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.