Plant responses to multiple antagonists are mediated by order of attack
and phytohormone crosstalk
Abstract
Plants are often attacked by multiple antagonists, and traits of the
attacking organisms, and their order of arrival onto hosts, may affect
plant defenses. However, few studies have assessed how multiple
antagonists, and varying attack order, affect plant defense or
nutrition. To address this, we assessed defensive and nutritional
responses of Pisum sativum plants after attack by a vector
herbivore (Acrythosiphon pisum), a non-vector herbivore
(Sitona lineatus), and a pathogen (Pea enation mosaic
virus, PEMV). We show PEMV-infectious A. pisum induced several
pathogen-specific plant defense signals, but these defenses were
inhibited when S. lineatus was present in peas infected with
PEMV. In contrast, feeding by S. lineatus induced anti-herbivore
defense signals, but these defenses were enhanced by PEMV. Sitona
lineatus also increased abundance of plant amino acids, but only
when they attacked after PEMV-infectious A. pisum. Our results
suggest that diverse communities of biotic antagonists alter defense 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.