Stress-Related Mitogen-Activated Protein Kinases Stimulate the Accumulation of Small Molecules and Proteins in Arabidopsis thaliana Root Exudates

Abstract

A delicate balance in cellular signaling is required for plants to respond to microorganisms or to changes in their environment. Mitogen-activated protein kinase (MAPK) cascades are one of the signaling modules that mediate transduction of extracellular microbial signals into appropriate cellular responses. Here, we employ a transgenic system that simulates activation of two pathogen/stress-responsive MAPKs to study release of metabolites and proteins into root exudates. The premise is based on our previous proteomics study that suggests upregulation of secretory processes in this transgenic system. An advantage of this experimental set-up is the direct focus on MAPK-regulated processes without the confounding complications of other signaling pathways activated by exposure to microbes or microbial molecules. Using non-targeted metabolomics and proteomics studies, we show that MAPK activation can indeed drive the appearance of dipeptides, defense-related metabolites and proteins in root apoplastic fluid. However, the relative levels of other compounds in the exudates were decreased. This points to a bidirectional control of metabolite and protein release into the apoplast. The putative roles for some of the identified apoplastic metabolites and proteins are discussed with respect to possible antimicrobial/defense or allelopathic properties. Overall, our findings demonstrate that sustained activation of MAPKs alters the composition of apoplastic root metabolites and proteins, presumably to influence the plant-microbe interactions in the rhizosphere. The reported metabolomics and proteomics data are available via Metabolights (Identifier: MTBLS441) and ProteomeXchange (Identifier: PXD006328), respectively.

Multi-omics analysis of early leaf development in Arabidopsis thaliana

“…However, this view has been challenged by a number of recent studies reporting dipeptides emerging as novel small-molecule regulators at the interface of protein degradation and metabolism. 28 , 29 , 30 , 31 , 32 , 33 Consistent with such a role, we report a number of dipeptides whose accumulation changes across early leaf development and are either proliferation or expansion specific, making them intriguing targets for detailed functional characterization.…”

Autophagy is responsible for the accumulation of proteogenic dipeptides in response to heat stress in Arabidopsis thaliana

“…In addition to the already given examples (see Introduction), dipeptides were shown, for instance, to activate the p38MAPK‐Smad3 signaling pathway in the rare chronic myelogenous leukemia (CML) stem cell population, and in line, pharmacological inhibition of dipeptide uptake inhibited CML stem cell activity [22]. Dipeptides were also reproducibly measured in the Arabidopsis root exudates, downstream of MPK3/6 signaling, suggesting a role in plant–microbe and plant–plant communication [23]. An inhibitory effect of five different dipeptides on maize root growth was reported previously, supporting such a role [24], while phenylalanine‐containing dipeptides accumulate in wheat upon treatment with deoxynivalenol, the major toxin and virulence factor of the fungal pathogen Fusarium graminearum [25].…”

pH effects on plant calcium fluxes: lessons from acidification-mediated calcium elevation induced by the γ-glutamyl-leucine dipeptide identified from Phytophthora infestans

“…infestans mycelium, its physiological function is unknown. In fact, the roles of most naturally occurring dipeptides are unknown; this includes the many dipeptides found in Arabidopsis root exudates 68 – 70 . Here, it is noteworthy that in the food industry, γ-Glu-Leu belongs to the so-called Kokumi taste-enhancing dipeptide family that is found, among others, in beans and mature cheese 71 , 72 .…”