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Acylsugars protect Nicotiana benthamiana against insect herbivory and desiccation

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Abstract

Key message

Nicotiana benthamiana acylsugar acyltransferase (ASAT) is required for protection against desiccation and insect herbivory. Knockout mutations provide a new resource for investigation of plant-aphid and plant-whitefly interactions.

Abstract

Nicotiana benthamiana is used extensively as a transient expression platform for functional analysis of genes from other species. Acylsugars, which are produced in the trichomes, are a hypothesized cause of the relatively high insect resistance that is observed in N. benthamiana. We characterized the N. benthamiana acylsugar profile, bioinformatically identified two acylsugar acyltransferase genes, ASAT1 and ASAT2, and used CRISPR/Cas9 mutagenesis to produce acylsugar-deficient plants for investigation of insect resistance and foliar water loss. Whereas asat1 mutations reduced accumulation, asat2 mutations caused almost complete depletion of foliar acylsucroses. Three hemipteran and three lepidopteran herbivores survived, gained weight, and/or reproduced significantly better on asat2 mutants than on wildtype N. benthamiana. Both asat1 and asat2 mutations reduced the water content and increased leaf temperature. Our results demonstrate the specific function of two ASAT proteins in N. benthamiana acylsugar biosynthesis, insect resistance, and desiccation tolerance. The improved growth of aphids and whiteflies on asat2 mutants will facilitate the use of N. benthamiana as a transient expression platform for the functional analysis of insect effectors and resistance genes from other plant species. Similarly, the absence of acylsugars in asat2 mutants will enable analysis of acylsugar biosynthesis genes from other Solanaceae by transient expression.

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All data generated or analyzed during this study are included in this published article and its supplementary information files.

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Acknowledgements

We thank Patricia Keen and Joyce Van Eck for their help with N. benthamiana stable transformation, Ning Zhang and Greg Martin for sharing the p201N-Cas9 construct and the Drm3 sgRNA control constructs, and William Stone and Thomas Lawton for providing custom image processing software.

Funding

This research was supported by Cornell startup funds to G.D.M., Deutsche Forschungsgemeinschaft award #411255989 to L.H.K., and United States Department of Agriculture Biotechnology Risk Assessment Grant 2017-33522-27006, US National Science Foundation award IOS-1645256, and Defense Advanced Research Projects Agency (DARPA) agreement HR0011-17-2-0053 to G.J, and US National Science Foundation award #1723926 to C.L.C. G.S. is part of a team supporting DARPA’s Insect Allies program under agreement HR0011-17-2-0055. M.A.G. is part of a team supporting DARPA’s Advanced Plant Technologies program under agreement HR0011-18-C-0146. The views and conclusions contained in this document are those of the authors and should not be interpreted as representing the official policies of the U.S. Government.

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Author notes

  1. Lars H. Kruse

    Present address: Michael Smith Laboratories, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada

  2. Jake D. Tracy

    Present address: Department of Plant Sciences and Plant Pathology, Montana State University, Bozeman, MT, 59717, USA

  3. Sara Shakir

    Present address: Gembloux Agro-Bio Tech Institute, The University of Liege, Gembloux, Belgium

  4. Hongxing Xu

    Present address: College of Life Science, The Shaanxi Normal University, Xi’an, China

  5. Alba Ruth Nava Fereira & Garry Sunter

    Present address: Department of Biological Sciences, Northern Illinois University, Dekalb, IL, 60115, USA

Authors and Affiliations

  1. Boyce Thompson Institute, Ithaca, NY, 14853, USA

    Honglin Feng, Seung Ho Chung, Sara Shakir, Hongxing Xu & Georg Jander

  2. Plant Breeding and Genetics Section, School of Integrative Plant Science, Cornell University, Ithaca, NY, 14853, USA

    Lucia Acosta-Gamboa & Michael A. Gore

  3. Plant Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY, 14853, USA

    Lars H. Kruse & Gaurav D. Moghe

  4. Plant-Microbe Biology and Plant Pathology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY, 14853, USA

    Jake D. Tracy & Clare L. Casteel

  5. Department of Biology, University of Texas San Antonio, San Antonio, TX, 78249, USA

    Alba Ruth Nava Fereira & Garry Sunter

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Contributions

GJ and HF conceived the original research plans; HF, SS, LA, HX, LK, JDT, SHC, and ANF performed the experiments; HF, LA, LK, and GDM analyzed the data; CLC, MAG, GDM, GS, and GJ supervised the experiments; HF and GJ wrote the article with contributions from all of the authors; GJ agrees to serve as the contact author responsible for communication and distribution of samples.

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Correspondence to Georg Jander.

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Feng, H., Acosta-Gamboa, L., Kruse, L.H. et al. Acylsugars protect Nicotiana benthamiana against insect herbivory and desiccation. Plant Mol Biol 109, 505–522 (2022). https://doi.org/10.1007/s11103-021-01191-3

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