Abstract
Herbivore-induced defenses are widespread, rapidly evolving and relevant for plant fitness. Such induced defenses are often mediated by early defense signaling (EDS) rapidly activated by the perception of herbivore associated elicitors (HAE) that includes transient accumulations of jasmonic acid (JA). Analyzing 60 HAE-induced leaf transcriptomes from closely-related Nicotiana species revealed a key gene co-expression network (M4 module) which is co-activated with the HAE-induced JA accumulations but is elicited independently of JA, as revealed in plants silenced in JA signaling. Functional annotations of the M4 module were consistent with roles in EDS and a newly identified hub gene of the M4 module (NaLRRK1) mediates a negative feedback loop with JA signaling. Phylogenomic analysis revealed preferential gene retention after genome-wide duplications shaped the evolution of HAE-induced EDS in Nicotiana. These results highlight the importance of genome-wide duplications in the evolution of adaptive traits in plants.
Highlights
Induced defense is widespread in plants and can improve the fitness of plants under herbivore attack (Baldwin, 1998; Kessler et al, 2004)
Many plants recognize and distinguish the damage caused by feeding insects from mechanical damage by perceiving herbivore-associated elicitors (HAE) to induce rapid early defense signaling (EDS) that includes the accumulation of jasmonic acid (JA) and its derivatives, phytohormones that play a central role in the activation of induced defenses (Erb et al, 2012; Howe and Jander, 2008; Wu and Baldwin, 2010)
N. obtusifolia and N. miersii, which did not respond to fatty acid-amino acid conjugate C18:3-Glu (FAC)-treatments by amplifying their wound-induced accumulations of jasmonic acid (JA) within 2 hr, showed overall little induced transcriptomic responses
Summary
Induced defense is widespread in plants and can improve the fitness of plants under herbivore attack (Baldwin, 1998; Kessler et al, 2004). Many plants recognize and distinguish the damage caused by feeding insects from mechanical damage by perceiving herbivore-associated elicitors (HAE) to induce rapid early defense signaling (EDS) that includes the accumulation of jasmonic acid (JA) and its derivatives, phytohormones that play a central role in the activation of induced defenses (Erb et al, 2012; Howe and Jander, 2008; Wu and Baldwin, 2010). In Nicotiana attenuata, an increase in endogenous JA levels by supplying methyl-jasmonic acid (MeJA) reduced plant fitness by 26% when plants were protected from herbivore attack (Baldwin, 1998). Induced JA accumulations can result in net fitness gains or losses depending on the cost/benefit ratio of induced defenses, which varies among attacking herbivore species and environmental conditions. A robust and complex signaling network that regulates and fine-tunes induced JA biosynthesis, metabolism and JA-dependent induced downstream defenses is essential for plants to realize their fitness optima
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