The plant cell wall plays an important role in damage-associated molecular pattern-induced resistance to pathogens and herbivorous insects. Our current understanding of cell wall-mediated resistance is largely based on the degree of pectin methylesterification. However, little is known about the role of pectin acetylesterification in plant immunity. This study describes how one pectin-modifying enzyme, PECTIN ACETYLESTERASE 9 (PAE9), affects the Arabidopsis (Arabidopsis thaliana) transcriptome, secondary metabolome, and aphid performance. Electro-penetration graphs showed that Myzus persicae aphids established phloem feeding earlier on pae9 mutants. Whole-genome transcriptome analysis revealed a set of 56 differentially expressed genes (DEGs) between uninfested pae9-2 mutants and wild-type plants. The majority of the DEGs were enriched for biotic stress responses and down-regulated in the pae9-2 mutant, including PAD3 and IGMT2, involved in camalexin and indole glucosinolate biosynthesis, respectively. Relative quantification of more than 100 secondary metabolites revealed decreased levels of several compounds, including camalexin and oxylipins, in two independent pae9 mutants. In addition, absolute quantification of phytohormones showed that jasmonic acid (JA), jasmonoyl-Ile, salicylic acid, abscisic acid, and indole-3-acetic acid were compromised due to PAE9 loss of function. After aphid infestation, however, pae9 mutants increased their levels of camalexin, glucosinolates, and JA, and no long-term effects were observed on aphid fitness. Overall, these data show that PAE9 is required for constitutive up-regulation of defense-related compounds, but that it is not required for aphid-induced defenses. The signatures of phenolic antioxidants, phytoprostanes, and oxidative stress-related transcripts indicate that the processes underlying PAE9 activity involve oxidation-reduction reactions.

Department of Biology Faculty of Science Arak University Arak 38156 8 8349 Iran

Department of Chemical Biology and Genetics Centre of the Region Haná for Biotechnological and Agricultural Research Faculty of Science Palacký University Šlechtitelů 27 CZ 78371 Olomouc Czech Republic

Department of Forest Genetics and Physiology Umeå Plant Science Centre Swedish Agriculture University S 90183 Umea Sweden

Department of Plant Physiology Umeå Plant Science Centre Umeå University S 90187 Umea Sweden

Laboratory of Entomology Wageningen University and Research 6700 AA Wageningen The Netherlands

Laboratory of Growth Regulators Centre of the Region Haná for Biotechnological and Agricultural Research Institute of Experimental Botany CAS and Faculty of Science of Palacký University Šlechtitelů 27 CZ 78371 Olomouc Czech Republic

Unité de recherche Inserm 1121 Université de Lorraine INRA Laboratoire Agronomie et Environnement ENSAIA 2 Avenue Forêt de Haye 54518 Vandœuvre lès Nancy France

Zobrazit více v PubMed

Abdel-Ghany SE, Burkhead JL, Gogolin KA, Andrés-Colás N, Bodecker JR, Puig S, Peñarrubia L, Pilon M (2005) AtCCS is a functional homolog of the yeast copper chaperone Ccs1/Lys7. FEBS Lett 579: 2307–2312 PubMed

Adolfsson L, Nziengui H, Abreu IN, Šimura J, Beebo A, Herdean A, Aboalizadeh J, Široká J, Moritz T, Novák O, et al. (2017) Enhanced secondary- and hormone metabolism in leaves of arbuscular mycorrhizal Medicago truncatula. Plant Physiol 175: 392–411 PubMed PMC

Akhter S, Uddin MN, Jeong IS, Kim DW, Liu XM, Bahk JD (2016) Role of Arabidopsis AtPI4Kγ3, a type II phosphoinositide 4-kinase, in abiotic stress responses and floral transition. Plant Biotechnol J 14: 215–230 PubMed PMC

Albersheim P, Jones TM, English PD (1969) Biochemistry of the cell wall in relation to infective processes. Annu Rev Phytopathol 7: 171–194 PubMed

Aldington S, McDougall GJ, Fry SC (1991) Structure‐activity relationships of biologically active oligosaccharides. Plant Cell Environ 14: 625–636

Bacete L, Mélida H, Miedes E, Molina A (2018) Plant cell wall-mediated immunity: Cell wall changes trigger disease resistance responses. Plant J 93: 614–636 PubMed

Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67: 48

Bethke G, Grundman RE, Sreekanta S, Truman W, Katagiri F, Glazebrook J (2014) Arabidopsis PECTIN METHYLESTERASEs contribute to immunity against Pseudomonas syringae. Plant Physiol 164: 1093–1107 PubMed PMC

Bethke G, Thao A, Xiong G, Li B, Soltis NE, Hatsugai N, Hillmer RA, Katagiri F, Kliebenstein DJ, Pauly M, Glazebrook J (2016) Pectin biosynthesis is critical for cell wall integrity and immunity in Arabidopsis thaliana. Plant Cell 28: 537–556 PubMed PMC

Bi R, Berglund J, Vilaplana F, McKee LS, Henriksson G (2016) The degree of acetylation affects the microbial degradability of mannans. Polym Degrad Stabil 133: 36–46

Bidhendi AJ, Geitmann A (2016) Relating the mechanics of the primary plant cell wall to morphogenesis. J Exp Bot 67: 449–461 PubMed

Biely P, MacKenzie CR, Puls J, Schneider H (1986) Cooperativity of esterases and xylanases in the enzymatic degradation of acetyl xylan. Nat Biotechnol 4: 731–733

Bindschedler LV, Dewdney J, Blee KA, Stone JM, Asai T, Plotnikov J, Denoux C, Hayes T, Gerrish C, Davies DR, et al. (2006) Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance. Plant J 47: 851–863 PubMed PMC

Blackman RL, Eastop VF (2006) Aphids on the World’s Herbaceous Plants and Schrubs, Vol 2 The Aphids. John Wiley & Sons, Ltd. & Natural History Museum, London

Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114–2120 PubMed PMC

Böttcher C, Westphal L, Schmotz C, Prade E, Scheel D, Glawischnig E (2009) The multifunctional enzyme CYP71B15 (PHYTOALEXIN DEFICIENT3) converts cysteine-indole-3-acetonitrile to camalexin in the indole-3-acetonitrile metabolic network of Arabidopsis thaliana. Plant Cell 21: 1830–1845 PubMed PMC

Bray NL, Pimentel H, Melsted P, Pachter L (2016) Near-optimal probabilistic RNA-seq quantification. Nat Biotechnol 34: 525–527 PubMed

Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G (2010) A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc Natl Acad Sci USA 107: 9452–9457 PubMed PMC

Cabrera JC, Boland A, Messiaen J, Cambier P, Van Cutsem P (2008) Egg box conformation of oligogalacturonides: The time-dependent stabilization of the elicitor-active conformation increases its biological activity. Glycobiology 18: 473–482 PubMed

Caffall KH, Mohnen D (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res 344: 1879–1900 PubMed

Cao H-H, Liu H-R, Zhang Z-F, Liu T-X (2016) The green peach aphid Myzus persicae perform better on pre-infested Chinese cabbage Brassica pekinensis by enhancing host plant nutritional quality. Sci Rep 6: 21954. PubMed PMC

Cheng CY, Krishnakumar V, Chan AP, Thibaud-Nissen F, Schobel S, Town CD (2017) Araport11: A complete reannotation of the Arabidopsis thaliana reference genome. Plant J 89: 789–804 PubMed

Cherqui A, Tjallingii WF (2000) Salivary proteins of aphids, a pilot study on identification, separation and immunolocalisation. J Insect Physiol 46: 1177–1186 PubMed

Cline MS, Smoot M, Cerami E, Kuchinsky A, Landys N, Workman C, Christmas R, Avila-Campilo I, Creech M, Gross B, et al. (2007) Integration of biological networks and gene expression data using Cytoscape. 2: 2366–2382 PubMed PMC

Cosgrove DJ. (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6: 850–861 PubMed

Cosgrove DJ. (2015) Plant expansins: Diversity and interactions with plant cell walls. Curr Opin Plant Biol 25: 162–172 PubMed PMC

Creelman RA, Mullet JE (1997) Oligosaccharins, brassinolides, and jasmonates: Nontraditional regulators of plant growth, development, and gene expression. Plant Cell 9: 1211–1223 PubMed PMC

Davis KR, Darvill AG, Albersheim P (1986) Several biotic and abiotic elicitors act synergistically in the induction of phytoalexin accumulation in soybean. Plant Mol Biol 6: 23–32 PubMed

De Lorenzo G, Brutus A, Savatin DV, Sicilia F, Cervone F (2011) Engineering plant resistance by constructing chimeric receptors that recognize damage-associated molecular patterns (DAMPs). FEBS Lett 585: 1521–1528 PubMed

de Souza A, Hull PA, Gille S, Pauly M (2014) Identification and functional characterization of the distinct plant pectin esterases PAE8 and PAE9 and their deletion mutants. Planta 240: 1123–1138 PubMed PMC

De Vos M, Jander G (2009) Myzus persicae (green peach aphid) salivary components induce defence responses in Arabidopsis thaliana. Plant Cell Environ 32: 1548–1560 PubMed

Decreux A, Messiaen J (2005) Wall-associated kinase WAK1 interacts with cell wall pectins in a calcium-induced conformation. Plant Cell Physiol 46: 268–278 PubMed

Delaunois B, Jeandet P, Clément C, Baillieul F, Dorey S, Cordelier S (2014) Uncovering plant-pathogen crosstalk through apoplastic proteomic studies. Front Plant Sci 5: 249. PubMed PMC

Divol F, Vilaine F, Thibivilliers S, Kusiak C, Sauge MH, Dinant S (2007) Involvement of the xyloglucan endotransglycosylase/hydrolases encoded by celery XTH1 and Arabidopsis XTH33 in the phloem response to aphids. Plant Cell Environ 30: 187–201 PubMed

Dixon AFG. (1973) Biology of Aphids The Institute of Biology, Studies in Biology. Cambridge Rare Books, Cambridge, United Kingdom, pp 1–58

Dreyer DL, Campbell BC (1987) Chemical basis of host plant resistance to aphids. Plant Cell Environ 10: 553–561

Ferrari S, Savatin DV, Sicilia F, Gramegna G, Cervone F, Lorenzo GD (2013) Oligogalacturonides: Plant damage-associated molecular patterns and regulators of growth and development. Front Plant Sci 4: 49. PubMed PMC

Floková K, Tarkowská D, Miersch O, Strnad M, Wasternack C, Novák O (2014) UHPLC-MS/MS based target profiling of stress-induced phytohormones. Phytochemistry 105: 147–157 PubMed

Foyer CH, Verrall SR, Hancock RD (2015) Systematic analysis of phloem-feeding insect-induced transcriptional reprogramming in Arabidopsis highlights common features and reveals distinct responses to specialist and generalist insects. J Exp Bot 66: 495–512 PubMed

Gao Q-M, Venugopal S, Navarre D, Kachroo A (2011) Low oleic acid-derived repression of jasmonic acid-inducible defense responses requires the WRKY50 and WRKY51 proteins. Plant Physiol 155: 464–476 PubMed PMC

Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, et al. (2004) Bioconductor: Open software development for computational biology and bioinformatics. Genome Biol 5: R80. PubMed PMC

Glawischnig E. (2007) Camalexin. Phytochemistry 68: 401–406 PubMed

Gullberg J, Jonsson P, Nordström A, Sjöström M, Moritz T (2004) Design of experiments: An efficient strategy to identify factors influencing extraction and derivatization of Arabidopsis thaliana samples in metabolomic studies with gas chromatography/mass spectrometry. Anal Biochem 331: 283–295 PubMed

Hahn MG, Darvill AG, Albersheim P (1981) Host-pathogen interactions: XIX. The endogenous elicitor, a fragment of a plant cell wall polysaccharide that elicits phytoalexin accumulation in soybeans. Plant Physiol 68: 1161–1169 PubMed PMC

Heil M, Land WG (2014) Danger signals - damaged-self recognition across the tree of life. Front Plant Sci 5: 578. PubMed PMC

Hlavac M. (2018) stargazer: Well-Formatted Regression and Summary Statistics Tables. R package version 5.2.2. https://sites.google.com/site/marekhlavac/software/stargazer (January 3, 2019)

Huang H-J, Cui J-R, Xia X, Chen J, Ye Y-X, Zhang C-X, Hong X-Y (2019) Salivary DNase II from Laodelphax striatellus acts as an effector that suppresses plant defence. New Phytol 224: 860–874 PubMed

Idänheimo N, Gauthier A, Salojärvi J, Siligato R, Brosché M, Kollist H, Mähönen AP, Kangasjärvi J, Wrzaczek M (2014) The Arabidopsis thaliana cysteine-rich receptor-like kinases CRK6 and CRK7 protect against apoplastic oxidative stress. Biochem Biophys Res Commun 445: 457–462 PubMed

Imbusch R, Mueller MJ (2000) Analysis of oxidative stress and wound-inducible dinor isoprostanes F(1) (phytoprostanes F(1)) in plants. Plant Physiol 124: 1293–1304 PubMed PMC

Jambunathan N. (2010) Determination and Detection of Reactive Oxygen Species (ROS), Lipid Peroxidation, and Electrolyte Leakage in Plants In Sunkar R, ed, Plant Stress Tolerance, Methods in Molecular Biology. Springer Science+Business Media, Hatfield, United Kingdom, pp 291–297 PubMed

Jarvis MC, Apperley DC (1995) Chain conformation in concentrated pectic gels: Evidence from 13C NMR. Carbohydr Res 275: 131–145

Kärkönen A, Kuchitsu K (2015) Reactive oxygen species in cell wall metabolism and development in plants. Phytochemistry 112: 22–32 PubMed

Kettles GJ, Drurey C, Schoonbeek HJ, Maule AJ, Hogenhout SA (2013) Resistance of Arabidopsis thaliana to the green peach aphid, Myzus persicae, involves camalexin and is regulated by microRNAs. New Phytol 198: 1178–1190 PubMed PMC

Kim JH, Lee BW, Schroeder FC, Jander G (2008) Identification of indole glucosinolate breakdown products with antifeedant effects on Myzus persicae (green peach aphid). Plant J 54: 1015–1026 PubMed

Kloth KJ, Busscher-Lange J, Wiegers GL, Kruijer W, Buijs G, Meyer RC, Albrectsen BR, Bouwmeester HJ, Dicke M, Jongsma MA (2017) SIEVE ELEMENT-LINING CHAPERONE 1 restricts aphid feeding on Arabidopsis during heat stress. Plant Cell 29: 2450–2464 PubMed PMC

Kloth KJ, Wiegers GL, Busscher-Lange J, van Haarst JC, Kruijer W, Bouwmeester HJ, Dicke M, Jongsma MA (2016) AtWRKY22 promotes susceptibility to aphids and modulates salicylic acid and jasmonic acid signalling. J Exp Bot 67: 3383–3396 PubMed PMC

Kohorn BD, Johansen S, Shishido A, Todorova T, Martinez R, Defeo E, Obregon P (2009) Pectin activation of MAP kinase and gene expression is WAK2 dependent. Plant J 60: 974–982 PubMed PMC

Kohorn BD, Kohorn SL, Saba NJ, Martinez VM (2014) Requirement for pectin methyl esterase and preference for fragmented over native pectins for wall-associated kinase-activated, EDS1/PAD4-dependent stress response in Arabidopsis. J Biol Chem 289: 18978–18986 PubMed PMC

Kohorn BD, Kohorn SL, Todorova T, Baptiste G, Stansky K, McCullough M (2012) A dominant allele of Arabidopsis pectin-binding wall-associated kinase induces a stress response suppressed by MPK6 but not MPK3 mutations. Mol Plant 5: 841–851 PubMed PMC

Kopylova E, Noé L, Touzet H (2012) SortMeRNA: Fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics 28: 3211–3217 PubMed

Kuśnierczyk A, Winge P, Jørstad TS, Troczyńska J, Rossiter JT, Bones AM (2008) Towards global understanding of plant defence against aphids--timing and dynamics of early Arabidopsis defence responses to cabbage aphid (Brevicoryne brassicae) attack. Plant Cell Environ 31: 1097–1115 PubMed

Landry LG, Chapple CC, Last RL (1995) Arabidopsis mutants lacking phenolic sunscreens exhibit enhanced ultraviolet-B injury and oxidative damage. Plant Physiol 109: 1159–1166 PubMed PMC

Levesque-Tremblay G, Pelloux J, Braybrook SA, Müller K (2015) Tuning of pectin methylesterification: Consequences for cell wall biomechanics and development. Planta 242: 791–811 PubMed

Liners F, Letesson J-J, Didembourg C, Van Cutsem P (1989) Monoclonal antibodies against pectin: recognition of a conformation induced by calcium. Plant Physiol 91: 1419–1424 PubMed PMC

Lionetti V, Fabri E, De Caroli M, Hansen AR, Willats WGT, Piro G, Bellincampi D (2017) Three pectin methylesterase inhibitors protect cell wall integrity for Arabidopsis immunity to Botrytis. Plant Physiol 173: 1844–1863 PubMed PMC

Lotze MT, Zeh HJ, Rubartelli A, Sparvero LJ, Amoscato AA, Washburn NR, Devera ME, Liang X, Tör M, Billiar T (2007) The grateful dead: Damage-associated molecular pattern molecules and reduction/oxidation regulate immunity. Immunol Rev 220: 60–81 PubMed

Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15: 550. PubMed PMC

Ma R, Reese JC, Black WC, Bramel-Cox P (1990) Detection of pectinesterase and polygalacturonase from salivary secretions of living greenbugs, Schizaphis graminum (Homoptera: Aphididae). J Insect Physiol 36: 507–512

Maere S, Heymans K, Kuiper M (2005) BiNGO: A Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21: 3448–3449 PubMed

Mao P, Duan M, Wei C, Li Y (2007) WRKY62 transcription factor acts downstream of cytosolic NPR1 and negatively regulates jasmonate-responsive gene expression. Plant Cell Physiol 48: 833–842 PubMed

Matzinger P. (1994) Tolerance, danger, and the extended family. Annu Rev Immunol 12: 991–1045 PubMed

Matzinger P. (2002) The danger model: A renewed sense of self. Science 296: 301–305 PubMed

McMillan GP, Hedley D, Fyffe L, Pérombelon MCM (1993) Potato resistance to soft-rot erwinias is related to cell wall pectin esterification. Physiol Mol Plant Pathol 42: 279–289

Mendy B, Wang’ombe MW, Radakovic ZS, Holbein J, Ilyas M, Chopra D, Holton N, Zipfel C, Grundler FMW, Siddique S (2017) Arabidopsis leucine-rich repeat receptor-like kinase NILR1 is required for induction of innate immunity to parasitic nematodes. PLoS Pathog 13: e1006284. PubMed PMC

Miles PW. (1999) Aphid saliva. Biol Rev Camb Philos Soc 74: 41–85

Mueller MJ. (2004) Archetype signals in plants: The phytoprostanes. Curr Opin Plant Biol 7: 441–448 PubMed

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

Neilson EH, Goodger JQD, Woodrow IE, Møller BL (2013) Plant chemical defense: At what cost? Trends Plant Sci 18: 250–258 PubMed

Nićiforović N, Abramovič H (2014) Sinapic acid and its derivatives: Natural sources and bioactivity. Compr Rev Food Sci Food Saf 13: 34–51 PubMed

Novaković L, Guo T, Bacic A, Sampathkumar A, Johnson KL (2018) Hitting the wall-sensing and signaling pathways involved in plant cell wall remodeling in response to abiotic stress. Plants (Basel) 7: 89 PubMed PMC

Osorio S, Castillejo C, Quesada MA, Medina-Escobar N, Brownsey GJ, Suau R, Heredia A, Botella MA, Valpuesta V (2008) Partial demethylation of oligogalacturonides by pectin methyl esterase 1 is required for eliciting defence responses in wild strawberry (Fragaria vesca). Plant J 54: 43–55 PubMed

Pegadaraju V, Louis J, Singh V, Reese JC, Bautor J, Feys BJ, Cook G, Parker JE, Shah J (2007) Phloem-based resistance to green peach aphid is controlled by Arabidopsis PHYTOALEXIN DEFICIENT4 without its signaling partner ENHANCED DISEASE SUSCEPTIBILITY1. Plant J 52: 332–341 PubMed

Pelloux J, Rustérucci C, Mellerowicz EJ (2007) New insights into pectin methylesterase structure and function. Trends Plant Sci 12: 267–277 PubMed

Pfalz M, Mikkelsen MD, Bednarek P, Olsen CE, Halkier BA, Kroymann J (2011) Metabolic engineering in Nicotiana benthamiana reveals key enzyme functions in Arabidopsis indole glucosinolate modification. Plant Cell 23: 716–729 PubMed PMC

Philippe F, Pelloux J, Rayon C (2017) Plant pectin acetylesterase structure and function: New insights from bioinformatic analysis. BMC Genomics 18: 456. PubMed PMC

Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2018) Linear and Nonlinear Mixed Effects Models. R package version 3.1-137. https://CRAN.R-project.org/package=nlme (January 3, 2019).

Podgórska A, Burian M, Szal B (2017) Extra-cellular but extra-ordinarily important for cells: Apoplastic reactive oxygen species metabolism. Front Plant Sci 8: 1353. PubMed PMC

Pogorelko G, Lionetti V, Bellincampi D, Zabotina O (2013a) Cell wall integrity: Targeted post-synthetic modifications to reveal its role in plant growth and defense against pathogens. Plant Signal Behav 8: e25435. PubMed PMC

Pogorelko G, Lionetti V, Fursova O, Sundaram RM, Qi M, Whitham SA, Bogdanove AJ, Bellincampi D, Zabotina OA (2013b) Arabidopsis and Brachypodium distachyon transgenic plants expressing Aspergillus nidulans acetylesterases have decreased degree of polysaccharide acetylation and increased resistance to pathogens. Plant Physiol 162: 9–23 PubMed PMC

R Core Team (2017) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria. http://www.R-project.org/ (June 1, 2019)

Raiola A, Lionetti V, Elmaghraby I, Immerzeel P, Mellerowicz EJ, Salvi G, Cervone F, Bellincampi D (2011) Pectin methylesterase is induced in Arabidopsis upon infection and is necessary for a successful colonization by necrotrophic pathogens. Mol Plant Microbe Interact 24: 432–440 PubMed

Ridley BL, O’Neill MA, Mohnen D (2001) Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry 57: 929–967 PubMed

Rodriguez PA, Bos JIB (2013) Toward understanding the role of aphid effectors in plant infestation. Mol Plant Microbe Interact 26: 25–30 PubMed

Sadhukhan A, Kobayashi Y, Nakano Y, Iuchi S, Kobayashi M, Sahoo L, Koyama H (2017) Genome-wide association study reveals that the aquaporin NIP1;1 contributes to variation in hydrogen peroxide sensitivity in Arabidopsis thaliana. Mol Plant 10: 1082–1094 PubMed

Schmidt R, Kunkowska AB, Schippers JHM (2016) Role of reactive oxygen species during cell expansion in leaves. Plant Physiol 172: 2098–2106 PubMed PMC

Schoonhoven LM, Loon JJA, Dicke M (2005) Insect–plant biology. Oxford University Press, Oxford

Schurch NJ, Schofield P, Gierliński M, Cole C, Sherstnev A, Singh V, Wrobel N, Gharbi K, Simpson GG, Owen-Hughes T, et al. (2016) How many biological replicates are needed in an RNA-seq experiment and which differential expression tool should you use? RNA 22: 839–851 PubMed PMC

Schwalb B, Tresch A, Torkler P, Duemcke S, Demel C, Ripley B, Venables B (2018) LSD: Lots of Superior Depictions. R package version 3.0. http://CRAN.R-project.org/package=LSD (February 20, 2018).

Sgherri C, Stevanovic B, Navari-Izzo F (2004) Role of phenolics in the antioxidative status of the resurrection plant Ramonda serbica during dehydration and rehydration. Physiol Plant 122: 478–485

Shaw SL, Long SR (2003) Nod factor inhibition of reactive oxygen efflux in a host legume. Plant Physiol 132: 2196–2204 PubMed PMC

Silva-Sanzana C, Celiz-Balboa J, Garzo E, Marcus SE, Parra-Rojas JP, Rojas B, Olmedo P, Rubilar MA, Rios I, Chorbadjian RA, et al. (2019) Pectin methylesterases modulate plant homogalacturonan status in defenses against the aphid Myzus persicae. Plant Cell 31: 1913–1929 PubMed PMC

Smith CM, Boyko EV (2007) The molecular bases of plant resistance and defense responses to aphid feeding: Current status. Entomol Exp Appl 122: 1–16

Soneson C, Love M, Robinson M (2015) Differential analyses for RNA-seq: Transcript-level estimates improve gene-level inferences PubMed PMC

Stolpe C, Giehren F, Krämer U, Müller C (2017) Both heavy metal-amendment of soil and aphid-infestation increase Cd and Zn concentrations in phloem exudates of a metal-hyperaccumulating plant. Phytochemistry 139: 109–117 PubMed

Supek F, Bošnjak M, Škunca N, Šmuc T (2011) REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One 6: e21800. PubMed PMC

ten Broeke CJM, Dicke M, van Loon JJA (2013) Performance and feeding behaviour of two biotypes of the black currant-lettuce aphid, Nasonovia ribisnigri, on resistant and susceptible Lactuca sativa near-isogenic lines. Bull Entomol Res 103: 511–521 PubMed

Tetyuk O, Benning UF, Hoffmann-Benning S (2013) Collection and analysis of Arabidopsis phloem exudates using the EDTA-facilitated Method. J Vis Exp 80: e51111 PubMed PMC

Thoma I, Loeffler C, Sinha AK, Gupta M, Krischke M, Steffan B, Roitsch T, Mueller MJ (2003) Cyclopentenone isoprostanes induced by reactive oxygen species trigger defense gene activation and phytoalexin accumulation in plants. Plant J 34: 363–375 PubMed

Tjallingii WF. (1988) Electrical recording of stylet penetration activities In Minks AK, and Harrewijn P, eds, Aphids, their biology, natural enemies and control, Vol 2B. Elsevier, Amsterdam, pp 95–108

Tjallingii WF. (1994) Sieve element acceptance by aphids. Eur J Entomol 91: 47–52

Tjallingii WF, Hogen Esch T (1993) Fine structure of aphid stylet routes in plant tissues in correlation with EPG signals. Physiol Entomol 18: 317–328

Trapalis M, Li SF, Parish RW (2017) The Arabidopsis GASA10 gene encodes a cell wall protein strongly expressed in developing anthers and seeds. Plant Sci 260: 71–79 PubMed

van Bel AJE, Will T (2016) Functional evaluation of proteins in watery and gel saliva of aphids. Front Plant Sci 7: 1840. PubMed PMC

Vorhölter F-J, Wiggerich H-G, Scheidle H, Sidhu VK, Mrozek K, Küster H, Pühler A, Niehaus K (2012) Involvement of bacterial TonB-dependent signaling in the generation of an oligogalacturonide damage-associated molecular pattern from plant cell walls exposed to Xanthomonas campestris pv. campestris pectate lyases. BMC Microbiol 12: 239. PubMed PMC

Vorwerk S, Somerville S, Somerville C (2004) The role of plant cell wall polysaccharide composition in disease resistance. Trends Plant Sci 9: 203–209 PubMed

Wagner TA, Kohorn BD (2001) Wall-associated kinases are expressed throughout plant development and are required for cell expansion. Plant Cell 13: 303–318 PubMed PMC

Walker GP, Medina-Ortega KJ (2012) Penetration of faba bean sieve elements by pea aphid does not trigger forisome dispersal. Entomol Exp Appl 144: 326–335

Waszczak C, Carmody M, Kangasjärvi J (2018) Reactive oxygen species in plant signaling. Annu Rev Plant Biol 69: 209–236 PubMed

Willats WGT, McCartney L, Mackie W, Knox JP (2001) Pectin: Cell biology and prospects for functional analysis. Plant Mol Biol 47: 9–27 PubMed

Williams KM, Martin WE, Smith J, Williams BS, Garner BL (2012) Production of protocatechuic acid in Bacillus Thuringiensis ATCC33679. Int J Mol Sci 13: 3765–3772 PubMed PMC

Wolf S. (2017) Plant cell wall signalling and receptor-like kinases. Biochem J 474: 471–492 PubMed

Wu J, Baldwin IT (2010) New insights into plant responses to the attack from insect herbivores. Annu Rev Genet 44: 1–24 PubMed

Zhang B, Van Aken O, Thatcher L, De Clercq I, Duncan O, Law SR, Murcha MW, van der Merwe M, Seifi HS, Carrie C, et al. (2014) The mitochondrial outer membrane AAA ATPase AtOM66 affects cell death and pathogen resistance in Arabidopsis thaliana. Plant J 80: 709–727 PubMed

Zhang Y, Talalay P, Cho CG, Posner GH (1992) A major inducer of anticarcinogenic protective enzymes from broccoli: Isolation and elucidation of structure. Proc Natl Acad Sci USA 89: 2399–2403 PubMed PMC

Zhou N, Tootle TL, Glazebrook J (1999) Arabidopsis PAD3, a gene required for camalexin biosynthesis, encodes a putative cytochrome P450 monooxygenase. Plant Cell 11: 2419–2428 PubMed PMC

Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428: 764–767 PubMed