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The Emergence of Grass Root Chemical Ecology

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The Emergence of Grass Root Chemical Ecology COMMENTARY The emergence of grass root chemical ecology Stephen O. Duke* Natural Products Utilization Research Unit, Agricultural Research Service, U.S. Department of Agriculture, P.O. Box 8048, University, MS 38677 llelopathy is defined by most isoxazolin-5-on-2yl)-alanine, which inhib- converted to L-DOPA, a known phyto- scientists as the adverse effect its root growth on nonlegume plant toxin. Bertin et al. state that this is un- of one plant species on another species (12), although this nonprotein likely because L-DOPA is significantly through production of phyto- amino acid is much less phytotoxic than less phytotoxic than m-tyrosine. How- Atoxins (allelochemicals), although more m-tyrosine. ever, m-tyrosine might be taken up expansive definitions have been formu- Finding that m-tyrosine is a potent more readily by plant cells than lated. Allelopathy is but one component phytotoxin leads to many interesting L-DOPA, leaving conversion to L-DOPA of plant/plant interference, the other questions deserving further inquiry. as a potentially more limiting step. Can being competition for resources such as First, how does the producing species m-tyrosine be converted to L-DOPA by nutrients, light, and water. Allelopathy protect itself from autotoxicity? It seems a cell-free extract of a species suscepti- has been a recognized phenomenon for that m-tyrosine is broadly phytotoxic ble to m-tyrosine? If so, is the process many years (1), but prominent ecologists with some differences in plant species highly efficient in vivo? Synthetic pro- have argued that allelopathy is seldom susceptibility, so what mechanism does herbicides that are inactive at the molec- a significant component of interference the producing plant use to avoid the ular target site are much more effective (e.g., ref. 2). This point of view was bol- effects seen on other species? Does the when applied to intact plants than the stered by the lack of scientific rigor of plant avoid accumulation of the com- active molecule to which they are con- much of the allelopathy research that verted in vivo. This is caused by superior attempted to explain allelopathy through cuticular and cellular uptake of the pro- the effects of known, weakly phytotoxic, Allelopathy has been a herbicide. Some potent natural phyto- easy-to-quantify phytochemicals such as toxins, such as hydantocidin (15), are ferulic acid. More recent studies using recognized phenomenon protoxins. bioassay-guided isolation and subse- How does the plant synthesize m- quent structure determination of potent, for many years. tyrosine? L-phenylalanine is a precur- root-exuded phytotoxins built strong sor of m-tyrosine synthesis in at least evidence for allelopathy, especially in some animal systems (16). Will isotopi- grass species (reviewed in refs. 3–5, and pound by secreting it almost as quickly cally labeled phenylalanine fed to roots see Table 1). The article by Bertin et al. as it is produced, in a manner similar to or cell-free preparations of roots of (6) in this issue of PNAS adds signifi- that of Sorghum species that produce allelopathic fescue generate labeled cantly to this growing body of support- the allelochemical sorgoleone only in m-tyrosine? If production of m- ive literature. root hairs that secrete it rapidly (13)? tyrosine is caused by one enzyme, can The work provides clear evidence of Apparently this is not the mechanism, the gene for it be manipulated to pro- a novel, root-exuded allelochemical because Bertin et al. (6) indicate that duce fescue lines with enhanced allelo- produced by an allelopathic grass, a although the dry weight of the root exu- pathic activity or to impart allelopathy variety of a Festuca rubra subspecies. It date consists of up to 43% m-tyrosine, it establishes that m-tyrosine is a highly to other species? The genetic compo- active allelochemical causing most, if is also a relatively abundant metabolite nents for root-specific production and not all, of the effects of the root exu- of the root. Is the compound seques- secretion, as well as resistance, might date of this allelopathic fescue variety tered into intracellular or intercellular be required for practical success. Nev- described in that article and an earlier locations where it can do little or no ertheless, this could be a simpler ap- one (7). harm? Duke et al. (14) discuss this proach to transgenically producing Although some nonprotein amino ac- strategy for avoidance of allelochemical weed-fighting plants than genetically ids have functions in plant primary me- autotoxicity. Bertin et al. (7) found in- engineering whole biosynthetic path- tabolism (e.g., ␦-aminolevulinic acid), tracellular bodies in roots that might be ways (e.g., ref. 17). others are thought to be involved in associated with m-tyrosine sequestra- Chemicals from target plant species protection of plants from a variety of tion. Or, is the plant resistant at a have recently been found to induce both biotic threats, particularly herbivores. molecular target site? If the latter, this rice (18) and sorghum (19) to increase The modes of action of these com- information could be helpful in determi- biosynthesis of their root-secreted pounds range from direct neurotoxicity, nation of the mechanism of action of allelochemicals, although in both cases, such as produced by ␤-N-methylamino- m-tyrosine on target species. synthesis is constitutive. This pheno- L-alanine (8), to incorporation into pro- Bertin et al. (6) have circumstantial menon has not been explored with teins to produce aberrant molecules, evidence that the mode of action of m- m-tyrosine synthesis, but water stress leading to multiple physiological prob- tyrosine is similar to that of some other was found to increase its production (7). lems (9). Nonprotein amino acids have nonprotein amino acids. That is, it sub- In summary, the work of Bertin et al. previously been implicated in allelopa- stitutes for at least one protein amino (6) provides another convincing example thy. For example, mimosine has been acid (apparently phenylalanine in this of allelopathy, complete with the identi- associated with allelopathy of the le- case) during translation, resulting in dys- gume tree Leucaena leucocephala (10). functional proteins. Demonstration of L-DOPA, a compound structurally re- significant loss of specific activity of Author contributions: S.O.D. wrote the paper. lated to m-tyrosine, has been implicated phenylalanine-containing enzymes The author declares no conflict of interest. in allelopathy of Mucuna pruriens (11). would support this hypothesis. An alter- See companion article on page 16964. Roots of pea (Pisum sativa) exude ␤-(3- native hypothesis is that m-tyrosine is *E-mail: [email protected]. www.pnas.org͞cgi͞doi͞10.1073͞pnas.0707837104 PNAS ͉ October 23, 2007 ͉ vol. 104 ͉ no. 43 ͉ 16729–16730 Downloaded by guest on October 1, 2021 Table 1. Highly phytotoxic root-secreted allelochemicals by grasses (5, 6) Induced by Species Allelochemicals other species Mode of action Sorghum spp. Sorgoleone Yes Photosystem II inhibition p-hydroxyphenylpyruvate dioxygenase inhibition Oryza sativa 5,7,4Ј-trihydoxy-3Ј,5Ј-dimethoxyflavone, Yes Unknown 2-isopropyl-5-acetoxy-cyclohexene-2-one-1, momilactone B F. rubra m-tyrosine ? Dysfunctional proteins? DOPA formation? Other? fication of a highly potent allelochemical viable alternatives to synthetic herbi- the widespread use of synthetic herbi- and a credible means of delivery to tar- cides, the most heavily used of all pesti- cides. The genetic information resulting get plants. Practical applications of such cides. The most successful transgenic from recent findings in allelopathy such findings are potentially significant. crops are those with transgenes impart- as those reported by Bertin et al. has the There are currently few economically ing herbicide resistance (20), sustaining potential to alter this situation. 1. Willis RJ (1985) J History Biol 18:71–102. 7. Bertin C, Paul RN, Duke SO, Weston LA (2003) Smeda RJ (1999) in Recent Advances in Allelopa- 2. Harper JL (1977) Population Biology of Plants J Chem Ecol 29:1919–1937. thy, eds Macias FA, Galindo JCG, Molinillo JMG, (Academic, London). 8. Schneider D, Wink M, Sporer F, Lounibos P Cutler HG (Servicio e Publicaciones, University 3. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco (2002) Naturwissenschaften 89:281–294. of Ca´diz, Ca´diz, Spain), Vol 1, pp 211–218. JM (2006) Annu Rev Plant Biol 57:233–266. 9. Lambein F, Kuo YH, Rozan P, Ikdegami F (2001) 15. Fonne´-PfisterR, Chemla P, Ward E, Giradet M, 4. Bertin C, Yang XH, Weston LA (2003) Plant Soil R Soc Chem 269:580–583. Kreutx KD, Hanzatko RB, Fromm HH, Scha¨r 256:67–83. 10. Xuan TD, Elzaawely AA, Deba F, Fukuta M, H-P, Gru¨tter MG, Gowan-Jacob SW (1996) Proc Tawata S (2006) Agron Sustain Dev 26:89–97. 5. Duke SO, Baerson SR, Rimando AM, Pan Z, Natl Acad Sci USA 93:9431–9436. 11. Nishihara E, Parvez MM, Araya H, Fujii Y (2004) Dayan FE, Belz RG (2007) in Novel Biotechnolo- 16. Ishimitsu S, Fujimoto S, Ohara A (1980) Chem Plant Growth Regul 42:181–189. gies for Biocontrol Agent Enhancement and Man- Pharm Bull 28:1653–1655. 12. Schenk SU, Werner D (1991) Phytochemistry agement, eds Vurro M, Gressel J (Springer, Dor- 17. Duke SO (2003) Trends Biotechnol 21:182–195. 30:467–470. drecht, The Netherlands), pp 75–86. 13. Czarnota MA, Paul RN, Weston LA, Duke SO 18. Kong C, Xu X, Zhou B, Hu F, Zhang C (2004) 6. Bertin C, Weston LA, Huang T, Jander G, Owens (2003) Int J Plant Sci 164:861–866. Phytochemistry 65:1123–1128. T, Meinwald J, Schroeder FC (2007) Proc Natl 14. Duke SO, Duke MV, Paul RN, Ferreira JFS, 19. Dayan FE (2006) Planta 224:339–346. Acad Sci USA 104:16964–16969.
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