Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs

Abstract

Plants resist infection and herbivory with innate immune responses that are often associated with reduced growth. Despite the importance of growth-defense tradeoffs in shaping plant productivity in natural and agricultural ecosystems, the molecular mechanisms that link growth and immunity are poorly understood. Here, we demonstrate that growth-defense tradeoffs mediated by the hormone jasmonate are uncoupled in an Arabidopsis mutant (jazQ phyB) lacking a quintet of Jasmonate ZIM-domain transcriptional repressors and the photoreceptor phyB. Analysis of epistatic interactions between jazQ and phyB reveal that growth inhibition associated with enhanced anti-insect resistance is likely not caused by diversion of photoassimilates from growth to defense but rather by a conserved transcriptional network that is hardwired to attenuate growth upon activation of jasmonate signalling. The ability to unlock growth-defense tradeoffs through relief of transcription repression provides an approach to assemble functional plant traits in new and potentially useful ways.

Molecular Profiles of Contrasting Shade Response Strategies in Wild Plants: Differential Control of Immunity and Shoot Elongation

“…We show here that G. robertianum, which occurs in forest understories, enhances its immunity against the fungal pathogen B. cinerea upon shade detection, rather than the reduced immunity observed in shade avoiding Arabidopsis and G. pyrenaicum. The mechanism through which low R:FR reduces pathogen resistance in shade-intolerant plants is not yet fully established but involves upregulation of the JAZ proteins, which are negative regulators of the JA pathway (Moreno et al, 2009;Cerrudo et al, 2012;Campos et al, 2016). Indeed, the Geranium ortholog of JAZ3 (OMCL7907) is induced by low R:FR in the evening in G. pyrenaicum, but not in G. robertianum ( Figure 5B).…”

RXLR Effector AVR2 Up-Regulates a Brassinosteroid-Responsive bHLH Transcription Factor to Suppress Immunity

“…Although there is some evidence in the literature indicating that growth and defense can be regulated simultaneously (Francisco et al, 2016;Campos et al, 2016;de Wit et al, 2013), much of the research done in the area of growth and immunity has shown that activation of plant defense responses requires a major reallocation of resources away from growth to immunity (Huot et al, 2014). Consequently, plants must tightly regulate and fine-tune the signals that control this trade-off.…”

The Role of Specialized Photoreceptors in the Protection of Energy‐Rich Tissues

“…The clearest examples of these trade-offs are constitutive defense mutants in which growth is severely hindered [45][46][47][48][49][50]. Photosynthesis is often reported to be decreased during defense responses, which would reduce growth and biomass if resources are limiting [51,52].…”

“…Chlorophyll degradation itself may be a defensive strategy, as degradation products have anti-insect activity [56]. Other studies have shown that photosynthetic rates are not perturbed when defense responses are activated in the absence of physical damage, suggesting that some reports of decreased photosynthesis could be a consequence of physical damage (e.g., localized water loss from disrupted cells) [48,49,57]. Importantly, active defense responses trigger reduced growth without a corresponding reduction in photosynthesis, demonstrating that decreased photosynthesis is not the main cause of reduced growth during defense responses [48,49].…”

“…Defense suppression is also uncoupled from SAS in the jaz10 phyB double mutant, which maintains constitutive SAS but with wild type JA sensitivity [91]. These points of cross-talk among growth and defense signaling pathways are establishing how complex networks of regulators govern these processes to properly respond to external conditions [49,95,96]. An emerging question is whether we can use the knowledge of these networks to manipulate growth-defense trade-offs (see Section 7 below).…”