Abstract
The jasmonate hormones are essential regulators of plant defense against herbivores and include several dozen derivatives of the oxylipin jasmonic acid (JA). Among these, the conjugate jasmonoyl isoleucine (JA-Ile) has been shown to interact directly with the jasmonate co-receptor complex to regulate responses to jasmonate signaling. However, functional studies indicate that some aspects of jasmonate-mediated defense are not regulated by JA-Ile. Thus, it is not clear whether JA-Ile is best characterized as the master jasmonate regulator of defense, or if it regulates more specific aspects. We investigated possible functions of JA-Ile in anti-herbivore resistance of the wild tobacco Nicotiana attenuata, a model system for plant-herbivore interactions. We first analyzed the soluble and volatile secondary metabolomes of irJAR4xirJAR6, asLOX3, and WT plants, as well as an RNAi line targeting the jasmonate co-receptor CORONATINE INSENSITIVE 1 (irCOI1), following a standardized herbivory treatment. irJAR4xirJAR6 were the most similar to WT plants, having a ca. 60% overlap in differentially regulated metabolites with either asLOX3 or irCOI1. In contrast, while at least 25 volatiles differed between irCOI1 or asLOX3 and WT plants, there were few or no differences in herbivore-induced volatile emission between irJAR4xirJAR6 and WT plants, in glasshouse- or field-collected samples. We then measured the susceptibility of jasmonate-deficient vs. JA-Ile-deficient plants in nature, in comparison to wild-type (WT) controls, and found that JA-Ile-deficient plants (irJAR4xirJAR6) are much better defended even than a mildly jasmonate-deficient line (asLOX3). The differences among lines could be attributed to differences in damage from specific herbivores, which appeared to prefer either one or the other jasmonate-deficient phenotype. We further investigated the elicitation of one herbivore-induced volatile known to be jasmonate-regulated and to mediate resistance to herbivores: (E)-α-bergamotene. We found that JA was a more potent elicitor of (E)-α-bergamotene emission than was JA-Ile, and when treated with JA, irJAR4xirJAR6 plants emitted 20- to 40-fold as much (E)-α-bergamotene than WT. We conclude that JA-Ile regulates specific aspects of herbivore resistance in N. attenuata. This specificity may allow plants flexibility in their responses to herbivores and in managing trade-offs between resistance, vs. growth and reproduction, over the course of ontogeny.
Highlights
Plants employ sophisticated defense systems in response to herbivore attack
JAR4 and JAR6 may regulate conjugation of jasmonic acid (JA)-Leu, which cannot be analytically distinguished from JA-Ile via standard mass spectrometry (MS) analysis, Wang and colleagues showed that JA-Ile application to irJAR4xirJAR6 plants was sufficient to restore gene expression, nicotine and trypsin protease inhibitors (TPI) production, and resistance to M. sexta larvae, to WT levels
Two different hemizygous crosses generated from two different independently transformed lines per construct both accumulated only about 16% as much JA-Ile, but the same amount of JA as WT plants after herbivore elicitation; JAR4 and JAR6 transcripts were almost undetectable in Northern blots, in comparison to a strong signal for WT plants (Wang et al, 2008)
Summary
Plants employ sophisticated defense systems in response to herbivore attack. These include both direct defenses: traits which directly impair herbivore performance such as toxins, antifeedants, and repellents; and indirect defenses, which attract parasitoids or predators of attacking herbivores (Dicke and Baldwin, 2010; Mithöfer and Boland, 2012). Herbivory-induced direct and indirect defenses are regulated by complex signaling systems, activated when plants detect tissue damage and herbivore-derived chemical cues (Erb et al, 2012; Schuman and Baldwin, 2016). JA biosynthesis begins with the hydrolysis of 9,12,15-octadecatrienoic acid (18:3) fatty acids from membrane lipids in the chloroplast These fatty acids are oxygenated by 13-lipoxygenases (LOX) to 13Shydroperoxy-18:3 or−16:3 fatty acid peroxides, and further oxidized and cyclized, leading to the formation of (9S,13S)12-oxophytodeinoic acid (OPDA). The binding of JA-Ile to the SCFCOI1JAZ-InsP5 complex triggers the ubiquitination and degradation of the JAZ repressor(s) (Chini et al, 2007; Thines et al, 2007; Katsir et al, 2008). JA-Ileinduced JAZ degradation releases these transcription factors, permitting the activation of defense metabolite biosynthesis (De Geyter et al, 2012)
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