Abstract

Allelopathy offers potential for selective biological weed management through the production and release of allelochemicals from leaves, flowers, seeds, stems, and roots of living or decomposing plant materials.  Under appropriate conditions, allelochemicals may be released in quantities suppressive to developing weed seedlings.  Allelopathy is strongly coupled with inherent stresses of the crop environment, including insects and disease, temperature extremes, nutrient and moisture variables, radiation, and herbicides.  These stress conditions often enhance allelochemical production, thus increasing the potential for allelopathic interference.  Rye is an example of a plant which provides excellent weed suppression through both allelopathic and competitive mechanisms.  Rye residues maintained on the soil surface release 2,4-dihydroxy-1,4(2H)-benzoxazin-3-one (DIBOA) and a breakdown product 2(3H)-benzoxazalinone (BOA) both of which are strongly inhibitory to germination and seedling growth of several dicot- and monocotyledenous plant species.  Further, microbially produced transformation products of BOA demonstrate several fold increases in phytotoxic levels.  Hence, a variety of natural products contribute to the herbicidal activity of rye residues.  Several studies have demonstrated the allelopathic characteristics of rye residues and root exudates containing DIBOA and BOA.  For example, experiments have shown marked reductions in germination and growth of several problem agronomic weeds including barnyardgrass (Echinochloa crusgalli L.), common lambsquarters (Chenopodium album L.), common ragweed (Ambrosia artemisiifolia L.), green foxtail [Setaria viridis (L.) Beauv.], and redroot pigweed (Amaranthus retroflexus L.).  Researchers are optimistic the results of these and future studies will provide the necessary information to develop alternative weed management strategies and cropping systems to enhance the sustainability of agriculture.

Introduction

Economic and environmental constraints of crop production systems have stimulated interest in alternative weed management strategies.  Allelopathy offers potential for selective biological weed management through the production and release of allelochemicals from leaves, flowers, seeds, stems, and roots of living or decomposing plant materials (Weston, 1996).  The term allelopathy refers to biochemical interactions among plants, including those mediated by microorganisms (Molisch, 1937).  This broad definition of allelopathy is appropriate because considerable research has indicated the involvement of microorganisms and lower plants in production of phytotoxins (Gagliardo and Chilton, 1992; Putnam, 1986).  A variety of allelochemicals have been identified, including the phenolic acids, coumarins, terpenoids, flavonoids, alkaloids, glycosides, and glucosinolates (Barnes, Putnam, and Burke, 1986; Blum, 1995).  Allelopathic inhibition typically results from the combined action of a group of allelochemicals which, collectively, interfere with severe physiological processes (Blum, 1996).  Allelopathy is strongly coupled with inherent stresses of the crop environment, including insects and disease, temperature extremes, nutrient and moisture variables, radiation, and herbicides (Einhellig, 1996).  These stress conditions often enhance allelochemical production, thus increasing the potential for allelopathic interference.

Rye is an example of a plant which provides excellent weed suppression through both competitive and allelopathic mechanisms.  Rye and its residues reduce weed and crop growth by modifying the microenvironment and releasing allelochemicals (Putnam et al., 1983; Rice, 1984).  Rye produces a dense canopy, which is more competitive than weeds for light, moisture, and nutrients.  In addition, rye residues on the soil surface reduce weed germination and growth by shading, lowering soil temperatures, moderating diurnal temperature fluctuation, and acting as a physical barrier (Barnes and Putnam, 1986; Putnam et al., 1983; Rice, 1984).  Rye residues maintained on the soil surface release phytotoxic acids which strongly inhibit germination and seedling growth of several dicot- and monocotyledenous plant species (Barnes et al., 1987).

The objective of this paper is to review current literature that characterizes the ability of rye to interfere with other crops and weeds through competition and allelopathy.
 

Rye allelochemicals identified

Understanding allelopathy may hold the key to new weed management strategies.  However, the difficulty of distinguishing chemical interference from competition has hindered studies of allelopathy in natural and cultivated plant communities (Weidenhamer, 1996).  To positively identify the effects of chemical interference in future studies, Fuerst and Putnam (1983) proposed a series of criteria, modeled after Koch's postulates in microbiology, for proving a hypothesis of allelopathy.  These are: (i) identify and quantify specific symptoms of interference; (ii) isolate, identify, and synthesize the toxin, characterizing its biological activity through bioassays; (iii) simulate the interference through applications mimicking natural rate; and (iv) quantify the amount of toxin released to the environment and taken up by the target plant.

Despite the acknowledgment of these essential criteria researchers remain skeptical about the feasibility of designing experiments that conclusively test the toxin hypothesis of plant interaction (Harper, 1977; Williamson, 1990).  Challenges posed by allelochemicals include: (i) continual application in the exact dosage released from its source plant; (ii) altered toxicity of allelochemicals through degradation; and (iii) interaction of allelochemicals in their effects thereby requiring knowledge of the chemical complex, the concentration of each component, and the release mechanism of each component.

Many studies of allelopathic residues have been conducted with rye because of its substantial biomass production and apparent phytotoxicity.  Putnam and DeFrank (1983) reported that rye residue reduced the emergence of common ragweed by 43%, green foxtail by 80%, redroot pigweed by 95%, and common purslane (Portulaca olearacea L.) by 100%.  Shilling et al. (1985) found that a surface mulch of desiccated rye in a no-till system reduced aboveground biomass of common lambsquarters by 99%, redroot pigweed by 96%, and common ragweed by 92% compared to an unmulched tilled control.  Creamer et al. (1996) demonstrated that allelochemicals could be leached from rye shoot residue and used as a control to separate the physical effects of weed suppression of surface rye mulch from other types of interference.  Leached rye inhibited emergence of eastern black nightshade (Solanum ptycanthum Dun.) by 98%.

Barnes and Putnam (1983) evaluated and confirmed that residues and aqueous extracts of rye shoots were toxic to several plant species.  Guided by criteria suggested by Fuerst and Putnam (1983) they proposed to identify and characterize the most toxic compounds through separation fractions and bioassays of their relative activity on the germination and seedling growth of cress (Lepidium sativum L. 'Curly') (Barnes et al., 1987).  Sequential partitioning of aqueous extracts against a series of solvents of increasing polarity separated the most active compounds in the Et2O fraction based on a cress root growth assay.  Bioassays after thin layer chromatography (TLC) indicated two major zones of toxicity.  Further separation of the Et2O extract revealed two new phytotoxic benzoxazinones in rye.  The compounds were identified as 2,4-dihydroxy-1,4(2H)-benzoxazin-3-one (DIBOA) and its decomposition product, 2(3H)-benzoxazolinone (BOA).  The pure DIBOA compound was subsequently assayed for activity on cress and showed reduced root and shoot length, but showed little effect on seed germination at these concentrations.

Shilling et al. (1985) had previously identified and implicated beta-phenyl-lactic acid (PLA) and beta-hydroxbutyric acid (HBA) in rye residue toxicity.  The relative activity of these compounds was compared with DIBOA and BOA (Barnes and Putnam, 1987).  Overall, DIBOA and BOA were consistently more inhibitory (2 to 30 times) than PLA and HBA to germination and seedling growth of all weeds and crops tested.  Of the four chemicals, DIBOA was most active against the monocot species and BOA was most inhibitory to germination of dicot species.  On average, the dicots were 30% more sensitive than the monocots to all rates of all chemicals tested.  Chlorosis was a symptom of injury by rye residues on several indicators and may be related to the effects of DIBOA and BOA on photophosphorylation and electron transport.

Once in the soil system, the benzoxazinones produced by rye would be susceptible to microbial transformation by various soil microbes.  For DIBOA and BOA to be involved in long-term allelopathic activity, they must be sufficiently resistant to such microbial transformations.  Alternatively, if the parent compounds are metabolized, it is conceivable that biologically active metabolites may be involved in the overall allelopathic process.

In a following experiment, Nair et al. (1990) thoroughly mixed BOA with sterile and non-sterile soils and allowed them to incubate at 26 C for 10 days.  The methanol extract of the control soil (sterile) was pale yellow, while the experimental soil (non-sterile) extract was intensely orange.  Using TLC a dark red compound appeared in only one spot.  This compound was removed and recrystallized from hexane-acetone to yield orange-red needles which was further characterized as 2,2'-oxo-1,1'-azobenzene (AZOB), an azoperoxide, produced from rye.  A similar experiment was conducted starting with DIBOA and the resulting extractions and purifications yielded BOA, AZOB, and unreacted DIBOA.  The sterile soils did not produce any AZOBs, suggesting that these compounds are produced by soil microbes.  A similar field study using commercial BOA (which demonstrated identical characteristics) also produced AZOB, suggesting that the microbes are present in the environment.

Barnes and Putnam (1987) found dicotyledonous species to be approximately 30% more sensitive to BOA and DIBOA than were monocotyledonous species.  Initial assays, conducted with cress and barnyardgrass as indicators, indicated a high degree of toxicity of AZOB to radicle elongation of both species.  It appeared AZOB was much more toxic than either BOA or DIBOA, and therefore could contribute to the overall toxicity of rye residues.

In a subsequent study by Chase et al. (1991b), Acinetobacter calcoaceticus, a gram-negative bacterium isolated from field soils in Michigan, was found to be responsible for the biotransformation of BOA to AZOB.  In these transformation studies, soil inoculated with A. calcoaceticus indicated that the production of AZOB increased linearly with the concentration of BOA in sterile soil and showed a quadratic trend in non-sterile soils.

Gagliardo and Chilton (1992) were skeptical of the conclusions reached by Chase et al. (1991b) which identified A. calcoaceticus as the microbial agent responsible for the transformation of BOA to AZOB.  Soil microorganisms are known to transform substituted anilines into azo compounds (Bartha and Pramer, 1972).  However, microbial formation of an oxygen-oxygen bond between phenols is uncommon.  The published structure of AZOB indicated an element of symmetry in the pigment leading to six carbon and four hydrogen signals of C12H8N2O2.  All isomeric structures with the required symmetry can be rejected based on published melting point and spectral data except one, o-benzoquinone azine reported to be the product obtained by silver(II) oxide oxidation of o-aminophenol (Ortiz et al., 1972).  The ultraviolet-visible spectrum and high melting point reported for this red oxidation product is the same as that reported for AZOB; therefore it appeared that the red soil transformation product and the product of silver(II) oxide oxidation of o-aminophenol might be identical.

After further investigation, Gagliardo and Chilton (1992) found that the product of silver(II) oxidation of o-aminophenol is in fact not o-benzoquinone azine, but rather 2-amino-3H-phenoxazin-3-one, from which it is indistinguishable by TLC, mass spectral fragmentation, and UV spectra.  They also identified the red pigment produced from BOA by non-sterile soil as 2-amino-3H-phenoxazin-3-one.  The [1H]NMR of aminophenoxazinone contains all of the signals reported for AZOB (Nair et al., 1990), with the same chemical shifts and multiplicities, but, in addition, contains two singlets and a broad singlet due to an NH2 not reported for the Michigan soil transformation product.

Additional similarities between AZOB and 2-amino-3H-phenoxazin-3-one offered by Gagliardo and Chilton (1992) were that non-sterile soil converts the allelochemical BOA into the phytotoxic pigment aminophenoxazinone, sterile soil does not.  The probable route of transformation of BOA is its hydrolysis to o-aminophenol (likely requiring microorganisms such as A. calcoaceticus), followed by oxidation to aminophenoxazinone.  Sterile soil in contact with air is capable of accomplishing the subsequent oxidation of o-aminophenol into aminophenoxazinone.  Additional studies conducted with aminophenoxazinone indicated that it is an order of magnitude more phytotoxic than BOA and therefore has the potential for increasing the allelopathic effect of rye mulch.

A response to Gagliardo and Chilton's paper (1992) was not found in the literature.  In any event, it appears to be commonly accepted that the two cyclic hydroxamic acids (DIBOA and BOA) are responsible for the base-line phytotoxic activity of rye mulch and microbially transformed products of BOA can often dramatically enhance phytotoxic levels.

Implications of rye allelochemicals for weed management

Chase et al. (1991a) conducted a study to determine the allelopathic effects of rye compounds (DIBOA, BOA, and AZOB) on several plant species including garden cress, barnyardgrass, cucumber (Cucumis sativus L.), and snap bean (Phaseolus vulgaris L.).  They found that larger-seeded and deeper-seeded species were less sensitive to the allelochemicals.  This was likely due to the highest concentrations of allelochemicals being near the soil surface where small seeded species typically germinate.  It appears that selectivity can be achieved based on seed size and seed placement; the same principle that has allowed the selective use of synthetic herbicides.  However, the regulation and placement of allelochemicals in the field will be much more difficult.

Perez and Ormeno-Nunez (1991) studied the effects of rye root exudates on wild oats (Avena fatua L.).  They stated that while hydroxamic acids (e.g., DIBOA and BOA) have demonstrated allelopathic effects, the ability of a plant to exude them as a defensive response has not been shown.  GC and HPLC analysis of roots and root exudates of rye cultivars with high hydroxamic acid levels in their leaves, demonstrated the presence of these compounds in their roots and root exudates.  Bioassays employing these root exudates inhibited root growth of wild oats, suggesting allelopathic interference.  It was determined by Friebe et al. (1997) that DIBOA and BOA inhibit the plasma membrane H+-ATPase of chloroplasts and mitochondria.  The location of the enzyme in the plasma membrane implies early interactions with absorbed allelochemicals.

Perez and Ormeno-Nunez (1991) added that simply identifying roots with high contents of hydroxamic acids is not adequate for the selection of varieties with allelopathic potential.  Root exudate analysis will also be required.  It was reported that stress and other factors such as plant age, plant nutrition, light, and moisture can greatly increase root exudation (Nye and Tinker, 1977).  The combination of these factors with high hydroxamic acid content will be required to select and develop allelopathically superior rye cultivars.  In a subsequent study (1993) Perez and Ormeno-Nunez identified the ability of rye (cultivar 'Forrajero-Baer') to reduce wild oat biomass by 84% and 86% compared to wheat and forage oats, respectively.  The main hydroxamic acid found in rye was DIBOA.  This compound exists in the plant as the glucoside DIBOA-glc the attached glucose molecule provides stability to DIBOA and prevents autotoxicity within the plant.  DIBOA-glc is readily hydrolyzed to DIBOA glucosidase when the tissue is wounded, breaking cellular membranes that separate the two compounds (Niemeyer, 1988).

Mwaja et al., (1995) found that rye toxicity is influenced by fertility regime and production environment.  The concentrations of BOA and DIBOA were highest in shoot tissues when rye was grown under low or moderate fertility rather than high fertility.  Ether extracts of dried rye shoots were also less inhibitory when grown under high fertility regimes.  Based on their field studies, rye residues and their allelochemicals can effectively control redroot pigweed for four to eight weeks, depending on weather conditions.

Duration of cover crop residue on the soil surface often determines the extent of an effective weed control period.  Yenish et al. (1995) found that 50% of the initial content of rye residue disappeared by 105 days after clipping.  However, the combined active compound concentrations of DIBOA-glc, DIBOA, and BOA disappeared 168 days after clipping.  Therefore, the reported duration of weed suppression by the rye cover crop more closely followed disappearance of allelochemical from rye residue than disappearance of the residue itself.

In another study by Yenish et al. (1996) cover crops including rye, crimson clover (Trifolium incarnatum L.), subterranean clover (Trifolium subterraneum L.), and hairy vetch (Vicia villosa Roth) were evaluated in no-till corn to determine their ability to replace herbicides.  Rye consistently produced the largest amount of biomass among the cover crops and resulted in the highest corn yields.  However, weed control by cover crops alone was inconsistent or inadequate.  Pre-emergence herbicides were needed for adequate season-long weed control and overall greatest corn yield.

Rye cover crop residue has shown to be effective at reducing light transmittance (quality and quantity) and soil temperature which in turn can reduce or delay germination and emergence of certain weed species (Teasdale and Mohler, 1993).  However, Teasdale and Mohler acknowledged that higher soil moisture under cover crop residue could have variable effects on weed seed germination.  During periods of drought, residue could maintain soil moisture at levels more favorable for germination than bare soil.

In recent years several weed species have developed resistance to specific herbicide families (Gressel et al., 1982).  In controlled studies, Przepiorkowski and Gorski (1994) evaluated the effects of rye residues on germination and growth of three triazine-resistant weed species, barnyardgrass, willowherb (Epilobium ciliatum Rafin), and horseweed (Conyza canadensis L.).  Barnyardgrass seed germination was generally not influenced by rye roots and associated soil, which supported previous studies (Barnes et al., 1986; Shilling et al., 1985).  Both willowherb and horseweed seed germination were sensitive to rye-root soil mixtures.  However, this effect did not increase in severity with increasing seeding rates of rye.  Thus, it appears that after an initial threshold effect was obtained, additional reductions in seed germination did not occur with increased rye seeding rates.  The growth of barnyardgrass was severely reduced by rye residues but the growth of the two dicot species were only slightly reduced.

Conclusions

While much progress has been made to isolate and characterize the allelochemicals of rye and their interactions with microorganisms, the indisputable proof of allelopathy in these interference studies has not been presented (Weidenhamer, 1996).  While appropriate experimental designs and techniques have not yet been developed to satisfy the criteria proposed by Fuerst and Putnam (1983), researchers tend to agree that the primary phytotoxic compounds in rye are the cyclic hydroxamic acids 2,4-dihydroxy-1,4(2H)-benzoxazin-3-one (DIBOA) and a breakdown product 2(3H)-benzoxazalinone (BOA).  Thus, researchers have continued to study the effects of DIBOA and BOA on several plant species.  The mounting evidence of allelopathic interference exerted by rye is certainly encouraging and future manipulations of its phytotoxic tendencies will be greatly welcomed by individuals interested in alternative weed management strategies and cropping systems.

 Literature Cited

Barnes, J.P. and A.R. Putnam.  1983.  Rye residues contribute weed suppression in no-tillage cropping systems.  J. Chem. Ecol. 9(8):1045-1057.

Barnes, J.P. and A.R. Putnam.  1986.  Evidence for allelopathy by residues and aqueous extracts of rye (Secale cereale).  Weed Sci. 34:384-390.

Barnes, J.P. and A.R. Putnam.  1987.  Role of benzoxazinones in allelopathy by rye (Secale cereale L.)  J. Chem. Ecol. 13(4):889-906.

Barnes, J.P., A.R. Putnam, and B.A. Burke.  1986.  Allelopathic activity of rye (Secale cereale L.).  In A.R. Putnam and C.S. Tang (eds.)  The Science of Allelopathy. John Wiley, New York, pp. 271-286.

Barnes, J.P., A.R. Putnam, B.A. Burke, and A.J. Aasen.  1987.  Isolation and characterization of allelochemicals in rye herbage.  Phytochemistry 26(5):1385-1390.

Bartha, R. and D. Pramer.  1972.  Biochemical transformation of herbicide-derived anilines: Requirements of molecular configuration.  Can. J. Microbiol. 161:1617-1622.

Blum, U.  1995.  The value of model plant-microbe-soil systems for understanding processes associated with allelopathic interactions.  In Inderjit, K.M.M. Dakshini, and F.A. Einhelig, (eds.)  Allelopathy: Organisms, processes, and applications.  ACS Symposium Series No. 582.  Washington DC: American Chemical Society, pp. 127-131.

Blum, U.  1996.  Allelopathic interactions involving phenolic acids.  J. Nematology 28:129-132.

Chase, W.R., M.G. Nair, and A.R. Putnam.  1991a.  2,2'-oxo-1,1'-azobenzene: selective toxicity of rye (Secale cereale L.) allelochemicals to weed and crop species: II.  J. Chem. Ecol. 17(1):9-19.

Chase, W.R., M.G. Nair, A.R. Putnam, and S.K. Mishra.  1991b.  2,2'-oxo-1,1'-azobenzene: microbial tranformation of rye (Secale cereale L.) allelochemical in field soils by Acinetobacter calcoaceticus. III.  J. Chem. Ecol. 17:1575-1584.

Creamer, N.G., M.A. Bennett, B.R. Stinner, J. Cardina, and E.E. Regnier.  1996.  Mechanisms of weed suppression in cover crop-based production systems.  HortSci. 31:410-413.

Einhellig, F.A..  1996.  Interaction involving allelopathy in cropping systems.  Agron. J. 88(6):886-893.

Friebe, A., U. Roth, P. Kuck, H. Schnabl, and M. Schulz.  1997.  Effects of 2,4-dihydroxy-1,4-benzoxazin-3-ones on the activity of plasma membrane H+-ATPase.  Phytochemistry 44(6):979-983.

Fuerst, E.P. and A.R. Putnam.  1983.  Separating the competitive and allelopathic components of interference: Theoretical principles.  J. Chem. Ecol. 9:937-944.

Gagliardo, R.W. and W.S. Chilton.  1992.  Soil transformation of 2(3H)-benzoxazolone of rye into phytotoxic 2-amino-3H-phenoxazin-3-one.  J. Chem. Ecol. 18(10):1683-1691.

Gressel, J., H.V. Ammon, H. Fogelford, J. Gasques, Q.O.N. Kay, and H. Knees.  1982.  Discovery and distribution of herbicide resistant weeds outside North America.  In H.M. Lebaron and J. Gressel (eds.)  Herbicide Resistance in Plants.  Wiley, New York, pp. 31-57.

Harper, J.L.  1977.  Population Biology of Plants.  Academic Press, London.

Molisch, H.  1937.  Der Einfluss einer Pflanze auf die andere-Allelopathie.  Fischer (Jena), Jena, Germany.

Mwaja, V.N., J.B. Masiunas, and L.A. Weston.  1995.  Effects of fertility on biomass, phytotoxicity, and allelochemical content of cereal rye.  J. Chem. Ecol. 21(1):81-96.

Nair, M.G., C.J. Whitenack, and A.R. Putnam.  1990.  2,2'-oxo-1,1'-azobenzene a microbially transformed allelochemical from 2,3-benzoxazolinone: I.  J Chem. Ecol. 16(2):353-364.

Niemeyer, H.M.  1988.  Hydroxamic acids (4-Hydroxy-1,4-benzoxazin-3-ones), defense chemicals in the Gramineae.  Phytochemistry 27:3349-3358.

Nye, P.H. and P.B. Tinker.  1977.  Solute movement on the soil root system.  In Vol. 4. Studies in Ecology, Blackwell, Oxford. pp. 342-355.

Ortiz, B., P. Villanueva, and F. Walls.  1972.  Silver(II) oxide as a reagent.  Reaction with aromatic amines and miscellaneous related compounds.  J. Org. Chem. 37:2748-2750.

Perez, F.J. and J. Ormeno-Nunez.  1991.  Difference in hydroxamic acid content in roots and root exudates of wheat (Triticum aestivum L.) and rye (Secale cereale L.): possible role in allelopathy.  J. Chem. Ecol. 17:1037-1043.

Perez, F.J. and J. Ormeno-Nunez.  1993.  Weed growth interference from temperate cereals: the effect of a hydroxamic-acids-exuding rye (Secale cereale L.) cultivar.  Weed Research 33:115-119.

Przepiorkowski T. and S.F. Gorski.  1994.  Influence of rye (Secale cereale) plant residues on germination and growth of three triazine-resistant and susceptible weeds.  Weed Technol. 8:744-747.

Putnam, A.R.  1986.  Allelopathy: Can it be managed to benefit horticulture?  HortSci. 21:411-413.

Putnam, A.R. and J. DeFrank.  1983.  Use of phytotoxic plant residues for selective weed control.  Crop Prot. 2:173-181.

Putnam, A.R., J. DeFrank, and J.P. Barnes.  1983.  Exploitation of allelopathy for weed control in annual and perennial cropping systems.  J. Chem. Ecol. 9(8):1001-1010.

Rice, E.L.  1984.  Allelopathy.  Second Edition, Academic Press, New York, 422 pp.

Shilling, D.G., R.A. Liebl, and A.D. Worsham.  1985.  Rye and wheat mulch: The suppression of certain broadleaved weeds and the isolation and identification of phytotoxins.  p. 243-271.  In A.C. Thompson (ed.)  The chemistry of allelopathy: Biochemical interactions among plants.  Am. Chem. Soc., Washington, DC.

Teasdale, J.R. and C.L. Mohler.  1993.  Light transmittance, soil temperature, and soil moisture under residue of hairy vetch and rye.  Agron. J. 85:673-680.

Weidenhamer, J.D.  1996.  Distinguishing resource competition and chemical interference: overcoming the methodological impasse.  Agron. J. 88:866-875.

Weston, L.A.  1996.  Utilization of allelopathy for weed management in agroecosystems.  Agron. J. 88(6):860-866.

Williamson, G.B.  1990.  Allelopathy, Koch's postulates, and the neck riddle.  In J.B. Grace and D. Tilman (ed.) Perspectives on plant competition.  Academic Press, San Diego pp. 143-161.

Yenish J.P., A.D. Worsham, and W.S. Chilton.  1995.  Disappearance of DIBOA-glucoside, DIBOA, and BOA from rye (Secale cereal L.) cover crop residue.  Weed Sci. 43:18-20.

Yenish J.P., A.D. Worsham, and A.C. York.  1996.  Cover crops for herbicide replacement in no-tillage corn (Zea mays).  Weed Technol. 10:815-821.