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The extremophile Nicotiana benthamiana has traded viral defence for early vigour

Nature Plants volume 1, Article number: 15165 (2015) Cite this article

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Abstract

A single lineage of Nicotiana benthamiana is widely used as a model plant1 and has been instrumental in making revolutionary discoveries about RNA interference (RNAi), viral defence and vaccine production. It is peerless in its susceptibility to viruses and its amenability in transiently expressing transgenes2,3. These unparalleled characteristics have been associated both positively and negatively with a disruptive insertion in the RNA-dependent RNA polymerase 1 gene, Rdr14–6. For a plant so routinely used in research, the origin, diversity and evolution of the species, and the basis of its unusual abilities, have been relatively unexplored. Here, by comparison with wild accessions from across the spectrum of the species’ natural distribution, we show that the laboratory strain of N. benthamiana is an extremophile originating from a population that has retained a mutation in Rdr1 for ∼0.8 Myr and thereby traded its defence capacity for early vigour and survival in the extreme habitat of central Australia. Reconstituting Rdr1 activity in this isolate provided protection. Silencing the functional allele in a wild strain rendered it hypersusceptible and was associated with a doubling of seed size and enhanced early growth rate. These findings open the way to a deeper understanding of the delicate balance between protection and vigour.

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Figure 1: Characterization of N. benthamiana isolates.
Figure 2: Responses of N. benthamiana isolates to virus infection and correlation with their Rdr1 genotype.
Figure 3: Phylogeny, molecular clock and geographic distribution of N. benthamiana isolates.
Figure 4: Flower structure, germination rate and early vigour of N. benthamiana isolates.

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Acknowledgements

We are grateful to D. Albrecht, T. Willing, K. Courtney, T. Bean, J. Randles, E. Newbiggin, P. Ladiges and E. Dodds for their help, resource provision and discussions, and K. Lee for excellent technical assistance.

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Authors and Affiliations

  1. Centre for Tropical Crops and Biocommodities, Queensland University of Technology, Brisbane, 4001, Queensland, Australia

    Julia Bally, Hyungtaek Jung, Fatima Naim, Roger P. Hellens, James L. Dale & Peter M. Waterhouse

  2. School of Molecular Biology, The University of Sydney, Sydney, 2006, New South Wales, Australia

    Julia Bally, Kenlee Nakasugi, Mei Wong, Chloe M. Paul & Peter M. Waterhouse

  3. School of Biological Sciences, The University of Sydney, Sydney, 2006, New South Wales, Australia

    Fangzhi Jia, Simon Y.W. Ho, Fatima Naim & Peter M. Waterhouse

  4. Mount Albert Research Centre, Plant and Food Research, Auckland, New Zealand

    Ross N. Crowhurst & Roger P. Hellens

  5. Commonwealth Scientific and Industrial Research Organisation–Plant Industry, Canberra, Australia

    Craig C. Wood

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  1. Julia Bally
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Contributions

J.B. and P.W. designed the experiments; J.B., F.J., M.W., C.P. and F.N. performed the experiments; J.B., K.N., H.J., P.W., S.H., R.C., C.W., R.H. and J.D. analysed data; J.B. and P.W. wrote the paper. All the authors discussed the results and commented on the manuscript.

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Correspondence to Peter M. Waterhouse.

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The authors declare no competing financial interests.

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Bally, J., Nakasugi, K., Jia, F. et al. The extremophile Nicotiana benthamiana has traded viral defence for early vigour. Nature Plants 1, 15165 (2015). https://doi.org/10.1038/nplants.2015.165

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