title: Turnabout Is Fair Play: Herbivory-Induced Plant Chitinases Excreted in Fall Armyworm Frass Suppress Herbivore Defenses in Maize.
abstract: The perception of herbivory by plants is known to be triggered by the deposition of insect-derived factors such as saliva and oral secretions, oviposition materials, and even feces. Such insect-derived materials harbor chemical cues that may elicit herbivore and/or pathogen-induced defenses in plants. Several insect-derived molecules that trigger herbivore-induced defenses in plants are known; however, insect-derived molecules suppressing them are largely unknown. In this study, we identified two plant chitinases from fall armyworm (Spodoptera frugiperda) larval frass that suppress herbivore defenses while simultaneously inducing pathogen defenses in maize (Zea mays). Fall armyworm larvae feed in enclosed whorls of maize plants, where frass accumulates over extended periods of time in close proximity to damaged leaf tissue. Our study shows that maize chitinases, Pr4 and Endochitinase A, are induced during herbivory and subsequently deposited on the host with the feces. These plant chitinases mediate the suppression of herbivore-induced defenses, thereby increasing the performance of the insect on the host. Pr4 and Endochitinase A also trigger the antagonistic pathogen defense pathway in maize and suppress fungal pathogen growth on maize leaves. Frass-induced suppression of herbivore defenses by deposition of the plant-derived chitinases Pr4 and Endochitinase A is a unique way an insect can co-opt the plant's defense proteins for its own benefit. It is also a phenomenon unlike the induction of herbivore defenses by insect oral secretions in most host-herbivore systems.
authors.affiliation: Department of Plant Science (S.R., I.G., S.J., Y.H., D.S.L.), Intercollegiate Graduate Program in Plant Biology, Huck Institutes of Life Sciences (S.R., S.J., D.S.L.), and Department of Entomology (F.E.A., M.P., G.W.F.), Pennsylvania State University, University Park, Pennsylvania 16802;Department of Plant Biotechnology, Universidade Federal de Lavras, Lavras 37200, Brazil (P.C.M.S.A.); andDepartment of Biochemistry and Molecular Biology, Quaid-i-azam University, Islamabad 45320, Pakistan (I.A., S.S.).
authors.forename: Swayamjit
authors.identifier: 0000-0002-1001-0785
authors.initials: S
authors.lastname: Ray
authors.affiliation: Department of Plant Science (S.R., I.G., S.J., Y.H., D.S.L.), Intercollegiate Graduate Program in Plant Biology, Huck Institutes of Life Sciences (S.R., S.J., D.S.L.), and Department of Entomology (F.E.A., M.P., G.W.F.), Pennsylvania State University, University Park, Pennsylvania 16802;Department of Plant Biotechnology, Universidade Federal de Lavras, Lavras 37200, Brazil (P.C.M.S.A.); andDepartment of Biochemistry and Molecular Biology, Quaid-i-azam University, Islamabad 45320, Pakistan (I.A., S.S.).
authors.forename: Patrick C M S
authors.initials: PC
authors.lastname: Alves
authors.affiliation: Department of Plant Science (S.R., I.G., S.J., Y.H., D.S.L.), Intercollegiate Graduate Program in Plant Biology, Huck Institutes of Life Sciences (S.R., S.J., D.S.L.), and Department of Entomology (F.E.A., M.P., G.W.F.), Pennsylvania State University, University Park, Pennsylvania 16802;Department of Plant Biotechnology, Universidade Federal de Lavras, Lavras 37200, Brazil (P.C.M.S.A.); andDepartment of Biochemistry and Molecular Biology, Quaid-i-azam University, Islamabad 45320, Pakistan (I.A., S.S.).
authors.forename: Imtiaz
authors.identifier: 0000-0001-9534-5498
authors.initials: I
authors.lastname: Ahmad
authors.affiliation: Department of Plant Science (S.R., I.G., S.J., Y.H., D.S.L.), Intercollegiate Graduate Program in Plant Biology, Huck Institutes of Life Sciences (S.R., S.J., D.S.L.), and Department of Entomology (F.E.A., M.P., G.W.F.), Pennsylvania State University, University Park, Pennsylvania 16802;Department of Plant Biotechnology, Universidade Federal de Lavras, Lavras 37200, Brazil (P.C.M.S.A.); andDepartment of Biochemistry and Molecular Biology, Quaid-i-azam University, Islamabad 45320, Pakistan (I.A., S.S.).
authors.forename: Iffa
authors.initials: I
authors.lastname: Gaffoor
authors.affiliation: Department of Plant Science (S.R., I.G., S.J., Y.H., D.S.L.), Intercollegiate Graduate Program in Plant Biology, Huck Institutes of Life Sciences (S.R., S.J., D.S.L.), and Department of Entomology (F.E.A., M.P., G.W.F.), Pennsylvania State University, University Park, Pennsylvania 16802;Department of Plant Biotechnology, Universidade Federal de Lavras, Lavras 37200, Brazil (P.C.M.S.A.); andDepartment of Biochemistry and Molecular Biology, Quaid-i-azam University, Islamabad 45320, Pakistan (I.A., S.S.).
authors.forename: Flor E
authors.initials: FE
authors.lastname: Acevedo
authors.affiliation: Department of Plant Science (S.R., I.G., S.J., Y.H., D.S.L.), Intercollegiate Graduate Program in Plant Biology, Huck Institutes of Life Sciences (S.R., S.J., D.S.L.), and Department of Entomology (F.E.A., M.P., G.W.F.), Pennsylvania State University, University Park, Pennsylvania 16802;Department of Plant Biotechnology, Universidade Federal de Lavras, Lavras 37200, Brazil (P.C.M.S.A.); andDepartment of Biochemistry and Molecular Biology, Quaid-i-azam University, Islamabad 45320, Pakistan (I.A., S.S.).
authors.forename: Michelle
authors.initials: M
authors.lastname: Peiffer
authors.affiliation: Department of Plant Science (S.R., I.G., S.J., Y.H., D.S.L.), Intercollegiate Graduate Program in Plant Biology, Huck Institutes of Life Sciences (S.R., S.J., D.S.L.), and Department of Entomology (F.E.A., M.P., G.W.F.), Pennsylvania State University, University Park, Pennsylvania 16802;Department of Plant Biotechnology, Universidade Federal de Lavras, Lavras 37200, Brazil (P.C.M.S.A.); andDepartment of Biochemistry and Molecular Biology, Quaid-i-azam University, Islamabad 45320, Pakistan (I.A., S.S.).
authors.forename: Shan
authors.initials: S
authors.lastname: Jin
authors.affiliation: Department of Plant Science (S.R., I.G., S.J., Y.H., D.S.L.), Intercollegiate Graduate Program in Plant Biology, Huck Institutes of Life Sciences (S.R., S.J., D.S.L.), and Department of Entomology (F.E.A., M.P., G.W.F.), Pennsylvania State University, University Park, Pennsylvania 16802;Department of Plant Biotechnology, Universidade Federal de Lavras, Lavras 37200, Brazil (P.C.M.S.A.); andDepartment of Biochemistry and Molecular Biology, Quaid-i-azam University, Islamabad 45320, Pakistan (I.A., S.S.).
authors.forename: Yang
authors.initials: Y
authors.lastname: Han
authors.affiliation: Department of Plant Science (S.R., I.G., S.J., Y.H., D.S.L.), Intercollegiate Graduate Program in Plant Biology, Huck Institutes of Life Sciences (S.R., S.J., D.S.L.), and Department of Entomology (F.E.A., M.P., G.W.F.), Pennsylvania State University, University Park, Pennsylvania 16802;Department of Plant Biotechnology, Universidade Federal de Lavras, Lavras 37200, Brazil (P.C.M.S.A.); andDepartment of Biochemistry and Molecular Biology, Quaid-i-azam University, Islamabad 45320, Pakistan (I.A., S.S.).
authors.forename: Samina
authors.initials: S
authors.lastname: Shakeel
authors.affiliation: Department of Plant Science (S.R., I.G., S.J., Y.H., D.S.L.), Intercollegiate Graduate Program in Plant Biology, Huck Institutes of Life Sciences (S.R., S.J., D.S.L.), and Department of Entomology (F.E.A., M.P., G.W.F.), Pennsylvania State University, University Park, Pennsylvania 16802;Department of Plant Biotechnology, Universidade Federal de Lavras, Lavras 37200, Brazil (P.C.M.S.A.); andDepartment of Biochemistry and Molecular Biology, Quaid-i-azam University, Islamabad 45320, Pakistan (I.A., S.S.).
authors.forename: Gary W
authors.initials: GW
authors.lastname: Felton
authors.affiliation: Department of Plant Science (S.R., I.G., S.J., Y.H., D.S.L.), Intercollegiate Graduate Program in Plant Biology, Huck Institutes of Life Sciences (S.R., S.J., D.S.L.), and Department of Entomology (F.E.A., M.P., G.W.F.), Pennsylvania State University, University Park, Pennsylvania 16802;Department of Plant Biotechnology, Universidade Federal de Lavras, Lavras 37200, Brazil (P.C.M.S.A.); andDepartment of Biochemistry and Molecular Biology, Quaid-i-azam University, Islamabad 45320, Pakistan (I.A., S.S.) dsl14@psu.edu.
authors.forename: Dawn S
authors.identifier: 0000-0002-1978-8825
authors.initials: DS
authors.lastname: Luthe
mesh_terms: D000818:Animals; D001203:Ascomycota / Q000472:pathogenicity; D002686:Chitin / Q000378:metabolism; D002688:Chitinases / Q000235:genetics / Q000378:metabolism*; D005243:Feces / Q000737:chemistry; D005260:Female; D060434:Herbivory; D054884:Host-Pathogen Interactions; D019476:Insect Proteins / Q000378:metabolism; D007814:Larva; D018515:Plant Leaves; D010940:Plant Proteins / Q000378:metabolism*; D040901:Proteomics / Q000379:methods; D018411:Spodoptera / Q000737:chemistry* / Q000254:growth & development; D003313:Zea mays / Q000201:enzymology* / Q000382:microbiology
chemical_list: D019476:Insect Proteins; D010940:Plant Proteins; D002686:Chitin; D002688:Chitinases