title: Ethylene Contributes to maize insect resistance1-Mediated Maize Defense against the Phloem Sap-Sucking Corn Leaf Aphid.
abstract: Signaling networks among multiple phytohormones fine-tune plant defense responses to insect herbivore attack. Previously, it was reported that the synergistic combination of ethylene (ET) and jasmonic acid (JA) was required for accumulation of the maize insect resistance1 (mir1) gene product, a cysteine (Cys) proteinase that is a key defensive protein against chewing insect pests in maize (Zea mays). However, this study suggests that mir1-mediated resistance to corn leaf aphid (CLA; Rhopalosiphum maidis), a phloem sap-sucking insect pest, is independent of JA but regulated by the ET-signaling pathway. Feeding by CLA triggers the rapid accumulation of mir1 transcripts in the resistant maize genotype, Mp708. Furthermore, Mp708 provided elevated levels of antibiosis (limits aphid population)- and antixenosis (deters aphid settling)-mediated resistance to CLA compared with B73 and Tx601 maize susceptible inbred lines. Synthetic diet aphid feeding trial bioassays with recombinant Mir1-Cys Protease demonstrates that Mir1-Cys Protease provides direct toxicity to CLA. Furthermore, foliar feeding by CLA rapidly sends defensive signal(s) to the roots that trigger belowground accumulation of the mir1, signifying a potential role of long-distance signaling in maize defense against the phloem-feeding insects. Collectively, our data indicate that ET-regulated mir1 transcript accumulation, uncoupled from JA, contributed to heightened resistance to CLA in maize. In addition, our results underscore the significance of ET acting as a central node in regulating mir1 expression to different feeding guilds of insect herbivores.
authors.affiliation: Department of Entomology (J.L., S.B., S.V.) and Department of Biochemistry (J.L.), University of Nebraska, Lincoln, Nebraska 68583; Department of Plant Science (L.C.-D., V.J., D.S.L.) and Department of Entomology (G.W.F.), Pennsylvania State University, University Park, Pennsylvania 16802; and United States Department of Agriculture-Agricultural Research Service, Corn Host Plant Resistance Research Unit (W.P.W.), Mississippi State, Mississippi 39762 joelouis@unl.edu.
authors.forename: Joe
authors.identifier: http://orcid.org/0000-0001-7137-8797
authors.initials: J
authors.lastname: Louis
authors.affiliation: Department of Entomology (J.L., S.B., S.V.) and Department of Biochemistry (J.L.), University of Nebraska, Lincoln, Nebraska 68583; Department of Plant Science (L.C.-D., V.J., D.S.L.) and Department of Entomology (G.W.F.), Pennsylvania State University, University Park, Pennsylvania 16802; and United States Department of Agriculture-Agricultural Research Service, Corn Host Plant Resistance Research Unit (W.P.W.), Mississippi State, Mississippi 39762.
authors.forename: Saumik
authors.identifier: http://orcid.org/0000-0002-3904-6984
authors.initials: S
authors.lastname: Basu
authors.affiliation: Department of Entomology (J.L., S.B., S.V.) and Department of Biochemistry (J.L.), University of Nebraska, Lincoln, Nebraska 68583; Department of Plant Science (L.C.-D., V.J., D.S.L.) and Department of Entomology (G.W.F.), Pennsylvania State University, University Park, Pennsylvania 16802; and United States Department of Agriculture-Agricultural Research Service, Corn Host Plant Resistance Research Unit (W.P.W.), Mississippi State, Mississippi 39762.
authors.forename: Suresh
authors.identifier: http://orcid.org/0000-0003-3192-978X
authors.initials: S
authors.lastname: Varsani
authors.affiliation: Department of Entomology (J.L., S.B., S.V.) and Department of Biochemistry (J.L.), University of Nebraska, Lincoln, Nebraska 68583; Department of Plant Science (L.C.-D., V.J., D.S.L.) and Department of Entomology (G.W.F.), Pennsylvania State University, University Park, Pennsylvania 16802; and United States Department of Agriculture-Agricultural Research Service, Corn Host Plant Resistance Research Unit (W.P.W.), Mississippi State, Mississippi 39762.
authors.forename: Lina
authors.initials: L
authors.lastname: Castano-Duque
authors.affiliation: Department of Entomology (J.L., S.B., S.V.) and Department of Biochemistry (J.L.), University of Nebraska, Lincoln, Nebraska 68583; Department of Plant Science (L.C.-D., V.J., D.S.L.) and Department of Entomology (G.W.F.), Pennsylvania State University, University Park, Pennsylvania 16802; and United States Department of Agriculture-Agricultural Research Service, Corn Host Plant Resistance Research Unit (W.P.W.), Mississippi State, Mississippi 39762.
authors.forename: Victoria
authors.identifier: http://orcid.org/0000-0002-3550-5522
authors.initials: V
authors.lastname: Jiang
authors.affiliation: Department of Entomology (J.L., S.B., S.V.) and Department of Biochemistry (J.L.), University of Nebraska, Lincoln, Nebraska 68583; Department of Plant Science (L.C.-D., V.J., D.S.L.) and Department of Entomology (G.W.F.), Pennsylvania State University, University Park, Pennsylvania 16802; and United States Department of Agriculture-Agricultural Research Service, Corn Host Plant Resistance Research Unit (W.P.W.), Mississippi State, Mississippi 39762.
authors.forename: W Paul
authors.identifier: http://orcid.org/0000-0001-9147-3871
authors.initials: WP
authors.lastname: Williams
authors.affiliation: Department of Entomology (J.L., S.B., S.V.) and Department of Biochemistry (J.L.), University of Nebraska, Lincoln, Nebraska 68583; Department of Plant Science (L.C.-D., V.J., D.S.L.) and Department of Entomology (G.W.F.), Pennsylvania State University, University Park, Pennsylvania 16802; and United States Department of Agriculture-Agricultural Research Service, Corn Host Plant Resistance Research Unit (W.P.W.), Mississippi State, Mississippi 39762.
authors.forename: Gary W
authors.initials: GW
authors.lastname: Felton
authors.affiliation: Department of Entomology (J.L., S.B., S.V.) and Department of Biochemistry (J.L.), University of Nebraska, Lincoln, Nebraska 68583; Department of Plant Science (L.C.-D., V.J., D.S.L.) and Department of Entomology (G.W.F.), Pennsylvania State University, University Park, Pennsylvania 16802; and United States Department of Agriculture-Agricultural Research Service, Corn Host Plant Resistance Research Unit (W.P.W.), Mississippi State, Mississippi 39762.
authors.forename: Dawn S
authors.initials: DS
authors.lastname: Luthe
mesh_terms: D000818:Animals; D001042:Aphids / Q000187:drug effects / Q000502:physiology*; D003517:Cyclopentanes / Q000494:pharmacology; D005030:Ethylenes / Q000494:pharmacology*; D018506:Gene Expression Regulation, Plant / Q000187:drug effects; D060434:Herbivory / Q000187:drug effects; D007178:Inbreeding; D008954:Models, Biological; D054883:Oxylipins / Q000494:pharmacology; D052585:Phloem / Q000187:drug effects / Q000469:parasitology*; D053147:Plant Exudates / Q000378:metabolism; D018515:Plant Leaves / Q000187:drug effects / Q000469:parasitology*; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism*; D020156:Salicylic Acid / Q000494:pharmacology; D015398:Signal Transduction / Q000187:drug effects; D003313:Zea mays / Q000187:drug effects / Q000235:genetics / Q000276:immunology* / Q000469:parasitology*
chemical_list: D003517:Cyclopentanes; D005030:Ethylenes; D054883:Oxylipins; D053147:Plant Exudates; D010940:Plant Proteins; C011006:jasmonic acid; C036216:ethylene; D020156:Salicylic Acid