Endosymbionts Differentially Alter Exploratory Probing Behavior of a Nonpersistent Plant Virus Vector

Abstract

Insect endosymbionts (hereafter, symbionts) can modify plant virus epidemiology by changing the physiology or behavior of vectors, but their role in nonpersistent virus pathosystems remains uninvestigated. Unlike propagative and circulative viruses, nonpersistent plant virus transmission occurs via transient contamination of mouthparts, making direct interaction between symbiont and virus unlikely. Nonpersistent virus transmission occurs during exploratory intracellular punctures with styletiform mouthparts when vectors assess potential host-plant quality prior to phloem feeding. Therefore, we used an electrical penetration graph (EPG) to evaluate plant probing of the cowpea aphid, Aphis craccivora Koch, an important vector of cucurbit viruses, in the presence and absence of two facultative, intracellular symbionts. We tested four isolines of A. craccivora: two isolines were from a clone from black locust (Robinia pseudoacacia L.), one infected with Arsenophonus sp. and one cured, and two derived from a clone from alfalfa (Medicago sativa L.), one infected with Hamiltonella defensa and one cured. We quantified exploratory intracellular punctures, indicated by a waveform potential drop recorded by the EPG, initiation speed and frequency within the initial 15 min on healthy and watermelon mosaic virus-infected pumpkins. Symbiont associations differentially modified exploratory intracellular puncture frequency by aphids, with H. defensa-infected aphids exhibiting depressed probing, and Arsenophonus-infected aphids an increased frequency of probing. Further, there was greater overall aphid probing on virus-infected plants, suggesting that viruses manipulate their vectors to enhance acquisition-transmission rates, independent of symbiont infection. These results suggest facultative symbionts differentially affect plant-host exploration behaviors and potentially nonpersistent virus transmission by vectors.

A fitness cost resulting fromHamiltonella defensainfection is associated with altered probing and feeding behaviour inRhopalosiphum padi

“…When probing into plant tissue, H. defensa -infected aphids displayed a characteristic pattern of more frequent and shorter exploratory intracellular punctures (EPG waveform pd) than uninfected aphids. The precise cause of this symbiont-associated effect on aphid probing is not clear, although a similar pattern was recently reported in H. defensa -infected cowpea aphids, Aphis craccivora (Angelella et al, 2018), and it is likely that changes in intracellular puncture frequency will affect the transmission of plant viruses (Fereres and Collar, 2001; Powell, 2005). A key difference between our study and the previous work of Angelella et al (2018) was that R. padi infected with H. defensa also showed differential feeding behaviour caused by altered stylet activities within the phloem.…”

“…The precise cause of this symbiont-associated effect on aphid probing is not clear, although a similar pattern was recently reported in H. defensa -infected cowpea aphids, Aphis craccivora (Angelella et al, 2018), and it is likely that changes in intracellular puncture frequency will affect the transmission of plant viruses (Fereres and Collar, 2001; Powell, 2005). A key difference between our study and the previous work of Angelella et al (2018) was that R. padi infected with H. defensa also showed differential feeding behaviour caused by altered stylet activities within the phloem. H. defensa -infected aphids spent less time salivating into the phloem and showed an overall increase in the percentage of phloem phases which contained phloem ingestion, including an increased proportion of these containing periods of sustained phloem ingestion.…”

“…This protective phenotype often depends on the association of H. defensa with virulent strains of the bacteriophage APSE (Acyrthosiphon pisum Secondary Endosymbiont) which secretes toxins that arrest the development of the parasitoid wasp larvae (Brandt et al, 2017). A recent study has shown that H. defensa infection can alter interactions at the aphid-plant interface by influencing aphid probing behaviour (Angelella et al, 2018). This observation suggests that altered aphid probing behaviour could affect aphid fitness by altering feeding success and thus potentially impacting on aphid nutrition.…”

“…A primary use of the EPG technique has been to identify plant tissue types involved in plant resistance against sap-feeding pests (Alvarez et al, 2006; Greenslade et al, 2016). However, the EPG technique can also be employed to examine insect physiological responses to a myriad of biotic and abiotic factors, such as environmental stress (Ponder et al, 2000), plant disease status (Angelella et al, 2018), plant association with mycorrhiza (Simon et al, 2017), and disruption of the obligate aphid endosymbiont B. aphidicola (Machado-Assefh and Alvarez, 2018).…”

Endosymbiotic Rickettsiella causes cytoplasmic incompatibility in a spider host

“…Reproductive manipulation by endosymbionts, through mechanisms such as CI, can 233 influence arthropod behavioral ecology [40], population dynamics [41], and evolutionary 234 trajectory [42]. As the known roster of symbionts capable of undertaking these manipulations 235 increases, the potential for understanding and potentially exploiting their effects on the biology 236 of their hosts increases as well.…”