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Natural fumigation as a mechanism for volatile transport between flower organs

Abstract

Plants synthesize volatile organic compounds (VOCs) to attract pollinators and beneficial microorganisms, to defend themselves against herbivores and pathogens, and for plant-plant communication. In general, VOCs accumulate in and are emitted from the tissue of their biosynthesis. However, using biochemical and reverse genetic approaches, we demonstrate a new physiological phenomenon: inter-organ aerial transport of VOCs via natural fumigation. Before petunia flowers open, a tube-specific terpene synthase produces sesquiterpenes, which are released inside the buds and then accumulate in the stigma, potentially defending the developing stigma from pathogens. These VOCs also affect reproductive organ development and seed yield, which are previously unknown functions of terpenoid compounds.

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Fig. 1: Characterization of sesquiterpene synthases expressed in petunia flowers.
Fig. 2: Analysis of inter-organ transport of PhTPS1 products in petunia buds.
Fig. 3: Effect of sesquiterpene fumigation on pistil development and seed yield.
Fig. 4: Proposed fumigation model.

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request. Plant material generated in this study is available from the corresponding author upon request. For the microbiome, Fastaq files of samples containing the sequences of the OTUs associated with Petunia and Brassica are deposited at the European Nucleotide Archive (PRJEB29416 (ERP111715)). The sequences reported in this paper have been deposited in GenBank database with the following accession numbers MK159027 for PhTPS1, MK159028 for PhTPS2, MK159029 for PhTPS3, and MK159030 for PhTPS4.

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Acknowledgements

This work was supported by grant IOS-1655438 from the National Science Foundation to J.A.M. and N.D. and by the United States Department of Agriculture (USDA) National Institute of Food and Agriculture Hatch project 177845 to N.D.

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Contributions

B.B. and N.D. conceived the study. B.B., S.R., J.Y., J.H.L., R.R.J., S.A.K., J.A.M., and N.D. planned experiments. B.B. performed metabolic profiling, identification, and characterization of TPSs, analysis of TPS activities in plants, stable isotope labeling, expression analysis, generation of transgenic plants and their analysis, and complementation experiments. S.R. performed wax analysis. J.Y. performed microscopy analysis. K.M.P.C. analyzed seed yield. J.H.L. performed complementation experiments, expression analysis of TPSs in transgenic plants, and metabolic profiling. R.R.J. performed microbiome analysis. B.B., S.R., J.Y., K.M.P.C., J.H.L., R.R.J., S.A.K., J.A.M., and N.D. analyzed and interpreted data. S.A.K., J.A.M., and N.D. supervised the study. B.B., J.H.L., and N.D. wrote the paper. All authors read and edited the manuscript.

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Correspondence to Natalia Dudareva.

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Supplementary information

Supplementary Information

Supplementary Figures 1–16, Supplementary Table 1

Reporting Summary

Supplementary Dataset 1

Microbiome analysis of flowers of Brassica rapa plants cultivated under sterile conditions from surface sterilized seeds (sample_33) or grown in soil in the laboratory after treatment with different bacteria. Microbiome analysis of pistils of wild-type and PhTPS1 RNAi-11 Petunia x hybrida flowers.

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Boachon, B., Lynch, J.H., Ray, S. et al. Natural fumigation as a mechanism for volatile transport between flower organs. Nat Chem Biol 15, 583–588 (2019). https://doi.org/10.1038/s41589-019-0287-5

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