title: Jasmonate-dependent depletion of soluble sugars compromises plant resistance to Manduca sexta.
abstract: Jasmonates regulate plant secondary metabolism and herbivore resistance. How they influence primary metabolites and how this may affect herbivore growth and performance are not well understood. We profiled sugars and starch of jasmonate biosynthesis-deficient and jasmonate-insensitive Nicotiana attenuata plants and manipulated leaf carbohydrates through genetic engineering and in vitro complementation to assess how jasmonate-dependent sugar accumulation affects the growth of Manduca sexta caterpillars. We found that jasmonates reduce the constitutive and herbivore-induced concentration of glucose and fructose in the leaves across different developmental stages. Diurnal, jasmonate-dependent inhibition of invertase activity was identified as a likely mechanism for this phenomenon. Contrary to our expectation, both in planta and in vitro approaches showed that the lower sugar concentrations led to increased M. sexta growth. As a consequence, jasmonate-dependent depletion of sugars rendered N. attenuata plants more susceptible to M. sexta attack. In conclusion, jasmonates are important regulators of leaf carbohydrate accumulation and this determines herbivore growth. Jasmonate-dependent resistance is reduced rather than enhanced through the suppression of glucose and fructose concentrations, which may contribute to the evolution of divergent resistance strategies of plants in nature.
authors.affiliation: Root-Herbivore Interactions Group, Max Planck Institute for Chemical Ecology, Hans-Knöll-Str. 8, 07745, Jena, Germany.|Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Hans-Knöll-Str. 8, 07745, Jena, Germany.
authors.forename: Ricardo A R
authors.initials: RAR
authors.lastname: Machado
authors.affiliation: Root-Herbivore Interactions Group, Max Planck Institute for Chemical Ecology, Hans-Knöll-Str. 8, 07745, Jena, Germany.|Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Hans-Knöll-Str. 8, 07745, Jena, Germany.|Department of Entomology, Universidade Federal de Viçosa, Avenida Peter Henry Rolfs, 36570-000, Viçosa, Brazil.
authors.forename: Carla C M
authors.initials: CCM
authors.lastname: Arce
authors.affiliation: Root-Herbivore Interactions Group, Max Planck Institute for Chemical Ecology, Hans-Knöll-Str. 8, 07745, Jena, Germany.|Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Hans-Knöll-Str. 8, 07745, Jena, Germany.
authors.forename: Abigail P
authors.initials: AP
authors.lastname: Ferrieri
authors.affiliation: Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Hans-Knöll-Str. 8, 07745, Jena, Germany.
authors.forename: Ian T
authors.initials: IT
authors.lastname: Baldwin
authors.affiliation: Root-Herbivore Interactions Group, Max Planck Institute for Chemical Ecology, Hans-Knöll-Str. 8, 07745, Jena, Germany.|Institute of Plant Sciences, University of Bern, Altenbergrain 21, CH-3013, Bern, Switzerland.
authors.forename: Matthias
authors.initials: M
authors.lastname: Erb
mesh_terms: D000818:Animals; D002241:Carbohydrates / Q000172:deficiency*; D002940:Circadian Rhythm; D003517:Cyclopentanes / Q000378:metabolism*; D060467:Disease Resistance; D005632:Fructose / Q000032:analysis; D005838:Genotype; D005947:Glucose / Q000032:analysis; D060434:Herbivory; D018402:Manduca / Q000254:growth & development / Q000502:physiology*; D054883:Oxylipins / Q000378:metabolism*; D010935:Plant Diseases / Q000276:immunology / Q000469:parasitology*; D018515:Plant Leaves / Q000737:chemistry; D010940:Plant Proteins / Q000378:metabolism; D030821:Plants, Genetically Modified; D012273:Ribulose-Bisphosphate Carboxylase / Q000378:metabolism; D064210:Secondary Metabolism; D015398:Signal Transduction; D012995:Solubility; D014026:Nicotiana / Q000235:genetics / Q000276:immunology* / Q000469:parasitology*; D015430:Weight Gain; D043324:beta-Fructofuranosidase / Q000378:metabolism
chemical_list: D002241:Carbohydrates; D003517:Cyclopentanes; D054883:Oxylipins; D010940:Plant Proteins; D005632:Fructose; C011006:jasmonic acid; D043324:beta-Fructofuranosidase; D012273:Ribulose-Bisphosphate Carboxylase; D005947:Glucose
keywords: Manduca sexta; Nicotiana attenuata; carbohydrates; insect nutrition; jasmonates; primary metabolism