How plants handle multiple stresses: hormonal interactions underlying responses to abiotic stress and insect herbivory

Abstract

Adaptive plant responses to specific abiotic stresses or biotic agents are fine-tuned by a network of hormonal signaling cascades, including abscisic acid (ABA), ethylene, jasmonic acid (JA) and salicylic acid. Moreover, hormonal cross-talk modulates plant responses to abiotic stresses and defenses against insect herbivores when they occur simultaneously. How such interactions affect plant responses under multiple stresses, however, is less understood, even though this may frequently occur in natural environments. Here, we review our current knowledge on how hormonal signaling regulates abiotic stress responses and defenses against insects, and discuss the few recent studies that attempted to dissect hormonal interactions occurring under simultaneous abiotic stress and herbivory. Based on this we hypothesize that drought stress enhances insect resistance due to synergistic interactions between JA and ABA signaling. Responses to flooding or waterlogging involve ethylene signaling, which likely reduces plant resistance to chewing herbivores due to its negative cross-talk with JA. However, the outcome of interactions between biotic and abiotic stress signaling is often plant and/or insect species-dependent and cannot simply be predicted based on general knowledge on the involvement of signaling pathways in single stress responses. More experimental data on non-model plant and insect species are needed to reveal general patterns and better understand the molecular mechanisms allowing plants to optimize their responses in complex environments.

Keywords: Drought; Flooding; Herbivory; Hormonal cross-talk; Induced resistance; Stress responses.

Fig. 1

Schematic overview of hormonal signaling. a A model of jasmonic acid (JA) signaling, adapted from Pauwels et al. (2010). In the absence of JA, JAZs recruit the co-repressor TPL and TPRs via the EAR motif of the adaptor protein NINJA to suppress JA-responsive gene expression. This can also occur directly via the JAZ’s EAR motif (Shyu et al. 2012). In the presence of JA, JA-isoleucine conjugates are formed and facilitate the interaction between JAZs and SCF^COI1, a multi-protein E3 ubiquitin ligase complex. This promotes JAZ ubiquitination and subsequent degradation by 26S proteasomes, resulting in the release of NINJA-TPL complex and activation of basic helix-loop-helix MYC transcription factors (TFs) to regulate JA-responsive genes. b A model for abscisic acid (ABA) signaling, adapted from Cutler et al. (2010). In the absence of ABA, PP2Cs are active to prevent SnRK2 activity. In the presence of ABA, PYR/PYL/RCARs bind to and inhibit PP2Cs, which allows phosphorylated SnRK2s to accumulate and subsequently phosphorylate ABFs to regulate ABA-responsive gene expression. c A model of ethylene (ET) signaling, adapted from Cho and Yoo (2014). In the absence of ET, the negative regulator CTR1 binds to membrane-bound ET receptors (ETRs) and inactivate the positive regulator EIN2. Moreover, the downstream primary TFs, EIN3 and EIL1, are constantly subjected to proteasomal degradation guided by EBF1 and EBF2. When ET has accumulated and binds to ET receptors, the ETR-CTR1 is inactivated. This leads to cleavage of C-terminal half of EIN2 and its translocation into nucleus to stabilize EIN3 by inactivating EBFs. EIN3 then regulates expression of downstream ET-responsive AP2/ERF TFs, such as ERF1 and ORA59

Fig. 2

Schematic representation of interactions between hormonal cascades regulating induced defenses against biotic agents (see text and legend Fig. 1 for further details and abbreviations). Insect herbivores induce JA-dependent MYC2 regulation of defense-related genes, which is enahnced by ABA signaling. Necrotrophic pathogens induce JA/ET-dependent signaling to regulate ERF1 and ORA59 and downstream defense-related genes. The two branches of defense responses mutually antagonize one another. GA and SA signaling generally inhibit JA-dependent defense responses

Fig. 3

Hormonal interactions regulating plant responses to abiotic stresses and defenses against biotic agents. Arrow heads indicate a positive interaction, whereas a T end, indicates an inhibitory effect. Abscisic acid (ABA) has strong synergistic effects on JA-dependent defenses, while jasmonic acid (JA) promotes ABA-mediated stomatal closure and leaf senescence, but not primary root growth. Dashed arrows indicate the mixed effects of ethylene (ET) on JA-dependent defenses: ET induces defense responses to necrotrophic pathogens and some responses to insect herbivores but suppresses other insect induced defenses. ABA and ET strongly antagonize each other in many responses, but both induce leaf senescence. Interactions between JA and gibberellic acid (GA) or auxin (AUX) to mediate growth-defense balance are also indicated