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Grass Roots Chemistry: Meta-Tyrosine, an Herbicidal Nonprotein Amino Acid

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Grass Roots Chemistry: Meta-Tyrosine, an Herbicidal Nonprotein Amino Acid Grass roots chemistry: meta-Tyrosine, an herbicidal nonprotein amino acid Ce´ cile Bertin†‡, Leslie A. Weston†, Tengfang Huang‡, Georg Jander‡, Thomas Owens§, Jerrold Meinwald¶ʈ, and Frank C. Schroeder¶ʈ Departments of †Horticulture, §Plant Biology, and ¶Chemistry and Chemical Biology and ‡Boyce Thompson Institute, Cornell University, Ithaca, NY 14853 Contributed by Jerrold Meinwald, July 31, 2007 (sent for review May 28, 2007) Fine fescue grasses displace neighboring plants by depositing large OH quantities of an aqueous phytotoxic root exudate in the soil O OH 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 NH2 NH2 than its structural isomers o- and p-tyrosine. We show that m- OH O tyrosine exposure results in growth inhibition for a wide range of juglone HO O HO O plant species and propose that the release of this nonprotein tyrosine m-tyrosine amino acid interferes with root development of competing plants. O "p-tyrosine" Acid hydrolysis of total root protein from Arabidopsis thaliana OH showed incorporation of m-tyrosine, suggesting this as a possible mechanism of phytotoxicity. m-Tyrosine inhibition of A. thaliana H3CO root growth is counteracted by exogenous addition of protein O sorgoleone amino acids, with phenylalanine having the most significant effect. Fig. 1. Structures of juglone, sorgoleone, the protein amino acid L-p- The discovery of m-tyrosine, as well as a further understanding of tyrosine, and its isomer, L-m-tyrosine. its mode(s) of action, could lead to the development of biorational approaches to weed control. inhibition of lettuce root growth, was selected for further allelopathy ͉ festuca ͉ rhizosphere ͉ root ecology ͉ Arabidopsis fractionation (Fig. 2) by reverse-phase column chromatography on C18-coated silica gel, followed by size exclusion chromatog- oot exudation of small molecules plays a major role in plant raphy with Sephadex LH20 beads. At all stages, biological Recosystems and is often associated with the development of activity was monitored by using the same filter paper assay. competitive advantage through allelopathy (1, 2). Juglone, a More than 80% of the resulting active fraction consisted of highly phytotoxic naphthoquinone produced by black walnut one major component, which was characterized without addi- (Juglans nigra L.), and sorgoleone, a substituted quinone from tional purification via a standard set of two-dimensional NMR sorghum (Sorghum spp.), are two classic examples of potently spectra,includingDQF-COSY,(1H,13C)-heteronuclearmultiple- active allelochemicals deposited via the plant’s living root system quantum correlation spectra, and (1H,13C)-heteronuclear mul- (Fig. 1) (3). Elucidation of the structures and mode of action of tiple-bond correlation spectra (6). The NMR-spectroscopic data previously unknown root-derived phytotoxins could lead to new suggested a 3Ј-substituted phenylalanine derivative as the struc- biorational approaches to weed control. ture of the major component. Additional analyses by high- Because of their stress tolerance and disease resistance, fescue resolution positive-ion electrospray mass spectrometry yielded a (Festuca spp.) grasses are commonly used in landscape, roadside, molecular formula of C9H11NO3. In combination with the results and pasture settings, as well as for conservation purposes (4, 5). from UV and infrared spectroscopic analysis, these data indi- The unusual ability of many fine leaf fescue species to outcom- cated that 3-hydroxyphenylalanine, commonly known as m- pete other plants is well known, and previous investigations tyrosine, is the major component of the active fraction isolated suggested that fescue root exudates have phytotoxic properties from the root exudates. This structural assignment was con- (4). Here, we report the isolation, identification, and biological firmed via an NMR-spectroscopic mixing experiment, whereby activity of m-tyrosine, a potent, structurally unusual broad- a small amount of synthetic m-tyrosine was added to the isolated spectrum phytotoxin exuded by the roots of some fine leaf fescue active fraction (7). Finally, the absolute configuration of the grasses. isolated m-tyrosine was determined to be L by NMR- spectroscopic comparison of its (S)-methoxytrifluoromethylphe- Results and Discussion nylacetic acid [(S)-MTPA] derivative with the (R)- and (S)- In an initial field evaluation of 80 fine fescue cultivars, 8 cultivars MTPA derivatives of synthetic m-tyrosine (8). with strong weed suppressive potential were identified and their allelopathic potential in laboratory settings was confirmed (4). Author contributions: C.B., L.A.W., G.J., T.O., and F.C.S. designed research; C.B., T.H., G.J., Based on both field and laboratory results, we selected ‘‘In- and F.C.S. performed research; C.B., T.H., G.J., and F.C.S. analyzed data; and L.A.W., G.J., trigue,’’ a common Chewing’s fescue cultivar (Festuca rubra L. J.M., and F.C.S. wrote the paper. ssp. commutata), for further studies. The authors declare no conflict of interest. To identify the allelopathic compound(s) contained in In- Abbreviations: MTPA, methoxytrifluoromethylphenylacetic acid; MS medium, Murashige trigue root exudates, we developed an activity-guided separation and Skoog medium. scheme based on the inhibition of lettuce (Lactuca sativa L.) See Commentary on page 16729. radicle elongation in a filter paper-based assay. By using this ʈTo whom correspondence may be addressed. E-mail: [email protected] or fs31@ assay, we compared the phytotoxicity of root surface washes cornell.edu. (hexanes, dichloromethane, methanol, and water) prepared This article contains supporting information online at www.pnas.org/cgi/content/full/ from 2-week-old Intrigue seedlings grown under soil-free con- 0707198104/DC1. ditions. The aqueous root wash, which showed the strongest © 2007 by The National Academy of Sciences of the USA 16964–16969 ͉ PNAS ͉ October 23, 2007 ͉ vol. 104 ͉ no. 43 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0707198104 Downloaded by guest on October 7, 2021 A A 1.8 1.6 SEE COMMENTARY )mc( htgnel toor ecutteL toor htgnel )mc( 1.4 160 µM 1.2 40 µM 80 µM 20 µM 1.0 control 0.8 0.6 Fresh roots crude extract 0.4 synthetic m-tyrosine 0.2 B H2O CH3OH CH2Cl2 Hexanes ** * o o 0.0 0 204080160 m-Tyrosine concentration (µµµM) Reversed-phase chromatography B 250 )lortnoc fo %( h %( fo )lortnoc H2O CH3OH:H2O CH3OHo ** * 200 Sephadex column 150 chromatography o-tyrosine t gn p-tyrosine e m-tyrosine l 100 1 ... … 8 9 10 t o o o ec or ** ** ECOLOGY HPLC + NMR/MS 50 u m-Tyrosine tteL 0 0 50 100 150 200 250 300 Fig. 2. Fractionation of fescue root exudates. (A) F. rubra rubra cv. Intrigue m-/o-/p-Tyrosine concentration (µµµM) roots. The slight yellowish discoloration near the root tips (arrows) indicates accumulation of root exudates on actively growing roots. (B) Activity-guided Fig. 3. Effect of m-tyrosine on lettuce. (A) Comparison of the effect of F. fraction of cv. Intrigue root exudates. Fractions are classified as strongly active rubra cv. Intrigue aqueous root exudate extract and authentic m-tyrosine on ( ), slightly active ( ), and not active (G) in our filter paper phytotoxicity assay ** * lettuce (L. sativa) seedling root growth (9). (Inset) Photograph of 3-day-old (7). 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). Analysis of aqueous extracts of root exudates from multiple fine fescue cultivars and related species showed that all Arizona fescue (F. arizonica), creeping red fescue (F. rubra ssp. rubra), tyrosine accounted for the majority of observed toxicity (Fig. and Chewing’s fescue (F. rubra ssp. commutata) cultivars pro- 3A). In assays using enantiomerically pure samples of m- duced large amounts of m-tyrosine, whereas hard (Festuca tyrosine, the D and L enantiomers proved equally effective in longifolia), sheep (Festuca ovina), and Idaho (Festuca idahoensis) inhibiting lettuce root growth, with the concentrations required fescues did not produce detectable amounts of m-tyrosine (9). to achieve 50% reduction of lettuce root growth (IC50) being 17 m-Tyrosine has been detected in only one other plant species, and 21 ␮M, respectively. Whereas lettuce roots exposed to Euphorbia myrsinitis (10), and we are not aware of any reports of m-tyrosine showed stunting and brownish, discolored roots, this nonprotein amino acid in natural soils. shoot growth of 5-day-old lettuce seedlings was only marginally HPLC analyses showed that m-tyrosine constitutes 33–43% of affected (Fig. 3A Inset). This could indicate that roots are the dry weight of Intrigue aqueous root exudate extract and is uniquely sensitive, or that m-tyrosine is not transported to the also an abundant metabolite in intact plant tissue. In 1-week-old shoots. After 7 days of m-tyrosine treatment, lettuce seedlings seedlings, m-tyrosine was 10-fold more abundant in roots (6,500 showed a significant reduction in shoot growth, possibly as a pmol/mg wet weight; mean Ϯ SD of n ϭ 6) than in leaves (590 Ϯ result of insufficient root development. In contrast to the root 160 pmol/mg wet weight; mean Ϯ SD of n ϭ 5). Free m-tyrosine growth inhibition by m-tyrosine, p-tyrosine and o-tyrosine ac- was present at much lower concentrations in seeds (24 Ϯ 8 tually stimulated lettuce root growth at concentrations as low as pmol/mg; mean Ϯ SD of n ϭ 6), suggesting that the biosynthesis 50 ␮M (Fig. 3B). of this metabolite is initiated after germination. Because me- Because our previous studies suggested that fine leaf fescue tabolite production is often highly dependent on plant age and may impact growth of a wide range of plant species (12), we environmental factors (11), the absolute amounts of m-tyrosine explored the m-tyrosine susceptibility of a selection of monocot produced by the various fescue species and cultivars will vary and dicot plants by measuring root growth in a filter paper assay with plant growth stage and in response to changes in growth [Fig.
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