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O-acyl sugars protect a wild tobacco from both native fungal pathogens and a specialist herbivore

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Luu,  Van Thi
Department of Molecular Ecology, Prof. I. T. Baldwin, MPI for Chemical Ecology, Max Planck Society;
IMPRS on Ecological Interactions, MPI for Chemical Ecology, Max Planck Society;

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Weinhold,  Alexander
Department of Molecular Ecology, Prof. I. T. Baldwin, MPI for Chemical Ecology, Max Planck Society;

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Ullah,  Chhana
Department of Biochemistry, Prof. J. Gershenzon, MPI for Chemical Ecology, Max Planck Society;
IMPRS on Ecological Interactions, MPI for Chemical Ecology, Max Planck Society;

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Dressel,  Stefanie
Department of Molecular Ecology, Prof. I. T. Baldwin, MPI for Chemical Ecology, Max Planck Society;

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Schoettner,  Matthias
Department of Molecular Ecology, Prof. I. T. Baldwin, MPI for Chemical Ecology, Max Planck Society;

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Gase,  Klaus
Department of Molecular Ecology, Prof. I. T. Baldwin, MPI for Chemical Ecology, Max Planck Society;

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Gaquerel,  Emmanuel
Department of Molecular Ecology, Prof. I. T. Baldwin, MPI for Chemical Ecology, Max Planck Society;

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Xu,  Shuqing
Department of Molecular Ecology, Prof. I. T. Baldwin, MPI for Chemical Ecology, Max Planck Society;

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Baldwin,  Ian Thomas
Department of Molecular Ecology, Prof. I. T. Baldwin, MPI for Chemical Ecology, Max Planck Society;

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Citation

Luu, V. T., Weinhold, A., Ullah, C., Dressel, S., Schoettner, M., Gase, K., et al. (2017). O-acyl sugars protect a wild tobacco from both native fungal pathogens and a specialist herbivore. Plant Physiology, 174, 370-386. doi:10.1104/pp.16.01904.


Cite as: http://hdl.handle.net/11858/00-001M-0000-002C-A120-B
Abstract
O-acyl sugars (O-AS) are abundant trichome-specific metabolites that function as indirect defenses against herbivores of the wild tobacco Nicotiana attenuata; whether they also function as generalized direct defenses against herbivores and pathogens remains unknown. We characterized natural variation in O-AS among 26 accessions and examined their influence on two native fungal pathogens, Fusarium brachygibbosum U4 and Alternaria sp. U10, and the specialist herbivore, Manduca sexta. At least 15 different O-AS structures belonging to three classes were found in N. attenuata leaves. A three-fold quantitative variation in total leaf O-AS was found among the natural accessions. Experiments with natural accessions and crosses between high- and low-O-AS accessions revealed that total O-AS levels were associated with resistance against herbivores and pathogens. Removing O-AS from the leaf surface increased M. sexta growth rate and plant fungal susceptibility. O-AS supplementation in artificial diets and germination medium reduced M. sexta growth and fungal spore germination, respectively. Finally, silencing the expression of a putative branched-chain alpha-ketoacid dehydrogenase E1 beta subunit encoding gene (NaBCKDE1B) in the trichomes reduced total leaf O-AS by 20-30% and increased susceptibility to Fusarium pathogens. We conclude that O-AS function as direct defenses to protect plants from attack from both native pathogenic fungi and a specialist herbivore, and infer that their diversification is likely shaped by the functional interactions among these biotic stresses.