Manipulation of Aphid Behavior by a Persistent Plant Virus

Maliheh Safari; Matthew J Ferrari; Marilyn J Roossinck

doi:10.1128/JVI.01781-18

Manipulation of Aphid Behavior by a Persistent Plant Virus

J Virol. 2019 Apr 17;93(9):e01781-18. doi: 10.1128/JVI.01781-18. Print 2019 May 1.

Authors

Maliheh Safari^{1

2}, Matthew J Ferrari^{2

3}, Marilyn J Roossinck^{4

2

3}

Affiliations

¹ Department of Plant Pathology and Environmental Microbiology, Pennsylvania State University, University Park, Pennsylvania, USA.
² Center for Infectious Disease Dynamics, Pennsylvania State University, University Park, Pennsylvania, USA.
³ Department of Biology, Pennsylvania State University, University Park, Pennsylvania, USA.
⁴ Department of Plant Pathology and Environmental Microbiology, Pennsylvania State University, University Park, Pennsylvania, USA mjr25@psu.edu.

Abstract

Plants are frequently infected with cytoplasmic RNA viruses that persist for many generations through nearly 100% vertical transmission without producing any symptoms. Movement between plant cells and horizontal transmission have not been observed with these viruses; instead, they are distributed to all host cells through host cell division. Jalapeño peppers (Capsicum annuum) are all infected with Pepper cryptic virus 1 (PCV-1; family Partitiviridae). We compared the effect of odor cues from PCV-1-infected (J+) and virus-free (J-) jalapeño peppers on the aphid Myzus persicae, a common vector of acute plant viruses. Pairwise preference experiments showed a stark contrast to insect-plant interactions in acute virus infections-that is, the virus-infected plants deterred aphids. The acute plant virus Cucumber mosaic virus (CMV) manipulates its host's volatile emissions to attract aphid vectors and facilitate its transmission. We inoculated J+ and J- plants with CMV. Volatiles of J+ and J- CMV-infected plants were more attractive to aphids than those of J+ and J- mock-inoculated plants. However, in pairwise preference experiments with J+ CMV- and J- CMV-infected plants, aphids preferred the J- CMV volatile blend. Aphid reproduction on J+ and J- plants was measured as an indicator of the effect of PCV-1 on host quality for aphids. Aphid reproduction on J+ plants was more than 2-fold lower than that on J- plants.IMPORTANCE This study demonstrates that a persistent plant virus can manipulate aphid behavior. This manipulation is in stark contrast to previously described effects of acute viruses on their hosts that facilitate their transmission. This study demonstrates a positive relationship between Pepper cryptic virus 1 and jalapeño pepper (Capsicum annuum) plants wherein the virus protects the plants from the vector of acute viruses and reduces aphid herbivory. This work reveals an important implication of persistent plant viruses for pest and pathogen management in agriculture.

Keywords: aphid behavior; beneficial virus; partitivirus; plant volatiles.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Aphids / physiology*
Behavior, Animal*
Capsicum* / metabolism
Capsicum* / virology
Cucumovirus / metabolism*
Oils, Volatile / metabolism*
Plant Diseases / virology*

Substances

Oils, Volatile