Aphid–Plant–Phytovirus Pathosystems: Influencing Factors from Vector Behaviour to Virus Spread

Abstract

Aphids are responsible for the spread of more than half of the known phytovirus species. Virus transmission within the plant–aphid–phytovirus pathosystem depends on vector mobility which allows the aphid to reach its host plant and on vector efficiency in terms of ability to transmit phytoviruses. However, several other factors can influence the phytoviruses transmission process and have significant epidemiological consequences. In this review, we aimed to analyse the aphid behaviours and influencing factors affecting phytovirus spread. We discussed the impact of vector host-seeking and dispersal behaviours mostly involved in aphid-born phytovirus spread but also the effect of feeding behaviours and life history traits involved in plant–aphid–phytovirus relationships on vector performances. We also noted that these behaviours are influenced by factors inherent to the interactions between pathosystem components (mode of transmission of phytoviruses, vector efficiency, plant resistance, …) and several biological, biochemical, chemical or physical factors related to the environment of these pathosystem components, most of them being manipulated as means to control vector-borne diseases in the crop fields.

Aphids on Aphid-Susceptible Cultivars Have Easy Access to Turnip Mosaic Virus, and Effective Inoculation on Aphid-Resistant Cultivars of Oilseed Rape (Brassica napus)

“…Aphids probe faster and longer after landing on a preferred host than on a non-preferred host [ 30 ]. The number of probe and non-probing phases before the first phloem phase are considered important events in host plant recognition and acceptance [ 2 ]. In our study, cabbage aphids on ‘Deleyou6’ spent more time per probe but less time on non-probing and non-phloemic behavior than those on ‘Zhongshuang11’, implying that aphids on ‘Deleyou6’ may spend more time in the phloem.…”

“…Most phytoviruses are transmitted to hosts by insect vectors [ 1 ]. Three events need to be taken into account for phytovirus transmission: (1) acquisition during the vector ingestion on an infected plant; (2) retention or circulation within the vector organism; and (3) inoculation during new vector ingestion on a healthy plant [ 2 ]. In the process of virus transmission, plant viruses can impact their vectors’ behavior and fitness both directly (via the presence of the virus in the vector’s body) and indirectly (by changes in the physiological and biochemical properties of the plant as a result of infection) to facilitate their spread [ 3 , 4 ].…”

“…Phytoviruses that are non-persistently and non-circulatively transmitted are only found at the vector’s stylet tips [ 2 ]. These viruses are acquired and transmitted by the insect vectors during brief probing punctures in plant epidermal and mesophyll cells [ 2 ] and tend to have temporary or context-specific associations with their vectors, which can have a variety of impacts, from increased attraction to infected plants, quick dispersal to preferred settlement and arrestment on infected plants, and improved fitness [ 5 ].…”

“…Additionally, numerous studies have demonstrated that non-persistent and non-circulative phytovirus-infected plants have less favorable aphid settling preferences and life history traits (for review: see Ref. [ 2 ]).…”

“…By analyzing EPG waveforms that have been characterized and defined, the hindering properties of different tissue levels on oilseed rape leave against aphids could be assessed [ 27 , 28 ]. Several studies based on the analysis of EPG variables have noted the alteration of aphid feeding behavior associated with the infectious state of the insect and/or the host plant that may influence the phytovirus spread [ 2 ]. Using EPGs, in the current study, we assessed the effects of three treatments on two cultivars of oilseed rape.…”