The dynamic response of the Arabidopsis root metabolome to auxin and ethylene is not predicted by changes in the transcriptome

Abstract

While the effects of phytohormones on plant gene expression have been well characterized, comparatively little is known about how hormones influence metabolite profiles. This study examined the effects of elevated auxin and ethylene on the metabolome of Arabidopsis roots using a highresolution 24 h time course, conducted in parallel to time-matched transcriptomic analyses. Mass spectrometry using orthogonal UPLC separation strategies (reversed phase and HILIC) in both positive and negative ionization modes was used to maximize identification of metabolites with altered levels. The findings show that the root metabolome responds rapidly to hormone stimulus and that compounds belonging to the same class of metabolites exhibit similar changes. The responses were dominated by changes in phenylpropanoid, glucosinolate, and fatty acid metabolism, although the nature and timing of the response was unique for each hormone. These alterations in the metabolome were not directly predicted by the corresponding transcriptome data, suggesting that post-transcriptional events such as changes in enzyme activity and/or transport processes drove the observed changes in the metabolome. These findings underscore the need to better understand the biochemical mechanisms underlying the temporal reconfiguration of plant metabolism, especially in relation to the hormone-metabolome interface and its subsequent physiological and morphological effects.are available in the supplementary materials (Table S1). Data mining for the specific metabolites rutin, IAA and ACC was performed by searching the detected masses of the features in the XCMS positive datasets for masses corresponding to [M + H] + ions and the negative XCMS datasets for masses corresponding to [M − H] − ions. Features were not observed that corresponded to either IAA or ACC, while the details regarding the assignment of rutin are included in Table S1. transcriptome data analysis. Microarray datasets for root samples generated under identical conditions 11,12 were examined for changes in the expression of genes associated with the synthesis, inactivation, or transport of hormone-responsive metabolites, identified from the KEGG database 78 or the recent literature (e.g., in the case of members of the GH, DAO, and PIN families). Results for genes exhibiting a SLR of ≥ 0.5 or ≤ −0.5 in all three biological replicates for at least one time point are presented in Tables 4 and 5, with the data for all examined genes provided in Datafile S5.

Ethylene signaling in plants

“…Thus EIN2-C provides both transcriptional and translational control to regulate EIN3 and the related EIL1 transcription factor to cause most ethylene responses. This is supported by a recent study where ethylene-stimulated changes in the metabolome did not always correlate with changes in the transcriptome (138). The exception to this model is that short-term, transient responses occur independently of these transcription factors, yet require EIN2 (101).…”

“…Additionally, research has identified specific histone acetylation marks that are important in ethyleneregulated gene expression by EIN3 (145)(146)(147). Even though more details about transcriptional regulation are being discovered, it is also clear from a recent metabolome study that changes in metabolism occur in response to ethylene that are not predicted by changes in the transcriptome (138). This indicates that there is additional regulation for responses to this hormone.…”

Advances in Plant Metabolomics and Its Applications in Stress and Single-Cell Biology

“…For examples, integrative metabolomics and proteomics revealed the intricate balance between JA and SA in the MAP kinase (MPK) 4-mediated plant immune response [153]. Increases of both auxin and ethylene caused changes in phenylpropanoid, glucosinolate, and fatty acid metabolism in Arabidopsis root metabolome, and the changes correlated negatively with the corresponding transcriptome data [154], indicating post-transcriptional events such as changes in enzyme activity and/or transport processes played a role in the metabolomic changes. Stomatal guard cells have been used as a model system for studying hormone function and crosstalk.…”

Dissection of full-length transcriptome and metabolome of Dichocarpum (Ranunculaceae): implications in evolution of specialized metabolism of Ranunculales medicinal plants

“…In a comprehensive analysis of metabolome and transcriptome of Arabidopsis thaliana over-expressing a MYB transcription factor, novel genes involved in flavonoid biosynthesis and novel anthocyanins were identified. Nevertheless, given the post-transcriptional modification and other levels of regulation, the dynamic response of the Arabidopsis metabolome to various factors may not be predicted by transcriptome changes ( Hildreth et al, 2020 ). The clues of regulatory mechanisms in Dichocarpum could also be identified by the integration of non-targeted metabolomics and full-length transcriptomics to gain a more objective understanding of the association between genes and specialized metabolites.…”