Major Signaling Pathways Modulate Arabidopsis Glucosinolate Accumulation and Response to Both Phloem-Feeding and Chewing Insects

Abstract

Plant responses to enemies are coordinated by several interacting signaling systems. Molecular and genetic studies with mutants and exogenous signal application suggest that jasmonate (JA)-, salicylate (SA)-, and ethylene (ET)-mediated pathways modulate expression of portions of the defense phenotype in Arabidopsis (Arabidopsis thaliana), but have not yet linked these observations directly with plant responses to insect attack. We compared the glucosinolate (GS) profiles of rosette leaves of 4-week-old mutant and transgenic Arabidopsis (Columbia) plants compromised in these three major signaling pathways, and characterized responses by those plants to feeding by two phloem-feeding aphids (generalist Myzus persicae and specialist Brevicoryne brassicae) and one generalist caterpillar species (Spodoptera exigua Hubner). Blocked JA signaling in coronatine-insensitive (coi1) and enhanced expression of SA-signaled disease resistance in hypersensitive response-like (hrl1) mutants reduced constitutive GS concentrations, while blocking SA signaling at the mediator protein npr1 mutant (NPR) increased them. There was no significant impact on constitutive GS contents of blocking ET signaling (at ETresistant [etr1]) or reducing SA concentrations (nahG transgene). We found increased GS accumulation in response to insect feeding, which required functional NPR1 and ETR1 but not COI1 or SA. Insect feeding caused increases primarily in short-chain aliphatic methylsulfinyl GS. By contrast, responses to exogenous JA, a frequent experimental surrogate for insect attack, were characterized by an increase in indolyl GS. Insect performance, measured as population increase or weight increase, was negatively related to GS levels, but we found evidence that other, ET-regulated factors may also be influential. Plant resistance to (consumption by) S. exigua was not related to insect growth because some plant chemistries inhibited growth while others inhibited feeding. These major signaling pathways modulate Arabidopsis GS accumulation and response to both phloem-feeding and chewing insects, often antagonistically; NPR appears to be central to these interactions. Our results indicate that exogenous signal application and plant consumption measures may not provide useful measures of plant responses to actual insect feeding.Plants have developed diverse defense mechanisms for dealing with enemies. Like all plants in the Brassicaceae, Arabidopsis (Arabidopsis thaliana) produces secondary metabolites, including glucosinolates (GS), phenolics, and terpenoids (Halkier, 1999;Madhuri and Reddy, 1999;Harrewijn et al., 2001;Mikkelsen et al., 2003), which may have defensive functions. GS are found mainly in the order Brassicales, which includes the Brassicaceae (Giamoustaris and Mithen, 1995;Tierens et al., 2001), where they function in defense against herbivores and pathogens. GS are sulfonated thioglycosides comprising a common glycone moiety with a variable aglycone side chain. Three major classes of GS are distinguished: aliphatic GS derived princi...

Intraspecific variation in defense against a generalist lepidopteran herbivore in populations of Eruca sativa (Mill.)

“…2003; Mewis et al. 2005, 2006), while SA signaling has been shown to suppress GS accumulation (Mewis et al. 2006).…”

Interaction between MYC2 and ETHYLENE INSENSITIVE3 Modulates Antagonism between Jasmonate and Ethylene Signaling inArabidopsis

“…However, such a synergistic regulatory model is inconsistent with the antagonistic roles of JA and ET signaling in many important processes. For example, JA antagonizes ET to repress apical hook formation (e.g., exaggerated hook formation in the coi1 mutant) (Figures 1 and 2) (Turner et al, 2002), whereas ET antagonizes JA to repress the expression of wound-responsive genes (VSP1, VSP2, and TAT3) and herbivore-inducible genes (CYP79B3, BCAT4, and BAT5) ( Figures 9A and 9B) (Rojo et al, 1999;Mikkelsen et al, 2003) and to attenuate plant defense against generalist herbivores ( Figures 9C and 9D) (Stotz et al, 2000;Mewis et al, 2005Mewis et al, , 2006Bodenhausen and Reymond, 2007).…”

“…On the other hand, in the ET signaling mutants (e.g., ein3 eil1 and ein2), the absence of EIN3 and EIL1 enables MYC2, MYC3, and MYC4 to induce the expression of wound-responsive genes (VSP1, VSP2, and TAT3) ( Figure 9A) (Rojo et al, 1999;Lorenzo et al, 2004) and herbivore-inducible genes (CYP79B3, BCAT4, and BAT5), and enhances plant defense against the herbivores S. littoralis and S. exigua (Figures 4, 8, 9, and 10A) (Stotz et al, 2000;Mewis et al, 2005Mewis et al, , 2006Bodenhausen and Reymond, 2007). In wild-type plants, antagonistic regulation between the ET-stabilized transcription factors (EIN3 and EIL1) and the JAactivated transcription factors (MYC2, MYC3, and MYC4) would lead to suitable expression of MYC2-dependent genes (VSP1, VSP2, TAT3, CYP79B3, BCAT4, and BAT5) and EIN3-regulated genes (HLS1, ERF1, ORA59, and PDF1.2), resulting in proper plant responses, such as hook formation and defense against the herbivores S. littoralis and S. exigua.…”

“…wound-responsive and herbivory-inducible genes ( Figures 9A and 9B), the myc2 myc3 myc4 triple mutant, which was almost completely devoid of glucosinolates (Schweizer et al, 2013), exhibited susceptibility to the generalist herbivores Spodoptera littoralis (Schweizer et al, 2013) and Spodoptera exigua ( Figures 9C and 9D), while plant defense against these generalist herbivores was enhanced in the ET-signaling mutants ein3 eil1 ( Figures 9C and 9D), etr1, and ein2 (Stotz et al, 2000;Mewis et al, 2005Mewis et al, , 2006Bodenhausen and Reymond, 2007). These results demonstrate that the abolishment of EIN3 and EIL1 derepresses MYC2, which enhances the expression of wound-responsive and herbivore-inducible genes and elevates plant defenses against generalist herbivores.…”

“…JA represses apical hook formation (Turner et al, 2002) and positively regulates plant defense against insect attack (Fernández-Calvo et al, 2011;Schweizer et al, 2013), while ET functions oppositely (Guzmán and Ecker, 1990;Mewis et al, 2005Mewis et al, , 2006Bodenhausen and Reymond, 2007). However, the molecular mechanism for such antagonism between JA and ET signaling remains unclear.…”