formed by BPHs on an artificial diet. Salivary sheaths from non-injected BPHs 859

(C) show a complete structure. BPHs injected with GFP-dsRNA (D) formed similar 860

types of sheaths. BPHs injected with NlMLP-dsRNA produced abnormal salivary 861



33

sheaths (E). Scale bar = 20 μm. 862

F, G and H, Fluorescence microscopy images showing the morphology of salivary 863

sheaths in rice plants. Rice plants were infested with BPH insects for 48 h and 864

investigated by paraffin sectioning. Sheaths produced by: F, non-injected BPHs; G, 865

BPHs injected with GFP-dsRNA; H, BPHs injected with NlMLP-dsRNA. Scale bar = 866

50 μm. 867

868

Figure 4. NlMLP causes cell death in rice protoplasts and N. benthamiana leaves. 869

A, Images of fluorescein diacetate (FDA)-stained viable rice protoplasts transformed 870

with GFP or NlMLP. Living cells were visualized using confocal laser-scanning 871

microscopy and images were taken 20 h after transformation. GFP is a control protein 872

that does not induce cell death. Scale bar = 25 μm. 873

B, Number of viable rice protoplasts transformed with GFP or NlMLP determined after 874

FDA staining. Average values and SEs were calculated from three independent 875

experiments, and 10 randomly selected microscopy fields were counted per experiment. 876

Asterisks above the columns indicate significant differences compared with GFP (**, 877

P < 0.01, Student’s t-test). 878

C, Luciferase (LUC) activity in rice protoplasts co-expressing LUC and NlMLP. Data 879

represent means ± SE of three independent experiments. Asterisks above the columns 880

indicate significant differences compared with GFP (**, P < 0.01, Student’s t-test). 881

D and E, Leaves of N. benthamiana were infiltrated with Agrobacterium tumefaciens 882

carrying GFP, INF1, and NlMLP. The leaves were photographed 5 days after 883

agroinfiltration (D), and the treated leaves were stained with trypan blue (E). INF1, a 884

control protein that induces cell death. GFP, INF1, and NlMLP with the YFP-HA 885

epitope tag; NlMLP-100, NlMLP with no epitope tag. 886

F, Quantification of cell death by measuring electrolyte leakage in N. benthamiana 887

leaves. Electrolyte leakage from the infiltrated leaf discs was measured as a percentage 888

of leakage from boiled discs 4 days after agroinfiltration. Data represent means ± SE of 889



34

four repeats. Asterisks above the columns indicate significant differences compared 890

with GFP (**, P < 0.01, Student’s t-test). 891

G and H, Silencing of NbMEK2 in N. benthamiana leaves compromises 892

NlMLP-induced cell death but not INF1-induced cell death. GFP, INF1, and NlMLP 893

were transiently expressed in N. benthamiana leaves expressing PVX vector (G) and 894

leaves in which NbMEK2 had been silenced by VIGS (H). The leaves were 895

photographed 5 days after agroinfiltration. 896

I, NbMEK2 transcript abundance in silenced N. benthamiana leaves, as measured by 897

qRT-PCR. Data represent means ± SE of three repeats. Asterisks above the columns 898

indicate significant differences compared with GFP (**, P < 0.01, Student’s t-test). 899

900

Figure 5. NlMLP affects plant defense responses during transfection. 901

A, Aniline blue staining of N. benthamiana leaves showing callose deposition spots in 902

areas transfected with GFP or NlMLP. Photographs were taken 48 h after inoculation. 903

Numbers indicate means ± SE of the number of callose spots in four individual leaf 904

discs. Scale bar = 100 mm. 905

B, Expression of the defense-related genes NbPR3, NbPR4, and NbPR1 following 906

transient expression of GFP and NlMLP in N. benthamiana leaves. Data represent 907

means ± SE of three repeats. Asterisks above the columns indicate significant 908

differences compared with GFP (**, P < 0.01, Student’s t-test). 909

910

Figure 6. Deletion analysis of NlMLP. 911

Left column, schematic diagram of NlMLP and the deletion mutants. 912

Middle column, Relative expression of NbPR4 in N. benthamiana leaves 913

agroinfiltrated with GFP or NlMLP deletion mutants, as determined by qRT-PCR. Data 914

represent means ± SE of three repeats. M, NlMLP or the deletion mutants. Asterisks 915

above the columns indicate significant differences compared with GFP (**, P < 0.01, 916

Student’s t-test). 917



35

Right column, Cell-death lesions in N. benthamiana leaves expressing the NlMLP 918

deletion mutants. +, +–, and – indicate obvious cell death, weak cell death, and no cell 919

death, respectively. Each experiment was repeated at least three times with similar 920

results. 921



36

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Figure 1. Molecular characterization of NlMLP.

A, Amino acid sequence of NlMLP. The solid underline indicates the signal peptide

predicted by SignalP. The asterisk (*) indicates the stop codon. The shaded amino acid

residues indicate the peptides detected in BPH-infested rice tissue by LC-MS/MS

analyses. Ser is shown in red. The repeat region is boxed.

B and C, Expression patterns of NlMLP at different developmental stages (B) and in

different tissues (C). Relative levels of NlMLP expression at the indicated

developmental stages (1st to 5

th, 1

st to 5

th instar; F, female adult; M, male adult) and in

different tissues (salivary gland, gut, fat body, and remaining carcass) normalized

against β-actin gene expression, as determined by qRT-PCR. Data represent means ±

SE of three repeats. N = 30. Different letters above the bars indicate significant

differences, as determined by a Tukey honest significant difference test (P < 0.05).

D, mRNA in situ hybridization of NlMLP in salivary glands. Signals from

anti-DIG-FITC (shown in green) bound to a DIG-labeled antisense riboprobe used for

hybridization to NIMLP transcripts were detected by confocal laser-scanning

microscopy. PG, principal gland. AG, accessory gland. Scale bar = 100 μm.



E, NlMLP localizes to the cytoplasm of rice cells. GFP or NlMLP-GFP fusion protein

was expressed in rice protoplasts by PEG-mediated transformation. Confocal

laser-scanning microscopy was used to investigate fusion protein distribution 16 h

after transformation. Scale bar = 5 μm.



Figure 2. Effects of NlMLP silencing on BPH feeding and performance.

A, The survival rates of BPH insects after injection were monitored daily. The survival

rates of BPHs injected with dsMLP was significantly reduced compared to BPHs with

no injection and those injected with dsGFP after 2 days of treatment (Student’s t-test).

C, BPHs with no injection. dsGFP, BPHs injected with GFP-dsRNA. dsMLP, BPHs

injected with NlMLP-dsRNA. The experiment was repeated five times, with 10 BPHs

per replicate. Data represent means ± SD of five repeats.

B, Honeydew excretion by BPH insects on filter paper. The intensity of the honeydew

color and area of the honeydew correspond to BPH feeding activity. The experiment

was repeated three times, with 10 filter papers per replicate. Data represent means ± SE

of three repeats. Different letters above the bars indicate significant differences, as

determined by a Tukey honest significant difference test (P < 0.05).

C and D, BPH weight gain (C) and BPH weight gain ratio (D) of BPHs after injection

with dsGFP or dsMLP. Data represent means ± SE of five independent experiments,

with 10 BPHs per replicate. Different letters above the bars indicate significant

differences, as determined by a Tukey honest significant difference test (P < 0.05).

E, Survival rates of BPH insects feeding on NlMLP-dsRNA-transgenic plants (SG33-2)

and WT plants. The experiment was repeated five times, with 20 BPHs per replicate.

Data represent means ± SD of five repeats. Asterisks above the columns indicate

significant differences compared with WT plants (*, P < 0.05; **, P < 0.01, Student's

t-test).

F, BPH weight after feeding for 10 days on NlMLP-dsRNA-transgenic plants (SG33-2)

and WT plants. The experiment was repeated five times, with 10 BPHs per replicate.

Data represent means ± SE of five repeats. Asterisks above the columns indicate

significant differences compared with WT plants (*, P < 0.05, Student’s t-test).



Figure 3. Effects of NlMLP silencing on salivary sheath formation.

A and B, Distribution of branch number (A) and length (B) of salivary sheaths formed

by BPHs on an artificial diet. BPH insects were fed with dietary sucrose for 48 h and the

salivary sheaths were collected and counted under a fluorescence microscope. C,

non-injected BPHs; dsGFP, BPHs injected with GFP-dsRNA; dsMLP, BPHs injected

with NlMLP-dsRNA. Data represent means ± SE of three repeats. Different letters

above the bars indicate significant differences, as determined by a Tukey honest

significant difference test (P < 0.05).

C, D and E, Scanning electron micrographs showing the morphology of salivary

sheaths formed by BPHs on an artificial diet. Salivary sheaths from non-injected BPHs

(C) show a complete structure. BPHs injected with GFP-dsRNA (D) formed similar

types of sheaths. BPHs injected with NlMLP-dsRNA produced abnormal salivary

sheaths (E). Scale bar = 20 μm.

F, G and H, Fluorescence microscopy images showing the morphology of salivary

sheaths in rice plants. Rice plants were infested with BPH insects for 48 h and

investigated by paraffin sectioning. Sheaths produced by: F, non-injected BPHs; G,

BPHs injected with GFP-dsRNA; H, BPHs injected with NlMLP-dsRNA. Scale bar =

50 μm.



Figure 4. NlMLP causes cell death in rice protoplasts and N. benthamiana leaves.

A, Images of fluorescein diacetate (FDA)-stained viable rice protoplasts transformed

with GFP or NlMLP. Living cells were visualized using confocal laser-scanning

microscopy and images were taken 20 h after transformation. GFP is a control protein

that does not induce cell death. Scale bar = 25 μm.

B, Number of viable rice protoplasts transformed with GFP or NlMLP determined after

FDA staining. Average values and SEs were calculated from three independent

experiments, and 10 randomly selected microscopy fields were counted per experiment.

Asterisks above the columns indicate significant differences compared with GFP (**,

P < 0.01, Student’s t-test).

C, Luciferase (LUC) activity in rice protoplasts co-expressing LUC and NlMLP. Data

represent means ± SE of three independent experiments. Asterisks above the columns

indicate significant differences compared with GFP (**, P < 0.01, Student’s t-test).

D and E, Leaves of N. benthamiana were infiltrated with Agrobacterium tumefaciens

carrying GFP, INF1, and NlMLP. The leaves were photographed 5 days after

agroinfiltration (D), and the treated leaves were stained with Trypan blue (E). INF1, a

control protein that induces cell death. GFP, INF1, and NlMLP with the YFP-HA

epitope tag; NlMLP-100, NlMLP with no epitope tag.

F, Quantification of cell death by measuring electrolyte leakage in N. benthamiana

leaves. Electrolyte leakage from the infiltrated leaf discs was measured as a percentage



of leakage from boiled discs 4 days after agroinfiltration. Data represent means ± SE of

four repeats. Asterisks above the columns indicate significant differences compared

with GFP (**, P < 0.01, Student’s t-test).

G and H, Silencing of NbMEK2 in N. benthamiana leaves compromises

NlMLP-induced cell death but not INF1-induced cell death. GFP, INF1, and NlMLP

were transiently expressed in N. benthamiana leaves expressing PVX vector (G) and

leaves in which NbMEK2 had been silenced by VIGS (H). The leaves were

photographed 5 days after agroinfiltration.

I, NbMEK2 transcript abundance in silenced N. benthamiana leaves, as measured by

qRT-PCR. Data represent means ± SE of three repeats. Asterisks above the columns

indicate significant differences compared with GFP (**, P < 0.01, Student’s t-test).



Figure 5. NlMLP affects plant defense responses during transfection.

A, Aniline blue staining of N. benthamiana leaves showing callose deposition spots in

areas transfected with GFP or NlMLP. Photographs were taken 48 h after inoculation.

Numbers indicate means ± SE of the number of callose spots in four individual leaf

discs. Scale bar = 100 mm.

B, Expression of the defense-related genes NbPR3, NbPR4, and NbPR1 following

transient expression of GFP and NlMLP in N. benthamiana leaves. Data represent

means ± SE of three repeats. Asterisks above the columns indicate significant

differences compared with GFP (**, P < 0.01, Student’s t-test).



Figure 6. Deletion analysis of NlMLP.

Left column, schematic diagram of NlMLP and the deletion mutants.

Middle column, Relative expression of NbPR4 in N. benthamiana leaves

agroinfiltrated with GFP or NlMLP deletion mutants, as determined by qRT-PCR. Data

represent means ± SE of three repeats. M, NlMLP or the deletion mutants. Asterisks

above the columns indicate significant differences compared with GFP (**, P < 0.01,

Student’s t-test).

Right column, Cell-death lesions in N. benthamiana leaves expressing the NlMLP

deletion mutants. +, +–, and – indicate obvious cell death, weak cell death, and no cell

death, respectively. Each experiment was repeated at least three times with similar

results.



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http://scholar.google.com/scholar?as_q=In planta expression or delivery of potato aphid Macrosiphum euphorbiae effectors Me10 and Me23 enhances aphid fecundity&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=Axelsson MA%2C Asker N%2C Hansson GC %281998%29 O%2Dglycosylated MUC2 monomer and dimer from LS 174T cells are water%2Dsoluble%2C whereas larger MUC2 species formed early during biosynthesis are insoluble and contain nonreducible intermolecular bonds%2E Journal of Biological Chemistry 273%3A 18864%2D18870&dopt=abstract

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Del Pozo O, Pedley KF, Martin GB (2004) MAPKKKαis a positive regulator of cell death associated with both plant immunity anddisease. The EMBO Journal 23: 3072-3082


Derevnina L, Dagdas YF, De la Concepcion JC, Bialas A, Kellner R, Petre B, Domazakis E, Du J, Wu C, Lin X, Aguilera-Galvez C, Cruz-Mireles N, Vleeshouwers VGAA, Kamoun S (2016) Nine things to know about elicitins. New Phytologist 212: 888-895


Du B, Zhang W, Liu B, Hu J, Wei Z, Shi Z, He R, Zhu L, Chen R, Han B, He G (2009) Identification and characterization of Bph14, a geneconferring resistance to brown planthopper in rice. Proc Natl Acad Sci USA 106: 22163-22168


Elzinga DA, De Vos M, Jander G (2014) Suppression of plant defenses by a Myzus persicae (green peach aphid) salivary effectorprotein. Mol Plant Microbe Interact 27: 747-756


Felton GW, Chung SH, Hernandez MGE, Louis J, Peiffer M, Tian D (2014) Herbivore oral secretions are the first line of protectionagainst plant-induced defences. Annual Plant Reviews 47: 37-76


Francischetti IM, Valenzuela JG, Pham VM, Garfield MK, Ribeiro JM (2002) Toward a catalog for the transcripts and proteins (sialome)from the salivary gland of the malaria vector Anopheles gambiae. J Exp Biol 205: 2429-2451


Fu Q, Zhang ZT, Hu C, Lai FX, Sun ZX (2001) A chemically defined diet enables continuous rearing of the brown planthopper,Nilaparvata lugens (Stal) (Homoptera : Delphacidae). Applied Entomology And Zoology 36: 111-116


Gornhardt B, Rouhara I, Schmelzer E (2000) Cyst germination proteins of the potato pathogen Phytophthora infestans share homologywith human mucins. Mol Plant Microbe Interact 13: 32-42


Hann DR, Rathjen JP (2007) Early events in the pathogenicity of Pseudomonas syringae on Nicotiana benthamiana. Plant J 49: 607-618Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Hao P, Liu C, Wang Y, Chen R, Tang M, Du B, Zhu L, He G (2008) Herbivore-induced callose deposition on the sieve plates of rice: animportant mechanism for host resistance. Plant Physiol 146: 1810-1820


Hattori M, Komatsu S, Noda H, Matsumoto Y (2015) Proteome analysis of watery saliva secreted by green rice leafhopper, Nephotettixcincticeps. PLoS One 10: e0123671.



http://www.ncbi.nlm.nih.gov/pubmed?term=Cheng XY%2C Zhu LL%2C He GC %282013%29 Towards understanding of molecular interactions between rice and the brown planthopper%2E Molecular Plant 6%3A 621%2D634&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Cheng XY, Zhu LL, He GC (2013) Towards understanding of molecular interactions between rice and the brown planthopper. Molecular Plant 6: 621-634

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http://search.crossref.org/?page=1&rows=2&q=Das S, Radtke A, Choi YJ, Mendes AM, Valenzuela JG, Dimopoulos G (2010) Transcriptomic and functional analysis of the Anopheles gambiae salivary gland in relation to blood feeding. BMC Genomics 11: 566.

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http://search.crossref.org/?page=1&rows=2&q=Del Pozo O, Pedley KF, Martin GB (2004) MAPKKK?is a positive regulator of cell death associated with both plant immunity and disease. The EMBO Journal 23: 3072-3082

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http://search.crossref.org/?page=1&rows=2&q=Derevnina L, Dagdas YF, De la Concepcion JC, Bialas A, Kellner R, Petre B, Domazakis E, Du J, Wu C, Lin X, Aguilera-Galvez C, Cruz-Mireles N, Vleeshouwers VGAA, Kamoun S (2016) Nine things to know about elicitins. New Phytologist 212: 888-895

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http://search.crossref.org/?page=1&rows=2&q=Du B, Zhang W, Liu B, Hu J, Wei Z, Shi Z, He R, Zhu L, Chen R, Han B, He G (2009) Identification and characterization of Bph14, a gene conferring resistance to brown planthopper in rice. Proc Natl Acad Sci USA 106: 22163-22168

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http://search.crossref.org/?page=1&rows=2&q=Elzinga DA, De Vos M, Jander G (2014) Suppression of plant defenses by a Myzus persicae (green peach aphid) salivary effector protein. Mol Plant Microbe Interact 27: 747-756

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http://search.crossref.org/?page=1&rows=2&q=Francischetti IM, Valenzuela JG, Pham VM, Garfield MK, Ribeiro JM (2002) Toward a catalog for the transcripts and proteins (sialome) from the salivary gland of the malaria vector Anopheles gambiae. J Exp Biol 205: 2429-2451

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http://www.ncbi.nlm.nih.gov/pubmed?term=Hattori M%2C Komatsu S%2C Noda H%2C Matsumoto Y %282015%29 Proteome analysis of watery saliva secreted by green rice leafhopper%2C Nephotettix cincticeps%2E PLoS One 10%3A e0123671%2E&dopt=abstract

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Hu J, Zhou J, Peng X, Xu H, Liu C, Du B, Yuan H, Zhu L, He G (2011) The Bphi008a gene interacts with the ethylene pathway andtranscriptionally regulates MAPK genes in the response of rice to brown planthopper feeding. Plant Physiol 156: 856-872


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http://search.crossref.org/?page=1&rows=2&q=Hogenhout SA, Bos JIB (2011) Effector proteins that modulate plant-insect interactions. Current Opinion In Plant Biology 14: 422-428

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http://search.crossref.org/?page=1&rows=2&q=Hu J, Zhou J, Peng X, Xu H, Liu C, Du B, Yuan H, Zhu L, He G (2011) The Bphi008a gene interacts with the ethylene pathway and transcriptionally regulates MAPK genes in the response of rice to brown planthopper feeding. Plant Physiol 156: 856-872

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http://www.ncbi.nlm.nih.gov/pubmed?term=Larousse M%2C Govetto B%2C S�assau A%2C Etienne C%2C Industri B%2C Theodorakopoulos N%2C Deleury E%2C Ponchet M%2C Panabi�res F%2C Galiana E %282014%29 Characterization of PPMUCL1%2F2%2F3%2C Three Members of a New Oomycete%2Dspecific Mucin%2Dlike Protein Family Residing in Phytophthora parasitica Biofilm%2E Protist 165%3A 275%2D292&dopt=abstract

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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%2C Reeck GR %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�??9969&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Naessens E%2C Dubreuil G%2C Giordanengo P%2C Baron OL%2C Minet%2DKebdani N%2C Keller H%2C Coustau C %282015%29 A secreted MIF cytokine enables aphid feeding and represses plant immune responses%2E Curr Biol 25%3A 1898%2D1903&dopt=abstract

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http://scholar.google.com/scholar?as_q=Immunodetection of a brown planthopper (Nilaparvata lugens Stal) salivary catalase-like protein into tissues of rice, Oryza sativa&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Petrova&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1


Pitino M, Hogenhout SA (2013) Aphid protein effectors promote aphid colonization in a plant species-specific manner. Mol PlantMicrobe Interact 26: 130–139


Reymond P (2013) Perception, signaling and molecular basis of oviposition-mediated plant responses. Planta 238: 247-258Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Reymond P, Weber H, Damond M, Farmer EE (2000) Differential gene expression in response to mechanical wounding and insectfeeding in Arabidopsis. Plant Cell 12: 707-719


Rodriguez PA, Stam R, Warbroek T, Bos JIB (2014) Mp10 and Mp42 from the aphid species Myzus persicae trigger plant defenses inNicotiana benthamiana through different activities. Molecular Plant-Microbe Interactions 27: 30-39


Rodriguez PA, Escudero-Martinez C, Bos JI, (2017) An aphid effector targets trafficking protein VPS52 in a host-specific manner topromote virulence. Plant Physiol. 173:1892-1903.


Sharma PC, Ito A, Shimizu T, Terauchi R, Kamoun S, Saitoh H (2003) Virus-induced silencing of WIPK and SIPK genes reducesresistance to a bacterial pathogen, but has no effect on the INF1-induced hypersensitive response (HR) in Nicotiana benthamiana.Molecular Genetics and Genomics 269 5: 583-591.


Takahashi Y, Nasir KH, Ito A, Kanzaki H, Matsumura H, Saitoh H, Fujisawa S, Kamoun S, Terauchi R (2007) A high-throughput screen ofcell-death-inducing factors in Nicotiana benthamiana identifies a novel MAPKK that mediates INF1-induced cell death signaling andnon-host resistance to Pseudomonas cichorii. Plant J 49: 1030-1040


Verma M, Davidson EA (1994) Mucin genes: structure, expression and regulation. Glycoconjugate Journal 11: 172-179Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Villarroel CA, Jonckheere W, Alba JM, Glas JJ, Dermauw W, Haring MA, Kant MR (2016). Salivary proteins of spider mites suppressdefenses in Nicotiana benthamiana and promote mite reproduction. Plant J 86: 119-131


Walling LL (2000) The myriad plant responses to herbivores. Journal Of Plant Growth Regulation 19: 195-216Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Walling LL (2008) Avoiding effective defenses: Strategies employed by phloem- feeding insects. Plant Physiol 146:859-866.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Wang P, Granados RR (1997) An intestinal mucin is the target substrate for a baculovirus enhancin. Proc Natl Acad Sci USA 94: 6977-6982


Will T, Tjallingii WF, Thönnessen A, van Bel AJ (2007) Molecular sabotage of plant defense by aphid saliva. Proceedings of the NationalAcademy of Sciences 104: 10536-10541



http://www.ncbi.nlm.nih.gov/pubmed?term=Pitino M%2C Hogenhout SA %282013%29 Aphid protein effectors promote aphid colonization in a plant species%2Dspecific manner%2E Mol Plant Microbe Interact 26%3A 130�??139&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Pitino M, Hogenhout SA (2013) Aphid protein effectors promote aphid colonization in a plant species-specific manner. Mol Plant Microbe Interact 26: 130?139

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http://www.ncbi.nlm.nih.gov/pubmed?term=Reymond P %282013%29 Perception%2C signaling and molecular basis of oviposition%2Dmediated plant responses%2E Planta 238%3A 247%2D258&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Reymond P (2013) Perception, signaling and molecular basis of oviposition-mediated plant responses. Planta 238: 247-258

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http://www.ncbi.nlm.nih.gov/pubmed?term=Reymond P%2C Weber H%2C Damond M%2C Farmer EE %282000%29 Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis%2E Plant Cell 12%3A 707%2D719&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Reymond P, Weber H, Damond M, Farmer EE (2000) Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12: 707-719

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

http://scholar.google.com/scholar?as_q=Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=Rodriguez PA%2C Stam R%2C Warbroek T%2C Bos JIB %282014%29 Mp10 and Mp42 from the aphid species Myzus persicae trigger plant defenses in Nicotiana benthamiana through different activities%2E Molecular Plant%2DMicrobe Interactions 27%3A 30%2D39&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Rodriguez PA, Stam R, Warbroek T, Bos JIB (2014) Mp10 and Mp42 from the aphid species Myzus persicae trigger plant defenses in Nicotiana benthamiana through different activities. Molecular Plant-Microbe Interactions 27: 30-39

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

http://scholar.google.com/scholar?as_q=Mp10 and Mp42 from the aphid species Myzus persicae trigger plant defenses in Nicotiana benthamiana through different activities&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=Mp10 and Mp42 from the aphid species Myzus persicae trigger plant defenses in Nicotiana benthamiana through different activities&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Rodriguez&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Rodriguez PA%2C Escudero%2DMartinez C%2C Bos JI%2C %282017%29 An aphid effector targets trafficking protein VPS52 in a host%2Dspecific manner to promote virulence%2E Plant Physiol%2E 173%3A1892%2D1903%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Rodriguez PA, Escudero-Martinez C, Bos JI, (2017) An aphid effector targets trafficking protein VPS52 in a host-specific manner to promote virulence. Plant Physiol. 173:1892-1903.

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

http://scholar.google.com/scholar?as_q=An aphid effector targets trafficking protein VPS52 in a host-specific manner to promote virulence&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=Sharma PC%2C Ito A%2C Shimizu T%2C Terauchi R%2C Kamoun S%2C Saitoh H %282003%29 Virus%2Dinduced silencing of WIPK and SIPK genes reduces resistance to a bacterial pathogen%2C but has no effect on the INF1%2Dinduced hypersensitive response %28HR%29 in Nicotiana benthamiana%2E Molecular Genetics and Genomics 269 5%3A 583%2D591%2E&dopt=abstract

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http://scholar.google.com/scholar?as_q=Virus-induced silencing of WIPK and SIPK genes reduces resistance to a bacterial pathogen, but has no effect on the INF1-induced hypersensitive response (HR) in Nicotiana benthamiana&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Sharma&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Takahashi Y%2C Nasir KH%2C Ito A%2C Kanzaki H%2C Matsumura H%2C Saitoh H%2C Fujisawa S%2C Kamoun S%2C Terauchi R %282007%29 A high%2Dthroughput screen of cell%2Ddeath%2Dinducing factors in Nicotiana benthamiana identifies a novel MAPKK that mediates INF1%2Dinduced cell death signaling and non%2Dhost resistance to Pseudomonas cichorii%2E Plant J 49%3A 1030%2D1040&dopt=abstract

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http://scholar.google.com/scholar?as_q=A high-throughput screen of cell-death-inducing factors in Nicotiana benthamiana identifies a novel MAPKK that mediates INF1-induced cell death signaling and non-host resistance to Pseudomonas cichorii&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Takahashi&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Verma M%2C Davidson EA %281994%29 Mucin genes%3A structure%2C expression and regulation%2E Glycoconjugate Journal 11%3A 172%2D179&dopt=abstract

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http://scholar.google.com/scholar?as_q=Mucin genes: structure, expression and regulation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Verma&as_ylo=1994&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Villarroel CA%2C Jonckheere W%2C Alba JM%2C Glas JJ%2C Dermauw W%2C Haring MA%2C Kant MR %282016%29%2E Salivary proteins of spider mites suppress defenses in Nicotiana benthamiana and promote mite reproduction%2E Plant J 86%3A 119%2D131&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Villarroel CA, Jonckheere W, Alba JM, Glas JJ, Dermauw W, Haring MA, Kant MR (2016). Salivary proteins of spider mites suppress defenses in Nicotiana benthamiana and promote mite reproduction. Plant J 86: 119-131

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http://www.ncbi.nlm.nih.gov/pubmed?term=Walling LL %282000%29 The myriad plant responses to herbivores%2E Journal Of Plant Growth Regulation 19%3A 195%2D216&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Walling LL (2000) The myriad plant responses to herbivores. Journal Of Plant Growth Regulation 19: 195-216

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http://www.ncbi.nlm.nih.gov/pubmed?term=Walling LL %282008%29 Avoiding effective defenses%3A Strategies employed by phloem%2D feeding insects%2E Plant Physiol 146%3A859%2D866%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Walling LL (2008) Avoiding effective defenses: Strategies employed by phloem- feeding insects. Plant Physiol 146:859-866.

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http://www.ncbi.nlm.nih.gov/pubmed?term=Wang P%2C Granados RR %281997%29 An intestinal mucin is the target substrate for a baculovirus enhancin%2E Proc Natl Acad Sci USA 94%3A 6977%2D6982&dopt=abstract

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http://scholar.google.com/scholar?as_q=An intestinal mucin is the target substrate for a baculovirus enhancin&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang&as_ylo=1997&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Will T%2C Tjallingii WF%2C Th�nnessen A%2C van Bel AJ %282007%29 Molecular sabotage of plant defense by aphid saliva%2E Proceedings of the National Academy of Sciences 104%3A 10536%2D10541&dopt=abstract

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Will T, Vilcinskas A (2015) The structural sheath protein of aphids is required for phloem feeding. Insect Biochem Mol Biol 57: 34-40Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Wu J, Baldwin IT (2010) New Insights into Plant Responses to the Attack from Insect Herbivores. In A Campbell, M Lichten, GSchupbach, eds, Annual Review of Genetics 44: 1-24


Wu J, Hettenhausen C, Meldau S, Baldwin IT (2007) Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regionsbut not between leaves of Nicotiana attenuata. Plant Cell 19: 1096-1122


Yang KY, Liu Y, Zhang S (2001) Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco.Proc Natl Acad Sci USA 98: 741-746


Ye W, Yu H, Jian Y, Zeng J, Ji R, Chen H, Lou Y (2017) A salivary EF-hand calcium-binding protein of the brown planthopper Nilaparvatalugens functions as an effector for defense responses in rice. Scientific Reports 7


Yu X, Tang J, Wang Q, Ye W, Tao K, Duan S, Lu C, Yang X, Dong S, Zheng X, Wang Y (2012) The RxLR effector Avh241 fromPhytophthora sojae requires plasma membrane localization to induce plant cell death. New Phytol 196: 247-260


Yuan H, Chen X, Zhu L, He G (2005) Identification of genes responsive to brown planthopper Nilaparvata lugens Stal (Homoptera:Delphacidae) feeding in rice. Planta 221: 105-112


Zha W, Peng X, Chen R, Du B, Zhu L, He G (2011) Knockdown of midgut genes by dsrna-transgenic plant-mediated RNA interference inthe hemipteran insect Nilaparvata lugens. PLoS One 6: e20504


Zhang L, Li Y, Lu W, Meng F, Wu CA, Guo X (2012) Cotton GhMKK5 affects disease resistance, induces HR-like cell death, and reducesthe tolerance to salt and drought stress in transgenic Nicotiana benthamiana. Journal of Experimental Botany 63: 3935-3951


Zhang Y, Su J, Duan S, Ao Y, Dai J, Liu J, Wang P, Li Y, Liu B, Feng D, Wang J, Wang H (2011) A highly efficient rice green tissueprotoplast system for transient gene expression and studying light/chloroplast-related processes. Plant Methods 7: 30


Zhao Y, Huang J, Wang Z, Jing S, Wang Y, Ouyang Y, Cai B, Xin X, Liu X, Zhang C (2016) Allelic diversity in an NLR gene BPH9 enablesrice to combat planthopper variation. Proceedings of the National Academy of Sciences 113: 12850-12855



http://www.ncbi.nlm.nih.gov/pubmed?term=Will T%2C Vilcinskas A %282015%29 The structural sheath protein of aphids is required for phloem feeding%2E Insect Biochem Mol Biol 57%3A 34%2D40&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Will T, Vilcinskas A (2015) The structural sheath protein of aphids is required for phloem feeding. Insect Biochem Mol Biol 57: 34-40

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

http://scholar.google.com/scholar?as_q=The structural sheath protein of aphids is required for phloem feeding&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The structural sheath protein of aphids is required for phloem feeding&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Will&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Wu J%2C Baldwin IT %282010%29 New Insights into Plant Responses to the Attack from Insect Herbivores%2E In A Campbell%2C M Lichten%2C G Schupbach%2C eds%2C Annual Review of Genetics 44%3A 1%2D24&dopt=abstract

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. In A Campbell, M Lichten, G Schupbach, eds, Annual Review of Genetics 44: 1-24

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

http://scholar.google.com/scholar?as_q=New Insights into Plant Responses to the Attack from Insect Herbivores&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=New Insights into Plant Responses to the Attack from Insect Herbivores&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wu&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Wu J%2C Hettenhausen C%2C Meldau S%2C Baldwin IT %282007%29 Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata%2E Plant Cell 19%3A 1096%2D1122&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Wu J, Hettenhausen C, Meldau S, Baldwin IT (2007) Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata. Plant Cell 19: 1096-1122

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

http://scholar.google.com/scholar?as_q=Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata&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=Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wu&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yang KY%2C Liu Y%2C Zhang S %282001%29 Activation of a mitogen%2Dactivated protein kinase pathway is involved in disease resistance in tobacco%2E Proc Natl Acad Sci USA 98%3A 741%2D746&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yang KY, Liu Y, Zhang S (2001) Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proc Natl Acad Sci USA 98: 741-746

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

http://scholar.google.com/scholar?as_q=Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco&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=Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yang&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Ye W%2C Yu H%2C Jian Y%2C Zeng J%2C Ji R%2C Chen H%2C Lou Y %282017%29 A salivary EF%2Dhand calcium%2Dbinding protein of the brown planthopper Nilaparvata lugens functions as an effector for defense responses in rice%2E Scientific Reports 7&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ye W, Yu H, Jian Y, Zeng J, Ji R, Chen H, Lou Y (2017) A salivary EF-hand calcium-binding protein of the brown planthopper Nilaparvata lugens functions as an effector for defense responses in rice. Scientific Reports 7

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

http://scholar.google.com/scholar?as_q=A salivary EF-hand calcium-binding protein of the brown planthopper Nilaparvata lugens functions as an effector for defense responses in rice.&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=A salivary EF-hand calcium-binding protein of the brown planthopper Nilaparvata lugens functions as an effector for defense responses in rice.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ye&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yu X%2C Tang J%2C Wang Q%2C Ye W%2C Tao K%2C Duan S%2C Lu C%2C Yang X%2C Dong S%2C Zheng X%2C Wang Y %282012%29 The RxLR effector Avh241 from Phytophthora sojae requires plasma membrane localization to induce plant cell death%2E New Phytol 196%3A 247%2D260&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yu X, Tang J, Wang Q, Ye W, Tao K, Duan S, Lu C, Yang X, Dong S, Zheng X, Wang Y (2012) The RxLR effector Avh241 from Phytophthora sojae requires plasma membrane localization to induce plant cell death. New Phytol 196: 247-260

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

http://scholar.google.com/scholar?as_q=The RxLR effector Avh241 from Phytophthora sojae requires plasma membrane localization to induce plant cell death&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The RxLR effector Avh241 from Phytophthora sojae requires plasma membrane localization to induce plant cell death&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yu&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yuan H%2C Chen X%2C Zhu L%2C He G %282005%29 Identification of genes responsive to brown planthopper Nilaparvata lugens Stal %28Homoptera%3A Delphacidae%29 feeding in rice%2E Planta 221%3A 105%2D112&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yuan H, Chen X, Zhu L, He G (2005) Identification of genes responsive to brown planthopper Nilaparvata lugens Stal (Homoptera: Delphacidae) feeding in rice. Planta 221: 105-112

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

http://scholar.google.com/scholar?as_q=Identification of genes responsive to brown planthopper Nilaparvata lugens Stal (Homoptera: Delphacidae) feeding in rice&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=Identification of genes responsive to brown planthopper Nilaparvata lugens Stal (Homoptera: Delphacidae) feeding in rice&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yuan&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zha W%2C Peng X%2C Chen R%2C Du B%2C Zhu L%2C He G %282011%29 Knockdown of midgut genes by dsrna%2Dtransgenic plant%2Dmediated RNA interference in the hemipteran insect Nilaparvata lugens%2E PLoS One 6%3A e20504&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zha W, Peng X, Chen R, Du B, Zhu L, He G (2011) Knockdown of midgut genes by dsrna-transgenic plant-mediated RNA interference in the hemipteran insect Nilaparvata lugens. PLoS One 6: e20504

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

http://scholar.google.com/scholar?as_q=Knockdown of midgut genes by dsrna-transgenic plant-mediated RNA interference in the hemipteran insect Nilaparvata lugens.&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=Knockdown of midgut genes by dsrna-transgenic plant-mediated RNA interference in the hemipteran insect Nilaparvata lugens.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zha&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang L%2C Li Y%2C Lu W%2C Meng F%2C Wu CA%2C Guo X %282012%29 Cotton GhMKK5 affects disease resistance%2C induces HR%2Dlike cell death%2C and reduces the tolerance to salt and drought stress in transgenic Nicotiana benthamiana%2E Journal of Experimental Botany 63%3A 3935%2D3951&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang L, Li Y, Lu W, Meng F, Wu CA, Guo X (2012) Cotton GhMKK5 affects disease resistance, induces HR-like cell death, and reduces the tolerance to salt and drought stress in transgenic Nicotiana benthamiana. Journal of Experimental Botany 63: 3935-3951

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=Cotton GhMKK5 affects disease resistance, induces HR-like cell death, and reduces the tolerance to salt and drought stress in transgenic Nicotiana benthamiana&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=Cotton GhMKK5 affects disease resistance, induces HR-like cell death, and reduces the tolerance to salt and drought stress in transgenic Nicotiana benthamiana&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang Y%2C Su J%2C Duan S%2C Ao Y%2C Dai J%2C Liu J%2C Wang P%2C Li Y%2C Liu B%2C Feng D%2C Wang J%2C Wang H %282011%29 A highly efficient rice green tissue protoplast system for transient gene expression and studying light%2Fchloroplast%2Drelated processes%2E Plant Methods 7%3A 30&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang Y, Su J, Duan S, Ao Y, Dai J, Liu J, Wang P, Li Y, Liu B, Feng D, Wang J, Wang H (2011) A highly efficient rice green tissue protoplast system for transient gene expression and studying light/chloroplast-related processes. Plant Methods 7: 30

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=A highly efficient rice green tissue protoplast system for transient gene expression and studying light/chloroplast-related processes.&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=A highly efficient rice green tissue protoplast system for transient gene expression and studying light/chloroplast-related processes.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhao Y%2C Huang J%2C Wang Z%2C Jing S%2C Wang Y%2C Ouyang Y%2C Cai B%2C Xin X%2C Liu X%2C Zhang C %282016%29 Allelic diversity in an NLR gene BPH9 enables rice to combat planthopper variation%2E Proceedings of the National Academy of Sciences 113%3A 12850%2D12855&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhao Y, Huang J, Wang Z, Jing S, Wang Y, Ouyang Y, Cai B, Xin X, Liu X, Zhang C (2016) Allelic diversity in an NLR gene BPH9 enables rice to combat planthopper variation. Proceedings of the National Academy of Sciences 113: 12850-12855

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

http://scholar.google.com/scholar?as_q=Allelic diversity in an NLR gene BPH9 enables rice to combat planthopper variation&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=Allelic diversity in an NLR gene BPH9 enables rice to combat planthopper variation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhao&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1


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A mucin-like protein of planthopper is required for ... · insect pest of rice that causes extensive yield losses and economic damage to rice both . 142. directly (by feeding) and