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, m-tyrosine 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 α-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.
Highlights
The chemical diversity of terrestrial plants is truly exceptional
Primary metabolites that are associated with essential cellular functions, e.g., nucleotides, amino acids, fatty acids, sugars, and organic acids, which are typically present in all organisms and cells
Our study focuses on meta-tyrosine (m-tyrosine, or m-Tyr), an oxidized byproduct of the aromatic amino acid phenylalanine, which inhibits early post-germination and seedling growth (Bertin et al, 2007; Bertin et al, 2009)
Summary
Plants are estimated to produce hundreds of thousands of different metabolites, probably the largest number among all other species (see e.g., Moghe and Last, 2015; Wurtzel and Kutchan, 2016; Obata, 2019) Such an exceptional diversity may be a consequence of the large diversification and rapid evolution of specialized metabolic pathways in plants since they occupied the terrestrial environment, about 500 million years ago (Morris et al, 2018). In E. myrsinites, m-tyrosine is produced via a transamination of m-hydroxyphenylpyruvate (Mothes et al, 1964), whereas the biosynthesis of m-tyrosine in F. rubra is mediated directly through the hydroxylation of phenylalanine (Bertin et al, 2007; Huang et al, 2012) These data indicate that different plants utilize m-tyrosine as a phytotoxic allelochemical using distinct metabolic pathways, activities which likely arose independently during the evolution of land plants (Huang et al, 2012). Proteomic analyses of young Arabidopsis seedlings, grown in the absence or presence of m-tyrosine, strongly support that m-tyrosine is misincorporated instead of Phe to various organellar (i.e., mitochondrial and plastidial) proteins, an activity which is likely mediated by a duallylocalized organellar phenylalanine-transfer RNA (tRNA) synthetase (PheRS) enzyme (Duchêne et al, 2005)
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