Abstract
Plants are commonly attacked by a variety of insect herbivores and have developed specific defenses against different types of attackers. At the molecular level, herbivore-specific signalling pathways are activated by plants in response to attackers with different feeding strategies. Feeding by leaf-chewing herbivores predominantly activates jasmonic acid (JA)-regulated defenses, whereas feeding by phloem-sucking herbivores generally activates salicylic acid (SA)-regulated defenses. When challenged sequentially by both phloem-sucking and leaf-chewing herbivores, SA-JA antagonism may constrain the plant’s ability to timely and adequately divert defense to the second herbivore that requires activation of a different defensive pathway. We investigated the effect of the temporal sequence of infestation by the aphid Brevicoryne brassicae and three caterpillar species, Plutella xylostella, Pieris brassicae, and Mamestra brassicae, on the interaction between JA and SA signal-transduction pathways in three wild cabbage populations. We found no support for SA-JA antagonism, irrespective of the temporal sequence of herbivore introduction or the identity of the caterpillar species based on the transcript levels of the JA- and SA-regulated marker genes LOX and PR-1, respectively, at the examined time points, 6, 24, and 48 h. In general, infestation with aphids alone had little effect on the transcript levels of the two marker genes, whereas the three caterpillar species upregulated not only LOX but also PR-1. Transcriptional changes were different for plants from the three different natural cabbage populations.
Highlights
Plants live in a hostile environment and are challenged by a diverse range of attackers, including microbial pathogens and insect herbivores that may attack the plant either simultaneously or sequentially
We addressed the following questions: 1) What is the effect of the sequence of herbivore attack on salicylic acid (SA)-jasmonic acid (JA) crosstalk? 2) How general is this response when using different species of chewing herbivores? and 3) Is there intraspecific variation in the plant’s responses to herbivory by aphids and caterpillars? We quantified the transcript levels of two marker genes related to JA- and SA-signalling, i.e., LIPOXYGENASE (LOX) and PATHOGENESIS-RELATED PROTEIN-1 (PR-1), respectively (Bell et al 1995; Jirage et al 2001), at different time points following inoculation by each of the three different chewing herbivore species and the piercing-sucking aphid when introduced alone, simultaneously, or sequentially on wild cabbage plants from populations
Feeding by P. xylostella caterpillars alone or in combination with B. brassicae aphids (Fig. 1a) up-regulated the expression of LOX (Px vs. Px + B, P = 0.32), whereas transcript levels of LOX were similar in the controls and in plants exposed to B. brassicae alone (C vs. B, P = 0.71)
Summary
Plants live in a hostile environment and are challenged by a diverse range of attackers, including microbial pathogens and insect herbivores that may attack the plant either simultaneously or sequentially. To cope with the diversity of biotic threats that may reduce the survival and fitness of plants, they are equipped with traits that prevent or reduce attack by biotic agents. These traits, both physical and chemical, can be constitutively expressed or may be activated or enhanced upon attack (Agrawal 1999; Dicke and Baldwin 2010; Karban and Baldwin 1997). Leaf chewing and phloem feeding insect herbivores are well studied in relation to defense induction in plants. Defenses against leaf-chewing and phloem-feeding herbivores are regulated by two major signal-transduction pathways
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