title: O-Acyl Sugars Protect a Wild Tobacco from Both Native Fungal Pathogens and a Specialist Herbivore.
abstract: O-Acyl sugars (O-AS) are abundant trichome-specific metabolites that function as indirect defenses against herbivores of the wild tobaccoNicotiana attenuata; whether they also function as generalized direct defenses against herbivores and pathogens remains unknown. We characterized natural variation inO-AS among 26 accessions and examined their influence on two native fungal pathogens,Fusarium brachygibbosumU4 andAlternariasp. U10, and the specialist herbivoreManduca sextaAt least 15 differentO-AS structures belonging to three classes were found inN. attenuataleaves. A 3-fold quantitative variation in total leafO-AS was found among the natural accessions. Experiments with natural accessions and crosses between high- and low-O-AS accessions revealed that totalO-AS levels were associated with resistance against herbivores and pathogens. RemovingO-AS from the leaf surface increasedM. sextagrowth rate and plant fungal susceptibility.O-AS supplementation in artificial diets and germination medium reducedM. sextagrowth and fungal spore germination, respectively. Finally, silencing the expression of a putative branched-chain α-ketoacid dehydrogenase E1 β-subunit-encoding gene (NaBCKDE1B) in the trichomes reduced total leafO-AS by 20% to 30% and increased susceptibility toFusariumpathogens. We conclude thatO-AS function as direct defenses to protect plants from attack by both native pathogenic fungi and a specialist herbivore and infer that their diversification is likely shaped by the functional interactions among these biotic stresses.
authors.affiliation: Department of Molecular Ecology (V.T.L., S.D., M.S., K.G., S.X., I.T.B.) and Department of Biochemistry (C.U.), Max Planck Institute for Chemical Ecology, Jena 07745, Germany.|Department of Molecular Interaction Ecology, German Centre for Integrative Biodiversity Research, Leipzig 04103, Germany (A.W); and.|Centre for Organismal Studies, University of Heidelberg, Heidelberg 69120, Germany (E.G.).
authors.forename: Van Thi
authors.identifier: http://orcid.org/0000-0002-0709-2783
authors.initials: VT
authors.lastname: Luu
authors.affiliation: Department of Molecular Ecology (V.T.L., S.D., M.S., K.G., S.X., I.T.B.) and Department of Biochemistry (C.U.), Max Planck Institute for Chemical Ecology, Jena 07745, Germany.|Department of Molecular Interaction Ecology, German Centre for Integrative Biodiversity Research, Leipzig 04103, Germany (A.W); and.|Centre for Organismal Studies, University of Heidelberg, Heidelberg 69120, Germany (E.G.).
authors.forename: Alexander
authors.initials: A
authors.lastname: Weinhold
authors.affiliation: Department of Molecular Ecology (V.T.L., S.D., M.S., K.G., S.X., I.T.B.) and Department of Biochemistry (C.U.), Max Planck Institute for Chemical Ecology, Jena 07745, Germany.|Department of Molecular Interaction Ecology, German Centre for Integrative Biodiversity Research, Leipzig 04103, Germany (A.W); and.|Centre for Organismal Studies, University of Heidelberg, Heidelberg 69120, Germany (E.G.).
authors.forename: Chhana
authors.identifier: http://orcid.org/0000-0002-8898-669X
authors.initials: C
authors.lastname: Ullah
authors.affiliation: Department of Molecular Ecology (V.T.L., S.D., M.S., K.G., S.X., I.T.B.) and Department of Biochemistry (C.U.), Max Planck Institute for Chemical Ecology, Jena 07745, Germany.|Department of Molecular Interaction Ecology, German Centre for Integrative Biodiversity Research, Leipzig 04103, Germany (A.W); and.|Centre for Organismal Studies, University of Heidelberg, Heidelberg 69120, Germany (E.G.).
authors.forename: Stefanie
authors.initials: S
authors.lastname: Dressel
authors.affiliation: Department of Molecular Ecology (V.T.L., S.D., M.S., K.G., S.X., I.T.B.) and Department of Biochemistry (C.U.), Max Planck Institute for Chemical Ecology, Jena 07745, Germany.|Department of Molecular Interaction Ecology, German Centre for Integrative Biodiversity Research, Leipzig 04103, Germany (A.W); and.|Centre for Organismal Studies, University of Heidelberg, Heidelberg 69120, Germany (E.G.).
authors.forename: Matthias
authors.identifier: http://orcid.org/0000-0001-7483-4567
authors.initials: M
authors.lastname: Schoettner
authors.affiliation: Department of Molecular Ecology (V.T.L., S.D., M.S., K.G., S.X., I.T.B.) and Department of Biochemistry (C.U.), Max Planck Institute for Chemical Ecology, Jena 07745, Germany.|Department of Molecular Interaction Ecology, German Centre for Integrative Biodiversity Research, Leipzig 04103, Germany (A.W); and.|Centre for Organismal Studies, University of Heidelberg, Heidelberg 69120, Germany (E.G.).
authors.forename: Klaus
authors.initials: K
authors.lastname: Gase
authors.affiliation: Department of Molecular Ecology (V.T.L., S.D., M.S., K.G., S.X., I.T.B.) and Department of Biochemistry (C.U.), Max Planck Institute for Chemical Ecology, Jena 07745, Germany.|Department of Molecular Interaction Ecology, German Centre for Integrative Biodiversity Research, Leipzig 04103, Germany (A.W); and.|Centre for Organismal Studies, University of Heidelberg, Heidelberg 69120, Germany (E.G.).
authors.forename: Emmanuel
authors.identifier: http://orcid.org/0000-0003-0796-6417
authors.initials: E
authors.lastname: Gaquerel
authors.affiliation: Department of Molecular Ecology (V.T.L., S.D., M.S., K.G., S.X., I.T.B.) and Department of Biochemistry (C.U.), Max Planck Institute for Chemical Ecology, Jena 07745, Germany.|Department of Molecular Interaction Ecology, German Centre for Integrative Biodiversity Research, Leipzig 04103, Germany (A.W); and.|Centre for Organismal Studies, University of Heidelberg, Heidelberg 69120, Germany (E.G.).
authors.forename: Shuqing
authors.identifier: http://orcid.org/0000-0001-7010-4604
authors.initials: S
authors.lastname: Xu
authors.affiliation: Department of Molecular Ecology (V.T.L., S.D., M.S., K.G., S.X., I.T.B.) and Department of Biochemistry (C.U.), Max Planck Institute for Chemical Ecology, Jena 07745, Germany; baldwin@ice.mpg.de.|Department of Molecular Interaction Ecology, German Centre for Integrative Biodiversity Research, Leipzig 04103, Germany (A.W); and baldwin@ice.mpg.de.|Centre for Organismal Studies, University of Heidelberg, Heidelberg 69120, Germany (E.G.) baldwin@ice.mpg.de.
authors.forename: Ian T
authors.identifier: http://orcid.org/0000-0001-5371-2974
authors.initials: IT
authors.lastname: Baldwin
mesh_terms: D042942:3-Methyl-2-Oxobutanoate Dehydrogenase (Lipoamide) / Q000235:genetics / Q000378:metabolism; D000215:Acylation; D000528:Alternaria / Q000502:physiology; D000818:Animals; D060467:Disease Resistance; D005670:Fusarium / Q000502:physiology; D020868:Gene Silencing; D060434:Herbivory / Q000502:physiology; D018402:Manduca / Q000502:physiology; D015394:Molecular Structure; D010935:Plant Diseases / Q000235:genetics / Q000382:microbiology / Q000469:parasitology; D018515:Plant Leaves / Q000737:chemistry* / Q000382:microbiology / Q000469:parasitology; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism; D021122:Protein Subunits / Q000235:genetics / Q000378:metabolism; D000073893:Sugars / Q000737:chemistry*; D014026:Nicotiana / Q000737:chemistry* / Q000382:microbiology / Q000469:parasitology; D064201:Trichomes / Q000235:genetics / Q000382:microbiology / Q000469:parasitology
chemical_list: D010940:Plant Proteins; D021122:Protein Subunits; D000073893:Sugars; D042942:3-Methyl-2-Oxobutanoate Dehydrogenase (Lipoamide)