The banana aphid, Pentalonia nigronervosa Coquerel (Hemiptera, Aphididae) is the vector agent of the Banana bunchy top virus (BBTV), a virus causing banana bunchy top disease (BBTD), which is the most serious viral disease of bananas worldwide1,2,3. Being a member of the family Nanoviridae and the genus Babuvirus, BBTV has a genome consisting of several segments of circular single-stranded DNA encapsulated in small isometric particles4,5,6,7. The disease is manifested by a general dwarfing of the plant, narrow leaves, chlorosis of the leaf margins, and dark green discontinuous streaks on the leaves, petioles and pseudotruncae. Leaves of infected plants are observed to become progressively smaller and erect, giving the plant a bushy appearance8.
The vector is not able to acquire the virus from these leaves9,10. BBTV is transmitted after a sap uptake by the aphid vector on an infected plant, in a persistent, circulative and non-propagative manner10,11. As persistent virus, acquisition of BBTV requires prolonged feeding for at least a few hours on an infected plant. Virions must pass through the insect gut to survive in the haemolymph to transverse salivary tissues (hence “circulatory transmission”), without replicating in the banana aphid (hence “non-propagative”)12,13.
We already know that host plant search and selection by aphids remain primarily facilitated by volatile organic compounds (VOC) emitted by plants14,15,16. We also know that the profiles of these VOC can vary in quality and quantity with the infection by the phytovirus. For example, in a study by17, the authors showed that P. nigronervosa was more attracted to infected banana plants than to healthy ones, through an increased in VOC emission. The preference of vectors to infected plants, as is the case for BBTV, could contribute to increased virus spread. However, a preference for infected plants will accelerate the spread of BBTV only when infected plants are rare, not when they become widespread in a plant population18,19. In this case, to facilitate the spread of the virus, it would be necessary that, once the virus acquired, the vector will be deterred from infected plants and attracted to healthy banana plants.
Indeed, the interaction between the plant and the pathogen often produces a feedback effect on the vectors. It was shown that while non-infectious vectors sometimes prefer infected plants, infectious vectors tend to prefer uninfected hosts favouring transmission and global spread19,20,21,22,23. This is the case in the study of 20, where non-virulent My. persicae preferred to settle on Barley yellow dwarf virus (BYDV)-infected potato plants compared to uninfected plants, while viruliferous My. persicae (carrying PLRV) preferentially settled on uninfected potato plants compared to infected plants. Similarly, in the in vitro study by19, the aphid Rhopalosiphum padi, after acquiring the barley yellow dwarf virus (BYDV), preferred uninfected wheat plants, while the non-infecting aphid preferred BYDV-infected plants. This change in behaviour should favour the spread of the virus since the preference of non-infectious vectors for infected plants will favour acquisition, while the preference of infectious vectors for non-infected hosts favour transmission. Natural selection on the parasite or pathogen has favoured the ability to induce host behaviour that enhances its transmission, what is usually called vector manipulation hypothesis (VMH)19,24
The question is thus how the virus can modify the behaviour of its host regarding to plant attractivity although its no-propagative nature. As the virus does not multiply in the aphids, we hypothesize that during development on an infected plant, the virus may act through a change in the plant quality on the alates’ phenotype, even if non-propagative viruses also interact with the vector at the cellular level during movement between tissues and organs and may potentially influence the physiology and behaviour of the vector25.
We have demonstrated that infection of banana with BBTV enhances the reproductive capabilities of P. nigronervosa, despite the decrease in the size of aphids reared on infected banana plants17. Moreover, other studies have reported that the size of an aphid can also vary according to virus infection26. On the other hand, aphids have olfactory receptor systems responsible for the detection of plant volatile compounds, through olfactory sensilla such as primary and secondary rhinaria on the antennae27,28, as shown in several electrophysiological studies29,30,31,32; and a flight system allowing dispersal of winged forms to other plants33.
Our aims is thus to determine the consequences of BBTV acquisition, during development on an infected plant, on the selection behaviour of banana plant by P. nigronervosa as well as on the wing size and antennal SR of the alates, knowing that it is the winged morphs that are actually responsible for the transmission of phytoviruses, and to this end are equipped with an elaborate sensory system for detection, flight and localization of host plants34. In the present study, we addressed the question of whether BBTV acquisition can directly modify the physiology and behaviour of the vector.
Healthy and infected seedlings of two of the most representative banana varieties in the world: Cavendish dessert banana (AAA genome) and Pacific plantain (AAB genome)35,36,37 were used in this work.