<i>O-</i>Acyl Sugars Protect a Wild Tobacco from Both Native Fungal Pathogens and a Specialist Herbivore

Abstract

<i>O</i>-Acyl sugars (<i>O</i>-AS) are abundant trichome-specific metabolites that function as indirect defenses against herbivores of the wild tobacco <i>Nicotiana attenuata</i>; whether they also function as generalized direct defenses against herbivores and pathogens remains unknown. We characterized natural variation in <i>O-</i>AS among 26 accessions and examined their influence on two native fungal pathogens, <i>Fusarium brachygibbosum</i> U4 and <i>Alternaria</i> sp. U10, and the specialist herbivore <i>Manduca sexta</i> At least 15 different <i>O-</i>AS structures belonging to three classes were found in <i>N. attenuata</i> leaves. A 3-fold quantitative variation in total leaf <i>O-</i>AS was found among the natural accessions. Experiments with natural accessions and crosses between high- and low-<i>O-</i>AS accessions revealed that total <i>O-</i>AS levels were associated with resistance against herbivores and pathogens. Removing <i>O-</i>AS from the leaf surface increased <i>M. sexta</i> growth rate and plant fungal susceptibility. <i>O</i>-AS supplementation in artificial diets and germination medium reduced <i>M. sexta</i> growth and fungal spore germination, respectively. Finally, silencing the expression of a putative branched-chain α-ketoacid dehydrogenase E1 β-subunit-encoding gene (<i>NaBCKDE1B</i>) in the trichomes reduced total leaf <i>O-</i>AS by 20% to 30% and increased susceptibility to <i>Fusarium</i> pathogens. We conclude that <i>O-</i>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.