Grass roots chemistry: meta-tyrosine, an herbicidal nonprotein amino acid

Abstract

Fine fescue grasses displace neighboring plants by depositing large quantities of an aqueous phytotoxic root exudate in the soil rhizosphere. Via activity-guided fractionation, we have isolated and identified the nonprotein amino acid m-tyrosine as the major active component. m-Tyrosine is significantly more phytotoxic than its structural isomers o- and p-tyrosine. We show that m-tyrosine exposure results in growth inhibition for a wide range of plant species and propose that the release of this nonprotein amino acid interferes with root development of competing plants. Acid hydrolysis of total root protein from Arabidopsis thaliana showed incorporation of m-tyrosine, suggesting this as a possible mechanism of phytotoxicity. m-Tyrosine inhibition of A. thaliana root growth is counteracted by exogenous addition of protein amino acids, with phenylalanine having the most significant effect. The discovery of m-tyrosine, as well as a further understanding of its mode(s) of action, could lead to the development of biorational approaches to weed control.

Fig. 1.

Structures of juglone, sorgoleone, the protein amino acid l-p-tyrosine, and its isomer, l-m-tyrosine.

Fig. 2.

Fractionation of fescue root exudates. (A) F. rubra rubra cv. Intrigue roots. The slight yellowish discoloration near the root tips (arrows) indicates accumulation of root exudates on actively growing roots. (B) Activity-guided fraction of cv. Intrigue root exudates. Fractions are classified as strongly active (**), slightly active (*), and not active () in our filter paper phytotoxicity assay (7).

Fig. 3.

Effect of m-tyrosine on lettuce. (A) Comparison of the effect of F. rubra cv. Intrigue aqueous root exudate extract and authentic m-tyrosine on lettuce (L. sativa) seedling root growth (9). (Inset) Photograph of 3-day-old lettuce seedlings exposed to various concentrations of aqueous root exudate extract, showing stunted growth and discoloration of root tips. (B) Effect of o-, m-, and p-tyrosine on lettuce seedling radicle elongation (9).

Fig. 4.

Effect of m-tyrosine on other plant species. (A) Effect of m-tyrosine on fescue. m-Tyrosine-producing F. rubra ssp. commutata (Intrigue, Sandpiper) is unaffected, whereas m-tyrosine nonproducing F. longifolia (Oxford) and F. ovina var. glauca (blue fescue) show strong root growth inhibition. (B and C) Effect of m-tyrosine on seedling radicle elongation for several common weed and crop species. For additional species examples, see SI Table 1.

Fig. 5.

m-Tyrosine inhibition and amino acid rescue of Arabidopsis root growth. (A) Photograph of 5-day-old Arabidopsis seedlings exposed to a series of m-tyrosine concentrations. (B) Rescue of 3 μM m-tyrosine toxicity by 40 μM or individual amino acids or NH₄NO₃. Root length after 1 week of growth on MS agar with 3 μM m-tyrosine and other amino acids at 40 μM. Shown is mean ± SD of n = 16–23. *, P < 0.01; t test, relative to the 3 μM m-tyrosine-only treatment.