Physiological Basis for Reduced Glyphosate Efficacy on Weeds Grown underLow Soil Nitrogen

J. Mithila, C. J. Swanton, R. E. Blackshaw, R. J. Cathcart, and J. Christopher Hall*

Growth room studies were conducted to determine the physiological basis of reduced glyphosate efficacy under low soilnitrogen using velvetleaf, common ragweed, and common lambsquarters as model species. Glyphosate dose–responseexperiments of weeds grown under low (1.5 mM) and high (15 mM) soil N were conducted. Velvetleaf andcommon lambsquarters grown under low N required 169 g ae ha21 glyphosate for a significant reduction in biomass, butonly 84 g ae ha21 were required when grown under high N. However, when common ragweed was grown under low orhigh soil N there was no significant difference in response to glyphosate at all doses tested. The reduced glyphosate efficacyon velvetleaf and common lambsquarters under low N was primarily due to decreased herbicide translocation to themeristem. It appears that low N may decrease the net assimilation of carbon in plants, resulting in a decrease in the netexport of sugars and hence glyphosate from mature leaves. Understanding the relationship between soil N and herbicideefficacy may help explain observed weed control failures with glyphosate and may contribute to our knowledge of theoccurrence of weed patchiness in fields. This is the first report illustrating a physiological basis for decreased glyphosateefficacy under low soil N in selected weed species.Nomenclature: Glyphosate; velvetleaf, Abutilon theophrasti Medic. ABUTH; common lambsquarters, Chenopodiumalbum L. CHEAL; common ragweed Ambrosia artemisiifolia L. AMBEL.Key words: Glyphosate, efficacy, herbicide translocation, net carbon assimilation, nitrogen concentration, photo-assimilates.

Nitrogen, an important plant nutrient, has been found toinfluence several crop–weed interactions including competi-tion and weed community structure (Tilman 1986). Ingeneral, weeds occurring in agronomic crops have beenreported to benefit more from applied soil nutrients,specifically N, than crop species (Blackshaw et al. 2003; DiTomaso 1995). It has also been reported that soil nutrientstatus can influence the phytotoxicity of soil-applied andPOST herbicides (Dickson et al. 1990; Doll et al. 1970). Forexample, Dickson et al. (1990) reported that tame oat (Avenasativa L.) was more tolerant to fluazifop and glyphosate whengrown in low soil N conditions. A recent study (Cathcart et al.2004) suggested that soil N can influence the efficacy ofseveral herbicides with various modes of action. These authorsproposed the hypothesis that herbicide efficacy will beinfluenced by soil N in which weeds are grown. This researchdemonstrated that under low vs. high soil N, higher doses ofnicosulfuron, glufosinate, mesotrione, and glyphosate wererequired to achieve a 50% reduction in green foxtail [Setariaviridis (L.) Beauv.], velvetleaf, and redroot pigweed (Amar-anthus retroflexus L.) biomass. Therefore, it appears thatchanges in soil N can affect plant growth and development,which in turn may influence physiological and biochemicalprocesses such as uptake, translocation, and metabolism ofherbicides. Although previous studies have provided consider-able evidence that herbicide efficacy is influenced by soil N,little information is available regarding the physiological basisfor this effect on weeds.

The mechanism of altered herbicide efficacy in relation tosoil N is not well understood because most studies conductedon the physiology of herbicide uptake and translocation wereperformed under optimal conditions. An understanding of thephysiological basis behind altered herbicide efficacy when

DOI: 10.1614/WS-07-072.1* First, second, and the fifth authors: University of Guelph, Guelph, ON,

Canada N1G 2W1; third author: AAFC, Lethbridge Research Centre,Lethbridge, AB, Canada T1J 4B1; fourth author: Alberta Agricultural Foodand Rural Development, Edmonton, AB, Canada T6H 5T6. Correspondingauthor’s E-mail: jchall@uoguelph.ca

Figure 1. Relative growth response of velvetleaf, common lambsquarters, andcommon ragweed recorded at the time of glyphosate application. a and b indicatethe plant biomass (dry weight) and leaf area, respectively. Vertical bars representstandard error of means.

Weed Science 2008 56:12–17

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plants are grown in soils with varying soil N content will beuseful to agronomists. For example, soil fertility will varyacross a landscape because of topography and soil character-istics. Knowledge of how herbicide efficacy is influenced bydifferences in soil fertility may help explain shifts in weedcommunities, the persistence of weed patches, or the failure inweed control after a herbicide treatment (Cathcart et al.2004). Therefore, this study was initiated to elucidate thephysiological basis behind the decreased efficacy of glyphosateunder low soil N by studying the uptake and translocation ofglyphosate using velvetleaf, common ragweed, and commonlambsquarters as model species.

Materials and Methods

Growth Room Dose–Response Experiments. Commonlambsquarters seed required stratification to break the seeddormancy and therefore the seeds were given a cold treatment

(4 C) for 1 wk before planting. Approximately 100 velvetleaf,common ragweed, and common lambsquarters seeds weregerminated in a tray containing Premier Promix1 in a growthchamber with a 16-h photoperiod and 25/20 (6 1) C day/night temperatures. The light intensity and the relativehumidity were maintained at 450 mmol m22 s21 and 75%(6 5%), respectively. The trays with three weed species werewatered with distilled water until seedlings emerged from thesoil (approximately 4 to 5 d for velvetleaf and commonlambsquarters as opposed to 7 d for common ragweed). Aftergermination, one seedling (, 1 to 2 cm tall) was transplantedinto a 450-ml plastic pot containing Turface.2 Each pot waswatered daily (, 60 ml) with a nutrient solution. Two Nregimes, i.e., high (15 mM) and low (1.5 mM), weremaintained using ammonium nitrate as the sole source ofN. The concentration and the source of other nutrients in 1 Lof nutrient solution were superphosphate (0.59 g), potassiumsulfate (0.35 g), Mg SO4 7H2O (0.4 g), Mn chelate (0.02 g),

Figure 2. Velvetleaf grown under low and high N. a and b illustrate untreated plants grown under low and high N, respectively; c and d indicate the effect of 84 g ha21

dose of glyphosate on plants grown under low and high (14 d after treatment) N, respectively.

Swanton et al.: Soil nitrogen effect on glyphosate efficacy N 13

micronutrient mix (0.012 g), CuSO4 5H2O (0.00154 g), andZn SO4 7H2O (0.00155 g). Once a week, the seedlings weresoaked with distilled water (, 200 ml) to rinse anyaccumulated nutrients from the growth media.

Six doses of glyphosate (0, 42, 84, 169, 338, or675 g ae ha21) were used in these experiments. Velvetleafplants (14 d after planting [DAP]) and common ragweed (10DAP) grown under low and high N were chosen for thetreatment with glyphosate, whereas common lambsquartersgrown under low (10 DAP) and high (7 DAP) N,respectively, were used for the glyphosate treatment. Eachtreatment consisted of four replications. Glyphosate wasapplied using a motorized hood sprayer equipped with a flat-fan nozzle (8002 E) and calibrated to deliver 200 L ha21 at276 kPa.

Glyphosate Uptake and Translocation Experiments. Radi-olabeled glyphosate3 was used for uptake and translocationexperiments. The specific activity of [14C]glyphosate was1,998 GBq/mmol with a radiochemical purity of . 96%. Allchemicals and reagents used were reagent quality or better.Glyphosate was selected for use in this experiment because it isused widely in corn (Zea mays L.) and soybean [Glycine max

(L.) Merr.] production. This herbicide is a nonselective,broad-spectrum POST phosphonic acid herbicide (Franz et al.1997) that inhibits 5-enopyruvyl shikimate 3-phosphatesynthase (Steinrucken and Amrhein 1980). Glyphosate isa phloem-mobile herbicide and its distribution pattern isgenerally similar to that of photoassimilates in a variety ofplant species (Gougler and Geiger 1984).

On the basis of the results from the dose–responseexperiments, only velvetleaf and common lambsquarters wereused for the glyphosate uptake and translocation experiments.Velvetleaf and common lambsquarters plants were raisedunder both low and high N as described previously (see dose–response experiments). Before [14C]glyphosate was appliedthe plants were treated with 169 g ae ha21 technical-gradeglyphosate. [14C]Glyphosate was dissolved in water. Fivemicroliters of this solution containing 3,333 Bq was appliedas 1-ml droplets with a 10-ml Wiretrol micropipet4 to theadaxial surface of fourth leaf. Plants (three replicates) wereharvested 0, 6, 8, 24, 48, and 96 h after treatment (HAT).

At each harvest time, plants were dissected into root,treated leaf, and nontreated foliage above and below thetreated leaf, respectively. At the time of harvest, the amount of[14C]glyphosate present on the surface of the treated leaf was

Figure 3. Common lambsquarters grown under low and high N. a and b illustrate untreated plants grown under low and high N, respectively; c and d indicate the effectof 84 g ha21 dose of glyphosate on plants grown under low and high (7 d after treatment) N, respectively.

14 N Weed Science 56, January–February 2008

determined using a foliar rinse treatment (i.e., with a streamof wash solution); 10 mL of aqueous 10% (v/v) ethanolcontaining 0.5% (v/v) Tween 20 was used to rinse the leafsurface. The rinse solution was collected in two 22-mlscintillation vials containing 5 ml of Ecolite (+)5 scintillationcocktail. Radioactivity was quantified by liquid scintillationspectrometry using a Beckman LS6K-SC scintillation count-er.6 Each plant part was wrapped in tissue paper7 and dried at60 C for 48 h. The quantity of radioactivity in each plant partwas determined by combustion of samples to 14CO2 usinga model OX-300 oxidizer.8 14CO2 was trapped in carbon-14scintillation cocktail. 14CO2 recovery was . 94% as de-termined by combusting known quantities of D-[14C]manni-tol.9

Weed Harvest and Statistical Analysis. Growth Room DoseResponse and Radiolabeled Experiments. Visual rating ofphytotoxic symptoms was determined 14 d after treatment(DAT) for velvetleaf and common ragweed as opposed to 7DAT for common lambsquarters grown under low and highN. Plants were harvested 7, 14, and 21 DAT for commonlambsquarters, common ragweed, and velvetleaf, respectively.Mortality and shoot dry weight were determined. At the timeof harvest the roots were rinsed with water to remove Turface,dried in paper envelops at 65 to 70 C for 2 to 3 d, and dryweights recorded. All dose–response experiments were re-peated three times and the data from each experiment weresubjected to an ANOVA (P # 0.01) before mean separationsusing LSD (P # 0.01). The uptake and translocationexperiments were repeated three times for velvetleaf and twicefor common lambsquarters. Radioactivity determined byoxidative combustion of all samples was expressed asa percentage of 14CO2 recovered and data were subjected toan ANOVA (P # 0.01).

Results and Discussion

Dose–Response Experiments. Before treatment with gly-phosate, the growth response (plant biomass and leaf area) ofvelveltleaf, common ragweed, and common lambsquartersgrown under low and high soil N were assessed. No significantdifferences between plants grown under low vs. high soil Nwere found (Figures 1a and 1b) up to the time of glyphosatetreatment. However, for common ragweed the data on leafarea could not be recorded because of leaf shape (i.e., the leafarea meter used was not able to measure accurately). Thus,plants grown under both low and high N conditions weretreated with glyphosate when they were at the same growthstage.

Upon treatment with 84 g ae ha21 glyphosate, velvetleaf(14 DAT) and common lambsquarters (7 DAT) grown underhigh soil N exhibited severe injury (chlorosis followed bynecrosis), whereas plants grown under low soil N did not(Figures 2a–d and 3a–d). Furthermore, when allowed to growto maturity (approximately 9 to 10 wk after treatment), theplants grown under low soil N produced seed and the plantsgrown under high N did not survive.

Doses of glyphosate above 42 g ha21 significantly reducedthe dry weight of velvetleaf (21 DAT) and commonlambsquarters (7 DAT) plants grown under both low andhigh soil N when compared with untreated controls(Figures 4a and 4b). However, when both species were grown

under high soil N, a 50% reduction in growth (comparedwith control) was observed below 169 g ha21 of glyphosate(Figures 4a and 4b). Higher doses of glyphosate (338 and675 g ha21) were required to obtain a similar growthreduction in plants grown under low soil N (Figures 4a and4b). Regardless of N there was no difference in the response ofcommon ragweed to glyphosate treatment (Figure 4c).

Uptake and Translocation Experiments. Velvetleaf plantsgrown under low as opposed to high soil N retained more 14C

Figure 4. Effect of glyphosate on dry weight of (a) velvetleaf (21 d aftertreatment [DAT]), (b) common lambsquarters (7 DAT), and (c) commonragweed (14 DAT) grown under low (solid line) and high (dashed line) N.Vertical bars represent standard error of means.

Swanton et al.: Soil nitrogen effect on glyphosate efficacy N 15

in the treated leaves at all harvest times except 24 HAT(Table 1). Conversely, there was less uptake of 14C bycommon lambsquarters at all harvest times except 48 HAT inplants grown under low vs. high soil N (Table 2). However,both velvetleaf and common lambsquarters grown under highvs. low soil N translocated more 14C throughout the plant 72and 96 HAT (Tables 1 and 2). Furthermore, when bothvelvetleaf and common lambsquarters were grown under highas opposed to low N more 14C was translocated to shootsabove the treated leaf 48, 72, and 96 HAT (Tables 1 and 2).

This is the first report describing a physiological basis fordecreased glyphosate efficacy under low soil N in velvetleafand common lambsquarters. This research supports theprevious dose–response results (growth room) of Cathcart etal. (2004), who demonstrated that higher doses of glyphosatewere required to achieve 50% reduction in velvetleaf grownunder low vs. high N. In addition, data from recent fieldexperiments also found a significant interaction between soilN and glyphosate dose for the control of commonlambsquarters and redroot pigweed (Swanton et al., un-published data). This response to glyphosate was speciesspecific, as common ragweed grown under low and high Ndid not respond differently to glyphosate (Figure 4c).

Since the primary goal of this study was to elucidate thephysiological (uptake and translocation) basis of the relation-ship between soil N and glyphosate efficacy, it is important tounderstand the pattern of distribution of glyphosate inside theplant. Glyphosate is a phloem-mobile herbicide and itstranslocation pattern predominantly follows the movement ofphotoassimilates (i.e., from source to sink, accumulating inactively growing meristems). As glyphosate inhibits theshikimic acid biosynthetic pathway (Steinrucken and Amrhein1980), cessation of growth occurs soon after glyphosatereaches the apical meristem. This inhibition of shikimatepathway results in the reduction in synthesis of phenylalanine,tyrosine, and tryptophan. Glyphosate also reduces net carbonexchange (NCE); an important factor influencing photosyn-thesis in plants (Geiger et al. 1986, 1987; Shaner and Lyon1979). Furthermore, this decrease in NCE is coupled witha reduction in leaf stomatal conductance (Shaner and Lyon1979) as well as reduced photosynthesis-based carbonmetabolism (Geiger et al. 1986). For example, in sugar beet(Beta vulgaris L.), glyphosate reduced phosphoglyceric acid aswell as ribulose-1,5-biphosphate carboxylase (RuBPCase)activity that was caused by assimilates being drained becauseglyphosate disrupts the shikimic acid pathway (Serviates et al.

Table 1. Distribution of radioactivity expressed as percentage of recovered 14C in velvetleaf grown under low (L) and high (H) N after treatment with [14C]glyphosate.

Distribution of [14C] % of recovereda

Harvest time, h

Plant part Growth condition 6 24 48 72 96

Leaf rinse (% not absorbed) L 89.11 (0.8) 82.82 (5.7) 74.06 (1.4) 49.53 (11.7) 56.33 (5.5)H 93.47 (0.6) 78.03 (3.0) 68.41 (6.4) 55.61 (2.9) 57.66 (5.7)

Total in plant L 10.71 (1.0) 17.17 (5.7) 25.93 (1.4) 50.46 (11.7)b 45.96 (6.6)b

H 6.51 (0.6) 21.95 (3.0) 31.57 (6.4) 44.38 (2.7)b 42.29 (5.7)b

Treated leaf L 9.99 (1.4)b 14.46 (5.3)b 21.49 (1.6)b 38.78 (9.6)b 35.00 (4.1)b

H 5.48 (0.3)b 19.97 (2.8)b 18.68 (4.2)b 25.78 (0.7)b 25.50 (3.7)b

Total translocated L 0.87 (0.4)b 2.71 (0.3)b 4.44 (0.1)b 11.68 (2.6)b 10.96 (3.5)b

H 1.03 (0.2)b 1.98 (0.4)b 12.89 (1.7)b 18.60 (2.7)b 16.79 (2.0)b

Above (treated leaf) L 0.24 (0.1) 0.82 (0.02) 1.67 (0.3)b 2.78 (0.6)b 2.64 (0.8)b

H 0.57 (0.1) 0.86 (0.2) 6.40 (1.2)b 4.98 (2.0)b 11.32 (2.7)b

Below (treated leaf) L 0.63 (0.2) 1.78 (0.3)b 2.76 (0.1)b 8.88 (2.0)b 8.32 (2.6)b

H 0.46 (0.1) 1.12 (0.3)b 6.47 (1.6)b 13.62 (1.0)b 5.47 (0.7)b

a Data from two experiments were pooled and presented as treatment means with standard error in parentheses.b Indicates significant difference between low and high N within a plant part at a harvest time.

Table 2. Distribution of radioactivity expressed as percentage of recovered 14C in common lambsquarters grown under low (L) and high (H) N after treatmentwith [14C]glyphosate

Distribution of [14C] % of recovereda

Harvest time h

Plant part Growth condition 6 24 48 72 96

Leaf rinse (% not absorbed) L 78.94 (2.4) 37.92 (18.9) 13.33 (1.7)b 34.76 (5.3) 10.34 (4.6)b

H 61.74 (6.5) 23.83 (1.32) 24.13 (1.5)b 8.54 (5.2) 2.18 (0.2)b

Total in plant L 21.05 (4.8)b 62.07 (2.2) 86.67 (1.5) 65.23 (5.3)b 89.65 (4.5)b

H 38.26 (6.2)b 76.14 (1.3) 75.86 (1.5) 91.45 (5.2)b 97.82 (0.1)b

Treated leaf L 18.60 (2.6)b 48.31 (2.7)b 73.28 (4.66)b 58.85 (2.9)b 77.39 (8.3)b

H 36.39 (6.7)b 71.86 (5.7)b 65.51 (5.41)b 67.63 (3.0)b 53.07 (2.7)b

Total translocated L 2.44 (3.6)b 13.75 (3.0)b 13.39 (3.02)b 6.38 (2.4)b 12.36 (8.4)b

H 1.87 (0.2)b 4.28 (2.0)b 10.35 (4.36)b 23.81 (7.3)b 44.75 (2.4)b

Above (treated leaf) L 1.32 (2.0) 6.30 (2.8)b 6.78 (2.43)b 3.78 (1.7)b 7.18 (4.7)b

H 1.24 (0.2) 1.79 (0.8)b 7.37 (3.16)b 11.08 (7.9)b 43.06 (2.7)b

Below (treatedleaf) L 1.12 (0.3)b 7.44 (3.2)b 6.60 (1.6)b 2.59 (0.9)b 5.07 (3.7)b

H 0.63 (0.2)b 2.49 (1.2)b 2.97 (1.27)b 12.71 (10.5)b 1.68 (0.6)b

a Data from two experiments were pooled and presented as treatment means with standard error in parentheses.b Indicates significant difference between low and high N within a plant part at a harvest time.

16 N Weed Science 56, January–February 2008

1987). As a result, fewer photoassimilates were available forexport via phloem. Therefore, in our study, it was likely thatsoil N had an effect on photosynthesis and consequently onphotoassimilate and glyphosate translocation.

There is considerable evidence that N stress reducesphotoassimilate synthesis and its translocation, which in turnresults in reduced glyphosate movement. For instance, inwheat (Triticum aestivum L.) a decrease in N reduced netcarbon assimilation rate as a result of a significant reduction inRuBPCase activity (Evans 1983). Similarly, RuBPCaseactivity in kidney bean (Phaseolus vulgaris L.) plants grownunder low N became limited, leading to reduced photosyn-thesis (Seemann and Sharkey 1986). In addition, in oat,herbicides such as glyphosate and fluazifop were found to beless toxic under low than high N (Dickson et al. 1990).Dickson et al. (1990) speculated that this decrease inglyphosate activity under low N was due to reduced transportof these herbicides to meristems. Furthermore, addition ofnitrogen to soils low in N enhanced control of quackgrass(Elymus repens L.) by glyphosate (Baird et al. 1974). Thisevidence suggests clearly that further studies are needed toexplore how herbicide physiology can be altered in response tosoil and plant nutrient status.

In conclusion, this study suggests a physiological basis fordecreased efficacy of glyphosate when velvetleaf and commonlambsquarters were grown under low vs. high soil N. Theinteraction of glyphosate efficacy and soil N may be speciesspecific, as common ragweed grown under low or high N didnot respond differently to glyphosate. Low soil N may result inweed control failures, increasing crop–weed competition andweed patchiness within farm fields, thereby creating weedmanagement problems. Furthermore, if the efficacy ofherbicides is reduced in response to variable levels of soil N,this may result in an increase in use of higher doses of herbiciderates that in turn will increase production costs and potentiallythe rate of occurrence of weed resistance to selected herbicides.

Sources of Materials

1 Premier Promix, Plant Products Company Ltd., 314 OrendaRoad, Brampton, Ontario, Canada L6T 1G1.

2 Turface, Plant Products Company Ltd., 314 Orenda Road,Brampton, Ontario, Canada L6T 1G1.

3 Radiolabeled glyphosate, Amersham, Life Science, U.K.4 Wiretrol micropipet, Drummond Scientific Company, 500

Parkway, Box 700, Broomall, PA 19008.5 Ecolite, ICN Biomedicals Inc., 15 Morgan, Irvine, CA 92618.6 Scintillation counter, Beckman Instruments Inc. 2500 Harbor

Blvd., Fullerton, CA 92634.

7 Tissue paper, Kimberely Clark Inc., Rosewell, GA 30076.8 Oxidizer, R. J. Harvey Instrument Coop., Hillsdale, NJ 07642.9 [14C]Mannitol, Sigma Aldrich Co., St. Louis, MO 63178.

Acknowledgments

The authors acknowledge the funding from Natural Science andEngineering Research Council of Canada (NSERC CRD#:CRDPJ305778-03) for this research. We also thank the technicalsupport of K. Chandler.

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Received April 16, 2007, and approved August 17, 2007.

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