title: Dynamic Maize Responses to Aphid Feeding Are Revealed by a Time Series of Transcriptomic and Metabolomic Assays.
abstract: As a response to insect attack, maize (Zea mays) has inducible defenses that involve large changes in gene expression and metabolism. Piercing/sucking insects such as corn leaf aphid (Rhopalosiphum maidis) cause direct damage by acquiring phloem nutrients as well as indirect damage through the transmission of plant viruses. To elucidate the metabolic processes and gene expression changes involved in maize responses to aphid attack, leaves of inbred line B73 were infested with corn leaf aphids for 2 to 96 h. Analysis of infested maize leaves showed two distinct response phases, with the most significant transcriptional and metabolic changes occurring in the first few hours after the initiation of aphid feeding. After 4 d, both gene expression and metabolite profiles of aphid-infested maize reverted to being more similar to those of control plants. Although there was a predominant effect of salicylic acid regulation, gene expression changes also indicated prolonged induction of oxylipins, although not necessarily jasmonic acid, in aphid-infested maize. The role of specific metabolic pathways was confirmed using Dissociator transposon insertions in maize inbred line W22. Mutations in three benzoxazinoid biosynthesis genes, Bx1, Bx2, and Bx6, increased aphid reproduction. In contrast, progeny production was greatly decreased by a transposon insertion in the single W22 homolog of the previously uncharacterized B73 terpene synthases TPS2 and TPS3. Together, these results show that maize leaves shift to implementation of physical and chemical defenses within hours after the initiation of aphid feeding and that the production of specific metabolites can have major effects in maize-aphid interactions.
authors.affiliation: Boyce Thompson Institute for Plant Research, Ithaca, New York 14853 (V.T., N.F.-P., K.R.A., L.N.M., H.K., L.A.M., G.J.);Martin Luther University Halle, Wittenberg Institute for Pharmacy, D-06108 Halle, Germany (A.R., J.D.);Division of Biological Sciences, University of California, La Jolla, California 92093 (E.A.S., A.H.);Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany (M.Scho., M.Schä.); andGraduate School of Agriculture, Kyoto University, Kyoto 808-8502, Japan (N.M.).
authors.forename: Vered
authors.identifier: http://orcid.org/0000-0002-5912-779X
authors.initials: V
authors.lastname: Tzin
authors.affiliation: Boyce Thompson Institute for Plant Research, Ithaca, New York 14853 (V.T., N.F.-P., K.R.A., L.N.M., H.K., L.A.M., G.J.);Martin Luther University Halle, Wittenberg Institute for Pharmacy, D-06108 Halle, Germany (A.R., J.D.);Division of Biological Sciences, University of California, La Jolla, California 92093 (E.A.S., A.H.);Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany (M.Scho., M.Schä.); andGraduate School of Agriculture, Kyoto University, Kyoto 808-8502, Japan (N.M.).
authors.forename: Noe
authors.initials: N
authors.lastname: Fernandez-Pozo
authors.affiliation: Boyce Thompson Institute for Plant Research, Ithaca, New York 14853 (V.T., N.F.-P., K.R.A., L.N.M., H.K., L.A.M., G.J.);Martin Luther University Halle, Wittenberg Institute for Pharmacy, D-06108 Halle, Germany (A.R., J.D.);Division of Biological Sciences, University of California, La Jolla, California 92093 (E.A.S., A.H.);Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany (M.Scho., M.Schä.); andGraduate School of Agriculture, Kyoto University, Kyoto 808-8502, Japan (N.M.).
authors.forename: Annett
authors.initials: A
authors.lastname: Richter
authors.affiliation: Boyce Thompson Institute for Plant Research, Ithaca, New York 14853 (V.T., N.F.-P., K.R.A., L.N.M., H.K., L.A.M., G.J.);Martin Luther University Halle, Wittenberg Institute for Pharmacy, D-06108 Halle, Germany (A.R., J.D.);Division of Biological Sciences, University of California, La Jolla, California 92093 (E.A.S., A.H.);Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany (M.Scho., M.Schä.); andGraduate School of Agriculture, Kyoto University, Kyoto 808-8502, Japan (N.M.).
authors.forename: Eric A
authors.identifier: http://orcid.org/0000-0002-2837-734X
authors.initials: EA
authors.lastname: Schmelz
authors.affiliation: Boyce Thompson Institute for Plant Research, Ithaca, New York 14853 (V.T., N.F.-P., K.R.A., L.N.M., H.K., L.A.M., G.J.);Martin Luther University Halle, Wittenberg Institute for Pharmacy, D-06108 Halle, Germany (A.R., J.D.);Division of Biological Sciences, University of California, La Jolla, California 92093 (E.A.S., A.H.);Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany (M.Scho., M.Schä.); andGraduate School of Agriculture, Kyoto University, Kyoto 808-8502, Japan (N.M.).
authors.forename: Matthias
authors.initials: M
authors.lastname: Schoettner
authors.affiliation: Boyce Thompson Institute for Plant Research, Ithaca, New York 14853 (V.T., N.F.-P., K.R.A., L.N.M., H.K., L.A.M., G.J.);Martin Luther University Halle, Wittenberg Institute for Pharmacy, D-06108 Halle, Germany (A.R., J.D.);Division of Biological Sciences, University of California, La Jolla, California 92093 (E.A.S., A.H.);Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany (M.Scho., M.Schä.); andGraduate School of Agriculture, Kyoto University, Kyoto 808-8502, Japan (N.M.).
authors.forename: Martin
authors.initials: M
authors.lastname: Schäfer
authors.affiliation: Boyce Thompson Institute for Plant Research, Ithaca, New York 14853 (V.T., N.F.-P., K.R.A., L.N.M., H.K., L.A.M., G.J.);Martin Luther University Halle, Wittenberg Institute for Pharmacy, D-06108 Halle, Germany (A.R., J.D.);Division of Biological Sciences, University of California, La Jolla, California 92093 (E.A.S., A.H.);Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany (M.Scho., M.Schä.); andGraduate School of Agriculture, Kyoto University, Kyoto 808-8502, Japan (N.M.).
authors.forename: Kevin R
authors.initials: KR
authors.lastname: Ahern
authors.affiliation: Boyce Thompson Institute for Plant Research, Ithaca, New York 14853 (V.T., N.F.-P., K.R.A., L.N.M., H.K., L.A.M., G.J.);Martin Luther University Halle, Wittenberg Institute for Pharmacy, D-06108 Halle, Germany (A.R., J.D.);Division of Biological Sciences, University of California, La Jolla, California 92093 (E.A.S., A.H.);Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany (M.Scho., M.Schä.); andGraduate School of Agriculture, Kyoto University, Kyoto 808-8502, Japan (N.M.).
authors.forename: Lisa N
authors.initials: LN
authors.lastname: Meihls
authors.affiliation: Boyce Thompson Institute for Plant Research, Ithaca, New York 14853 (V.T., N.F.-P., K.R.A., L.N.M., H.K., L.A.M., G.J.);Martin Luther University Halle, Wittenberg Institute for Pharmacy, D-06108 Halle, Germany (A.R., J.D.);Division of Biological Sciences, University of California, La Jolla, California 92093 (E.A.S., A.H.);Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany (M.Scho., M.Schä.); andGraduate School of Agriculture, Kyoto University, Kyoto 808-8502, Japan (N.M.).
authors.forename: Harleen
authors.identifier: http://orcid.org/0000-0003-1367-6619
authors.initials: H
authors.lastname: Kaur
authors.affiliation: Boyce Thompson Institute for Plant Research, Ithaca, New York 14853 (V.T., N.F.-P., K.R.A., L.N.M., H.K., L.A.M., G.J.);Martin Luther University Halle, Wittenberg Institute for Pharmacy, D-06108 Halle, Germany (A.R., J.D.);Division of Biological Sciences, University of California, La Jolla, California 92093 (E.A.S., A.H.);Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany (M.Scho., M.Schä.); andGraduate School of Agriculture, Kyoto University, Kyoto 808-8502, Japan (N.M.).
authors.forename: Alisa
authors.identifier: http://orcid.org/0000-0002-3886-8433
authors.initials: A
authors.lastname: Huffaker
authors.affiliation: Boyce Thompson Institute for Plant Research, Ithaca, New York 14853 (V.T., N.F.-P., K.R.A., L.N.M., H.K., L.A.M., G.J.);Martin Luther University Halle, Wittenberg Institute for Pharmacy, D-06108 Halle, Germany (A.R., J.D.);Division of Biological Sciences, University of California, La Jolla, California 92093 (E.A.S., A.H.);Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany (M.Scho., M.Schä.); andGraduate School of Agriculture, Kyoto University, Kyoto 808-8502, Japan (N.M.).
authors.forename: Naoki
authors.initials: N
authors.lastname: Mori
authors.affiliation: Boyce Thompson Institute for Plant Research, Ithaca, New York 14853 (V.T., N.F.-P., K.R.A., L.N.M., H.K., L.A.M., G.J.);Martin Luther University Halle, Wittenberg Institute for Pharmacy, D-06108 Halle, Germany (A.R., J.D.);Division of Biological Sciences, University of California, La Jolla, California 92093 (E.A.S., A.H.);Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany (M.Scho., M.Schä.); andGraduate School of Agriculture, Kyoto University, Kyoto 808-8502, Japan (N.M.).
authors.forename: Joerg
authors.initials: J
authors.lastname: Degenhardt
authors.affiliation: Boyce Thompson Institute for Plant Research, Ithaca, New York 14853 (V.T., N.F.-P., K.R.A., L.N.M., H.K., L.A.M., G.J.);Martin Luther University Halle, Wittenberg Institute for Pharmacy, D-06108 Halle, Germany (A.R., J.D.);Division of Biological Sciences, University of California, La Jolla, California 92093 (E.A.S., A.H.);Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany (M.Scho., M.Schä.); andGraduate School of Agriculture, Kyoto University, Kyoto 808-8502, Japan (N.M.).
authors.forename: Lukas A
authors.initials: LA
authors.lastname: Mueller
authors.affiliation: Boyce Thompson Institute for Plant Research, Ithaca, New York 14853 (V.T., N.F.-P., K.R.A., L.N.M., H.K., L.A.M., G.J.);Martin Luther University Halle, Wittenberg Institute for Pharmacy, D-06108 Halle, Germany (A.R., J.D.);Division of Biological Sciences, University of California, La Jolla, California 92093 (E.A.S., A.H.);Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany (M.Scho., M.Schä.); andGraduate School of Agriculture, Kyoto University, Kyoto 808-8502, Japan (N.M.) gj32@cornell.edu.
authors.forename: Georg
authors.identifier: http://orcid.org/0000-0002-9675-934X
authors.initials: G
authors.lastname: Jander
mesh_terms: D000818:Animals; D001042:Aphids / Q000502:physiology*; D048588:Benzoxazines / Q000378:metabolism; D003517:Cyclopentanes / Q000378:metabolism; D004251:DNA Transposable Elements; D020869:Gene Expression Profiling; D018506:Gene Expression Regulation, Plant; D006790:Host-Parasite Interactions; D055432:Metabolomics; D009154:Mutation; D054883:Oxylipins / Q000378:metabolism; D052585:Phloem / Q000235:genetics / Q000276:immunology / Q000378:metabolism; D010935:Plant Diseases / Q000276:immunology*; D010937:Plant Growth Regulators / Q000378:metabolism*; D018515:Plant Leaves / Q000235:genetics / Q000276:immunology / Q000378:metabolism; D020156:Salicylic Acid / Q000378:metabolism; D013997:Time Factors; D003313:Zea mays / Q000235:genetics* / Q000276:immunology / Q000378:metabolism
chemical_list: D048588:Benzoxazines; D003517:Cyclopentanes; D004251:DNA Transposable Elements; D054883:Oxylipins; D010937:Plant Growth Regulators; C011006:jasmonic acid; D020156:Salicylic Acid