title: Dynamic Precision Phenotyping Reveals Mechanism of Crop Tolerance to Root Herbivory.
abstract: The western corn rootworm (WCR; Diabrotica virgifera virgifera LeConte) is a major pest of maize (Zea mays) that is well adapted to most crop management strategies. Breeding for tolerance is a promising alternative to combat WCR but is currently constrained by a lack of physiological understanding and phenotyping tools. We developed dynamic precision phenotyping approaches using11C with positron emission tomography, root autoradiography, and radiometabolite flux analysis to understand maize tolerance to WCR Our results reveal that WCR attack induces specific patterns of lateral root growth that are associated with a shift in auxin biosynthesis from indole-3-pyruvic acid to indole-3-acetonitrile. WCR attack also increases transport of newly synthesized amino acids to the roots, including the accumulation of Gln. Finally, the regrowth zones of WCR-attacked roots show an increase in Gln turnover, which strongly correlates with the induction of indole-3-acetonitrile-dependent auxin biosynthesis. In summary, our findings identify local changes in the auxin biosynthesis flux network as a promising marker for induced WCR tolerance.
authors.affiliation: Department of Biology, Brookhaven National Laboratory, Upton, New York 11973 (W.Q., Y.X., M.J.S., C.S., D.A., S.J.L., J.S.F., R.A.F.);Biotic Interactions, Institute of Plant Sciences, University of Bern, 3013 Bern, Switzerland (C.A.M.R., M.E.);Plant Genetics Research Unit, United States Department of Agriculture Agricultural Research Service, University of Missouri, Columbia, Missouri 65211 (B.E.H.); andInstitut für Kernchemie, Johannes Gutenberg-Universität, 55128 Mainz, Germany (M.P., T.G., B.R., L.K., A.S.C., A.T.K.).
authors.forename: Wenchao
authors.identifier: 0000-0003-3107-7281
authors.initials: W
authors.lastname: Qu
authors.affiliation: Department of Biology, Brookhaven National Laboratory, Upton, New York 11973 (W.Q., Y.X., M.J.S., C.S., D.A., S.J.L., J.S.F., R.A.F.);Biotic Interactions, Institute of Plant Sciences, University of Bern, 3013 Bern, Switzerland (C.A.M.R., M.E.);Plant Genetics Research Unit, United States Department of Agriculture Agricultural Research Service, University of Missouri, Columbia, Missouri 65211 (B.E.H.); andInstitut für Kernchemie, Johannes Gutenberg-Universität, 55128 Mainz, Germany (M.P., T.G., B.R., L.K., A.S.C., A.T.K.).
authors.forename: Christelle A M
authors.initials: CA
authors.lastname: Robert
authors.affiliation: Department of Biology, Brookhaven National Laboratory, Upton, New York 11973 (W.Q., Y.X., M.J.S., C.S., D.A., S.J.L., J.S.F., R.A.F.);Biotic Interactions, Institute of Plant Sciences, University of Bern, 3013 Bern, Switzerland (C.A.M.R., M.E.);Plant Genetics Research Unit, United States Department of Agriculture Agricultural Research Service, University of Missouri, Columbia, Missouri 65211 (B.E.H.); andInstitut für Kernchemie, Johannes Gutenberg-Universität, 55128 Mainz, Germany (M.P., T.G., B.R., L.K., A.S.C., A.T.K.).
authors.forename: Matthias
authors.initials: M
authors.lastname: Erb
authors.affiliation: Department of Biology, Brookhaven National Laboratory, Upton, New York 11973 (W.Q., Y.X., M.J.S., C.S., D.A., S.J.L., J.S.F., R.A.F.);Biotic Interactions, Institute of Plant Sciences, University of Bern, 3013 Bern, Switzerland (C.A.M.R., M.E.);Plant Genetics Research Unit, United States Department of Agriculture Agricultural Research Service, University of Missouri, Columbia, Missouri 65211 (B.E.H.); andInstitut für Kernchemie, Johannes Gutenberg-Universität, 55128 Mainz, Germany (M.P., T.G., B.R., L.K., A.S.C., A.T.K.).
authors.forename: Bruce E
authors.initials: BE
authors.lastname: Hibbard
authors.affiliation: Department of Biology, Brookhaven National Laboratory, Upton, New York 11973 (W.Q., Y.X., M.J.S., C.S., D.A., S.J.L., J.S.F., R.A.F.);Biotic Interactions, Institute of Plant Sciences, University of Bern, 3013 Bern, Switzerland (C.A.M.R., M.E.);Plant Genetics Research Unit, United States Department of Agriculture Agricultural Research Service, University of Missouri, Columbia, Missouri 65211 (B.E.H.); andInstitut für Kernchemie, Johannes Gutenberg-Universität, 55128 Mainz, Germany (M.P., T.G., B.R., L.K., A.S.C., A.T.K.).
authors.forename: Maxim
authors.initials: M
authors.lastname: Paven
authors.affiliation: Department of Biology, Brookhaven National Laboratory, Upton, New York 11973 (W.Q., Y.X., M.J.S., C.S., D.A., S.J.L., J.S.F., R.A.F.);Biotic Interactions, Institute of Plant Sciences, University of Bern, 3013 Bern, Switzerland (C.A.M.R., M.E.);Plant Genetics Research Unit, United States Department of Agriculture Agricultural Research Service, University of Missouri, Columbia, Missouri 65211 (B.E.H.); andInstitut für Kernchemie, Johannes Gutenberg-Universität, 55128 Mainz, Germany (M.P., T.G., B.R., L.K., A.S.C., A.T.K.).
authors.forename: Tassilo
authors.initials: T
authors.lastname: Gleede
authors.affiliation: Department of Biology, Brookhaven National Laboratory, Upton, New York 11973 (W.Q., Y.X., M.J.S., C.S., D.A., S.J.L., J.S.F., R.A.F.);Biotic Interactions, Institute of Plant Sciences, University of Bern, 3013 Bern, Switzerland (C.A.M.R., M.E.);Plant Genetics Research Unit, United States Department of Agriculture Agricultural Research Service, University of Missouri, Columbia, Missouri 65211 (B.E.H.); andInstitut für Kernchemie, Johannes Gutenberg-Universität, 55128 Mainz, Germany (M.P., T.G., B.R., L.K., A.S.C., A.T.K.).
authors.forename: Barbara
authors.initials: B
authors.lastname: Riehl
authors.affiliation: Department of Biology, Brookhaven National Laboratory, Upton, New York 11973 (W.Q., Y.X., M.J.S., C.S., D.A., S.J.L., J.S.F., R.A.F.);Biotic Interactions, Institute of Plant Sciences, University of Bern, 3013 Bern, Switzerland (C.A.M.R., M.E.);Plant Genetics Research Unit, United States Department of Agriculture Agricultural Research Service, University of Missouri, Columbia, Missouri 65211 (B.E.H.); andInstitut für Kernchemie, Johannes Gutenberg-Universität, 55128 Mainz, Germany (M.P., T.G., B.R., L.K., A.S.C., A.T.K.).
authors.forename: Lena
authors.initials: L
authors.lastname: Kersting
authors.affiliation: Department of Biology, Brookhaven National Laboratory, Upton, New York 11973 (W.Q., Y.X., M.J.S., C.S., D.A., S.J.L., J.S.F., R.A.F.);Biotic Interactions, Institute of Plant Sciences, University of Bern, 3013 Bern, Switzerland (C.A.M.R., M.E.);Plant Genetics Research Unit, United States Department of Agriculture Agricultural Research Service, University of Missouri, Columbia, Missouri 65211 (B.E.H.); andInstitut für Kernchemie, Johannes Gutenberg-Universität, 55128 Mainz, Germany (M.P., T.G., B.R., L.K., A.S.C., A.T.K.).
authors.forename: Aylin S
authors.initials: AS
authors.lastname: Cankaya
authors.affiliation: Department of Biology, Brookhaven National Laboratory, Upton, New York 11973 (W.Q., Y.X., M.J.S., C.S., D.A., S.J.L., J.S.F., R.A.F.);Biotic Interactions, Institute of Plant Sciences, University of Bern, 3013 Bern, Switzerland (C.A.M.R., M.E.);Plant Genetics Research Unit, United States Department of Agriculture Agricultural Research Service, University of Missouri, Columbia, Missouri 65211 (B.E.H.); andInstitut für Kernchemie, Johannes Gutenberg-Universität, 55128 Mainz, Germany (M.P., T.G., B.R., L.K., A.S.C., A.T.K.).
authors.forename: Anna T
authors.initials: AT
authors.lastname: Kunert
authors.affiliation: Department of Biology, Brookhaven National Laboratory, Upton, New York 11973 (W.Q., Y.X., M.J.S., C.S., D.A., S.J.L., J.S.F., R.A.F.);Biotic Interactions, Institute of Plant Sciences, University of Bern, 3013 Bern, Switzerland (C.A.M.R., M.E.);Plant Genetics Research Unit, United States Department of Agriculture Agricultural Research Service, University of Missouri, Columbia, Missouri 65211 (B.E.H.); andInstitut für Kernchemie, Johannes Gutenberg-Universität, 55128 Mainz, Germany (M.P., T.G., B.R., L.K., A.S.C., A.T.K.).
authors.forename: Youwen
authors.initials: Y
authors.lastname: Xu
authors.affiliation: Department of Biology, Brookhaven National Laboratory, Upton, New York 11973 (W.Q., Y.X., M.J.S., C.S., D.A., S.J.L., J.S.F., R.A.F.);Biotic Interactions, Institute of Plant Sciences, University of Bern, 3013 Bern, Switzerland (C.A.M.R., M.E.);Plant Genetics Research Unit, United States Department of Agriculture Agricultural Research Service, University of Missouri, Columbia, Missouri 65211 (B.E.H.); andInstitut für Kernchemie, Johannes Gutenberg-Universität, 55128 Mainz, Germany (M.P., T.G., B.R., L.K., A.S.C., A.T.K.).
authors.forename: Michael J
authors.initials: MJ
authors.lastname: Schueller
authors.affiliation: Department of Biology, Brookhaven National Laboratory, Upton, New York 11973 (W.Q., Y.X., M.J.S., C.S., D.A., S.J.L., J.S.F., R.A.F.);Biotic Interactions, Institute of Plant Sciences, University of Bern, 3013 Bern, Switzerland (C.A.M.R., M.E.);Plant Genetics Research Unit, United States Department of Agriculture Agricultural Research Service, University of Missouri, Columbia, Missouri 65211 (B.E.H.); andInstitut für Kernchemie, Johannes Gutenberg-Universität, 55128 Mainz, Germany (M.P., T.G., B.R., L.K., A.S.C., A.T.K.).
authors.forename: Colleen
authors.identifier: 0000-0003-4608-9592
authors.initials: C
authors.lastname: Shea
authors.affiliation: Department of Biology, Brookhaven National Laboratory, Upton, New York 11973 (W.Q., Y.X., M.J.S., C.S., D.A., S.J.L., J.S.F., R.A.F.);Biotic Interactions, Institute of Plant Sciences, University of Bern, 3013 Bern, Switzerland (C.A.M.R., M.E.);Plant Genetics Research Unit, United States Department of Agriculture Agricultural Research Service, University of Missouri, Columbia, Missouri 65211 (B.E.H.); andInstitut für Kernchemie, Johannes Gutenberg-Universität, 55128 Mainz, Germany (M.P., T.G., B.R., L.K., A.S.C., A.T.K.).
authors.forename: David
authors.initials: D
authors.lastname: Alexoff
authors.affiliation: Department of Biology, Brookhaven National Laboratory, Upton, New York 11973 (W.Q., Y.X., M.J.S., C.S., D.A., S.J.L., J.S.F., R.A.F.);Biotic Interactions, Institute of Plant Sciences, University of Bern, 3013 Bern, Switzerland (C.A.M.R., M.E.);Plant Genetics Research Unit, United States Department of Agriculture Agricultural Research Service, University of Missouri, Columbia, Missouri 65211 (B.E.H.); andInstitut für Kernchemie, Johannes Gutenberg-Universität, 55128 Mainz, Germany (M.P., T.G., B.R., L.K., A.S.C., A.T.K.).
authors.forename: So Jeong
authors.initials: SJ
authors.lastname: Lee
authors.affiliation: Department of Biology, Brookhaven National Laboratory, Upton, New York 11973 (W.Q., Y.X., M.J.S., C.S., D.A., S.J.L., J.S.F., R.A.F.);Biotic Interactions, Institute of Plant Sciences, University of Bern, 3013 Bern, Switzerland (C.A.M.R., M.E.);Plant Genetics Research Unit, United States Department of Agriculture Agricultural Research Service, University of Missouri, Columbia, Missouri 65211 (B.E.H.); andInstitut für Kernchemie, Johannes Gutenberg-Universität, 55128 Mainz, Germany (M.P., T.G., B.R., L.K., A.S.C., A.T.K.).
authors.forename: Joanna S
authors.initials: JS
authors.lastname: Fowler
authors.affiliation: Department of Biology, Brookhaven National Laboratory, Upton, New York 11973 (W.Q., Y.X., M.J.S., C.S., D.A., S.J.L., J.S.F., R.A.F.);Biotic Interactions, Institute of Plant Sciences, University of Bern, 3013 Bern, Switzerland (C.A.M.R., M.E.);Plant Genetics Research Unit, United States Department of Agriculture Agricultural Research Service, University of Missouri, Columbia, Missouri 65211 (B.E.H.); andInstitut für Kernchemie, Johannes Gutenberg-Universität, 55128 Mainz, Germany (M.P., T.G., B.R., L.K., A.S.C., A.T.K.) ferrierir@missouri.edu.
authors.forename: Richard A
authors.identifier: 0000-0002-2604-0014
authors.initials: RA
authors.lastname: Ferrieri
mesh_terms: D000596:Amino Acids / Q000096:biosynthesis; D000818:Animals; D001692:Biological Transport; D002250:Carbon Radioisotopes / Q000378:metabolism; D001517:Coleoptera / Q000502:physiology*; D018556:Crops, Agricultural / Q000235:genetics / Q000378:metabolism / Q000469:parasitology*; D005973:Glutamine / Q000378:metabolism; D060434:Herbivory / Q000502:physiology; D006790:Host-Parasite Interactions; D007210:Indoleacetic Acids / Q000378:metabolism; D007211:Indoles / Q000378:metabolism; D010641:Phenotype; D010935:Plant Diseases / Q000235:genetics / Q000469:parasitology; D018517:Plant Roots / Q000235:genetics / Q000378:metabolism / Q000469:parasitology*; D049268:Positron-Emission Tomography; D003313:Zea mays / Q000235:genetics / Q000378:metabolism / Q000469:parasitology*
chemical_list: D000596:Amino Acids; D002250:Carbon Radioisotopes; D007210:Indoleacetic Acids; D007211:Indoles; D005973:Glutamine; C008122:indol-3-yl pyruvic acid; C016516:indole-3-acetonitrile