1 Running Title: OPDA regulates maize defense against aphids 2 - … · Varsani et al. 4 94 ABSTRACT 95 The corn leaf aphid (CLA; Rhopalosiphum maidis) is a phloem sap-sucking insect

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Running Title: OPDA regulates maize defense against aphids 1

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Author for Correspondence: Joe Louis 4

Department of Entomology and Department of Biochemistry 5

University of Nebraska-Lincoln 6

Lincoln, NE 68583, USA 7

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Phone: (402) 472-8098 9

Fax: (402) 472-4687 10

E-mail: [email protected] 11

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Research Area: Signaling and Response 15

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Plant Physiology Preview. Published on January 14, 2019, as DOI:10.1104/pp.18.01472

Copyright 2019 by the American Society of Plant Biologists

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12-Oxo-phytodienoic acid acts as a regulator of maize defense against corn leaf aphid 32

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Suresh Varsani, Sajjan Grover, Shaoqun Zhou, Kyle G. Koch, Pei-Cheng Huang, Michael V. 35

Kolomiets, W. Paul Williams, Tiffany Heng-Moss, Gautam Sarath, Dawn S. Luthe, 36

Georg Jander, and Joe Louis* 37

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Department of Entomology (S.V., S.G., K.G.K., T.H-M., J.L.) and Department of Biochemistry 40

(J.L.), University of Nebraska-Lincoln, Lincoln, NE 68583 41

Boyce Thompson Institute (S.Z., G.J.) and School of Integrated Plant Sciences, Cornell 42

University (S.Z.), Ithaca, NY 14853 43

Department of Plant Pathology and Microbiology (P-C.H., M.V.K.), Texas A & M University, 44

College Station, TX 77843 45

USDA-ARS Corn Host Plant Resistance Research Unit (W.P.W.), Mississippi State, MS 39762 46

Wheat, Sorghum, and Forage Research Unit (G.S.), USDA-ARS, Lincoln, NE 68583 47

Department of Plant Science (D.S.L.), Pennsylvania State University, University Park, PA 16802 48

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*Corresponding author 51

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One-sentence summary 54

12-Oxo-phytodienoic acid promotes enhanced callose accumulation and heightened maize 55

resistance against aphids. 56

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FOOTNOTES 63

Funding information: This work was partially supported by the Nebraska Agricultural 64

Experiment Station with funding from the Hatch Act (Accession # 1007272) through the USDA 65

National Institute of Food and Agriculture and start-up research funds from the University of 66

Nebraska-Lincoln to J.L. Work in G.J. laboratory was supported by US National Science 67

Foundation award #1339237. Work in M.V.K. laboratory was supported by USDA-NIFA grant # 68

2017-67013-26524. Work in T.H-M. and G.S. laboratories was supported in part by USDA-69

NIFA grant # 2011-67009-30096, and by the USDA-ARS CRIS project grant # 3042-21000-70

030-00D (G.S.). 71

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The author responsible for distribution of materials integral to the findings presented in this 73

article in accordance with the Journal policy described in the Instructions for Authors 74

(http://www.plantphysiol.org) is: Joe Louis ([email protected]). 75

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Author contributions: S.V. and J.L. conceived and designed the research; S.V. conducted most 77

of the experiments; S.G. assisted with the aphid feeding behavior experiments and data analysis; 78

S.Z. performed the benzoxazinoids quantification experiments; G.J. supervised the 79

benzoxazinoids quantification and analysis; K.G.K., T.H-M., G.S., and D.S.L. contributed to 80

methods development, reagents, and data analysis; W.P.W., P.-C.H., and M.V.K. developed the 81

maize genotypes used in the study; S.V. and J.L. wrote the article with contributions from all 82

authors. 83

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ABSTRACT 94

The corn leaf aphid (CLA; Rhopalosiphum maidis) is a phloem sap-sucking insect that attacks 95

many cereal crops, including maize (Zea mays). We previously showed that the maize inbred line 96

Mp708, which was developed by classical plant breeding, provides enhanced resistance to CLA. 97

Here, using electrophysiological monitoring of aphid feeding behavior, we demonstrate that 98

Mp708 provides phloem-mediated resistance to CLA. Furthermore, feeding by CLA on Mp708 99

plants enhanced callose deposition, a potential defense mechanism utilized by plants to limit 100

aphid feeding and subsequent colonization. In maize, benzoxazinoids (BX) or BX-derived 101

metabolites contribute to enhanced callose deposition by providing heightened resistance to 102

CLA. However, BX and BX-derived metabolites were not significantly altered in CLA-infested 103

Mp708 plants, indicating BX-independent defense against CLA. Evidence presented here 104

suggests that the constitutively higher levels of 12-oxo-phytodienoic acid (OPDA) in Mp708 105

plants contributed to enhanced callose accumulation and heightened CLA resistance. OPDA 106

enhanced the expression of ethylene biosynthesis and receptor genes, and the synergistic 107

interactions of OPDA and CLA feeding significantly induced the expression of the transcripts 108

encoding Maize insect resistance1-Cysteine Protease (Mir1-CP), a key defensive protein against 109

insect pests, in Mp708 plants. Furthermore, exogenous application of OPDA on maize jasmonic 110

acid (JA)-deficient plants caused enhanced callose accumulation and heightened resistance to 111

CLA, suggesting that the OPDA-mediated resistance to CLA is independent of the JA pathway. 112

We further demonstrate that the signaling function of OPDA, rather than a direct toxic effect, 113

contributes to enhanced CLA resistance in Mp708. 114

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INTRODUCTION 125

Despite being a major cereal crop grown worldwide for food, feed, and fuel, maize (Zea mays) is 126

attacked by a plethora of insect pests. Among these insect pests, corn leaf aphids (CLA; 127

Rhopalosiphum maidis) constitute the largest group of phloem-feeding insects that limit maize 128

productivity (Bing and Guthrie, 1991; Meihls et al., 2012). In addition to removing nutrients 129

from phloem sap and altering source-sink patterns, which negatively affects plant productivity, 130

CLA also is a vector for several plant viral diseases (Thongmeearkom et al., 1976; Carena and 131

Glogoza, 2004; So et al., 2010). Furthermore, heavy CLA infestations on maize result in wilting, 132

curling, and discoloration of leaves. Digestive waste products of CLA (e.g., honeydew), which 133

are deposited on the maize leaf surface, promote mold growth and reduce photosynthetic 134

efficiency, thereby accentuating damage (Carena and Glogoza, 2004). 135

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Phloem-sap-sucking insects, such as CLA, utilize their long slender stylets to penetrate 137

plant tissues and consume nutrients in the sap. Salivary secretions released by aphids enable 138

them to successfully colonize host plants and circumvent activation of plant defenses. Aphids, 139

while feeding on the host plants, inject salivary secretions that potentially interfere with sealing 140

of sieve elements. Aphids release two types of salivary secretions: gelling or sheath saliva and 141

watery saliva. Sheath saliva rapidly sets and seals the wound imposed by stylet penetration and 142

impedes the release of host factors that contribute to the plugging of phloem sieve plates upon 143

aphid stylet insertion (Miles, 1999; Will and Vilcinskas, 2015). On the other hand, watery saliva 144

is secreted continuously during feeding and interacts with phloem proteins, thereby blocking 145

their coagulation. Moreover, the watery saliva contains several enzymes that inhibit phloem 146

sealing and callose deposition, thereby allowing aphids to feed continuously from a single sieve 147

element (Miles, 1999). In addition, several studies have shown that some of these aphid salivary 148

components function as effectors that modulate the plant defense responses (Mutti et al., 2008; 149

Atamian et al., 2013; Chaudhary et al., 2014; Elzinga et al., 2014; Kettles and Kaloshian, 2016; 150

Mugford et al., 2016; Rodriguez et al., 2017). In response, plants use an extensive array of 151

defenses to prevent aphid feeding and colonization. Callose deposition, one of the defense 152

mechanisms utilized by plants, contributes to sieve element occlusion and, thus, control of 153

infestation by phloem-feeding insects (Will and van Bel, 2006). For example, callose deposition 154

in the sieve elements is associated with resistance in rice (Oryza sativa) against brown 155



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planthopper (Nilaparvata lugens) (Hao et al., 2008). In addition, Arabidopsis (Arabidopsis 156

thaliana) responds to silverleaf whitefly (Bemisia tabaci) and green peach aphid (Myzus 157

persicae) infestations by enhancing callose deposition and expression of the callose synthase 158

encoding genes (Kempema et al., 2007; Casteel et al., 2014; Mondal et al., 2018). 159

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Benzoxazinoids (BX), a class of secondary metabolites, contribute to maize defense 161

against CLA (Ahmad et al., 2011). The CLA population was significantly higher on BX-162

deficient maize plants. Furthermore, the enhanced CLA numbers on BX-deficient maize lines 163

correlated with the reduced accumulation of callose (Ahmad et al., 2011). 2,4-Dihydroxy-7-164

methoxy-1,4-benzoxazin-3-one (DIMBOA), an intermediate compound in the BX pathway, acts 165

as a signaling molecule in regulating CLA feeding-induced callose accumulation in resistant 166

maize lines (Ahmad et al., 2011). Indeed, infiltration of DIMBOA into the maize leaves 167

stimulated callose accumulation. In addition, the parental lines of the maize nested association 168

mapping (NAM) population that had elevated levels of 2,4-dihydroxy-7-methoxy-1,4-169

benzoxazin-3-one glucoside (DIMBOA-Glc), the precursor for 2,4-dihydroxy-7-methoxy-1,4-170

benzoxazin-3-one (DIMBOA), were more resistant to CLA by enhancing callose accumulation 171

(Meihls et al., 2013). These studies confirm that the BX or BX-derived metabolites are involved 172

in enhancing callose accumulation, thus providing elevated maize resistance to CLA. 173

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We have previously shown that the maize inbred line Mp708 has enhanced defense 175

against CLA (Louis et al., 2015). CLA feeding on Mp708 plants rapidly induced the 176

accumulation of the transcripts encoding Maize insect resistance1-Cysteine Protease (Mir1-CP) 177

defensive protein. Mir1-CP is localized to the vascular tissues, and feeding trial bioassays have 178

confirmed that the recombinant Mir1-CP adversely influences CLA fecundity (Lopez et al., 179

2007; Louis et al., 2015). Furthermore, aboveground feeding by CLA rapidly sends as yet 180

unidentified signals to the roots that trigger belowground accumulation of mir1 (Louis et al., 181

2015; Varsani et al., 2016). In support of a role for an aboveground-belowground signaling 182

mechanism, CLA-feeding-induced mir1 expression provided enhanced resistance to subsequent 183

belowground feeding of western corn rootworm (Diabrotica virgifera virgifera) (Varsani et al., 184

2016). Root removal prior to CLA infestation significantly affected the accumulation of mir1 185

transcripts in the aboveground whorl region of Mp708 plants. These results, in conjunction with 186



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the observation that roots act as a site for Mir1-CP synthesis in response to foliar CLA feeding, 187

suggest that the presence of Mir1-CP in the vascular tissues contributes to enhanced resistance to 188

CLA. 189

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In addition to defensive proteins, phytohormones, including jasmonic acid (JA), salicylic 191

acid (SA), and ethylene (ET), interactively modulate plant defenses against insect herbivory 192

(Howe and Jander, 2008; Erb et al., 2012; Louis and Shah, 2013). For example, it has been 193

shown that elevated levels of SA due to loss of FATTY ACID DESATURASE7 (FAD7) activity in 194

tomato (Solanum lycopersicum) resulted in hyperresistance against potato aphids (Macrosiphum 195

euphorbiae) (Avila et al., 2012). In addition to SA, JA plays a critical role in providing resistance 196

against aphids. In sorghum (Sorghum bicolor), methyl jasmonate treatment of seedlings resulted 197

in fewer numbers of greenbug aphids (Schizaphis graminum) compared to the untreated control 198

plants, suggesting the significance of JA-pathway-mediated defense in sorghum against aphids 199

(Zhu-Salzman et al., 2004). In addition, it has been shown that AKR (Acyrthosiphon kondoi 200

resistance)-mediated resistance against blue green aphids (Acyrthosiphon kondoi) in Medicago 201

truncatula and Arabidopsis resistance against cabbage aphids (Brevicoryne brassicae) require 202

the JA pathway (Gao et al., 2007; Kuśnierczyk et al., 2011). ET, primarily considered to be 203

synergistic with JA, also was shown to be induced by aphid infestation in resistant varieties of 204

tomato and melon (Anstead et al., 2010). Recent studies on maize-CLA interaction suggested a 205

potential role of SA-JA antagonism and ET in modulating defenses against aphids (Louis et al., 206

2015; Tzin et al., 2015). The maize Mp708 genotype has constitutively elevated levels of JA and 207

12-oxo-phytodienoic acid (OPDA) (Shivaji et al., 2010). Previously, it was suggested that JA 208

acts upstream of ET in activating mir1-mediated defenses in maize against chewing insects 209

(Ankala et al., 2009). However, JA was not a critical component in the mir1-determined 210

enhanced resistance to CLA (Louis et al., 2015). Instead, the enhanced mir1-determined 211

resistance to CLA in the Mp708 genotype depended only on the ET pathway (Louis et al., 2015). 212

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OPDA, an intermediate in the JA biosynthesis pathway, can contribute to plant defense 214

against insect pests. For example, OPDA stimulates enhanced resistance in rice and wheat 215

(Triticum aestivum) against brown planthopper and Hessian fly (Mayetiola destructor), 216

respectively (Guo et al., 2014; Cheng et al., 2018). Similarly, Arabidopsis opr3 plants, which are 217



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deficient in JA but accumulate elevated levels of OPDA, were shown to have enhanced 218

resistance to the dipteran insect Bradysia impatiens (Stintzi et al., 2001). By contrast, cabbage 219

loopers (Trichoplusia ni) reared on the Arabidopsis opr3 plants had significantly higher weight 220

than the wild-type plant, suggesting that OPDA may not be a critical component in providing 221

resistance to chewing herbivores (Chehab et al., 2011). As mentioned before, insects release 222

salivary secretions while feeding, which could potentially activate wound-induced signaling 223

molecules, such as OPDA, and trigger the downstream defenses in plants (Park et al., 2013; 224

Bosch et al., 2014a, 2014b; Guo et al., 2014; López-Galiano et al., 2017). More recent studies 225

have suggested that oxylipins, a large family of oxidized lipids including OPDA, are involved in 226

enhancing callose accumulation in host plants to limit pathogen infection (Marcos et al., 2015; 227

Scalschi et al., 2015), which is also a potential defense mechanism utilized by plants to disrupt 228

aphid colonization. 229

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In this study, we investigated whether the constitutively elevated levels of OPDA in the 231

Mp708 genotype are critical for the mir1-mediated defense against CLA. We demonstrate that 232

the Mp708 genotype provides enhanced resistance to CLA by promoting callose accumulation, 233

independent of the BX pathway. Our data suggest that OPDA is involved in activating callose 234

formation and enhanced resistance to CLA in Mp708 plants. OPDA application enhances the 235

expression of ET biosynthesis and receptor genes, which act as a central node in regulating mir1 236

expression to different feeding guilds of insect herbivores (Louis et al., 2015). We further show 237

that the OPDA-mediated enhanced callose accumulation and resistance to CLA is independent of 238

the JA pathway. Our results also suggest that the signaling function of OPDA (Taki et al., 2005; 239

Böttcher and Pollman, 2009), not the direct toxic effect, contributes to heightened resistance to 240

CLA in Mp708 plants. 241

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RESULTS 244

The Maize Inbred Line Mp708 Promotes Phloem-Based Resistance to CLA 245

Previously, we showed that Mp708 promotes enhanced resistance to CLA (Louis et al., 2015). 246

We utilized the electrical penetration graph (EPG) technique to monitor and quantify the 247

different CLA feeding patterns on resistant (Mp708) and susceptible (Tx601 and B73) maize 248



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genotypes. The different waveform patterns quantified from the EPG experiments include (1) 249

total duration of the pathway phase (PP) that includes both the inter- and/or intracellular aphid 250

stylet routes during the brief sampling of cells; (2) total duration of nonprobing phase (NP) that 251

includes relatively no aphid stylet movement or activity on the plant tissues; (3) time to reach 252

first sieve element phase (f-SEP); (4) total duration of sieve element phase (SEP) or phloem 253

phase when the aphid stylets are in the phloem/sieve element and actively ingest nutrients; and 254

(5) total duration of xylem phase (XP) when the aphid inserts its stylets into the xylem and feeds 255

on the xylem sap. There were no significant differences (P > 0.05; Kruskal-Wallis test) in the PP, 256

NP, f-SEP, and XP waveform patterns measured for CLA feeding behavior on the resistant 257

Mp708 and susceptible Tx601 genotypes (Fig. 1; Table 1). However, CLA spent significantly 258

less time in the sieve elements of the resistant maize genotype Mp708 compared to Tx601 plants, 259

suggesting that Mp708’s resistance to CLA is phloem-localized (Fig. 1; Table 1). Figure 1B 260

shows the representative EPG waveform patterns produced by CLA feeding on resistant Mp708 261

and susceptible Tx601 genotypes. Similarly, comparison of CLA feeding behavioral activities 262

between Mp708 and B73, a reference maize line that supports CLA numbers comparable to the 263

Tx601 genotype (Louis et al., 2015), revealed that CLA spent significantly less time feeding 264

from the sieve elements of Mp708 plants (Supplemental Fig. S1, A and B). These data suggest 265

that Mp708 promotes phloem-based resistance to CLA and restricts the sustained feeding of 266

CLA from the sieve elements. 267

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CLA Infestation Enhanced Callose Deposition in Mp708 Plants 269

Callose deposition is an important plant defense mechanism that contributes to phloem occlusion 270

and thereby controls the infestation of phloem-feeding insects (Will and van Bel, 2006; Hao et 271

al., 2008; Mondal et al., 2018). Since Mp708 plants restrict CLA ability to continuously feed 272

from the sieve elements, we monitored the temporal accumulation of callose in Mp708 and 273

Tx601 maize genotypes before and after CLA infestation. Interestingly, Mp708 plants had 274

constitutively higher callose spots compared to Tx601 genotypes (Fig. 2A). In addition, Mp708 275

plants had significantly higher callose accumulation through 24 h of CLA infestation compared 276

to the Tx601 genotype (Fig. 2A). We also monitored the expression of Tie-dyed2 (Tdy2), a gene 277

highly expressed in the vascular tissues and involved in the synthesis of callose in maize 278

(Slewinski et al., 2012), to investigate whether the enhanced callose accumulation in resistant 279



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maize plants correlates with the higher expression of callose synthase gene. Although Tdy2 280

expression was not significantly different between Mp708 and Tx601 plants before CLA 281

infestation, CLA feeding for 24 h significantly increased the expression of Tdy2 in Mp708 plants 282

compared to Tx601 plants (Fig. 2B). These findings, coupled with the EPG experiments in which 283

we observed reduced aphid feeding from the sieve elements of Mp708 plants, suggest that 284

enhanced callose deposition in the resistant maize genotype restricts sustained aphid feeding. 285

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BX or BX-Derived Metabolites Are Not Significantly Altered in CLA-Infested Mp708 287

Plants 288

Indole-derived BX act as key defensive secondary metabolites against insect attack in maize 289

(Meihls et al., 2012). DIMBOA-Glc and 2-hydroxy-4,7- dimethoxy-1,4-benzoxazin-3-one 290

glucoside (HDMBOA-Glc) constitute the most abundant BX in maize (Frey et al., 2009; Meihls 291

et al., 2013). Furthermore, DIMBOA, a breakdown product of DIMBOA-Glc, was sufficient to 292

trigger callose deposition in maize (Ahmad et al., 2011; Meihls et al., 2012, 2013; Betsiashvili et 293

al., 2015). To test the possible role of DIMBOA and breakdown products of DIMBOA in 294

enhanced callose accumulation in Mp708 plants, we monitored the temporal accumulation of 295

BX-derived metabolites before and after CLA infestation. As shown in Figure 3A, comparison of 296

Tx601 and Mp708 plants revealed that DIMBOA-Glc concentration was not changed at early 297

time points of CLA feeding but was significantly increased in the susceptible Tx601 plants after 298

24 h of CLA feeding. DIMBOA-Glc concentration in the resistant Mp708 genotype was not 299

significantly altered over the 24-h period of CLA feeding (Fig. 3A). HDMBOA-Glc and 300

DIMBOA abundance were comparable in the Tx601 and Mp708 plants before and after CLA 301

infestation (Fig. 3, B and C). Similarly, two downstream metabolites of DIMBOA-Glc, 2,4-302

dihydroxy-7,8-dimethoxy-1,4-benzoxazin-3-one glucoside (DIM2BOA-Glc) and 2,4-dihydroxy-303

7,8-dimethoxy-1,4-benzoxazin-3-one (DIM2BOA) that can also contribute to CLA resistance 304

(Handrick et al., 2016), were not significantly altered before and after CLA infestation in the 305

Tx601 and Mp708 plants (Fig. 3, D and E). Furthermore, we monitored the expression of several 306

genes involved in the BX biosynthesis (Tzin et al., 2017), before and after CLA infestation. 307

Although Mp708 plants had constitutively elevated expression of BX1 compared to Tx601 308

plants, CLA feeding for 24 h suppressed the expression of BX1 in Mp708 plants and was 309

comparable to the susceptible Tx601 plants (Supplemental Fig. S2A). Additionally, expression 310



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of BX7 and BX11 genes was comparable in Tx601 and Mp708 plants before and after CLA 311

infestation for 24 h (Supplemental Fig. S2, B and C). Although there was higher expression of 312

BX13 in CLA uninfested Tx601 and Mp708 plants, CLA feeding for 24 h significantly decreased 313

BX13 transcript expression on both maize genotypes and was comparable in Tx601 and Mp708 314

plants (Supplemental Fig. S2D). Collectively, these data suggest that BX or BX-derived 315

metabolites are not major contributors to the Mp708 resistance to CLA, and defense signals other 316

than DIMBOA and/or BX-derived metabolites may be involved in activating aphid-induced 317

callose formation in Mp708 plants. 318

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OPDA Promotes Enhanced Callose Deposition and Heightened Resistance to CLA in 320

Mp708 Plants 321

As found previously (Shivaji et al., 2010), resistant Mp708 plants had constitutively higher levels 322

of OPDA and JA compared to susceptible Tx601 plants. However, higher levels of JA were not 323

critical for providing defense against CLA in Mp708 plants (Louis et al., 2015). OPDA, a 324

precursor for JA biosynthesis, is also involved in activating plant defenses not related to the JA 325

pathway (Taki et al., 2005; Böttcher and Pollman, 2009). Furthermore, it has been shown that 326

OPDA enhances plant defenses by inducing callose accumulation (Scalschi et al., 2015). To 327

investigate whether the elevated levels of OPDA contribute to callose accumulation in maize 328

plants, we pretreated Tx601 and Mp708 genotypes with OPDA for 24 h. Our results indicate that 329

the OPDA pretreatment (+ OPDA) alone significantly increased callose accumulation and 330

expression of Tdy2 in Mp708 plants (+ OPDA) compared with Mp708 control plants (- OPDA) 331

(Fig. 4A; Supplemental Fig. S3A). In contrast, exogenous application of OPDA did not elicit a 332

significant increase in the callose accumulation and Tdy2 transcript levels in Tx601 plants (+ 333

OPDA) compared to Tx601 control plants (- OPDA) (Fig. 4A; Supplemental Fig. S3B). When 334

compared with Mp708 plants infested with CLA, exogenous application of OPDA and 335

subsequent feeding by CLA significantly increased the callose deposition in Mp708 plants (Fig. 336

4A). However, this was not the case with Tx601 plants, where we observed no significant 337

difference in the callose accumulation after CLA infestation with and without exogenous 338

application of OPDA (Fig. 4A). These results indicate that the OPDA and CLA feeding interact 339

synergistically to promote enhanced callose deposition in Mp708 plants. 340

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To test whether exogenous application of OPDA contributes to enhanced resistance to 342

CLA, we pretreated maize plants with OPDA (50 µM) 24 h prior to aphid release. OPDA 343

pretreatment contributed to enhanced resistance in Mp708 plants compared with Mp708 control 344

plants (- OPDA) (Fig. 4B). However, OPDA pretreatment of Tx601 plants did not adversely 345

affect the CLA population compared with Tx601 control plants (- OPDA) (Fig. 4B). These 346

results further confirmed the positive influence of OPDA on callose deposition and heightened 347

resistance to CLA in Mp708 plants. 348

349

To confirm the observed role of OPDA in promoting enhanced callose deposition and 350

heightened resistance to CLA in Mp708 plants, we pretreated the plants with either 2-deoxy-D-351

glucose (DDG), an inhibitor of callose synthesis in plants (Jakab et al., 2001; Hamiduzzaman et 352

al., 2005), OPDA, or coapplied OPDA and DDG 24 h prior to CLA infestation. DDG application 353

on Mp708 leaves suppressed the expression of callose synthase Tdy2 transcript abundance 354

(Supplemental Fig. S4). Mp708 plants treated with DDG prior to CLA infestation supported 355

higher numbers of aphids in a no-choice bioassay compared to Mp708 control plants (Fig. 5). As 356

expected, OPDA-treated Mp708 plants provided enhanced resistance to CLA compared to 357

Mp708 control plants. However, coapplication of OPDA and DDG did not restore the resistance 358

phenotype of Mp708 plants against CLA. The aphid numbers were comparable to Mp708 plants 359

that were pretreated with DDG alone (Fig. 5), indicating that OPDA acts upstream of callose 360

accumulation and may have a direct role in the regulation of callose accumulation in Mp708 361

plants. In contrast, no differences in CLA numbers were observed between the control and DDG 362

pretreated Tx601 plants (Supplemental Fig. S5). The aphid bioassay data, which indicate that 363

OPDA promotes heightened resistance to CLA (Fig. 5), was further supported by EPG studies 364

where we monitored the feeding behavior of CLA on Mp708 plants after pretreatment with either 365

DDG, OPDA, or coapplication with OPDA and DDG 24 h prior to CLA infestation. The 366

duration of time spent by CLA in the sieve element phase (SEP) was considerably shorter in 367

OPDA-pretreated Mp708 plants compared to Mp708 control plants (Supplemental Table S1), 368

indicating that OPDA-promoted callose accumulation deters CLA feeding from sieve elements. 369

However, the aphids were able to overcome this feeding block when the Mp708 plants were 370

pretreated with DDG or coapplied with OPDA and DDG (Supplemental Table S1). In addition, 371

we observed a corresponding reduction in the duration of the pathway phase, during which the 372



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aphids puncture the different plant cells to locate sieve elements, when the plants were pretreated 373

with DDG or coapplied with OPDA and DDG compared to control Mp708 plants (Supplemental 374

Table S1). These results suggest that the OPDA-mediated callose accumulation deters aphid 375

feeding from sieve elements and subsequently promotes enhanced resistance to CLA in the 376

Mp708 genotype. 377

378

OPDA Application Enhances CLA-Feeding-Induced mir1 and Ethylene Biosynthesis and 379

Receptor Genes in Mp708 Plants 380

To further examine the role of OPDA in activating other defense responses in Mp708 plants, 381

including the ET pathway and its interaction with the mir1 defensive gene (Louis et al., 2015), 382

we monitored the expression of maize ethylene biosynthesis and receptor genes (Young et al., 383

2004; Yamauchi et al., 2016) and mir1 gene activation. Pretreatment of Mp708 plants with 384

OPDA significantly induced the expression of maize ethylene biosynthesis (Aminocyclopropane-385

1-Carboxylic acid Synthase 2 [ACS2], ACS6, and ACC Oxidase 15 [ACO15]) and receptor 386

(Ethylene Response Sensor 14 [ERS14]) genes (Fig. 6, A-D). However, the same treatment did 387

not significantly alter the response of ethylene biosynthesis gene in Tx601 plants (Supplemental 388

Fig. S3C). In addition, exogenous OPDA application and subsequent feeding by CLA 389

significantly increased the expression of maize ethylene biosynthesis and receptor genes in 390

Mp708 plants compared to Mp708 plants infested with CLA (Fig. 6, A-D). Analysis of mir1 391

expression revealed that OPDA treatment alone did not enhance the mir1 transcript 392

accumulation. However, synergistic interactions of OPDA and CLA feeding significantly 393

increased mir1 transcript accumulation compared to CLA feeding alone on Mp708 plants (Fig. 394

6E). These results suggest that OPDA activates the ET pathway and potentially regulates mir1 395

transcript accumulation in Mp708 plants. 396

397

Exogenous Application of Methyl Jasmonate Did Not Significantly Increase the Callose 398

Deposition in Mp708 Plants 399

Previously, we showed that the exogenous application of Mp708 plants with methyl jasmonate 400

(MeJA) did not significantly alter the CLA population size compared to Mp708 control plants 401

(Louis et al., 2015). Here, we pretreated the Mp708 plants with MeJA for 24 h and monitored the 402

accumulation of callose in Mp708 plants before and after MeJA treatment. Our results indicate 403



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that the MeJA pretreatment alone did not significantly increase the number of callose spots 404

compared to untreated Mp708 control plants (Fig. 7). Furthermore, there was no significant 405

difference in the number of callose spots when comparing Mp708 plants infested with CLA and 406

exogenous application of MeJA followed by CLA feeding (Fig. 7). These findings indicate that 407

the JA is not required for enhanced callose accumulation in Mp708 plants. 408

409

OPDA-Mediated Resistance to CLA Is Independent of the JA Pathway 410

To determine whether the OPDA-mediated resistance to CLA in maize can occur independently 411

of the JA pathway, we used a maize JA-deficient mutant line in B73 background, which is 412

disrupted in two 12-Oxo-Phytodienoic acid Reductase (OPR7 and OPR8) genes (Yan at al., 413

2012). Wound-induced OPDA levels in opr7 opr8 double mutants were comparable to wild-type 414

plants, whereas JA induction was not detectable in opr7 opr8, indicating that OPR7 and OPR8 415

function in the conversion of OPDA to JA (Yan et al., 2012). Aphid no-choice bioassays showed 416

comparable numbers of CLA on the wild-type and opr7 opr8 controls plants after 4 days post 417

infestation, whereas CLA counts were significantly lower on the opr7 opr8 plants that were 418

pretreated with OPDA for 24 h (Fig. 8A). We further determined whether the exogenous 419

application of OPDA could also increase callose deposition in the opr7 opr8 plants. Our results 420

indicate that the OPDA pretreatment alone did not significantly increase the number of callose 421

spots in opr7 opr8 plants compared with the wild-type plants (Fig. 8B). However, exogenous 422

application of OPDA and subsequent feeding by CLA significantly increased the callose spots in 423

opr7 opr8 plants compared with the opr7 opr8 control plants and wild-type plants with or 424

without OPDA treatment (Fig. 8B). These results indicate that JA is not required for CLA 425

resistance and that the OPDA-mediated resistance to CLA is independent of the JA pathway. 426

427

In comparison to Tx601 plants, Mp708 plants had constitutively elevated levels of 428

OPDA, JA, and JA-related defenses (Shivaji et al., 2010). We further quantified the levels of 429

OPDA, JA, and JA-Ile before and after treating the Mp708 plants with OPDA. As shown 430

previously (Shivaji et al., 2010), Mp708 plants had constitutively higher levels of OPDA, JA, 431

and JA-Ile compared to Tx601 plants (Supplemental Fig. S6). Exogenous application of OPDA 432

on Mp708 plants did not significantly increase the levels of JA and JA-Ile compared to Mp708 433

control plants. In fact, OPDA treatment of Mp708 plants significantly reduced the levels of JA 434



Varsani et al.

15

and JA-Ile compared to Mp708 control plants (Supplemental Fig. S6). These results further 435

confirm a JA-independent role of OPDA in regulating defense against CLA. 436

437

OPDA Does Not Have a Direct Negative Impact on CLA Growth and Fecundity 438

To determine whether OPDA has a direct negative effect on CLA growth and fecundity, we 439

performed a feeding trial bioassay in which CLA was reared on an artificial diet containing 50 or 440

200 µM OPDA for 4 days. Our aphid feeding assays confirmed that OPDA in the artificial diet 441

did not negatively affect the CLA growth and fecundity compared to CLA reared on diet alone 442

and the diet mixed with DMSO, the solvent used to make the OPDA stock solution (Fig. 9). This 443

result suggests that the elevated level of OPDA in Mp708 is unlikely to directly contribute to 444

Mp708 resistance to CLA. Instead, OPDA-induced activation of downstream defenses likely 445

contributes to the resistant phenotype of Mp708 against CLA. 446

447

448

DISCUSSION 449

Besides acting as a precursor for JA biosynthesis, OPDA can activate downstream signaling 450

mechanisms and promote enhanced callose accumulation (Taki et al., 2005; Böttcher and 451

Pollman, 2009; Scalschi et al., 2015; Wasternack and Hause, 2016; Wasternack and Strnad, 452

2016; Monte et al., 2018). Mp708 plants had constitutively elevated levels of both JA and OPDA 453

(Shivaji et al., 2010). However, previously, we suggested that Mp708 resistance against CLA is 454

independent of the JA pathway (Louis et al., 2015). Here, we monitored whether elevated levels 455

of OPDA can contribute to maize defense against CLA. Exogenous OPDA application promoted 456

increased callose deposition and heightened CLA resistance in Mp708 plants (Fig. 4). 457

Furthermore, OPDA pretreatment and CLA feeding triggered the ET pathway and mir1 458

transcript accumulation (Fig. 6), suggesting that OPDA acts as a signaling molecule to trigger 459

downstream defense responses. 460

461

Several studies have suggested an important role for oxylipins in modulating plant 462

defenses against aphids (Smith et al., 2010; Nalam et al., 2012; Avila et al., 2013; Guo et al., 463

2014). For example, the oxylipin 9-hydroxyoctadecadienoic acid (9-HOD) was involved in 464

promoting aphid colonization and fecundity on Arabidopsis (Nalam et al., 2012). In contrast, α-465



Varsani et al.

16

dioxygenases (α-DOX1)-derived oxylipins contributed to aphid resistance in both Arabidopsis 466

and tomato (Avila et al., 2013). Similarly, OPDA was involved in activating plant defense 467

responses to aphids in both wheat and radish (Raphanus sp.) (Smith et al., 2010; Guo et al., 468

2014). Several diverse lipids, including oxylipins, have been identified in phloem sap as well 469

(Madey et al., 2002; Harmel et al., 2007; Benning et al., 2012). However, it is not known 470

whether the oxylipin-based defenses against aphids are exerted within or outside of the phloem 471

sap. Our results demonstrate that it is highly unlikely that OPDA has a direct negative effect on 472

aphid growth and fecundity because artificial diet assays confirmed that OPDA does not limit 473

CLA growth and fecundity (Fig. 9). Alternatively, aphids may have the ability to convert the 474

ingested OPDA into a less toxic form. In fact, it has been shown that some chewing insects 475

isomerize OPDA into a less toxic form that is excreted in the frass (Dabrowska et al., 2009). 476

Although the exact mechanisms by which aphids sequester and/or avoid the effect of OPDA on 477

aphid physiology is unknown, our results suggest that the signaling function of OPDA is likely 478

responsible for providing enhanced defense against CLA in Mp708 plants. 479

480

OPDA treatment triggers the expression of ET biosynthesis and receptor genes (Fig. 6, 481

A-D) that are involved in the production of ET in maize (Young et al., 2004; Yamauchi et al., 482

2016). In a previous study, the ET signaling pathway was correlated with promoting pathogen-483

induced callose deposition in Arabidopsis, thereby providing enhanced resistance (Clay et al., 484

2009). However, it was also reported that Arabidopsis plants can induce pathogen-triggered 485

callose accumulation in a glucosinolate-independent manner (Frerigmann et al., 2016). Whatever 486

the precise mechanisms involved, our data suggest that the OPDA-triggered ET pathway and its 487

interaction with the mir1 defensive gene (Fig. 6; Louis et al., 2015) contribute to enhanced 488

resistance to CLA potentially by enhancing callose accumulation and limiting the aphid growth. 489

Furthermore, MeJA, which is derived from JA, antagonizes the ET pathway and suppresses 490

pathogen-triggered callose deposition in Arabidopsis (Clay et al., 2009). Similarly, exogenous 491

application of JA on tomato plants was negatively correlated with callose accumulation (Scalschi 492

et al., 2015), further suggesting that JA or MeJA suppresses callose accumulation in plants. 493

Although elevated JA levels in Mp708 were not required for the mir1-dependent defense against 494

CLA (Louis et al., 2015), we cannot rule out the possibility that the JA and/or JA-derived 495

compounds also modulate callose deposition in maize. However, this is less likely, considering 496



Varsani et al.

17

the fact that we observed no significant differences in the number of callose spots on MeJA-497

pretreated Mp708 plants compared to control plants (Fig. 7). In addition, OPDA pretreatment 498

followed by CLA feeding on the JA-deficient opr7 opr8 mutant plants significantly enhanced 499

callose accumulation compared with opr7 opr8 control plants and wild-type plants (Fig. 8B), 500

pointing to a role of OPDA in defense against CLA that is independent of JA. Surprisingly, 501

OPDA pretreatment did not alter the CLA population size on B73 and Tx601 plants (Figs. 4B 502

and 8A). One possible explanation is that the OPDA conversion to JA is highly stimulated in 503

both B73 and Tx601 plants, which leads to a corresponding increase in JA and/or JA-dependent 504

defenses and simultaneously weakens the OPDA-modulated defense arm that is independent of 505

the JA pathway. Alternatively, unlike Mp708 plants where there is an effective defense protein 506

such as Mir1-CP, both B73 and Tx601 plants may lack effective defensive proteins that could 507

respond to OPDA and induce downstream defense mechanisms (for example, enhanced callose 508

accumulation). 509

510

Callose accumulation that contributes to aphid resistance could occur within and/or 511

outside of the sieve elements (Hao et al., 2008; Du et al., 2009; Mondal et al., 2018). In both 512

scenarios, it severely hinders the aphid’s ability to find and feed continuously from the phloem 513

sap. EPG analysis indicated that Mp708’s resistance to CLA is phloem-localized. Furthermore, it 514

is apparent from the EPG experiments that CLA took similar amounts of time to reach the first 515

SEP on both Mp708 and Tx601 plants (Fig. 1), indicating that the callose deposited on the sieve 516

elements could potentially play a significant role in hindering CLA ability to feed continuously 517

on resistant maize plants. Furthermore, OPDA-treated Mp708 plants provided enhanced 518

resistance and prevented aphids from sustained feeding from the sieve elements compared to 519

Mp708 control plants (Fig. 5; Supplemental Table S1). Mp708 plants also had constitutively 520

higher numbers of callose spots compared to Tx601 plants. The endogenous OPDA levels were 521

sufficient to promote constitutively higher callose spots in Mp708 plants compared to Tx601 522

plants (Figs. 2A and 4A). However, we observed comparable levels of callose synthase gene 523

expression (Tdy2) in both Mp708 and Tx601 genotypes prior to CLA infestation (Fig. 2B). In 524

contrast, CLA feeding for 24 h significantly increased Tdy2 expression in Mp708 compared to 525

Tx601 plants (Fig. 2B). It is plausible that, since Tdy2 is highly expressed in the vascular tissues 526

and involved in the synthesis of callose, Mp708 plants initially need to perceive the salivary 527



Varsani et al.

18

signals from CLA to promote enhanced callose accumulation in the sieve elements. Similarly, 528

OPDA treatment alone did not significantly induce the accumulation of mir1 (Fig. 6E), a gene 529

that is highly expressed in the vascular tissues of Mp708 plants (Lopez et al., 2007), which may 530

also require the interaction of OPDA and CLA salivary signals to promote mir1-dependent 531

defense against CLA. Indeed, we previously showed that the CLA-feeding-induced accumulation 532

of defense molecules or factors in the vascular sap of Mp708 plants contributes to enhanced 533

defense against CLA (Louis et al., 2015). 534

535

Callose synthesis inhibitor treatment of susceptible Tx601 plants did not affect CLA 536

growth and reproduction (Supplemental Fig. S5), suggesting that OPDA-mediated callose 537

accumulation, and thus defenses, are attenuated in the susceptible maize plants. Alternatively, 538

CLA salivary secretions may cause unplugging of the sieve element occlusions in the susceptible 539

Tx601 plants. The latter is in agreement with our observation that CLA spent a longer time 540

feeding in the sieve elements of susceptible maize plants (Fig. 1; Supplemental Fig. S1). 541

Furthermore, consistent with our observation that the CLA-susceptible plants were unable to 542

mount appropriate defenses, the B73 maize inbred line, which is susceptible to CLA compared to 543

Mp708 plants (Louis et al., 2015), also demonstrated reduced levels of OPDA or OPDA 544

conjugates after CLA infestation (Tzin et al., 2015). Collectively, our data suggest that the 545

elevated levels of OPDA, in conjunction with CLA feeding, trigger the activation of downstream 546

defenses and callose accumulation in the resistant Mp708 plants. 547

548

549

CONCLUSION 550

In this study, we provide evidence that the signaling function of OPDA, but not JA, promotes 551

phloem-localized resistance to aphids in maize. Our data suggest that OPDA, in addition to 552

acting as a precursor for JA biosynthesis, is also involved in activating callose formation in 553

resistant maize plants. Moreover, our results indicate that OPDA can influence the ET pathway 554

and its interaction with the mir1 defensive gene to provide heightened resistance to CLA. The 555

identification of OPDA as a key modulator in regulating defense-signaling pathways could be 556

utilized for enhancing maize resistance to phloem-sap-sucking pests. 557

558



Varsani et al.

19

559

MATERIALS AND METHODS 560

561

Aphid Propagation 562

A CLA colony was reared on barley (Hordeum vulgare) plants as described previously (Louis et 563

al., 2015). The barley seeds were obtained from P. Stephen Baenziger, University of Nebraska-564

Lincoln (UNL). The aphid colonies were grown in a Percival growth chamber with a 14:10 565

(light:dark) photoperiod, 160 μE m-2

s-1

, 23°C, and 50 to 60% relative humidity. 566

567

Plants and Growth Conditions 568

Mp708 and Tx601 maize (Zea mays) plants were grown in soil mixed with vermiculite and 569

perlite (PRO-MIX BX BIOFUNGICIDE + MYCORRHIZAE, Premier Tech Horticulture) in 570

growth chambers with a 14:10 (light:dark) photoperiod, 160 μE m-2

s-1

, 25°C, and 50 to 60% 571

relative humidity. The opr7 opr8 mutant line has been described previously (Yan et al., 2012). 572

The opr7 opr8 plants used in this study were at the BC7 stage in the B73 background. Seeds 573

segregating for the opr7 opr8 double mutation in a 1:3 ratio were used in this study. Phenotypic 574

differences (lack of anthocyanin pigmentation in brace roots and leaf collar) and PCR-based 575

genotyping were used to identify the opr7 opr8 homozygous double mutants as described 576

previously (Yan et al., 2012). Since opr7 opr8 plants are nonviable in nonsterile soil due to 577

Pythium spp. infection (Yan et al., 2012), the opr7 opr8 and the wild-type (B73) control plants 578

were grown in sterile soil. All plants for the experiments were used at the V2-V3 developmental 579

stage (~2 weeks) (Ritchie et al., 1998). These plants were grown in 3.8 cm x 21.0-cm plastic 580

Cone-tainers (Hummert International). 581

582

Aphid Feeding Behavior Analysis 583

The EPG technique (Tjallingii, 1988; Walker, 2000; Louis et al., 2012) was used to monitor the 584

CLA feeding behavior on different maize genotypes, as described previously (Pegadaraju et al., 585

2007). Briefly, a thin gold wire was attached to the dorsum of apterous adult CLA using 586

conductive water-based silver glue. The wired aphid was placed on a plant that was connected to 587

an EPG-recording system using a copper electrode inserted into the soil. The plants and insects 588

were contained in a Faraday cage during EPG recordings to avoid external electrical noise. The 589



Varsani et al.

20

recordings were performed for 8 h under constant light at an ambient room temperature of 22°C. 590

An eight-channel GIGA-8 direct current amplifier (http://www.epgsystems.eu/; W.F. Tjallingii, 591

Wageningen University, Wageningen, The Netherlands) was used for EPG recordings. Plants 592

were randomized to the eight channels for each recording, and at least 12 replicates of individual 593

aphids (one aphid per plant) were obtained for each maize genotype. The different waveforms 594

obtained were analyzed using the EPG analysis software Stylet+ (http://www.epgsystems.eu/; 595

W.F. Tjallingii, Wageningen University, Wageningen, The Netherlands). 596

597

Callose Staining and Quantification 598

Callose staining and quantification of callose spots were done as described previously (Luna et 599

al., 2011). Briefly, leaves were collected after 24 h of OPDA (50 µM) or MeJA (500 µM) 600

treatment. Control plants were treated with 0.1% DMSO or 0.1% Tween, which were used to 601

dissolve OPDA or MeJA, respectively. Ten adult apterous CLAs were clip-caged on the leaves 602

for CLA-infested plants. Control plants had empty cages. The leaves were placed in 98% ethanol 603

for 48 h to clear the chlorophyll, and once the leaves become transparent, the leaves were placed 604

in 70% ethanol. The leaves were then gently washed three times using distilled water and stained 605

for 3 to 4 h in 150 nM K2HPO4 (pH 9.5) containing 0.01% aniline blue (Sigma-Aldrich). The 606

leaves were mounted on slides using 50% glycerol and were examined with an EVOS FL 607

epifluorescence microscope. Callose spots were counted per mm2 of leaf tissue on the adaxial 608

side of each clip-caged leaf segment using ImageJ (http://imagej.nih.gov/ij/). 609

610

Aphid Bioassays 611

Aphid no-choice bioassays were performed as described previously (Louis et al., 2015). 612

613

Artificial Diet Feeding Trial Bioassays 614

Aphid feeding trial bioassays were carried out using an artificial diet (Meihls et al., 2013) as 615

previously described (Louis et al., 2015). OPDA (50 or 200 µM; Cayman Chemical) dissolved in 616

0.1% DMSO (Sigma-Aldrich) or aphid diet mixed with 0.1% DMSO was used as the control for 617

artificial diet feeding assays. 618

619

RNA Extraction and Reverse Transcription Quantitative PCR (RT-qPCR) 620



Varsani et al.

21

Maize leaf tissues (80-100 mg) were ground using a 2010 Geno/Grinder (SPEX SamplePrep) for 621

40 seconds at 1,400 strokes min-1

under liquid nitrogen conditions. Total RNA was extracted 622

from the homogenized tissue using the Qiagen RNeasy Plant Mini Kit. Extracted total RNA was 623

quantified with a Nanodrop 2000c spectrophotometer (Thermo Fisher Scientific). 624

Complementary DNAs (cDNAs) were synthesized from 1 μg of total RNA using the High 625

Capacity cDNA reverse transcriptase kit (Applied Biosystems). cDNAs were diluted to 1:10 626

before using them for RT-qPCR. The RT-qPCR was performed with iTaq Universal SYBR 627

Green Supermix (Bio-Rad) on a StepOnePlus Real-Time PCR System (Applied Biosystems). 628

Gene-specific primers used for RT-qPCR are listed in Supplemental Table 2. At least three 629

independent biological replicates were used for RT-qPCR, and each biological replicate 630

contained three technical replicates. Primer efficiencies and relative expression levels were 631

calculated as described previously (Pfaffl, 2001). 632

633

BX Quantification 634

Maize plants were infested with 10 adult apterous CLA using clip cages, and at different time 635

points, CLAs were removed from the leaves and tissues were harvested. Leaves were weighed 636

and immediately flash-frozen in liquid nitrogen. Maize BX extraction and quantification were 637

carried out as described previously (Handrick et al., 2016). Three microliters of extraction 638

solvent (30:69.9:0.1 methanol, LC-MS-grade water [Sigma-Aldrich], formic acid; with 0.075 639

mM 2-benzoxazolinone) was added per milligram of maize tissue. Samples were mixed by 640

vortexing and were incubated on a Labquake Rotisserie Shaker (Thermo Fisher Scientific) at 4°C 641

for 40 min. After centrifugation at 11,000g for 10 minutes, 200 µL of the supernatant was 642

filtered using a 0.45-micron filter-bottom plate and centrifugation at 200g for 3 min. Samples 643

were analyzed using an Ultimate 3000 UPLC system attached to a 3000 Ultimate diode array 644

detector and a Thermo Q Exactive mass spectrometer (Thermo Fisher Scientific). The samples 645

were separated on a Titan C18 7.5 cm x 2.1 mm x 1.9 μm Supelco Analytical Column (Sigma-646

Aldrich), with the flow rate of 0.5 mL min-1

. A gradient of 0.1% formic acid in LC-MS-grade 647

water (eluent A) and 0.1% formic acid in acetonitrile (eluent B) was set up as follows: 0% B at 0 648

min, linear gradient to 100% B at 7 min, and linear gradient to 0% B at 11 min. Mass spectral 649

parameters were set as follows: negative spray voltage 3500 V, capillary temperature 300°C, 650

sheath gas 35 (arbitrary units), aux gas 10 (arbitrary units), and probe heater temperature 200°C 651



Varsani et al.

22

with an HESI probe. Full-scan mass spectra were collected (R:35000 full width at half 652

maximum, m/z 200; mass range: m/z 50 to 750) in negative mode. Excalibur 3.0 software was 653

used to quantify peak areas using a SIM chromatogram measured for m/z 240. The relative 654

DIM2BOA content of each sample was estimated from the ratio of the DIM2BOA peak area 655

(mass range of m/z 240.0-240.2 and retention time 2.25 min) relative to 2-benzoxazolinone (mass 656

range of m/z 134.0-134.2 and retention time 3.26 min), which was used as an internal standard. 657

658

Chemical Treatment on Plants 659

OPDA (50 µM) dissolved in 0.1% DMSO was used for exogenous application on maize plants. 660

Control plants were sprayed with 0.1% DMSO. Twenty-four hours after treatment, 10 adult 661

apterous CLAs were introduced and clip-caged on the leaves. Twenty-four hours after CLA 662

feeding, tissues were harvested and processed for RNA isolation. DDG (1 mM; Sigma-Aldrich) 663

dissolved in water was exogenously sprayed on Mp708 and Tx601 plants. Control plants were 664

sprayed with water. Twenty-four hours after spraying, plants were infested with five adult 665

apterous CLAs, and aphid numbers were counted after 4 days. For monitoring Tdy2 gene 666

expression levels after DDG treatment, plants were sprayed with DDG and water (control). 667

Twenty-four hours after treatment, leaf tissues were harvested for RNA extraction and 668

subsequent RT-qPCR. The Mp708 plants that received coapplication of OPDA and DDG for 669

bioassay and EPG feeding experiments were first sprayed with 50 µM OPDA and then sprayed 670

with 1 mM DDG 3 to 4 h later. Twenty-four hours after DDG spraying, the plants were used for 671

aphid bioassays or EPG experiments. 672

673

Phytohormone Quantification 674

Plants were treated with 50 μM OPDA as described above. Control plants were sprayed with 675

0.1% DMSO or did not receive any treatment. Twenty-four hours after treatment, leaf tissues 676

were collected, weighed, and flash-frozen in liquid nitrogen. The tissue samples were ground 677

using a 2010 Geno/Grinder (SPEX SamplePrep) for 40 seconds at 1,400 strokes min-1

under 678

liquid nitrogen conditions. The phytohormone analysis was carried out by the Proteomics & 679

Metabolomics Facility at the Center for Biotechnology, University of Nebraska-Lincoln. The 680

ground tissue was dissolved in cold methanol:acetonitrile (50:50, v/v) spiked with deuterium-681

labeled internal standards (D2-JA; TCI America). After centrifugation at 16,000g, the 682



Varsani et al.

23

supernatants were collected, and extraction of the pellet was repeated. The supernatants were 683

pooled and dried down using a speed-vac. The pellets were redissolved in 200 μL of 15% 684

methanol. For LC separation, the ZORBAX Eclipse Plus C18 column (2.1 mm × 100 mm; 685

Agilent) was used at a flow rate of 0.45 mL/min. The gradient of the mobile phases A (0.1% 686

acetic acid) and B (0.1% acetic acid/90% acetonitrile) was 5% B for 1 min, to 60% B in 4 min, to 687

100% B in 2 min, hold at 100% B for 3 min, to 5% B in 0.5 min. The Shimadzu LC system was 688

interfaced with a Sciex QTRAP 6500+ mass spectrometer equipped with a TurboIonSpray (TIS) 689

electrospray ion source. Analyst software (version 1.6.3) was used to control sample acquisition 690

and data analysis. The QTRAP 6500+ mass spectrometer was tuned and calibrated according to 691

the manufacturer’s recommendations. The hormones were detected using MRM transitions that 692

were optimized using standards. The instrument was set up to acquire data in positive and 693

negative ion switching modes. For quantification, an external standard curve was prepared using 694

a series of standard samples containing different concentrations of unlabeled hormones and fixed 695

concentrations of the deuterium-labeled standards mixture. 696

697

Statistical Analyses 698

The statistical analyses were performed using PROC GLIMMIX in SAS 9.4 (SAS Institute). To 699

evaluate the effect of genotype and treatment, and their interaction, two-way analysis of variance 700

(ANOVA) was used. Pairwise comparisons between treatments were carried out by comparing 701

the means with Tukey’s honestly significant difference tests (P < 0.05). For different EPG 702

parameters, the mean time spent by aphids on various feeding activities was analyzed using the 703

nonparametric Kruskal-Wallis test (P < 0.05). 704

705

706

ACKNOWLEDGEMENTS 707

We thank Ming Guo, Fan Yang, and Ezhumalai Muthukrishnan for assistance with callose 708

staining and visualization, and Sathish Natarajan for access to the epifluorescence microscope. 709

Thanks to Saumik Basu for technical, greenhouse, and laboratory assistance. We also thank the 710

Proteomics & Metabolomics Facility at the Center for Biotechnology, University of Nebraska-711

Lincoln for phytohormone anlaysis. 712

713



Varsani et al.

24

SUPPLEMENTAL DATA 714

The following materials are available in the online version of this article. 715

716

Supplemental Figure S1. Mp708 provides phloem-based resistance to corn leaf aphids. 717

Supplemental Figure S2. RT-qPCR analysis of BX pathway genes in Tx601 and Mp708 plants 718

before and after (24 h) CLA infestation. 719

Supplemental Figure S3. Expression of Tdy2 and ACS6 transcripts after exogenous application 720

of OPDA on maize genotypes. 721

Supplemental Figure S4. Pretreatment of Mp708 plants with callose synthesis inhibitor reduces 722

the expression of Tdy2. 723

Supplemental Figure S5. Blocking callose synthesis attenuates the resistant phenotype of 724

Mp708 plants. 725

Supplemental Figure S6. OPDA treatment did not enhance the levels of JA and JA-Ile in 726

Mp708 plants. 727

Supplemental Table S1. CLA feeding activities on the maize Mp708 genotype after various 728

chemical treatments. 729

Supplemental Table S2. Primers used for RT-qPCR study. 730

731

732

733

734

735

736

737

738

739

740

741

742

743

744



Varsani et al.

25

Table 1. CLA feeding activities on the maize Tx601 and Mp708 genotypes. 745

746

CLA feeding activity Tx601 Mp708 P Value

Total duration of pathway phase (PP) 3.64 ± 0.36 4.66 ± 0.58 0.367

Total duration of nonprobing phase (NP) 0.91 ± 0.32 0.88 ± 0.2 0.525

Time to first sieve element phase (f-SEP) 3.23 ± 0.41 2.86 ± 0.34 0.564

Total duration of SEP 2.53 ± 0.31 1.77 ± 0.25 0.031*

Total duration of xylem phase (XP) 0.96 ± 0.26 0.69 ± 0.11 0.335

747

Values represent mean time (h) ± SE spent by CLA on various activities in each 8 h of recording 748

(n =12). An asterisk represents a significant difference (P < 0.05, Kruskal-Wallis test) in the time 749

spent by CLA for the indicated activity on the Tx601 and Mp708 plants. 750

751

752

753

754

755

756

757

758

759

760

761

762

763

764

765

766

767

768

769



Varsani et al.

26

FIGURE LEGENDS 770

771

Figure 1. Mp708 provides phloem-based resistance to CLA. A, Mean time spent by CLA for 772

various activities (PP, pathway phase; NP, nonprobing phase; f-SEP, the time to reach first sieve 773

element phase; SEP, the total duration of SEP; XP, xylem phase) on Tx601 and Mp708 maize 774

genotypes. Each value is the mean SE of 12 replications. An asterisk represents a significant 775

difference (P < 0.05; Kruskal-Wallis test) in the time spent by CLA for the indicated activity on 776

the Tx601 and Mp708 plants. B, Representative EPG waveform patterns over an 8-h period of 777

CLA feeding on Tx601 and Mp708 maize genotypes. 778

779

Figure 2. CLA feeding promotes enhanced callose accumulation in the Mp708 genotype. A, 780

Number of callose spots ( SEM) per mm2 of leaf tissue in CLA-infested and uninfested leaves 781

at different time points (n = 3-4). B, RT-qPCR analysis of Tdy2 transcripts in uninfested (0 h) 782

and CLA-infested leaves (24 h) on Tx601 and Mp708 maize plants (n = 4). Different letters 783

above the bars indicate values that are significantly different from each other (P < 0.05; Tukey’s 784

test). Error bars represent SEM. 785

786

Figure 3. BX or BX-derived metabolites are not significantly altered in CLA-infested Mp708 787

plants. A-E, Comparison of BX derivatives in Tx601 and Mp708 maize genotypes after 0, 6, 12, 788

and 24 h of CLA feeding (n = 4). FW, Fresh weight; DIMBOA-Glc, 2,4-dihydroxy-7-methoxy-789

1,4-benzoxazin-3-one glucoside; HDMBOA-Glc, 2-hydroxy-4,7- dimethoxy-1,4-benzoxazin-3-790

one; DIMBOA, 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one; DIM2BOA-Glc, 2,4-791

dihydroxy-7,8-dimethoxy-1,4- benzoxazin-3-one glucoside; DIM2BOA, 2,4-dihydroxy-7,8-792

dimethoxy-1,4-benzoxazin-3-one. Different letters above the bars indicate values that are 793

significantly different from each other (P < 0.05; Tukey’s test). Error bars represent SEM. 794

795

Figure 4. OPDA pretreatment enhances callose accumulation and heightened resistance to CLA 796

in Mp708 plants. A, Number of callose spots ( SEM) per mm2 of leaf tissue with (+) and 797

without (-) prior treatment of OPDA and CLA infestation (24 h). Plants that were treated with 798

DMSO (solvent-only control) and plants that did not receive any treatment were used as the 799

negative controls (n = 3-4). B, Total number of CLA adults and nymphs recovered 4 days after 800



Varsani et al.

27

infestation of Tx601 and Mp708 plants that were pretreated with OPDA for 24 h. Plants that 801

were treated with DMSO (solvent-only control) and plants that did not receive any treatment 802

were used as the controls. Plants were infested with five adult apterous aphids/plant after 24 h of 803

OPDA treatment (n = 12). For A and B, different letters above the bars indicate values that are 804


806

Figure 5. Blocking callose synthesis attenuates the resistant phenotype of Mp708 plants. Total 807

number of CLA adults and nymphs recovered 4 days after infestation of Mp708 plants that were 808

pretreated with either 2-deoxy-D-glucose (DDG), OPDA, or coapplied with OPDA and DDG for 809

24 h. Plants that were treated with water and DMSO (solvent-only controls) and plants that did 810

not receive any treatment were used as the controls. Plants were infested with five adult apterous 811

aphids/plant after 24 h of chemical/water treatment. Values represent the mean SEM of CLA 812

numbers (n = 12). Different letters above the bars indicate values that are significantly different 813

from each other (P < 0.05; Tukey’s test). 814

815

Figure 6. OPDA application enhances the expression of ethylene biosynthesis and receptor 816

genes and mir1 transcripts in Mp708 plants. RT-qPCR analysis of ACS2 (A), ACS6 (B), ACO15 817

(C), ERS14 (D), and mir1 (E) in Mp708 leaves before (-) and after (+) OPDA and CLA 818

infestation (24 h). Plants treated with DMSO (solvent-only control) and plants that did not 819

receive any treatment were used as the negative controls (n = 3-4). Different letters above the 820

bars indicate values that are significantly different from each other (P < 0.05; Tukey’s test). 821

Error bars represent SEM. 822

823

Figure 7. MeJA pretreatment did not significantly alter callose accumulation in Mp708 plants. 824

The number of callose spots ( SEM) per mm2 of leaf tissue with and without prior treatment of 825

MeJA and CLA infestation (24 h) on Mp708 plants is shown. Plants treated with 0.1% Tween to 826

dissolve MeJA and plants that did not receive any treatment were used as the negative controls (n 827

= 3-4). Different letters above the bars indicate values that are significantly different from each 828

other (P < 0.05; Tukey’s test). Error bars represent SEM. 829

830



Varsani et al.

28

Figure 8. Maize resistance to CLA is independent of the JA pathway. A, Total number of CLA 831

adults and nymphs recovered 4 days after infestation of wild-type (B73) and JA-deficient (opr7 832

opr8) maize plants that were pretreated with OPDA for 24 h. Plants that were treated with 833


controls. Plants were infested with five adult apterous aphids/plant after 24 h of OPDA treatment 835

(n = 15 [B73] and n = 6-8 [opr7 opr8] for each treatment). B, Number of callose spots ( SEM) 836

per mm2 of leaf tissue with (+) and without (-) prior treatment of OPDA and CLA infestation (24 837

h). Plants treated with DMSO to dissolve OPDA and plants that did not receive any treatment 838

were used as the negative controls (n = 3). For A and B, different letters above the bars indicate 839

values that are significantly different from each other (P < 0.05; Tukey’s test). Error bars 840

represent SEM. 841

842

Figure 9. OPDA does not have a direct effect on CLA fecundity. Comparison of CLA numbers 843

on artificial diet supplemented with two different concentrations of OPDA. Diet alone and diet 844

supplemented with DMSO, which was used as a solvent for the OPDA, were used as the 845

controls. For feeding trial bioassays, three adult apterous CLAs were introduced into each 846

feeding chamber and allowed to feed on the diet. The total numbers of aphids (adults and 847

nymphs) in each chamber were counted after 4 days (n = 8). This experiment was conducted 848

twice with similar results. No significant differences were observed among any of the treatments 849

(P > 0.05; Tukey’s test). Error bars represent SEM. 850

851

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853

854

855

856

857

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Varsani et al.

29

SUPPLEMENTAL FIGURE LEGENDS 862

863

Supplemental Figure S1. Mp708 provides phloem-based resistance to corn leaf aphids (CLA). 864

A, Mean time spent by CLA for various activities (PP, pathway phase; NP, nonprobing phase; f-865

SEP, the time to reach first sieve element phase; SEP, the total duration of SEP; XP, xylem phase) 866

on B73 and Mp708 maize genotypes. Each value is the mean SE of 14 replications. An asterisk 867

represents a significant difference (P < 0.05; Kruskal-Wallis test) in the time spent by CLA for 868

the indicated activity on the B73 and Mp708 plants. B, Representative EPG waveform patterns 869

over an 8-h period of CLA feeding on B73 and Mp708 maize genotypes. 870

871

Supplemental Figure S2. RT-qPCR analysis of BX pathway genes in Tx601 and Mp708 plants 872

before and after (24 h) CLA infestation (n = 3-4). Different letters above the bars indicate values 873

that are significantly different from each other (P < 0.05; Tukey’s test). Error bars represent 874

SEM. 875

876

Supplemental Figure S3. Expression of Tdy2 and ACS6 transcripts after exogenous application 877

of OPDA on maize genotypes. RT-qPCR analysis of Tdy2 in Mp708 (A) and Tx601 plants (B) 878

before and after OPDA treatment. C, RT-qPCR analysis of ET biosynthetic pathway gene ACS6 879

in Tx601 plants before and after OPDA treatment. Plants treated with DMSO (solvent-only 880

control) and plants that did not receive any treatment were used as the controls. For experiments 881

A-C, n = 3. Different letters above the bars indicate values that are significantly different from 882

each other (P < 0.05; Tukey’s test). Error bars represent SEM. 883

884

Supplemental Figure S4. Pretreatment of Mp708 plants with callose synthesis inhibitor reduces 885

the expression of Tdy2. RT-qPCR analysis of Tdy2 in Mp708 leaves before and after 2-deoxy-D-886

glucose (DDG) treatment for 24 h. Plants that were treated with water (solvent-only control) and 887

plants that did not receive any treatment were used as the controls (n = 3). Different letters above 888

the bars indicate values that are significantly different from each other (P < 0.05; Tukey’s test). 889

Error bars represent SEM. 890

891



Varsani et al.

30

Supplemental Figure S5. Blocking callose synthesis attenuates the resistance phenotype of 892

Mp708 plants. The total number of CLA adults and nymphs recovered 4 days after infestation of 893

Tx601 and Mp708 plants that were pretreated with DDG for 24 h is shown. Plants that were 894

treated with water (solvent-only control) and plants that did not receive any treatment were used 895

as the controls. Plants were infested with five adult apterous aphids/plant after 24 h of DDG 896

treatment. Values represent the mean SEM of CLA numbers (n = 12). Different letters above 897

the bars indicate values that are significantly different from each other (P < 0.05; Tukey’s test). 898

899

Supplemental Figure S6. OPDA treatment did not enhance the levels of JA and JA-Ile in 900

Mp708 plants. Constitutive levels of OPDA (A), JA (B), and JA-Ile (C) in Tx601 and Mp708 901

genotypes and after treatment with 50 µM OPDA for 24 h on Mp708 plants. Plants treated with 902


controls (n = 3). FW, Fresh weight. Different letters above the bars indicate values that are 904


906

907

908

909

910

911

912

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914

915

916

917

918

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Figure 1

Figure 1. Mp708 provides phloem-based resistance to CLA. A, Mean time spent by CLA for

various activities (PP, pathway phase; NP, nonprobing phase; f-SEP, the time to reach first sieve

element phase; SEP, the total duration of SEP; XP, xylem phase) on Tx601 and Mp708 maize

genotypes. Each value is the mean SE of 12 replications. An asterisk represents a significant

difference (P < 0.05; Kruskal-Wallis test) in the time spent by CLA for the indicated activity on

the Tx601 and Mp708 plants. B, Representative EPG waveform patterns over an 8-h period of

CLA feeding on Tx601 and Mp708 maize genotypes.

0

-5

+5

Vo

lt (

V)

Tx601

B

SEP PP

0

-5

+5

Vo

lt (

V)

Mp708

0 4 8

Time (h)

XP SEP PP

A

Tim

e (

h)

*

0

1

2

3

4

5

PP NP f-SEP SEP XP



Varsani et al.

Figure 2

Figure 2. CLA feeding promotes enhanced callose accumulation in the Mp708 genotype. A,

Number of callose spots ( SEM) per mm2 of leaf tissue in CLA-infested and uninfested

leaves at different time points (n = 3-4). B, RT-qPCR analysis of Tdy2 transcripts in uninfested

(0 h) and CLA-infested leaves (24 h) on Tx601 and Mp708 maize plants (n = 4). Different

letters above the bars indicate values that are significantly different from each other (P < 0.05;

Tukey’s test). Error bars represent SEM.

A

0

100

200

300

400

0 h 6 h 12 h 24 h

Ca

llose

sp

ots

/mm

2

a

b

c d d

c

e f

Tx601 Mp708

0

1

2

3

4

5 Tx601 Mp708

0 h 24 h

a

b b b

Re

lative

exp

ressio

n T

dy2

B



Varsani et al.

Figure 3

Tx601 Mp708

A

0

200

400

600

800

0 h 6 h 12 h 24 h

Co

ncentr

ation

[µg

*g F

W-1

]

DIMBOA-Glc

a

b

b

ab ab

ab

b b

B

0

1000

2000

3000

4000

5000

6000

7000

0 h 6 h 12 h 24 h

Co

ncentr

ation

[µg

*g F

W-1

]

HDMBOA-Glc a

a

a

a a

a

a a

D C

0

500

1000

1500

2000

2500

0 h 6 h 12 h 24 h

Co

ncentr

ation

[µg

*g F

W-1

]

DIMBOA

a a

a a

a

a

a a

0

200

400

600

800

1000

0 h 6 h 12 h 24 h

Co

ncentr

ation

[µg

*g F

W-1

] DIM2BOA-Glc

a

a

a a

a

a

a a

DIM2BOA

0

200

400

600

0 h 6 h 12 h 24 h

Co

ncentr

ation

[µg

*g F

W-1

]

a

a a

a a a

a

a

E



Varsani et al.

Figure 3

Figure 3. BX or BX-derived metabolites are not significantly altered in CLA-infested

Mp708 plants. A-E, Comparison of BX derivatives in Tx601 and Mp708 maize genotypes

after 0, 6, 12, and 24 h of CLA feeding (n = 4). FW, Fresh weight; DIMBOA-Glc, 2,4-

dihydroxy-7-methoxy-1,4-benzoxazin-3-one glucoside; HDMBOA-Glc, 2-hydroxy-4,7-

dimethoxy-1,4-benzoxazin-3-one; DIMBOA, 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-

one; DIM2BOA-Glc, 2,4-dihydroxy-7,8-dimethoxy-1,4- benzoxazin-3-one glucoside;

DIM2BOA, 2,4-dihydroxy-7,8-dimethoxy-1,4-benzoxazin-3-one. Different letters above the

bars indicate values that are significantly different from each other (P < 0.05; Tukey’s test).

Error bars represent SEM.



Varsani et al.

Figure 4

Tx601 Mp708

e

d d

e e

c c

b

c

a

0

100

200

300

400

500

Ca

llose

sp

ots

/mm

2

OPDA

DMSO

CLA

+ + + +

+ +

+ + + +

+ +

+ + + +

A

B

0

4

8

12

16

OPDA

DMSO + + + +

+ +

CL

A n

um

bers

a a a

b b

c



Varsani et al.

Figure 4

Figure 4. OPDA pretreatment enhances callose accumulation and heightened resistance to

CLA in Mp708 plants. A, Number of callose spots ( SEM) per mm2 of leaf tissue with (+)

and without (-) prior treatment of OPDA and CLA infestation (24 h). Plants that were treated

with DMSO to dissolve OPDA and plants that did not receive any treatment were used as the

negative controls (n = 3-4). B, Total number of CLA adults and nymphs recovered 4 days

after infestation of Tx601 and Mp708 plants that were pretreated with OPDA for 24 h. Plants

that were treated with DMSO (solvent-only control) and plants that did not receive any

treatment were used as the controls. Plants were infested with five adult apterous aphids/plant

after 24 h of OPDA treatment (n = 12). For A and B, different letters above the bars indicate

values that are significantly different from each other (P < 0.05; Tukey’s test). Error bars

represent SEM.



Varsani et al.

Figure 5

Figure 5. Blocking callose synthesis attenuates the resistant phenotype of Mp708 plants.

Total number of CLA adults and nymphs recovered 4 days after infestation of Mp708 plants

that were pretreated with either 2-deoxy-D-glucose (DDG), OPDA, or coapplied with

OPDA and DDG for 24 h. Plants that were treated with water and DMSO (solvent-only

controls) and plants that did not receive any treatment were used as the controls. Plants were

infested with five adult apterous aphids/plant after 24 h of chemical/water treatment. Values

represent the mean SEM of CLA numbers (n = 12). Different letters above the bars

indicate values that are significantly different from each other (P < 0.05; Tukey’s test).

0

3

6

9

12

15

CL

A n

um

bers

a a

c

b b b



0

4

8

12

16

20

Control DMSO CLA (24 h)

OPDA + +

Re

lative

exp

ressio

n A

CS

2

b b

c c

a

A

0

5

10

15

20

25


OPDA + +

b b

c c

a

Re

lative

exp

ressio

n A

CS

6

B

0

5

10

15

20

25


OPDA + +

b b

c c

a R

ela

tive

exp

ressio

n E

RS

14

D

0

4

8

12

16


OPDA + +

b

b

c c

a

Re

lative

exp

ressio

n A

CO

15

C

0

5

10

15

20

25

30


OPDA + +

Re

lative

exp

ressio

n m

ir1

b

c c c

a

E

Varsani et al.

Figure 6



Figure 6. OPDA application enhances the expression of ethylene biosynthesis and receptor

genes and mir1 transcripts in Mp708 plants. RT-qPCR analysis of ACS2 (A), ACS6 (B),

ACO15 (C), ERS14 (D), and mir1 (E) in Mp708 leaves before (-) and after (+) OPDA and

CLA infestation (24 h). Plants treated with DMSO (solvent-only control) and plants that did

not receive any treatment were used as the negative controls (n = 3-4). Different letters

above the bars indicate values that are significantly different from each other (P < 0.05;

Tukey’s test). Error bars represent SEM.

Varsani et al.

Figure 6



Varsani et al.

Figure 7

0

50

100

150

200

250

300

350

Control Tween MeJA CLA MeJA

+ CLA

Ca

llose

sp

ots

/mm

2 b b

b

a a

Figure 7. MeJA pretreatment did not significantly alter callose accumulation in Mp708

plants. The number of callose spots ( SEM) per mm2 of leaf tissue with and without prior

treatment of MeJA and CLA infestation (24 h) on Mp708 plants is shown. Plants treated with

0.1% Tween to dissolve MeJA and plants that did not receive any treatment were used as the

negative controls (n = 3-4). Different letters above the bars indicate values that are

significantly different from each other (P < 0.05; Tukey’s test). Error bars represent SEM.



Varsani et al.

Figure 8

0

50

100

150

200

250

Ca

llose

sp

ots

/mm

2

OPDA

DMSO

CLA

+ + + +

+ +

+ + + +

+ +

+ + + +

a

b

c c

d d d d d d

B

A B73 opr7 opr8

OPDA

DMSO + + + +

+ +

CL

A n

um

bers

a

a

a a a

b

0

4

8

12

16

20



Figure 8. Maize resistance to CLA is independent of the JA pathway. A, Total number of

CLA adults and nymphs recovered 4 days after infestation of wild-type (B73) and JA-

deficient (opr7 opr8) maize plants that were pretreated with OPDA for 24 h. Plants that were

treated with DMSO (solvent-only control) and plants that did not receive any treatment were

used as the controls. Plants were infested with five adult apterous aphids/plant after 24 h of

OPDA treatment (n = 15 [B73] and n = 6-8 [opr7 opr8] for each treatment). B, Number of

callose spots ( SEM) per mm2 of leaf tissue with (+) and without (-) prior treatment of

OPDA and CLA infestation (24 h). Plants treated with DMSO to dissolve OPDA and plants

that did not receive any treatment were used as the negative controls (n = 3). For A and B,

different letters above the bars indicate values that are significantly different from each other

(P < 0.05; Tukey’s test). Error bars represent SEM.

Varsani et al.

Figure 8



Varsani et al.

Figure 9

0

5

10

15

20

25

Diet DMSO 50 200

OPDA (µM)

CL

A n

um

bers

Figure 9. OPDA does not have a direct effect on CLA fecundity. Comparison of CLA

numbers on artificial diet supplemented with two different concentrations of OPDA. Diet

alone and diet supplemented with DMSO, which was used as a solvent for the OPDA, were

used as the controls. For feeding trial bioassays, three adult apterous CLAs were introduced

into each feeding chamber and allowed to feed on the diet. The total numbers of aphids

(adults and nymphs) in each chamber were counted after 4 days (n = 8). This experiment

was conducted twice with similar results. No significant differences were observed among

any of the treatments (P > 0.05; Tukey’s test). ). Error bars represent SEM.



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Anstead J, Samuel P, Song N, Wu C, Thompson GA, Goggin F (2010) Activation of ethylene-related genes in response to aphid feedingon resistant and susceptible melon and tomato plants. Entomol Exp Appl 134: 170–181


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


Avila CA, Arévalo-Soliz LM, Jia L, Navarre DA, Chen Z, Howe GA, Meng Q-W, Smith JE, Goggin FL (2012) Loss of function of FATTYACID DESATURASE7 in tomato enhances basal aphid resistance in a salicylate-dependent manner. Plant Physiol 158: 2028–2041


Avila CA, Arevalo-Soliz LM, Lorence A, Goggin FL (2013) Expression of α-DIOXYGENASE 1 in tomato and Arabidopsis contributes toplant defenses against aphids. Mol Plant Microbe Interact 26: 977–986


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Betsiashvili M, Ahern KR, Jander G (2015) Additive effects of two quantitative trait loci that confer Rhopalosiphum maidis (corn leafaphid) resistance in maize inbred line Mo17. J Exp Bot 66: 571–578


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Bosch M, Berger S, Schaller A, Stintzi A (2014a) Jasmonate-dependent induction of polyphenol oxidase activity in tomato foliage isimportant for defense against Spodoptera exigua but not against Manduca sexta. BMC Plant Biol 14: 257


Bosch M, Wright LP, Gershenzon J, Wasternack C, Hause B, Schaller A, Stintzi A (2014b) Jasmonic Acid and its precursor 12-Oxophytodienoic acid control different aspects of constitutive and induced herbivore defenses in tomato. Plant Physiol 166: 396–410


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Pubmed: Author and Title www.plantphysiol.orgon September 1, 2020 - Published by Downloaded from Copyright © 2019 American Society of Plant Biologists. All rights reserved.

https://www.ncbi.nlm.nih.gov/pubmed?term=Ahmad S%2C Veyrat N%2C Gordon%2DWeeks R%2C Zhang Y%2C Martin J%2C Smart L%2C Glauser G%2C Erb M%2C Flors V%2C Frey M%2C Ton J %282011%29 Benzoxazinoid metabolites regulate innate immunity against aphids and fungi in maize%2E Plant Physiol 157%3A 317%26%23x&dopt=abstract

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

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https://www.ncbi.nlm.nih.gov/pubmed?term=Ankala A%2C Luthe DS%2C Williams WP%2C Wilkinson JR %282009%29 Integration of ethylene and jasmonic acid signaling pathways in the expression of maize defense protein Mir1%2DCP%2E Mol Plant Microbe Interact 22%3A 1555%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Anstead J%2C Samuel P%2C Song N%2C Wu C%2C Thompson GA%2C Goggin F %282010%29 Activation of ethylene%2Drelated genes in response to aphid feeding on resistant and susceptible melon and tomato plants%2E Entomol Exp Appl 134%3A 170%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Atamian HS%2C Chaudhary R%2C Cin VD%2C Bao E%2C Girke T%2C Kaloshian I %282013%29 In planta expression or delivery of potato aphid Macrosiphum euphorbiae effectors Me10 and Me23 enhances aphid fecundity%2E Mol Plant Microbe Interact 26%3A 67%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Avila CA%2C Ar�valo%2DSoliz LM%2C Jia L%2C Navarre DA%2C Chen Z%2C Howe GA%2C Meng Q%2DW%2C Smith JE%2C Goggin FL %282012%29 Loss of function of FATTY ACID DESATURASE7 in tomato enhances basal aphid resistance in a salicylate%2Ddependent manner%2E Plant Physiol 158%3A 2028%26%23x&dopt=abstract

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https://scholar.google.com/scholar?as_q=Expression of �?±-DIOXYGENASE 1 in tomato and Arabidopsis contributes to plant defenses against aphids.&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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https://www.ncbi.nlm.nih.gov/pubmed?term=Betsiashvili M%2C Ahern KR%2C Jander G %282015%29 Additive effects of two quantitative trait loci that confer Rhopalosiphum maidis %28corn leaf aphid%29 resistance in maize inbred line Mo17%2E J Exp Bot 66%3A 571%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Bing JW%2C Guthrie WD %281991%29 Generation mean analysis for resistance in maize to the corn leaf aphid %28Homoptera%3A Aphididae%29%2E J Econ Entomol 84%3A 1080%26%23x&dopt=abstract

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Madey E, Nowack LM, Thompson JE (2002) Isolation and characterization of lipid in phloem sap of canola. Planta 214: 625–634Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Marcos R, Izquierdo Y, Vellosillo T, Kulasekaran S, Cascón T, Hamberg M, Castresana C (2015) 9-Lipoxygenase-derived oxylipinsactivate brassinosteroid signaling to promote cell wall-based defense and limit pathogen infection. Plant Physiol 169: 2324–2334


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Meihls LN, Kaur H, Jander G (2012) Natural variation in maize defense against insect herbivores. Cold Spring Harb Symp Quant Biol77: 269–283 www.plantphysiol.orgon September 1, 2020 - Published by Downloaded from

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https://www.ncbi.nlm.nih.gov/pubmed?term=Tzin V%2C Hojo Y%2C Strickler SR%2C Bartsch LJ%2C Archer CM%2C Ahern KR%2C Zhou S%2C Christensen SA%2C Galis I%2C Mueller LA%2C Jander G %282017%29 Rapid defense responses in maize leaves induced by Spodoptera exigua caterpillar feeding%2E J Exp Bot 68%3A 4709%26%23x&dopt=abstract

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Documents

1 Running Title: OPDA regulates maize defense against aphids 2 - … · Varsani et al. 4 94 ABSTRACT 95 The corn leaf aphid (CLA; Rhopalosiphum maidis) is a phloem sap-sucking insect