Responses of pea plants to multiple antagonists are mediated by order of attack and phytohormone crosstalk.

Plants are often attacked by multiple antagonists and traits of the attacking organisms and their order of arrival onto hosts may affect plant defences. However, few studies have assessed how multiple antagonists, and varying attack order, affect plant defence or nutrition. To address this, we assessed defensive and nutritional responses of Pisum sativum plants after attack by a vector herbivore (Acrythosiphon pisum), a nonvector herbivore (Sitona lineatus), and a pathogen (Pea enation mosaic virus, PEMV). We show viruliferous A. pisum induced several antipathogen plant defence signals, but these defences were inhibited by S. lineatus feeding on peas infected with PEMV. In contrast, S. lineatus feeding induced antiherbivore defence signals, and these plant defences were enhanced by PEMV. Sitona lineatus also increased abundance of plant amino acids, but only when they attacked after viruliferous A. pisum. Our results suggest that diverse communities of biotic antagonists alter defence and nutritional traits of plants through complex pathways that depend on the identity of attackers and their order of arrival onto hosts. Moreover, we show interactions among a group of biotic stressors can vary along a spectrum from antagonism to enhancement/synergism based on the identity and order of attackers, and these interactions are mediated by a multitude of phytohormone pathways.

Reciprocal plant-mediated interactions between a virus and a non-vector herbivore.

Vector-borne viruses alter many physical and chemical traits of their plant hosts, indirectly affecting the fitness and behavior of vectors in ways that promote virus transmission. However, it is unclear whether viruses induce plant-mediated shifts in the behavior and fitness of non-vector herbivores, or if non-vectors affect the dynamics of vector-borne viruses. Here we evaluated reciprocal interactions between Pea enation mosaic virus (PEMV), a pathogen transmitted by the aphid Acrythosiphon pisum, and a non-vector weevil, Sitona lineatus. In the field, PEMV-infected plants experienced more defoliation from S. lineatus than uninfected plants; behavioral assays similarly showed S. lineatus adults preferred to feed on infected plants. In turn, infectious A. pisum preferred plants damaged by S. lineatus, and S. lineatus herbivory led to increased PEMV titer. These interactions may be mediated by plant phytohormone levels, as S. lineatus induced jasmonic acid, while PEMV induced salicylic acid. Levels of abscisic acid were not affected by attack from either PEMV or S. lineatus alone, but plants challenged by both had elevated levels of this phytohormone. As plant viruses and their vectors often exist in diverse communities, our study highlights the importance of non-vector species in influencing plant pathogens and their vectors through host-mediated effects.

Tri-trophic interactions mediate the spread of a vector-borne plant pathogen.

Many insect herbivores are vectors that transmit plant pathogens as they forage. Within food webs, vectors interact with a range of host plants, other herbivores, and predators. Yet, few studies have examined how tri-trophic interactions involving vectors affect the spread of pathogens. Here we assessed effects of food web structure on aphid vectors and the prevalence of an aphid-borne persistent pathogen (Pea enation mosaic virus, PEMV) in pea plants. We experimentally manipulated ladybird predators, alternative host plants, and non-vector herbivores and assessed responses of pea aphids and PEMV using structural equation models. We show that variation in bottom-up, top-down, and horizontal interactions mediated PEMV prevalence. Predators reduced PEMV prevalence by consuming aphids, but an alternative host plant (vetch) had the opposite effect by promoting aphid movement and abundance. Non-vector herbivores (pea leaf weevil) increased PEMV susceptibility in peas. In turn, weevils offset the positive effects of predators on PEMV, but increased the negative effects of vetch. Our results show that tri-trophic interactions within insect and plant food webs can mediate vector biology with synergistic and opposing effects on pathogens. Continuing to assess how community-wide interactions affect vectors will aid in our understanding of vector-borne pathosystems.