The Phytotoxicity of Meta-Tyrosine Is Associated With Altered Phenylalanine Metabolism and Misincorporation of This Non-Proteinogenic Phe-Analog to the Plant's Proteome

Abstract

Plants produce a myriad of specialized (secondary) metabolites that are highly diverse chemically, and exhibit distinct biological functions. Here, we focus on meta-tyrosine (m-tyrosine), a non-proteinogenic byproduct that is often formed by a direct oxidation of phenylalanine (Phe). Some plant species (e.g., Euphorbia myrsinites and Festuca rubra) produce and accumulate high levels of m-tyrosine in their root-tips via enzymatic pathways. Upon its release to soil, the Phe-analog, m-tyrosine, affects early post-germination development (i.e., altered root development, cotyledon or leaf chlorosis, and retarded growth) of nearby plant life. However, the molecular basis of m-tyrosine-mediated (phyto)toxicity remains, to date, insufficiently understood and are still awaiting their functional characterization. It is anticipated that upon its uptake, mtyrosine impairs key metabolic processes, or affects essential cellular activities in the plant. Here, we provide evidences that the phytotoxic effects of m-tyrosine involve two distinct molecular pathways. These include reduced steady state levels of several amino acids, and in particularly altered biosynthesis of the phenylalanine (Phe), an essential a-amino acid, which is also required for the folding and activities of proteins. In addition, proteomic studies indicate that m-tyrosine is misincorporated in place of Phe, mainly into the plant organellar proteomes. These data are supported by analyses of adt mutants, which are affected in Phe-metabolism, as well as of var2 mutants, which lack FtsH2, a major component of the chloroplast FtsH proteolytic machinery, which show higher sensitivity to m-tyrosine. Plants treated with m-tyrosine show organellar biogenesis defects, reduced respiration and photosynthetic activities and growth and developmental defect phenotypes.

Field evaluation of weed suppression in fine fescue (Festuca spp.)

“…Assumptions could therefore be made that the ST and CH accessions tested in our study also would have this allelopathic ability. Oxidation of phenylalanine results in the formation of L‐ m tyrosine, and incorporation of this nonproteinogenic amino acid in lieu of phenylalanine during protein synthesis can negatively affect protein folding and further metabolic function (Zer et al., 2020). In fact, this known allelochemical has been shown to reduce the growth of several plant seedlings including large crabgrass (Bertin et al., 2003; Bertin et al., 2007; Zer et al., 2020); hence, the decrease of smooth crabgrass biomass observed with these accessions could be attributed to L‐ m ‐tyrosine.…”

“…Oxidation of phenylalanine results in the formation of L-m tyrosine, and incorporation of this nonproteinogenic amino acid in lieu of phenylalanine during protein synthesis can negatively affect protein folding and further metabolic function (Zer et al, 2020). In fact, this known allelochemical has been shown to reduce the growth of several plant seedlings including large crabgrass (Bertin et al, 2003;Bertin et al, 2007;Zer et al, 2020); hence, the decrease of smooth crabgrass biomass observed with these accessions could be attributed to L-mtyrosine. However, to what extent L-m-tyrosine aids in weed suppression in the field is unknown; for example, if all CH and ST cultivars in F. rubra L. aggregate exude this allelochemical, then why are all not weed suppressive?…”

Review: Allelochemicals as multi‐kingdom plant defence compounds: towards an integrated approach

“…91 Leaf necrosis has also been reported in m-tyrosine-treated Arabidopsis at a concentration of 40 μM. 92 Nonprotein amino acids are thought to have phytotoxic properties through their substitution of protein amino acids during translation, modifying protein folding as a result. 73 This mode of action has recently been verified for m-tyrosine, which is specifically misincorporated in place of phenylalanine.…”

“…73 This mode of action has recently been verified for m-tyrosine, which is specifically misincorporated in place of phenylalanine. 92 Despite its apparent specificity to plant proteins in terms of their mode of action, 73 there is evidence of allelopathy towards other organisms by m-tyrosine. A higher concentration than that required to confer phytoallelopathy (50 mM) results in antifeedant and toxic effects on the termite Coptotermes formosanus.…”

“…Arabidopsis root tip browning was observed in the phytoallelopathic activity of m ‐tyrosine, indicative of cell necrosis 91 . Leaf necrosis has also been reported in m ‐tyrosine‐treated Arabidopsis at a concentration of 40 μ m 92 . Nonprotein amino acids are thought to have phytotoxic properties through their substitution of protein amino acids during translation, modifying protein folding as a result 73 .…”