Skip to main content

Acylsugars protect Nicotiana benthamiana against insect herbivory and desiccation

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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Data availability

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

References

  1. Arntzen C (2015) Plant-made pharmaceuticals: from ‘Edible Vaccines’ to Ebola therapeutics. Plant Biotechnol J 13:1013–1016

    PubMed  PubMed Central  Article  Google Scholar 

  2. Arrendale RF, Severson RF, Sisson VA, Costello CE, Leary JA, Himmelsbach DS, Vanhalbeek H (1990) Characterization of the sucrose ester fraction from Nicotiana glutinosa. J Agric Food Chem 38:75–85

    CAS  Article  Google Scholar 

  3. Bally J, Jung H, Mortimer C, Naim F, Philips JG, Hellens R, Bombarely A, Goodin MM, Waterhouse PM (2018) The rise and rise of Nicotiana benthamiana: a plant for all reasons. Ann Rev Phytopathol 56 56:405–426

    Article  CAS  Google Scholar 

  4. Bertani G (1951) Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol 62:293–300

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  5. Bombarely A, Rosli HG, Vrebalov J, Moffett P, Mueller LA, Martin GB (2012) A draft genome sequence of Nicotiana benthamiana to enhance molecular plant-microbe biology research. Mol Plant-Micr Int 25:1523–1530

    CAS  Article  Google Scholar 

  6. Bos JI, Prince D, Pitino M, Maffei ME, Win J, Hogenhout SA (2010) A functional genomics approach identifies candidate effectors from the aphid species Myzus persicae (green peach aphid). PLoS Genet 6:e1001216

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  7. Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  8. Cardoso MZ (2008) Herbivore handling of a plant’s trichome: The case of Heliconius charithonia (L.) (Lepidoptera: Nymphalidae) and Passiflora Lobata (Killip) Hutch. (Passifloraceae). Neotropical Entomol 37:247–252

    Article  Google Scholar 

  9. Casteel CL, Yang C, Nanduri AC, De Jong HN, Whitham SA, Jander G (2014) The NIa-Pro protein of turnip mosaic virus improves growth and reproduction of the aphid vector, Myzus persicae (green peach aphid). Plant J 77: 653–663

    CAS  PubMed  Article  Google Scholar 

  10. Chortyk OT, Pomonis JG, Johnson AW (1996) Syntheses and characterizations of insecticidal sucrose esters. J Ag Food Chem 44:1551–1557

    CAS  Article  Google Scholar 

  11. Chortyk OT, Severson RF, Cutler HC, Sisson VA (1993) Antibiotic activities of sugar esters isolated from selected Nicotiana species. Biosci Biotechnol Biochem 57:1355–1356

    CAS  PubMed  Article  Google Scholar 

  12. Clay N, Adio A, Denoux C, Jander G, Ausubel F (2009) Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323:95–101

    CAS  PubMed  Article  Google Scholar 

  13. D’Auria JC (2006) Acyltransferases in plants: a good time to be BAHD. Curr Opin Plant Biol 9: 331–340

  14. Egan AN, Moore S, Stellari GM, Kang BC, Jahn MM (2019) Tandem gene duplication and recombination at the AT3 locus in the Solanaceae, a gene essential for capsaicinoid biosynthesis in Capsicum. Plos One 14:e0210510

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  15. Egea I, Albaladejo I, Meco V, Morales B, Sevilla A, Bolarin MC, Flores FB (2018) The drought-tolerant Solanum pennellii regulates leaf water loss and induces genes involved in amino acid and ethylene/jasmonate metabolism under dehydration. Sci Rep 8:2791

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  16. Ellison EE, Nagalakshmi U, Gamo ME, Huang PJ, Dinesh-Kumar S, Voytas DF (2020) Multiplexed heritable gene editing using RNA viruses and mobile single guide RNAs. Nat Plants 6:620–624

    CAS  PubMed  Article  Google Scholar 

  17. Elzinga DA, De Vos M, Jander G (2014) Suppression of plant defenses by a Myzus persicae (green peach aphid) salivary effector protein. Mol Plant Microbe Interact 27: 747–756

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  18. Fan P, Leong BJ, Last RL (2019) Tip of the trichome: evolution of acylsugar metabolic diversity in Solanaceae. Curr Opin Plant Biol 49:8–16

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  19. Fan P, Miller AM, Schilmiller AL, Liu X, Ofner I, Jones AD, Zamir D, Last RL (2016) In vitro reconstruction and analysis of evolutionary variation of the tomato acylsucrose metabolic network. Proc Natl Acad Sci USA 113:E239–E248

    CAS  PubMed  Article  Google Scholar 

  20. Feng H, Jander G (2021) Rapid screening of emopenMyzus persicaeemclose (green peach aphid) RNAi targets using emopenTobacco rattle virusemclose. Methods Mol Biol 2360:105–117

    Google Scholar 

  21. Fobes JF, Mudd JB, Marsden MP (1985) Epicuticular lipid accumulation on the leaves of Lycopersicon pennellii (Corr.) D’Arcy and Lycopersicon esculentum Mill. Plant Physiol 77:567–570

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  22. Gaquerel E, Kotkar H, Onkokesung N, Galis I, Baldwin IT (2013) Silencing an N-acyltransferase-like involved in lignin biosynthesis in Nicotiana attenuata dramatically alters herbivory-induced phenolamide metabolism. Plos One 8:e62336

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  23. Gitelson A, Merzlyak MN (1994) Spectral reflectance changes associated with autumn senescence of Aesculus hippocastanum L. and Acer platanoides L. leaves - spectral features and relation to chlorophyll estimation. J Plant Physiol 143:286–292

    CAS  Article  Google Scholar 

  24. Glas JJ, Schimmel BCJ, Alba JM, Escobar-Bravo R, Schuurink RC, Kant MR (2012) Plant glandular trichomes as targets for breeding or engineering of resistance to herbivores. Int J Mol Sci 13:17077–17103

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  25. Gong P, Zhang J, Li H, Yang C, Zhang C, Zhang X, Khurram Z, Zhang Y, Wang T, Fei Z, Ye Z (2010) Transcriptional profiles of drought-responsive genes in modulating transcription signal transduction, and biochemical pathways in tomato. J Exp Bot 61:3563–3575

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  26. Goodin MM, Zaitlin D, Naidu RA, Lommel SA (2008) Nicotiana benthamiana: its history and future as a model for plant-pathogen interactions. Mol Plant Microbe Interact 21:1015–1026

    CAS  PubMed  Article  Google Scholar 

  27. Hagimori M, Matsui M, Matsuzaki T, Shinozaki Y, Shinoda T, Harada H (1993) Production of somatic hybrids between Nicotiana benthamiana and Nicotiana tabacum and their resistance to aphids. Plant Sci 91:213–222

    CAS  Article  Google Scholar 

  28. Jacobs TB, LaFayette PR, Schmitz RJ, Parrott WA (2015) Targeted genome modifications in soybean with CRISPR/Cas9. Bmc Biotechnol 15:16

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  29. Karabourniotis G, Kotsabassidis D, Manetas Y (1995) Trichome density and its protective potential against ultraviolet-B radiation damage during leaf development. Canadian J Botany Revue Canadienne De Botanique 73:376–383

    Google Scholar 

  30. Kim J, Kang K, Gonzales-Vigil E, Shi F, Jones AD, Barry CS, Last RL (2012) Striking natural diversity in glandular trichome acylsugar composition is shaped by variation at the Acyltransferase2 locus in the wild tomato Solanum habrochaites. Plant Physiol 160:1854–1870

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  31. Kroumova AB, Wagner GJ (2003) Different elongation pathways in the biosynthesis of acyl groups of trichome exudate sugar esters from various solanaceous plants. Planta 216:1013–1021

    CAS  PubMed  Article  Google Scholar 

  32. Kroumova ABM, Zaitlin D, Wagner GJ (2016) Natural variability in acyl moieties of sugar esters produced by certain tobacco and other Solanaceae species. Phytochemistry 130:218–227

    CAS  PubMed  Article  Google Scholar 

  33. Landis JB, Miller CM, Broz AK, Bennett AA, Carrasquilla-Garcia N, Cook DR, Last RL, Bedinger PA, Moghe GD (2021) Migration through a major Andean ecogeographic disruption as a driver of genetic and phenotypic diversity in a wild tomato species. Mol Biol Evol 38:3202–3219

    PubMed  PubMed Central  Article  Google Scholar 

  34. Laue G, Preston CA, Baldwin IT (2000) Fast track to the trichome: induction of N-acyl nornicotines precedes nicotine induction in Nicotiana repanda. Planta 210:510–514

    CAS  PubMed  Article  Google Scholar 

  35. Leong BJ, Hurney SM, Fiesel PD, Moghe GD, Jones AD, Last RL (2020) Specialized metabolism in a nonmodel nightshade: Trichome acylinositol biosynthesis. Plant Physiol 183:915–924

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  36. Leong BJ, Lybrand DB, Lou YR, Fan PX, Schilmiller AL, Last RL (2019) Evolution of metabolic novelty: A trichome-expressed invertase creates specialized metabolic diversity in wild tomato. Sci Adv 5:eaaw3754

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  37. Liu H, Ding YD, Zhou YQ, Jin WQ, Xie KB, Chen LL (2017) CRISPR-P 2.0: an improved CRISPR-Cas9 tool for genome editing in plants. Mol Plant 10:530–532

    CAS  PubMed  Article  Google Scholar 

  38. Lou YR, Anthony TM, Fiesel PD, Arking RE, Christensen EM, Jones AD, Last RL (2021) It happened again: convergent evolution of acylglucose specialized metabolism in black nightshade and wild tomato. 10.1101/2021.06.08.447545

  39. Luu VT, Weinhold A, Ullah C, Dressel S, Schoettner M, Gase K, Gaquerel E, Xu S, Baldwin IT (2017) O-Acyl sugars protect a wild tobacco from both native fungal pathogens and a specialist herbivore. Plant Physiol 174:370–386

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  40. Marchant WG, Legarrea S, Smeda JR, Mutschler MA, Srinivasan R (2020) Evaluating acylsugars-mediated resistance in tomato against Bemisia tabaci and transmission of tomato yyellow leaf curl virus. Insects 11:842

    PubMed Central  Article  PubMed  Google Scholar 

  41. Matsuzaki T, Shinozaki Y, Hagimori M, Tobita T, Shigematsu H, Koiwai A (1992) Novel glycerolipids and glycolipids from the surface-lipids of Nicotiana benthamiana. Biosci Biotechnol Biochem 56:1565–1569

    CAS  Article  Google Scholar 

  42. Matsuzaki T, Shinozaki Y, Suhara S, Ninomiya M, Shigematsu H, Koiwai A (1989) Isolation of glycolipids from the surface-lipids of Nicotiana bigelovii and their distribution in Nicotiana species. Agric Biol Chem 53:3079–3082

    CAS  Google Scholar 

  43. McKenzie CL, Puterka GJ (2004) Effect of sucrose octanoate on survival of nymphal and adult Diaphorina citri (Homoptera: Psyllidae). J Econ Entomol 97:970–975

    CAS  PubMed  Article  Google Scholar 

  44. McKenzie CL, Weathersbee AA, 3rd, Puterka GJ (2005) Toxicity of sucrose octanoate to egg, nymphal, and adult Bemisia tabaci (Hemiptera: Aleyrodidae) using a novel plant-based bioassay. J Econ Entomol 98: 1242–1247

    CAS  PubMed  Article  Google Scholar 

  45. Meihls LN, Handrick V, Glauser G, Barbier H, Kaur H, Haribal MM, Lipka AE, Gershenzon J, Buckler ES, Erb M, Köllner TG, Jander G (2013) Natural variation in maize aphid resistance is associated with 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one glucoside methyltransferase activity. Plant Cell 25:2341–2355

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  46. Moghe GD, Leong BJ, Hurney SM, Daniel Jones A, Last RL (2017) Evolutionary routes to biochemical innovation revealed by integrative analysis of a plant-defense related specialized metabolic pathway. Elife 6:e28468

    PubMed  PubMed Central  Article  Google Scholar 

  47. Nadakuduti SS, Uebler JB, Liu X, Jones AD, Barry CS (2017) Characterization of trichome-expressed BAHD acyltransferases in Petunia axillaris reveals distinct acylsugar assembly mechanisms within the Solanaceae. Plant Physiol 175:36–50

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  48. Ning J, Moghe GD, Leong B, Kim J, Ofner I, Wang Z, Adams C, Jones AD, Zamir D, Last RL (2015) A feedback-insensitive isopropylmalate synthase affects acylsugar composition in cultivated and wild tomato. Plant Physiol 169:1821–1835

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Nonomura T, Xu L, Wada M, Kawamura S, Miyajima T, Nishitomi A, Kakutani K, Takikawa Y, Matsuda Y, Toyoda H (2009) Trichome exudates of Lycopersicon pennellii form a chemical barrier to suppress leaf-surface germination of Oidium neolycopersici conidia. Plant Sci 176:31–37

    CAS  Article  Google Scholar 

  50. O’Connell MA, Medina AL, Sanchez Pena P, Trevino MB (2007) Molecular genetics of drought resistance response in tomato and related species. In: Razdan MK, Mattoo AK (eds). Genetic improvement of solanaceous crops Enfield USA, pp 261–283

  51. Penuelas J, Filella I, Biel C, Serrano L, Save R (1993) The reflectance at the 950–970 nm region as an indicator of plant water status. Int J Remote Sens 14:1887–1905

    Article  Google Scholar 

  52. Powell JD (2015) From pandemic preparedness to biofuel production: tobacco finds its biotechnology niche in North America. Agriculture Basel 5:901–917

    CAS  Article  Google Scholar 

  53. Ramsey JS, Elzinga DA, Sarkar P, Xin YR, Ghanim M, Jander G (2014) Adaptation to nicotine feeding in Myzus persicae. J Chem Ecol 40:869–877

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  54. Ramsey JS, Wilson AC, De Vos M, Sun Q, Tamborindeguy C, Winfield A, Malloch G, Smith DM, Fenton B, Gray SM, Jander G (2007) Genomic resources for Myzus persicae: EST sequencing, SNP identification, and microarray design. BMC Genom 8: 423

    Article  Google Scholar 

  55. Rodriguez AE, Tingey WM, Mutschler MA (1993) Acylsugars of Lycopersicon pennellii deter settling and feeding of the green peach aphid (Homoptera, Aphididae). J Econ Entomol 86:34–39

    CAS  Article  Google Scholar 

  56. Rodriguez PA, Stam R, Warbroek T, Bos JI (2014) Mp10 and Mp42 from the aphid species Myzus persicae trigger plant defenses in Nicotiana benthamiana through different activities. Mol Plant Microbe Interact 27:30–39

    CAS  PubMed  Article  Google Scholar 

  57. Schiavinato M, Strasser R, Mach L, Dohm JC, Himmelbauer H (2019) Genome and transcriptome characterization of the glycoengineered Nicotiana benthamiana line DeltaXT/FT. BMC Genom 20:594

    Article  CAS  Google Scholar 

  58. Schilmiller A, Shi F, Kim J, Charbonneau AL, Holmes D, Jones AD, Last RL (2010) Mass spectrometry screening reveals widespread diversity in trichome specialized metabolites of tomato chromosomal substitution lines. Plant J 62:391–403

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  59. Schilmiller AL, Charbonneau AL, Last RL (2012) Identification of a BAHD acetyltransferase that produces protective acyl sugars in tomato trichomes. Proc Natl Acad Sci USA 109:16377–16382

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  60. Schilmiller AL, Moghe GD, Fan P, Ghosh B, Ning J, Jones AD, Last RL (2015) Functionally divergent alleles and duplicated loci encoding an acyltransferase contribute to acylsugar metabolite diversity in Solanum trichomes. Plant Cell 27:1002–1017

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  61. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  62. Shepherd RW, Wagner GJ (2007) Phylloplane proteins: emerging defenses at the aerial frontline? Trends Plant Sci 12:51–56

    CAS  PubMed  Article  Google Scholar 

  63. Simmons AT, Gurr GM, McGrath D, Martin PM, Nicol HI (2004) Entrapment of Helicoverpa armigera (Hubner) (Lepidoptera:Noctuidae) on glandular trichomes of Lycopersicon species. Aust J Entomol 43:196–200

    Article  Google Scholar 

  64. Simon B, Cenis JL, Demichelis S, Rapisarda C, Caciagli P, Bosco D (2003) Survey of Bemisia tabaci (Hemiptera: Aleyrodidae) biotypes in Italy with the description of a new biotype (T) from Euphorbia characias. Bull Entomol Res 93:259–264

    CAS  PubMed  Article  Google Scholar 

  65. Slocombe SP, Schauvinhold I, McQuinn RP, Besser K, Welsby NA, Harper A, Aziz N, Li Y, Larson TR, Giovannoni J, Dixon RA, Broun P (2008) Transcriptomic and reverse genetic analyses of branched-chain fatty acid and acyl sugar production in Solanum pennellii and Nicotiana benthamiana. Plant Physiol 148:1830–1846

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  66. Song Z, Li S, Chen X, Liu L, Song Z (2006) Synthesis of sucrose esters. For Stud China 8:26–29

    CAS  Article  Google Scholar 

  67. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  68. Stone WD, Pellicore MJ, Hagstrom S, Lawton TJ (2020) HSIviewer: pushbutton hyperspectral image analysis for rapid plant phenotyping. in review

  69. Thompson JD, Higgins DG, Gibson TJ (1994) Clustal-W - Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  70. Thurston R (1961) Resistance in Nicotiana to the green peach aphids and some other tobacco insect pest. J Econ Entomol 54:946–949

    Article  Google Scholar 

  71. Van Eck J, Keen P, Tjahjadi M (2019) Agrobacterium tumefaciens-mediated transformation of tomato. Methods Mol Biol 1864: 225–234

    PubMed  Article  CAS  Google Scholar 

  72. Van T, Weinhold A, Ullah C, Dressel S, Schoettner M, Gase K, Gaquerel E, Xu SQ, Baldwin IT (2017) O-acyl sugars protect a wild tobacco from both native fungal pathogens and a specialist herbivore. Plant Physiol 174:370–386

    Article  CAS  Google Scholar 

  73. Wagner GJ, Wang E, Shepherd RW (2004) New approaches for studying and exploiting an old protuberance, the plant trichome. Ann Bot 93:3–11

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  74. Weinhold A, Baldwin IT (2011) Trichome-derived O-acyl sugars are a first meal for caterpillars that tags them for predation. Proc Natl Acad Sci USA 108:7855–7859

    CAS  PubMed  PubMed Central  Article  Google Scholar 

Download references

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.

Author information

Affiliations

Authors

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.

Corresponding author

Correspondence to Georg Jander.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Feng, H., Acosta-Gamboa, L., Kruse, L.H. et al. Acylsugars protect Nicotiana benthamiana against insect herbivory and desiccation. Plant Mol Biol (2021). https://doi.org/10.1007/s11103-021-01191-3

Download citation

Keywords

  • Acylsugar
  • Aphid
  • ASAT
  • Desiccation
  • Nicotiana benthamiana
  • Whitefly