Published online 3 October 2006
Published in Agron J 98:1526-1531 (2006)
DOI: 10.2134/agronj2006.0030
© 2006 American Society of Agronomy
677 S. Segoe Rd., Madison, WI 53711 USA
Sugarcane
Allelopathic, Autotoxic, and Hormetic Effects of Postharvest Sugarcane Residue
Ryan P. Viatora,*,
Richard M. Johnsona,
Casey C. Grimmb and
Edward P. Richard, Jr.a
a USDA-ARS Southern Regional Res. Cent., Sugarcane Res. Lab., 5883 USDA Rd., Houma, LA 70360
b USDA-ARS Southern Regional Res. Cent., Food Processing and Sensory Quality Unit, 1100 Robert E. Lee Blvd., New Orleans, LA, 70124
* Corresponding author (rviator{at}srrc.ars.usda.gov)
Received for publication January 31, 2006.
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ABSTRACT
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With green sugarcane (interspecific hybrids of Saccharum spp.) harvesting, 6 to 24 Mg ha–1 of postharvest residue is deposited on the field surface covering the sugarcane stubble that must reemerge for several ratoon crops. The objectives of this research were to: (i) determine if postharvest residue possesses allelopathic, autotoxic, and hormetic properties; (ii) determine the interaction of soil type with possible autotoxic effects; and (iii) identify a reliable indicator species. Extract concentrations consisted of 0, 0.1, 10, 25, and 100% of the original solution of a 1:28 tissue to water extract. The higher concentrations of residue extracts exhibited autotoxicity by delaying early leaf development. The lower extract concentration of 10% increased sugarcane bud germination by 45% compared with the control, indicating hormetic effects. Allelopathic activity on tall morninglory (Ipomoea hederacea Jacq.) was more pronounced on a light soil; germination and radical length were reduced by all concentrations by an average of 42% and 8 mm, respectively, compared with the control. Seedling dry weights were reduced by an average of 10 mg by the 10, 25, and 100% extract concentrations relative to the control. On the heavy soil, only the 100% concentration reduced radical length and weight by 5 mm and 4 mg, respectively, relative to the control. Extract effects on oat (Avena nuda L.), rye (Secale cereale L.), and tomato (Lycopersicon esculentum Mill.) showed poor correlation with effects on sugarcane. Chemical analysis by gas chromatography/mass spectrotometry indicated the extract contained benzoic acid. Further studies are needed to establish the impact of benzoic acid in natural settings.
Abbreviations: GC, gas chromatography • MS, mass spectrotometry
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INTRODUCTION
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SUGAR INDUSTRIES throughout the world are rapidly adopting green-cane harvesting mainly due to public pressure to reduce smoke and soot resulting from the burning of standing sugarcane, the potential for increased sugar recovery with this system, and the desire to prevent soil degradation, erosion, and environmental pollution (Richard et al., 2001; Sampietro and Vattuone, 2006a). With green-cane harvesting, 6 to 24 Mg ha–1 of postharvest residue, regardless of whether the sugarcane is manually or mechanically harvested, is deposited on the field surface. Postharvest residues consist of nonmature stalk materials (such as green leaves and immature internodes), senesced leaves, and small pieces of mature stalks that result from the harvesting process. Sugarcane must then reemerge through this debris to produce ratoon crops, as sugarcane is a perennial crop that is grown for 3 to 8 yr from a single planting.
Considerable research has been conducted concerning sugarcane allelopathy. Allelochemicals have been identified and isolated from sugarcane leaves (Singh et al., 2003). These phytotoxic compounds include 2,4-dihydroxi-1,4-benzoxazin-3-one and 2-benzoxazolinone. Concentrations of these two compounds ranging from 0.45 mM to 1.25 mM reduced root growth of lentil (Lens culinaris Medik.) seedlings, but seed germination was not affected at these concentrations. Earlier research suggested that phenolics may be involved in the phytotoxicity caused by sugarcane straw (Wang et al., 1967). Ferulic, vanillic, and syringic acids have also been identified as phytotoxins in sugarcane straw (Sampietro et al., 2005; Sampietro and Vattuone, 2006b). These compounds increased root cell leakage, inhibited dehydrogenase activity, and reduced chlorophyll content in lettuce (Sampietro et al., 2005). In another study, extracts from green sugarcane leaves reduced the germination of lettuce (Lactuca sativa L.) seeds, but senesced leaves had no effect on germination of lettuce (de Carvalho et al., 1996). Leachate from sugarcane straw that was air-dried for 48 h at 60°C contained water-soluble phenolics that interfered with seedling growth of beggarticks (Bidens subalternans L.) and wild mustard (Brassica campestris L.). Leachate incorporated in biotic soil inhibited weed root growth more than leachate incorporated in abiotic soil, suggesting that microbial activity is involved in allelopathic activity. Soil characteristics evaluated in soil treated with sugarcane straw leachate suggested that straw phytotoxicity is not related with variations in inorganic nutrients (Sampietro and Vattuone, 2006a).
In addition to allelopathic effects, autotoxicity has been reported in sugarcane. Autotoxicity is an interspecific form of allelopathy that occurs when a plant releases chemicals harmful to its growth and development (Miller, 1996). Sterilized leachates from soils where sugarcane was previously grown inhibited the growth of sugarcane test plants (Magarey and Bull, 1994). In both field and laboratory experiments, Wang et al. (1984) found that decomposing residues contained ferulic, p-hydroxybenzoic, vanillic, p-coumaric, and syringic acid, which caused sugarcane phytotoxicity.
Allelopathy and autotoxicity are influenced by many environmental factors. Leaching of allelopathic compounds from sorghum residue in field experiments depended on precipitation (Roth et al., 2000). Laboratory studies showed that severity of alfalfa autotoxicity is influenced by soil type and rainfall patterns (Jennings and Nelson, 1998). Allelochemicals may be transported through the soil and can be transformed, metabolized, or become bound to organic matter during this process (Inderjit, 2001a). Inconsistent allelopathic effects suggest that the severity and duration of field autotoxicity may vary with environment and geographic location (Jennings and Nelson, 2002). Thus, in laboratory investigations, it is critical that concentrations of chemicals tested reflect those that exist in the soil–plant system under investigation (Al Hamdi et al., 2001; Inderjit, 2001a). Therefore, tissue to water ratios should be based on field residue densities and average rainfall for the areas under investigation. Moreover, allelopathy research on sugarcane is often conducted using oven-dried tissue to make leachates (Sampietro et al., 2005; Sampietro and Vattuone, 2006a; Sampietro and Vattuone, 2006b) even though in field conditions nondried residue is causing yield decline (Viator et al., 2005).
A common approach used in autotoxicity research is the identification and use of an indicator or test species. The indicator species and the species under investigation must show a similar response to the allelochemicals; the indicator species allows for the advantages of uniform seed quality, high sensitivity, and ease of use. For example, several researchers reported a strong correlation between the allelopathic activity of rice (Oryza sativa L.) on lettuce and ducksalad [Heteranthera limosa (Sw.) Willd.] (Ebana et al., 2001). A reliable indicator species would greatly enhance sugarcane bioassays because storage of sugarcane stalks for long periods leads to deterioration, which reduces germination (Weekes, 2004) and leads to desiccation of buds (Ellis and Merry, 2004). Moreover, bud germination varies along the sugarcane stalk after exposure to cold weather.
Preliminary field experiments in Louisiana indicated that the yield effects from postharvest residue are inconsistent; in some cases, residue retention did not reduce yields. This inconsistent effect may be due to autotoxic and/or hormetic properties of the residue itself. Hormesis is a form of allelopathy where subinhibitory levels of a phytotoxic substance have stimulatory effects on an organism (Southman and Ehrlich, 1943; Thiamann, 1956). The objectives of this research were to: (i) determine if fresh postharvest residue from a sugarcane cultivar commonly grown in over 10 different countries, ‘LCP 85-384’, possesses allelopathic, autotoxic, and hormetic properties at residue densities representative of the Louisiana growing region; (ii) determine the interaction of soil type with possible autotoxic and allelopathic effects; and (iii) identify a reliable indicator species for use in postharvest residue bioassays.
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MATERIALS AND METHODS
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Fresh sugarcane postharvest residue was collected from four fields of LCP 85-384 (Milligan et al., 1994) on the same day the sugarcane was harvested using a chopper harvester (3 Dec. 2004, 20 Dec. 2004, 15 Dec. 2005, 15 Jan. 2006). LCP 85-384 was planted to 91% of the sugarcane acreage in Louisiana in 2004 (Legendre and Gravois, 2004). Nine 1-m2 sections of residue were randomly collected manually from each field location. This postharvest residue consisted of all material that the harvester removed from the cane stalks and deposited on the field surface. Residue was immediately stored in burlap sacks at 45°C. On the day following each collection, a cold-water procedure was used to extract possible allelochemicals using distilled water in a temperature-controlled water bath at 25°C with a 1:28 tissue to water weight ratio (Harper and Lynch, 1982). Temperature and residue concentrations were based on historical weather records during the months of residue decomposition in Louisiana (October–March). The extract was then filtered with cheese-cloth and diluted (Bergeron et al., 2002). Final concentrations were 0, 0.1, 10, 25, and 100% of the original extract solution.
The aqueous sugarcane extract, consisting of 10-mL aliquots, was washed with 2 mL of ethyl acetate, and the aqueous portions discarded. A 1-mL injection of the organic phase was made into the injector of an HP5973 gas chromatography (GC) mass spectrotometry (MS) held at a temperature of 270°C. Helium was employed as the carrier gas at a rate of 1 mL/min. The GC oven temperature was initially held for 1 min at 80°C and then increased at 5°C min–1 to 125°C. The temperature was further increased at a rate of 10°C min–1 to 325°C where the oven was held for 4 min for a total run time of 34 min. The GC employed a 30-m by 0.25-µm diam., with a 0.5-µm DB-5 film, capillary column. The MS was operated in scan mode and employed electron ionization. Initial identification was made using the seventh edition of the Wiley mass spectral library (McLafferty, 2005). Solid phase microextraction was also performed directly on the aqueous extract. Aliquots of 5 mL were placed in 10-mL vials and sealed. Samples were heated to 65°C, and a Carboxen/DVB/PDMS SPME fiber was then introduced into the headspace of the vial. Following a 15-min adsorption period, SPME fibers were then desorbed in the injection port for 1 min with GC/MS run parameters as above.
To determine possible autotoxic and hormetic properties of the extract, soil bioassays were conducted using both light- and heavy-textured soils. Bulk samples from the plow layer (top 15 cm) of a Commerce silt loam (fine-silty, mixed, nonacid, thermic Aeric Fluvaquents) soil and a Sharkey clay (very-fine, montmorillonitic, nonacid, thermic Vertic Haplaquepts) soil were collected on 15 July 2003 in Lafourche Parish, Louisiana from two fields of each soil type. Twenty samples consisting of 0.3 m2 were collected randomly from each field using a large probe. Soils were collected from fallow ground that had been disked at frequent intervals beginning in March to ensure destruction of the previous ratoon crop to reduce potential accumulation of autotoxic chemicals that may occur in soils previously cropped with sugarcane. These fields did not have any residual herbicides applied to them in the 14 mo before sampling. Soils from the different fields were air-dried and sieved through a 6-mm screen and then stored separately in sealed metal storage containers at 20°C. Soils were analyzed for chemical composition by A&L Laboratories (Memphis, TN) (Table 1). Phosphorus and major cations present in soil samples were estimated using the Mehlich 3 extraction procedure and inductively coupled plasma-atomic emission spectrophotometry (USEPA Method 200.7), respectively. Soil organic matter was determined by Walkley–Black oxidation (Nelson and Sommers, 1996). Soil pH was determined in a 1:1 soil to water suspension and soil buffer pH using the SMP buffer (Thomas, 1996). The soil cation exchange capacity was calculated by summing exchangeable cations.
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Table 1. Chemical properties for the two soils used in the greenhouse experiments investigating the interaction of soil type with allelochemicals.
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Pots, 15 cm in diameter, were filled with 2 kg of soil. Eye pieces of sugarcane cultivar LCP 85-384 were germinated in distilled water-moistened tissue paper and then planted in pots on 15 Jan. 2005 and 30 Jan. 2005. Pots were hand-watered daily at a rate of 150 mL of extracts (made from the residue collected on 3 Dec. 2004 and 20 Dec. 2004), which maintained soils near field capacity. Leaf number and plant height were recorded every 2 wk for 8 wk. At the termination of the experiment, final height, leaf number, fresh weight, and dry weight were recorded. The experimental design was a randomized complete block with four replications for all treatments; the experiment was conducted twice using different residue and soil samples for the two trials. Replication was based on the distance from an external greenhouse wall to block for a slight temperature gradient. Plants were grown for 8 wk in a greenhouse under natural light with controlled relative humidity of 60 to 80% and temperature of 30/25°C (day/night).
Allelopathic properties of the extracts were determined using tall morningglory (Ipomoea hederacea Jacq.) that was scarified for 15 s. Similar to methods described in Sampietro and Vattuone (2006b), 15 g of either the Commerce silt loam or Sharkey clay soil was used as the extract absorber in 9.5-cm sterile Petri dishes. Ten seeds were placed approximately 2 mm into this soil layer and were then moistened with 10 mL of the various extract concentrations (made from the residue collected on 15 Dec. 2005 and 15 Jan. 2006). Dishes were immediately sealed with parafilm and incubated in the dark at a constant 26°C in an environmentally controlled incubator. Four replications/dishes were used, and the experiment was conducted twice. Percentage germination was recorded 4 d after incubation with radicals protruding at least 1 mm through the seed coat considered germinated. Radical length and seedling dry weight were recorded at this time.
To identify a possible indicator species, the inhibitory activity of the various concentrations of the extract were determined by seed germination and radical growth bioassays on three test species: oat (Avena nuda L.) cultivar Rodeo, common rye (Secale cereale L.), and tomato (Lycopersicon esculentum Mill.) cultivar Celebrity and sugarcane cultivar LCP 85-384. Radical length for sugarcane was not measured because radicals from the bud do not appear until several weeks after germination; the newly germinated bud depends entirely on roots formed from the mother stalk piece until it forms its radicals (James, 2004). High quality seed were used; oat, rye, and tomato each had at least 80% germination. Fifty seeds of oat, rye, and tomato, and 10 nodal buds of sugarcane were germinated in 9.5-cm Petri dishes on Whatman no. 541 filter paper, with 5 mL of the various extract concentrations (made from the residue collected on 3 Dec. 2004 and 20 Dec. 2004) used to moisten the filter paper (Ahn and Chung, 2000; Ebana et al., 2001). Dishes were immediately sealed with parafilm and incubated in the dark at a constant 26°C in an environmentally controlled incubator. Three replications/dishes were used for each plant species, and the experiment was conducted twice. Percentage germination was recorded 7 d after incubation with radicals protruding at least 1 mm through the seed coat considered germinated. Radical length was also recorded at this time using the same seedlings for oat, rye, and tomato. Percentage sugarcane germination was recorded 14 d after incubation with buds protruding at least 1 cm from the stalk tissue considered germinated.
All data were analyzed using SAS with PROC MIXED (SAS Inst., 2001) with extract concentrations and soil type as fixed variables and trial and replication as random variables. Percentage data was transformed by the arc sine square root transformation. Differences between treatment least square means were compared using the pdiff option (Saxton, 1998) at the 0.05 probability level. Correlation analysis was made between the extract effects on sugarcane and the possible indicator species of rye, oat, and tomato. Data were also analyzed taking into account possible hormetic effects using methods described by Schabenberger et al. (1999) using the following equation:
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where E[Y|x] represents the average response at x dosage, 
and 
are the upper and lower asymptotes of the response, 
is the initial slope, ß is the point of inflection of the curve, and RD50 is the effective dosage at which 50% of the total effect is demonstrated.
A pseudo-r2 value was calculated using methods described by Schabenberger et al. (1999) with the following equation:
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RESULTS AND DISCUSSION
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Compounds identified by GC/MS from sugarcane extracts included: benzoic acid, decane, diacetyl glycol, methyl hexadecanoic acid, and phthalic acid ester. Of these compounds, benzoic acid and its derivatives have been shown to have allelopathic properties on several species including cotton (Gossypium hirsutum L.), wheat (Triticum aestivum L.), ryegrass (Lolium spp.), cucumber (Cucumis sativa L.), and radish (Raphanus sativus L.) (Inderjit and Bhowmik, 2004; Lodhi et al., 1987; Wu et al., 2002). Previous sugarcane research indicated that phenolics were involved in the phytotoxicity caused by sugarcane straw (Wang et al., 1967). Derivatives of benzoic acids can alter leaf stomatal conductance and transpiration, ion uptake, and net assimilation rate as well as induce oxidative cell damage (Yu et al., 2003; Politycka, 1996).
Generally, sugarcane development beyond germination was not effected by the extract, except for leaf development (Table 2). Leaf number was reduced by 0.5 leaves at 2 wk after treatment by the 1.0 and 100% concentrations. At 4 wk after treatment, the 1, 10, and 100% concentrations reduced leaf number relative to the control. Other research showed that allelopathic activity from sugarcane leachates did not affect growth of weed seeds if sown 10 d after leachates were applied, suggesting microbial degradation, chemical decomposition, and sorption (Inderjit, 2001b; Sampietro et al., 2005). Similar to sugarcane, corn (Zea mays L.) residues, containing vanillic, syringic, p-coumaric, and ferulic acids, inhibited the shoot growth of corn. On the other hand, this corn phytotoxicity persisted longer (10 wk) (Ai-Mezori et al., 1999). It was hypothesized that soil type would interact with the autotoxicity of the extract, but there was no significant soil type by concentration interaction in this experiment (data not shown).
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Table 2. Comparisons of means for sugarcane growth in a greenhouse as a function of increasing water-soluble extract concentration from sugarcane postharvest residue for two trials with four replications each averaged across Commerce silt loam and Sharkey clay soils.
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On the other hand, there was a significant soil type x concentration interaction for the morningglory allelopathy experiment, and thus data were analyzed by soil type. Morningglory germination was affected only when seeds were incubated in the Commerce silt loam (Table 3). The 0.1, 1, 10, 25, and 100% extract concentrations decreased percentage germination by 24, 40, 38, 53, and 51%, respectively, compared with the control. At the 25 and 100% concentrations, germination percentages were 18% lower than the average of all other concentrations. Radical growth was affected by extracts for both soils (Table 3). On the Commerce soil, the 0.1, 1, 10, 25, and 100% extract concentrations decreased radical length by 6, 7, 7, 10, and 10 mm, respectively, compared with the control. The 25 and 100% concentrations reduced radical length by 3 mm compared with the mean of all other concentrations. On the Sharkey clay, the 100% extract concentration reduced radical length by 5, 4, 5, and 5 mm compared with the control, 0.1, 1, and 10% concentrations. On the Commerce silt loam, seedling dry weight was reduced by 8 (42%), 11 (58%), and 12 mg (63%) for the 10, 25, and 100% concentrations relative to the control. The two highest concentrations decreased weight by 9 mg compared with the 0.1 and 1% concentrations. Only the 100% concentration affected seedling weight on the Sharkey clay. This treatment reduced weight by 4 (24%) and 5 (28%) mg relative to the control and the mean of all other extract concentrations. Previous research indicated that leachates from sugarcane straw did not affect Ipomoea species (Lorenzi et al., 1989; Manechini et al., 2005). Overall, allelopathic activity appeared more pronounced on the lighter-textured soil compared with the heavy-textured soil. One possible explanation is that the pH of the Commerce silt loam was 7.1 compared with 8.0 for the Sharkey clay. Research has indicated that pH can affect levels of allelopathic activity (Fujita and Kubo, 2003; Furubayashi et al., 2005).
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Table 3. Comparisons of means for tall morningglory germination, radical length, and seedling fresh weight when grown in an incubator in Commerce silt loam and Sharkey clay soil as a function of increasing water-soluble extract concentration from sugarcane postharvest residue based on two trials with four replications each.
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Postharvest residue extract significantly affected germination of oat and rye (Table 4). Oat germination was only affected by the two highest concentrations when compared with the control, with a 17% reduction recorded for the 25 and 100% concentrations. Rye seed germination was reduced only by the 10, 25, and 100% concentrations by 12, 12, and 17%, respectively. Radical growth of oat was reduced by all extract concentrations by 33 to 60% as compared with the control radicals. The 0.1% concentration increased rye radical growth by 4, 4, and 5 mm compared with the 10, 25, and 100% concentrations. Extracts, though, did not reduce rye radical growth compared with the control. This contradicts previous research that demonstrated that benzoic acid from wheat seedling root exudates inhibited the root growth of annual ryegrass (Wu et al., 2002). In contrast to oat and rye, tomato seed germination and radical growth was not affected by extract treatment. Tomato growth may not have been affected because it is a dicot unlike rye and oat. Differential species specificity has been reported with other allelochemicals (Batish et al., 2004). Previous sugarcane allelopathy research has indicated inhibitory effects of leachates on root elongation of beggerticks and wild mustard, root growth of lentil, and seed germination of lettuce (de Carvalho et al., 1996; Sampietro and Vattuone, 2006a; Singh et al., 2003). Other research has shown that sugarcane leachates stimulated root growth of a subset of test plants including pigweed (Amaranthus spp.), radish, sorghum [Sorghum bicolor (L.) Moench], wheat, and wild mustard at 6 g dry straw L–1 but inhibited growth at higher concentrations. Synthetic phenolics at 19 mg L–1 stimulated the growth of lettuce, pigweed, arrowleaf sida (Sida rhombifolia L.), beggerticks, wild mustard, radish, sorghum, and wheat (Sampietro et al., 2005).
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Table 4. Comparisons of means for oat, rye, tomato, and sugarcane germination and radical growth of oat, rye, and tomato when grown in an incubator as a function of increasing water-soluble extract concentration from sugarcane postharvest residue based on two trials with three replications each.
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Sugarcane bud germination was increased by 45% by the 10% extract concentration compared with the control (Table 4). Statistical analysis for hormetic effects did reveal that the response curve for sugarcane germination was due to hormesis (r2 = 0.82) (Fig. 1
). Oat, rye, and tomato did not exhibit hormesis based on nonconvergence to the log-logistic model (data not shown). Pearson correlation coefficient responses of sugarcane, rye, oat, and tomato to the extract were low. Oat, rye, and tomato had correlation coefficients of 0.26, 0.12, and 0.19, respectively; thus, these would not appear to be good indicator species for sugarcane. A good indicator species shows correlation coefficients greater than 0.90 with the species under investigation (Ebana et al., 2001). One of the main reasons these species had poor correlation with the sugarcane response was because of the hormetic effects demonstrated only with sugarcane.
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Fig. 1. Hormetic response of sugarcane bud germination to various concentrations of postharvest sugarcane residue extracts using the equation described by Schabenberger et al. (1999): E[Y|x] = + { – /1 + exp[ßln(x/RD50)]}. E[Y|x] represents the average response at x dosage, and are the upper and lower asymptotes of the response, is the initial slope, ß is the point of inflection of the curve, and RD50 is the effective dosage at which 50% of the total effect is demonstrated. F = 185.9, p < 0.0001, r2 = 0.84, = 225, = 25, = 190, ß = 16, and RD50 = 25.
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CONCLUSIONS
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Sugarcane postharvest residue showed allelopathic, autotoxic, and hormetic properties under controlled incubator and greenhouse environments. Benzoic acid was present in the extracts. Allelopathic activity appeared more pronounced on the lighter-textured soil compared with the heavy-textured soil. Due to the hormetic effects only on sugarcane germination, oat, rye, and tomato were not good indicator species for sugarcane. Further studies are needed to establish the impact of benzoic acid in natural settings.
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ACKNOWLEDGMENTS
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The authors thank the American Sugarcane League and the Terrebonne-Barataria National Estuary Program for financial support to conduct this research.
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INTRODUCTION
