Abstract
Many of the proteins and defense pathways in maize that are activated in an organ-specific manner in leaves and roots during aboveground caterpillar attack have not yet been identified. In this study, we examined systemic and organ-specific defenses in the insect-resistant maize genotype, Mp708, when infested aboveground with fall armyworm (FAW, Spodoptera frugiperda). We used proteomic and network biology analyses and then integrated these data with known FAW resistance QTL to create a protein abundance QTL (pQTL) subnetwork. Using 10-plex tandem mass spectrometry tags (TMT) proteomics technique, we identified a total of 4675 proteins in leaves and roots of control and FAW-infested plants. Among the identified proteins, 794 had significant differences in abundance in response to FAW herbivory. Proteins that were upregulated in leaves during FAW infestation included jasmonic acid biosynthetic enzymes, cysteine proteases, protease inhibitors, REDOX-related proteins, and peroxidases. In roots, highly abundant proteins were involved in ET biosynthesis, DNA expression regulation, and pyruvate biosynthesis. We found many proteins that possibly contribute different defense functions to FAW resistance in Mp708. One potential resistance mechanism identified was that trade-offs between growth and defense responses were reduced in Mp708. Some of the proteins involved in this trade-off that were found within the pQTL subnetwork were the Kinesin-like protein (GRMZM2G046186_P01) and Pi starvation-induced protein (GRMZM2G118037_P01). We proposed other mechanisms contributing to resistance that suggest that jasmonic acid and ethylene control the local accumulation of insecticidal cysteine protease (MIR1-CP) in leaves, while ethylene controlled the systemic accumulation of MIR1-CP in roots. Finally, we hypothesized that receptor kinases such as receptor protein kinase 1 (GRMZM2G055678) could be involved in the activation of root-specific defense responses during aboveground insect infestation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ali A, Luttrell RG, Schneider JC (1990) Effects of temperature and larval diet on development of the fall armyworm (Lepidoptera: Noctuidae). Ann Entomol Soc Am 83:725–733. doi:10.1093/aesa/83.4.725
Almagro L, Ros LVG, Belchi-Navarro S, Bru R, Barcelo AR, Pedreno MA (2009) Class III peroxidases in plant defence reactions. J Exp Bot 60:377–390. doi:10.1093/jxb/ern277
Ankala A, Luthe DS, Williams WP, Wilkinson JR (2009) Integration of ethylene and jasmonic acid signaling pathways in the expression of maize defense protein Mir1-CP. Mol Plant Microbe Interact 22:1555–1564. doi:10.1094/mpmi-22-12-1555
Ankala A, Kelley RY, Rowe DE, Williams WP, Luthe DS (2013) Foliar herbivory triggers local and long distance defense responses in maize. Plant Sci 199:103–112. doi:10.1016/j.plantsci.2012.09.017
Aranda B et al (2010) The IntAct molecular interaction database in 2010. Nucleic Acids Res 38:D525–D531. doi:10.1093/nar/gkp878
Arraes FBM et al (2015) Implications of ethylene biosynthesis and signaling in soybean drought stress tolerance Bmc. Plant Biol 15:213. doi:10.1186/s12870-015-0597-z
Augustine RC, Vidali L, Kleinman KP, Bezanilla M (2008) Actin depolymerizing factor is essential for viability in plants, and its phosphoregulation is important for tip growth. Plant J 54:863–875. doi:10.1111/j.1365-313X.2008.03451.x
Ballare CL (2011) Jasmonate-induced defenses: a tale of intelligence, collaborators and rascals. Trends Plant Sci 16:249–257. doi:10.1016/j.tplants.2010.12.001
Barah P, Bones AM (2015) Multidimensional approaches for studying plant defence against insects: from ecology to omics and synthetic biology. J Exp Bot 66:479–493. doi:10.1093/jxb/eru489
Bassel GW, Gudinier A, Brady SM, Hennig L, Rhee S, Smet ID (2012) Systems analysis of plant functional, transcriptional, physical interaction, and metabolic networks. Plant Cell 24:3859–3875. doi:10.1105/tpc.112.100776
Bergeron F, Leduc R, Day R (2000) Subtilase-like pro-protein convertases: from molecular specificity to therapeutic applications. J Mol Endocrinol 24:1–22. doi:10.1677/jme.0.0240001
Bindea G et al (2009) ClueGO: a cytoscape plug-into decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics 25(8):1091–1093. doi:10.1093/bioinformatics/btp101
Broekgaarden C, Caarls L, Vos IA, Pieterse CMJ, Van Wees SCM (2015) Ethylene: traffic controller on hormonal crossroads to defense. Plant Physiol 169:2371–2379. doi:10.1104/pp.15.01020
Brooks TD, Willcox MC, Williams WP, Buckley PM (2005) Quantitative trait loci conferring resistance to fall armyworm and southwestern corn borer leaf feeding damage. Crop Sci 45:2430–2434. doi:10.2135/cropsci2004.0656
Brooks TD, Bushman BS, Williams WP, McMullen MD, Buckley PM (2007) Genetic basis of resistance to fall armyworm (Lepidoptera : Noctuidae) and southwestern corn borer (Lepidoptera: Crambidae) leaf-feeding damage in maize. J Econ Entomol 100:1470–1475
Brown AE, Smith WEC, Shivaji R, Williams WP, Luthe DS, Sandoya GV, Smith C (2011) Mp708 a maize (Zea mays) line resistant to herbivory constitutively releases (E)-b-caryophyllene. J Econ Entomol 105:120–128. doi:10.1603/EC11107
Chatr-aryamontri A, Ceol A, Palazzi LM, Nardelli G, Schneider MV, Castagnoli L, Cesareni G (2007) MINT: the molecular INTeraction database. Nucleic Acids Res 35:D572–D574. doi:10.1093/nar/gkl950
Cheval C, Aldon D, Galaud JP, Ranty B (2013) Calcium/calmodulin-mediated regulation of plant immunity biochimica et biophysica acta-molecular. Cell Res 1833:1766–1771. doi:10.1016/j.bbamcr.2013.01.031
Chini A et al (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666–671. doi:10.1038/nature06006
Chuang W-P, Herde M, Ray S, Castano-Duque L, Howe GA, Luthe DS (2014) Caterpillar attack triggers accumulation of the toxic maize protein RIP2. New Phytol 201:928–939. doi:10.1111/nph.12581
Cline MS et al (2007) Integration of biological networks and gene expression data using cytoscape. Nat Protoc 2:2366–2386. doi:10.1038/nprot.2007.324
Corwin JA, Kliebenstein DJ (2017) Quantitative resistance: more than just perception of a pathogen. Plant Cell 29:655–665. doi:10.1105/tpc.16.00915
Doncheva NT, Assenov Y, Domingues FS, Albrecht M (2012) Topological analysis and interactive visualization of biological networks and protein structures. Nat Protoc 7:670–685. doi:10.1038/nprot.2012.004
Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:W64–W70. doi:10.1093/nar/gkq310
Dudareva N, Klempien A, Muhlemann JK, Kaplan I (2013) Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol 198:16–32. doi:10.1111/nph.12145
Eleazar Ruiz-Najera R, Molina-Ochoa J, Carpenter JE, Espinosa-Moreno JA, Alfredo Ruiz-Najera J, Lezama-Gutierrez R, Foster JE (2007) Survey for Hymenopteran and Dipteran parasitoids of the fall armyworm (Lepidoptera: Noctuidae) in Chiapas. Mexico J Agric Urban Entomol 24:35–42. doi:10.3954/1523-5475-24.1.35
Erb M, Glauser G (2010) Family business: multiple members of major phytohormone classes orchestrate plant stress responses chemistry-a. European J 16:10280–10289. doi:10.1002/chem.201001219
Erb M, Glauser G, Robert CAM (2012) Induced immunity against belowground insect herbivores-activation of defenses in the absence of a jasmonate burst. J Chem Ecol 38:240–629. doi:10.1007/s10886-012-0107-9
Erb M, Veyrat N, Robert CAM, Xu H, Frey M, Ton J, Turlings TCJ (2015) Indole is an essential herbivore-induced volatile priming signal in maize. Nature Commun 6:6273. doi:10.1038/ncomms7273
Fonseca S et al (2009) (+)-7-iso-Jasmonoyl-l-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol 5:344–350. doi:10.1038/nchembio.161
Galis I, Gaquerel E, Pandey SP, Baldwin IT (2009) Molecular mechanisms underlying plant memory in JA-mediated defence responses. Plant Cell Environ 32:617–627. doi:10.1111/j.1365-3040.2008.01862.x
Galli M et al (2015) Auxin signaling modules regulate maize inflorescence architecture. Proc Natl Acad Sci 112:13372–13377
Gill TA, Sandoya G, Williams P, Luthe DS (2011) Belowground resistance to western corn rootworm in lepidopteran-resistant maize genotypes. J Econ Entomol 104:299–307. doi:10.1603/ec10117
Goergen G, Kumar PL, Sankung SB, Togola A, Tamò M (2016) First report of outbreaks of the fall armyworm Spodoptera frugiperda (J E Smith) (Lepidoptera, Noctuidae), a new alien invasive pest in west and central Africa. PLoS ONE 11:e0165632. doi:10.1371/journal.pone.0165632
Green TR, Ryan CA (1972) Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175:776–777. doi:10.1126/science.175.4023.776
Gulati J, Baldwin IT, Gaquerel E (2014) The roots of plant defenses: integrative multivariate analyses uncover dynamic behaviors of roots’ gene and metabolic networks elicited by leaf herbivory. Plant J 77:880–892. doi:10.1111/tpj.12439
Harfouche AL, Shivaji R, Stocker R, Williams PW, Luthe DS (2006) Ethylene signaling mediates a maize defense response to insect herbivory. Mol Plant Microbe Interact 19:189–199. doi:10.1094/MPMI-19-0189
Hoang A (2010) The role of peroxidase in the defense response of buffalograss to chinch bugs. University of Nebraska, Lincoln
Hu F, Huang J, Xu Y, Gian X, Zhong J-J (2006) Responses of defense signals, biosynthetic gene transcription and taxoid biosynthesis to elicitation by a novel synthetic jasmonate in cell cultures of Taxus chinensis. Biotechnol Bioeng 94:1064–1071. doi:10.1002/bit.20921
Ideker T, Ozier O, Schwikowski B, Siegel AF (2002) Discovering regulatory and signalling circuits in molecular interaction networks. Bioinformatics (Oxford, England) 18(Suppl 1):S233–S240. doi:10.1093/bioinformatics/18.suppl_1.S233
Iven T et al (2012) Transcriptional activation and production of tryptophan-derived secondary metabolites in arabidopsis roots contributes to the defense against the fungal vascular pathogen Verticillium longisporum. Mol Plant 5:1389–1402. doi:10.1093/mp/sss044
Jiang BH, Siregar U, Willeford KO, Luthe DS, Williams WP (1995) Association of a 33-kilodalton cysteine proteinase found in corn callus with the inhibition of fall armyworm larval growth. Plant Physiol 108:1631–1640. doi:10.1104/pp.108.4.1631
Johnson KL, Jones BJ, Bacic A, Schultz CJ (2003) The fasciclin-like arabinogalactan proteins of arabidopsis. A multigene family of putative cell adhesion molecules. Plant Physiol 133:1911–1925. doi:10.1104/pp.103.031237
Kant MR et al (2015) Mechanisms and ecological consequences of plant defence induction and suppression in herbivore communities. Ann Bot 115:1015–1051. doi:10.1093/aob/mcv054
Kim S-Y, Volsky DJ (2005) PAGE: parametric analysis of gene set enrichment. BMC Bioinform 6:144. doi:10.1186/1471-2105-6-144
Koo AJK, Howe GA (2009) The wound hormone jasmonate. Phytochemistry 70:1571–1580. doi:10.1016/j.phytochem.2009.07.018
Lambers H, Atkin OK, Millenaar FF (1996) Respiratory patterns in roots in relation to their functioning. In: Waisel Y, Eshel A, Kafkaki U (eds) Plant Roots. The Hidden Half. 3 edn. Marcel Dekker, New York, pp 521-552. doi:10.1201/9780203909423.pt6
Lee JS et al (1986) Molecular characterization and phylogenetic studies of a wound-inducible proteinase inhibitor I gene in Lycopersicon species. Proc Natl Acad Sci USA 83:7277–7281. doi:10.1073/pnas.83.19.7277
Lopez L, Camas A, Shivaji R, Ankala A, Williams P, Luthe D (2007) Mir1-CP, a novel defense cysteine protease accumulates in maize vascular tissues in response to herbivory. Planta 226:517–527. doi:10.1007/s00425-007-0501-7
Louis J et al (2015) Ethylene contributes to maize insect resistance1-mediated maize defense against the phloem sap-sucking corn leaf aphid. Plant Physiol 169:313–324. doi:10.1104/pp.15.00958
Marti G et al (2012) Metabolomics reveals herbivore-induced metabolites of resistance and susceptibility in maize leaves and roots. Plant Cell Environ 36:621–623. doi:10.1111/pce.12002
Matern S, Peskan-Berghoefer T, Gromes R, Kiesel RV, Rausch T (2015) Imposed glutathione-mediated redox switch modulates the tobacco wound-induced protein kinase and salicylic acid-induced protein kinase activation state and impacts on defence against Pseudomonas syringae. J Exp Bot 66:1935–1950. doi:10.1093/jxb/eru546
McConn M, Creelman RA, Bell E, Mullet JE, Browse J (1997) Jasmonate is essential for insect defense Arabidopsis. Proc Natl Acad Sci USA 94:5473–5477. doi:10.1073/pnas.94.10.5473
McDermott JE, Diamond DL, Corley C, Rasmussen AL, Katze MG, Waters KM (2012) Topological analysis of protein co-abundance networks identifies novel host targets important for HCV infection and pathogenesis Bmc. Sys Biol 6:28. doi:10.1186/1752-0509-6-28
Mierziak J, Kostyn K, Kulma A (2014) Flavonoids as important molecules of plant interactions with the environment. Molecules 19:16240–16265. doi:10.3390/molecules191016240
Mohan S, Ma PWK, Pechan T, Bassford ER, Williams WP, Luthe DS (2006) Degradation of the S. frugiperda peritrophic matrix by an inducible maize cysteine protease. J Insect Physiol 52:21–28. doi:10.1016/j.jinsphys.2005.08.011
Mohan S, Ma PWK, Williams WP, Luthe DS (2008) A naturally occurring plant cysteine protease possesses remarkable toxicity against insect pests and synergizes Bacillus thuringiensis toxin. PLoS ONE 3:e1786. doi:10.1371/journal.pone.0001786
Mou SL, Liu ZQ, Guan DY, Qiu AL, Lai Y, He SL (2013) Functional analysis and expressional characterization of rice ankyrin repeat-containing protein, OsPIANK1, in basal defense against Magnaporthe oryzae attack. PLoS ONE 8:e59699. doi:10.1371/journal.pone.0059699
Musungu B, Bhatnagar D, Brown RL, Fakhoury AM, Geisler M (2015) A predicted protein interactome identifies conserved global networks and disease resistance subnetworks in maize. Front Genetics 6:201. doi:10.3389/fgene.2015.00201
Paez-Garcia A, Motes CM, Scheible W-R, Chen R, Blancaflor EB, Monteros MJ (2015) Root traits and phenotyping strategies for plant improvement. Plants-Basel 4:334–355. doi:10.3390/plants4020334
Pare PW, Tumlinson JH (1999) Plant volatiles as a defense against insect herbivores. Plant Physiol 121:325–331. doi:10.1104/pp.121.2.325
Paudel J, Copley T, Amirizian A, Prado A, Bede JC (2013) Arabidopsis redox status in response to caterpillar herbivory Frontiers. Plant Sci 4:113. doi:10.3389/fpls.2013.00113
Pechan T et al (2000) A unique 33-kD cysteine proteinase accumulates in response to larval feeding in maize genotypes resistant to fall armyworm and other lepidoptera. Plant cell 12:1031–1041. doi:10.2307/3871253
Provart N (2012) Correlation networks visualization. Front Plant Sci 3:240. doi:10.3389/fpls.2012.00240
Qi J et al (2016) Oral secretions from Mythimna separata insects specifically induce defence responses in maize as revealed by high-dimensional biological data. Plant Cell Environ 39:1749–1766. doi:10.1111/pce.12735
Ritchie JT, Singh U, Godwin DC (1998) Cereal growth, development and yield. In: Tsuji GY, Hoogenboom G, Thornton PK (eds) Understanding options for agricultural production. Kluwer academic publishers, Dordrecht, pp 78–98
Rohrmeier T, Lehle L (1993) WIP1, a wound-inducible gene from maize with homology to Bowman–Birk proteinase inhibitors. Plant Mol Biol 22:783–792. doi:10.1007/BF00027365
Roux F et al (2014) Resistance to phytopathogens e tutti quanti: placing plant quantitative disease resistance on the map. Mol Plant Pathol 15:427–432. doi:10.1111/mpp.12138
Saathoff AJ et al (2013) Towards uncovering the roles of switchgrass peroxidases in plant processes Frontiers. Plant Sci 4:202. doi:10.3389/fpls.2013.00202
Salwinski L, Miller CS, Smith AJ, Pettit FK, Bowie JU, Eisenberg D (2004) The database of interacting proteins: 2004 update. Nucleic Acids Res 32:D449–D451. doi:10.1093/nar/gkh086
Sarazin V et al (2015) Arabidopsis BNT1, an atypical TIR-NBS-LRR gene, acting as a regulator of the hormonal response to stress. Plant Sci 239:216–229. doi:10.1016/j.plantsci.2015.07.017
Schellingen K, Van der Straeten D, Remans T, Loix C, Vangronsveld J, Cuypers A (2015) Ethylene biosynthesis is involved in the early oxidative challenge induced by moderate Cd exposure in Arabidopsis thaliana. Environ Exp Bot 117:1–11. doi:10.1016/j.envexpbot.2015.04.005
Schmelz EA, Alborn HT, Tumlinson JH (2003) Synergistic interactions between volicitin, jasmonic acid and ethylene mediate insect-induced volatile emission in Zea mays. Physiol Plant 117:403–412. doi:10.1034/j.1399-3054.2003.00054.x
Scholz SS, Heyer M, Vadassery J, Mithöfer A (2016) A role for calmodulin-like proteins in herbivore defense pathways in plants. J Endocytobiosis Cell Res 27:1–12
Shivaji R et al (2010) Plants on constant alert: elevated levels of jasmonic acid and jasmonate-induced transcripts in caterpillar-resistant maize. J Chem Ecol 36:179–191. doi:10.1007/s10886-010-9752-z
Song S et al (2014) Interaction between MYC2 and ETHYLENE INSENSITIVE3 modulates antagonism between jasmonate and ethylene signaling in arabidopsis. Plant Cell 26:263–279. doi:10.1105/tpc.113.120394
Stark C, Breitkreutz B-J, Reguly T, Boucher L, Breitkreutz A, Tyers M (2006) BioGRID: a general repository for interaction datasets. Nucleic Acids Res 34:D535–D539. doi:10.1093/nar/gkj109
Studham ME, Macintosh G (2012) Phytohormone signaling pathway analysis method for comparing hormone responses in plant-pest interactions. BMC Res Notes 5:392. doi:10.1186/1756-0500-5-392
Supek F, Bosnjak M, Skunca N, Smuc T (2011) REVIGO summarizes and visualizes long lists of gene ontology terms. Plos One 6:e21800. doi:10.1371/journal.pone.0021800
Suzuki H, Dowd PF, Johnson ET, Hum-Musser SM, Musser RO (2012) Effects of elevated peroxidase levels and corn earworm feeding on gene expression in tomato. J Chem Ecol 38:1247–1263. doi:10.1007/s10886-012-0205-8
Team RC (2015) R: a language and environment for statistical computing. R foundation for statistical computing. https://www.R-project.org
Thines B et al (2007) JAZ repressor proteins are targets of the SCFCO11 complex during jasmonate signalling. Nature 448:661–665. doi:10.1038/nature05960
Tian DL, Peiffer M, De Moraes CM, Felton GW (2014) Roles of ethylene and jasmonic acid in systemic induced defense in tomato (Solanum lycopersicum) against Helicoverpa zea. Planta 239:577–589. doi:10.1007/s00425-013-1997-7
Venu RC et al (2010) Deep and comparative transcriptome analysis of rice plants infested by the beet armyworm (Spodoptera exigua) and water weevil (Lissorhoptrus oryzophilus). Rice 3:22–35. doi:10.1007/s12284-010-9037-8
Walter A, Mazars C, Maitrejean M, Hopke J, Ranjeva R, Boland W, Mithöfer A (2007) Structural requirements of jasmonates and synthetic analogues as inducers of Ca2+ signals in the nucleus and the cytosol of plant cells. Angew Chem Int Ed 46:4783–4785. doi:10.1002/anie.200604989
War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC (2012) Mechanisms of plant defense against insect herbivores. Plant Signal Behav 7:1306–1320. doi:10.4161/psb.21663
Weckwerth W (2011) Green systems biology—from single genomes, proteomes and metabolomes to ecosystems research and biotechnology. J Proteom 75:284–305. doi:10.1016/j.jprot.2011.07.010
Williams WP, Buckley PM, Davis FM (1985) Larval growth and behavior of the Fall Armyworm (Lepidoptera: Noctuidae) on callus initiated from susceptible and resistant corn hybrids. J Econ Entomol 78:951–954. doi:10.1093/jee/78.4.951
Williams WP, Davis FM, Windham GL (1990) Registration of Mp708 germplasm line of maize. Crop Sci 30:757
Wouters FC, Blanchette B, Gershenzon J, Vassão DG (2016) Plant defense and herbivore counter-defense: benzoxazinoids and insect herbivores. Phytochem Rev 15:1127–1151. doi:10.1007/s11101-016-9481-1
Zhang S, Yang X, Sun M, Sun F, Deng S, Dong H (2009) Riboflavin-induced priming for pathogen defense in Arabidopsis thaliana. J Integr Plant Biol 51:167–174. doi:10.1111/j.1744-7909.2008.00763.x
Zhao YY, Wang DF, Wu TQ, Guo A, Dong HS, Zhang CL (2014) Transgenic expression of a rice riboflavin synthase gene in tobacco enhances plant growth and resistance to tobacco mosaic virus. Can J Plant Path 36:100–109. doi:10.1080/07060661.2014.881921
Zhou S, Lou Y-R, Tzin V, Jander G (2015) Alteration of plant primary metabolism in response to insect herbivory. Plant Physiol 169:1488–1498. doi:10.1104/pp.15.01405
Zhu L (2010) Study of defense genes expression induced by leaf herbivory in roots of insect-resistant maize. The Pennsylvania State University, State College
Zhu Z et al (2011) Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proc Natl Acad Sci USA 108:12539–12544. doi:10.1073/pnas.1103959108
Acknowledgements
We thank Dr. Reka Albert for advice in the systems biology data analysis. This material is based upon the work supported by the National Science Foundation Graduate Research Fellowship Program under Grant No. DGE1255832.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Ritu Chaudhary.
Electronic supplementary material
Below is the link to the electronic supplementary material.
11829_2017_9562_MOESM2_ESM.xlsx
Supplementary material 2 (XLSX 2712 kb) . Table S1. Identified proteins present in leaves and roots of control and FAW infested plants (95 % false discovery rate) with their protein abundance ratios. Logarithm of protein abundance ratios were analyzed using multiple-factor ANOVA followed by honest significant difference (HSD) Tukey pairwise comparison test. Letters represent results of the HSD (P<0.05) and error bars show the standard error
11829_2017_9562_MOESM3_ESM.xlsx
Supplementary material 3 (XLSX 795 kb). Table S2. Proteins and gene ontology annotation from the hierarchical clustering analysis. The 10 k-mean groups are labeled as protein families and represent 10 different protein abundance patterns determined by using an Euclidian similarity distance method to determine abundance patterns using a maximum of 10 k-means cut off
11829_2017_9562_MOESM4_ESM.xlsx
Supplementary material 4 (XLSX 150 kb). Table S3. Proteins and their annotations present in the abundance correlation network from the Supplemental Cytoscape file 1
11829_2017_9562_MOESM5_ESM.xlsx
Supplementary material 5 (XLSX 301 kb). Table S4. Proteins and their annotations present in the protein-protein interaction network from the Supplemental Cytoscape file 2
11829_2017_9562_MOESM6_ESM.cys
Supplementary material 6 (CYS 6919 kb). Supplemental File S1. Protein abundance correlation network built with Cytoscape (813 nodes and 17197 edges)
11829_2017_9562_MOESM7_ESM.cys
Supplementary material 7 (CYS 5596 kb). Supplemental File S2. Protein-protein interaction network built with Cytoscape, using TMT data (1181 nodes and 4142 edges)
Rights and permissions
About this article
Cite this article
Castano-Duque, L., Luthe, D.S. Protein networks reveal organ-specific defense strategies in maize in response to an aboveground herbivore. Arthropod-Plant Interactions 12, 147–175 (2018). https://doi.org/10.1007/s11829-017-9562-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11829-017-9562-0