Transcriptome and metabolome analysis reveal that oral secretions from Helicoverpa armigera and Spodoptera litura influence wound-induced host response in cotton

Howe, 2008, Plant immunity to insect herbivores, Annu. Rev. Plant Biol., 59, 41, 10.1146/annurev.arplant.59.032607.092825 Wu, 2007, Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata, Plant Cell, 19, 1096, 10.1105/tpc.106.049353 Schmelz, 2009, Phytohormone-based activity mapping of insect herbivore-produced elicitors, Proc. Natl. Acad. Sci. U. S. A., 106, 653, 10.1073/pnas.0811861106 Erb, 2012, Role of phytohormones in insect-specific plant reactions, Trends Plant Sci., 17, 250, 10.1016/j.tplants.2012.01.003 Hu, 2018, OsLRR-RLK1, an early responsive leucine-rich repeat receptor-like kinase, initiates rice defense responses against a chewing herbivore, New Phytol., 219, 1097, 10.1111/nph.15247 Morris, 2003, Receptor-like protein kinases: the keys to response, Curr. Opin. Plant Biol., 6, 339, 10.1016/S1369-5266(03)00055-4 Wu, 2016, Genome-wide expression pattern analyses of the Arabidopsis leucine-rich repeat receptor-like kinases, Mol. Plant, 9, 289, 10.1016/j.molp.2015.12.011 Wu, 2010, New insights into plant responses to the attack from insect herbivores, Annu. Rev. Genet., 44, 1, 10.1146/annurev-genet-102209-163500 Furstenberg Hagg, 2013, Plant defense against insect herbivores, Int. J. Mol. Sci., 14, 10242, 10.3390/ijms140510242 War, 2012, Mechanisms of plant defense against insect herbivores, Plant Signal. Behav., 7, 1306, 10.4161/psb.21663 Mithofer, 2012, Plant defense against herbivores: chemical aspects, Annu. Rev. Plant Biol., 63, 431, 10.1146/annurev-arplant-042110-103854 Hopkins, 2009, Role of glucosinolates in insect-plant relationships and multitrophic interactions, Annu. Rev. Entomol., 54, 57, 10.1146/annurev.ento.54.110807.090623 Alamgir, 2016, Systematic analysis of rice (Oryza sativa) metabolic responses to herbivory, Plant Cell Environ., 39, 453, 10.1111/pce.12640 Hu, 2018, Laccase GhLac1 modulates broad-spectrum biotic stress tolerance via manipulating phenylpropanoid pathway and jasmonic acid synthesis, Plant Physiol., 176, 1808, 10.1104/pp.17.01628 Wang, 2018, CYP6AE gene cluster knockout in Helicoverpa armigera reveals role in detoxification of phytochemicals and insecticides, Nat. Commun., 9, 4820, 10.1038/s41467-018-07226-6 Alba, 2015, Spider mites suppress tomato defenses downstream of jasmonate and salicylate independently of hormonal crosstalk, New Phytol., 205, 828, 10.1111/nph.13075 Villarroel, 2016, Salivary proteins of spider mites suppress defenses in Nicotiana benthamiana and promote mite reproduction, Plant J., 86, 119, 10.1111/tpj.13152 Sarmento, 2011, A herbivore that manipulates plant defence, Ecol. Lett., 14, 229, 10.1111/j.1461-0248.2010.01575.x Kelli, 2010, Microbial symbionts in insects influence down-regulation of defense genes in maize, PLoS One, 5, 11339, 10.1371/journal.pone.0011339 Chen, 2019, An effector from cotton bollworm oral secretion impairs host plant defense signaling, Proc. Natl. Acad. Sci. U. S. A., 116, 14331, 10.1073/pnas.1905471116 Hosokawa, 2007, Obligate symbiont involved in pest status of host insect, Proc. Biol. Sci., 274, 1979 Kaiser, 2010, Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts, Proc. Biol. Sci., 277, 2311 Qi, 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, 10.1111/pce.12735 Hui, 2003, Molecular interactions between the specialist herbivore Manduca sexta (lepidoptera, sphingidae) and its natural host Nicotiana attenuata: V. microarray analysis and further characterization of large-scale changes in herbivore-induced mRNAs, Plant Physiol., 131, 1877, 10.1104/pp.102.018176 Lortzing, 2017, Transcriptomic responses of Solanum dulcamara to natural and simulated herbivory, Mol. Ecol. Resour., e196, 10.1111/1755-0998.12687 Ma, 2018, Resequencing a core collection of upland cotton identifies genomic variation and loci influencing fiber quality and yield, Nat. Genet., 50, 803, 10.1038/s41588-018-0119-7 Wang, 2017, Asymmetric subgenome selection and cis-regulatory divergence during cotton domestication, Nat. Genet., 49, 579, 10.1038/ng.3807 Wilson, 2018, The management of insect pests in Australian cotton: an evolving story, Annu. Rev. Entomol., 63, 215, 10.1146/annurev-ento-020117-043432 Liu, 2017, Dynamic metabolic responses of brown planthoppers towards susceptible and resistant rice plants, Plant Biotechnol. J., 15, 1346, 10.1111/pbi.12721 Guo, 2018, Bph6 encodes an exocyst-localized protein and confers broad resistance to planthoppers in rice, Nat. Genet., 50, 297, 10.1038/s41588-018-0039-6 Guo, 2019, The Asian corn borer Ostrinia furnacalis feeding increases the direct and indirect defence of mid-whorl stage commercial maize in the field, Plant Biotechnol. J., 17, 88, 10.1111/pbi.12949 Trapnell, 2009, TopHat: discovering splice junctions with RNA-Seq, Bioinformatics, 25, 1105, 10.1093/bioinformatics/btp120 Trapnell, 2012, Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks, Nat. Protoc., 7, 562, 10.1038/nprot.2012.016 Zhang, 2015, Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement, Nat. Biotechnol., 33, 531, 10.1038/nbt.3207 Ye, 2018, WEGO 2.0: a web tool for analyzing and plotting GO annotations, 2018 update, Nucleic Acids Res., 46, W71, 10.1093/nar/gky400 Wu, 2006, KOBAS server: a web-based platform for automated annotation and pathway identification, Nucleic Acids Res., 34, W720, 10.1093/nar/gkl167 Smith, 2006, XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification, Anal. Chem., 78, 779, 10.1021/ac051437y Kuhl, 2012, CAMERA: an integrated strategy for compound spectra extraction and annotation of liquid chromatography/mass spectrometry data sets, Anal. Chem., 84, 283, 10.1021/ac202450g Dunn, 2011, Procedures for large-scale metabolic profiling of serum and plasma using gas chromatography and liquid chromatography coupled to mass spectrometry, Nat. Protoc., 6, 1060, 10.1038/nprot.2011.335 Xia, 2015, MetaboAnalyst 3.0—making metabolomics more meaningful, Nucleic Acids Res., 43, W251, 10.1093/nar/gkv380 Simmonds, 2003, Flavonoid–insect interactions: recent advances in our knowledge, Phytochemistry, 64, 21, 10.1016/S0031-9422(03)00293-0 Misra, 2010, Modulation of transcriptome and metabolome of tobacco by Arabidopsis transcription factor, AtMYB12, leads to insect resistance, Plant Physiol., 152, 2258, 10.1104/pp.109.150979 Wu, 2008, A comparison of two Nicotiana attenuata accessions reveals large differences in signaling induced by oral secretions of the specialist herbivore Manduca sexta, Plant Physiol., 146, 927, 10.1104/pp.107.114785 Wang, 2016, Herbivore oral secreted bacteria trigger distinct defense responses in preferred and non-preferred host plants, J. Chem. Ecol., 42, 463, 10.1007/s10886-016-0712-0 de Torres Zabala, 2015, Chloroplasts play a central role in plant defence and are targeted by pathogen effectors, Nat. Plants, 1, 15074, 10.1038/nplants.2015.74 Bilgin, 2010, Biotic stress globally downregulates photosynthesis genes, Plant Cell Environ., 33, 1597, 10.1111/j.1365-3040.2010.02167.x Su, 2018, Active photosynthetic inhibition mediated by MPK3/MPK6 is critical to effector-triggered immunity, PLoS Biol., 16, 10.1371/journal.pbio.2004122 Kessler, 2004, Silencing the jasmonate cascade: induced plant defenses and insect populations, Science, 305, 665, 10.1126/science.1096931 Pieterse, 2012, Hormonal modulation of plant immunity, Annu. Rev. Cell Dev. Biol., 28, 489, 10.1146/annurev-cellbio-092910-154055 Reymond, 2004, A conserved transcript pattern in response to a specialist and a generalist herbivore, Plant Cell, 16, 3132, 10.1105/tpc.104.026120 Thaler, 2012, Evolution of jasmonate and salicylate signal crosstalk, Trends Plant Sci., 17, 260, 10.1016/j.tplants.2012.02.010 Anderson, 2004, Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis, Plant Cell, 16, 3460, 10.1105/tpc.104.025833 Huffaker, 2013, Plant elicitor peptides are conserved signals regulating direct and indirect antiherbivore defense, Proc. Natl. Acad. Sci. U. S. A., 110, 5707, 10.1073/pnas.1214668110 Huffaker, 2011, ZmPep1, an ortholog of Arabidopsis elicitor peptide 1, regulates maize innate immunity and enhances disease resistance, Plant Physiol., 155, 1325, 10.1104/pp.110.166710 Hou, 2014, The secreted peptide PIP1 amplifies immunity through receptor-like kinase 7, PLoS Pathog., 10, 10.1371/journal.ppat.1004331 Hander, 2019, Damage on plants activates Ca(2+)-dependent metacaspases for release of immunomodulatory peptides, Science, 363, 10.1126/science.aar7486 Lu, 2018, qPrimerDB: a thermodynamics-based gene-specific qPCR primer database for 147 organisms, Nucleic Acids Res., 46, 1229, 10.1093/nar/gkx725