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Virus effects on plant quality and vector behavior are species specific and do not depend on host physiological phenotype

  • Quentin Chesnais
  • Kerry E. Mauck
  • Florent Bogaert
  • Antoine Bamière
  • Manuella Catterou
  • Fabien Spicher
  • Véronique Brault
  • Mark Tepfer
  • Arnaud AmelineEmail author
Original Paper

Abstract

There is growing evidence that plant viruses manipulate host plants to increase transmission-conducive behaviors by vectors. Reports of this phenomenon frequently include only highly susceptible, domesticated annual plants as hosts, which constrains our ability to determine whether virus effects are a component of an adaptive strategy on the part of the pathogen or simply by-products of pathology. Here, we tested the hypothesis that transmission-conducive effects of a virus (Turnip yellows virus [TuYV]) on host palatability and vector behavior (Myzus persicae) are linked with host plant tolerance and physiological phenotype. Our study system consisted of a cultivated crop, false flax (Camelina sativa) (Brassicales: Brassicaceae), a wild congener (C. microcarpa), and a viable F1 hybrid of these two species. We found that the most tolerant host (C. microcarpa) exhibited the most transmission-conducive changes in phenotype relative to mock-inoculated healthy plants: Aphids preferred to settle and feed on TuYV-infected C. microcarpa and did not experience fitness changes due to infection—both of which will increase viruliferous aphid numbers. In contrast, TuYV induced transmission-limiting phenotypes in the least tolerant host (C. sativa) and to a greater degree in the F1 hybrid, which exhibited intermediate tolerance to infection. Our results provide no evidence that virus effects track with infection tolerance or physiological phenotype. Instead, vector preferences and performance are driven by host-specific changes in carbohydrates under TuYV infection. These results provide evidence that induction of transmission-enhancing phenotypes by plant viruses is not simply a by-product of general pathology, as has been proposed as an explanation for putative instances of parasite manipulation by viruses and many other taxa.

Keywords

Camelina genotypes Myzus persicae Pathogen transmission Physiological phenotypes Plant domestication Vector–host interactions Vector manipulation 

Notes

Acknowledgements

This work was performed, in partnership with the SAS PIVERT, within the frame of the French Institute for the Energy Transition (Institut pour la Transition Energétique (ITE) P.I.V.E.R.T. (www.institut-pivert.com) selected as an Investment for the Future (“Investissements d’Avenir”). This work was supported, as part of the Investments for the Future, by the French Government under the reference ANR-001-01. This work was partially supported by a public grant overseen by the French National Research Agency (ANR) (Reference: VIRAPHIPLANT ANR-14-CE19-0010). Dr. Kerry Mauck is supported by startup funds from the University of California, Riverside.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The article does not contain any studies with human participants or vertebrate animals.

Supplementary material

10340_2019_1082_MOESM1_ESM.docx (657 kb)
Supplementary material 1 (DOCX 656 kb)

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© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.UMR CNRS 7058 EDYSAN (Écologie et Dynamique des Systèmes Anthropisés)Université de Picardie Jules VerneAmiens CedexFrance
  2. 2.Department of EntomologyUniversity of California, Entomology BuildingRiversideUSA
  3. 3.UMR 1131, SVQV, INRA-UDSColmar CedexFrance
  4. 4.Institut Jean-Pierre Bourgin (IJPB), INRA, AgroParisTech, CNRSUniversité Paris-SaclayVersailles CedexFrance

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