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RESEARCH ARTICLE formerly Planta Daninha SPECIAL TOPICS New Insights Peanut and sorghum are excellent phytoremediators of 14Ctebuthiuron in herbicidecontaminated soil Paulo A Conciania Kassio F Mendesb Rodrigo N de Sousac Andrew de P Ribeirob Rodrigo F Pimpinatoa Valdemar L Tornisieloa a Laboratory of Ecotoxicology Center for Nuclear Energy in Agriculture University of São Paulo Piracicaba SP Brazil b Department of Agronomy Federal University of Viçosa Viçosa MG Brazil c Department of Soil Science Luiz de Queiroz College of Agriculture Piracicaba SP Brazil Journal Information ISSN 26759462 Website httpawsjournalorg Journal of the Brazilian Weed Science Society How to cite Conciani PA Mendes KF Sousa RN Ribeiro AP Pimpinato RF Tornisielo VL Peanut and sorghum are excellent phytoremediators of 14Ctebuthiuron in herbicide contaminated soil Adv Weed Sci202341e020220068 httpsdoiorg1051694AdvWeedSci20234100002 Approved by Editor in Chief Carol Ann MallorySmith Associate Editor Marcos Yannicari Conflict of Interest The authors declare that there is no conflict of interest regarding the publication of this manuscript Received September 28 2022 Approved November 17 2022 Corresponding author kfmendesufvbr 1 This is an openaccess article distributed under the terms of the Creative Commons Attribution License which permits unrestricted use distribution and reproduction in any medium provided that the original author and source are credited 1 Introduction The contamination of the environment by pesticides including herbicides is a major global concern and can be considered a major obstacle to the development of sustainable agriculture Mendes et al 2020 There is social and scientific appeal for the minimization of environmental impacts caused by the use of herbicides in the large areas cultivated with sugarcane and the increase of areas treated with long residual effect herbicides such as tebuthiuron Tebuthiuron 15tertbutyl134thiadiazol2yl13dimethylurea is a systemic herbicide absorbed by roots and translocated in weeds widely used in sugarcane with a photosystem II PSII inhibitors mode of action of the urea chemical group Mendes et al 2022 This herbicide has a high leaching potential due to its high water solubility Sw 2500 mg L1 and low sorption sorption coefficient Kd 132 and 085 L Kg1 in clay and loamy sand soil respectively Guimarães et al 2022 A positive correlation among clay content soil organic matter SOM and tebuthiuron sorption was found by Mendes et al 2021 Also this herbicide has a high persistence in the soil 90 degradation time DT90 385 and 334 d Guimarães et al 2022 However bacteria can effectively degrade tebuthiuron in soil Lima et al 2022 and seawater Mercurio et al 2015 The application of herbicides with residual effects in the soil is essential for weed control in preemergence Nevertheless if the residual effect is greater than the cycle of the crop it can cause injury in the next crop rotationsuccession a process commonly known as carryover On the other hand tebuthiuron can have negative impacts on soil microorganisms Faria et al 2018 and water Bernardes et al 2014 In the sugarcane fieldsurrounding aquatic environment tebuthiuron distribution ranged from 0007 to 0022 mg L1 leading to a high risk at in aquatic ecosystems Qian et al 2017 as DNA damage in exposed small fish Oreochromis niloticus can occur Bernardes et al 2014 Then using strategies to remediate herbicides in contaminated soils is critical in agricultural systems Phytoremediation is one option to reduce the environment in soil contaminated by residual herbicides such as tebuthiuron Mendes et al 2021a and 2021b Abstract Background Phytoremediation is a technique used in soils contaminated with residual herbicides such as tebuthiuron However the herbicide presence in the soil and plant matrices are not generally quantified Objective This study aimed to select plant species to evaluate the phytoremediation of 14Ctebuthiuron by showy rattlepod Crotalaria spectabilis sorghum Sorghum bicolor radish Raphanus sativus peanut Arachis hypogaea and alfalfa Medicago sativa in herbicidecontaminated soil Methods The selection of the five herbicide phytoremediation plants was with the application of five rates of tebuthiuron 300 600 1200 2400 and 4800 g ai ha1 and compared to a control Peanuts and sorghum herbicidetolerant plants were sown in soil contaminated with tebuthiuron 600 g ai ha1 applied through a working solution containing 1747 kBq of 14Ctebuthiuron The total of herbicide was analyzed in the soil and plant at three phenological stages Results Showy rattlepod radish and alfalfa were sensitive to the herbicide even at the lowest application rate Sorghum was tolerant to the herbicide up to 600 g ha1 with the application of 1200 g ha1 there was 80 injury peanut was tolerant even at the highest rate 4800 g ha1 with only 40 injury Peanut and sorghum were able to phytoremediate the soil although peanut was more efficient in decreasing tebuthiuron contamination by 76 while sorghum reduced at by 45 at 3rd phenological stage Conclusions Thus both plants can be recommended in succession rotation with crops that had tebuthiuron applied from preemergence weed control Keywords Root absorption Rhizodegradation Radiolabeled herbicide Decontamination Crop Copyright 2022 Advances in Weed Science Conciani PA Mendes KF Sousa RN Ribeiro AP Pimpinato RF Tornisielo VL Results showed preliminary evidence of effective 22 Installation ofthe studies phytoremediation capacity by velvet bean Mucuna Two experiments were carried out for the development pruriens pearl millet Pennisetum glaucum and sunn of this study The first was to select five species of hemp Crotalaria juncea in tebuthiuron contaminatedsoil agronomic interest for phytoremediation at different Ferreira et al 2021 In the highest rate of tebuthiuron levels of soil imation by tebuthi Seeds f 1500 ha applied jack bean C ensiformis white evels of soil contamination by tebuthiuron Seeds from le tous i 1 mill t 2 ol the herbicide tolerant species that survived in the first upin Lupinus albus and pearl millet P glaucum were tud Ilected and d in th d stud the species with better phytoremediation effects Pires et ch the hvemedhstion o f cor hee aad ane al 2008 When the soil was treated with tebuthiuron at i P y db hi 8 d P d 1000 g ha jack bean followed by white lupin and velvet sot contaminate y tebut turon was determined The bean were the species that had better phytoremediation studies were conducted in a glass greenhouse for one year Pires et al 2006 However the phenological stages of During this period the averages observed for maximum the phytoremediation species and their association with 538C ne and average temperatures were 304 172 and rhizosphere microorganisms can directly interfere in the Fespecuvey amount of herbicide degraded The phytoremediation technique increases in 221 Plant selection for phytoremediation of tebuthiuron in complexity as researchers try to select species that present contaminated soil remediation capacity and other agronomic benefits to The experiment was set up in a randomized block farmers However phytoremediation is sustainable and desion j factorial sch 5x6 with th re effective less expensive and destructive when compared to Send f ac ea seneme m 1 nee i has eeds oO ve plant species showy rattlepod sorghum other soil decontamination processes and can be applied dish P d If y P oa d large areas Paiva Mendes 2021 radish peanut and alfalfa were grown in pots fille oe Then h techni tes of use of herbicides radiolabeled with soil sprayed simulated contamination by six rates ith Mc ti q ble t ty th tential of of tebuthiuron Ox 14x 12x x 2x and 4x in which x wi 1S Posstbie fo very ene porenna represents the maximum rate recommended for field phytoremediation of plant species at the laboratory re 1 fo application of the herbicide 1200 g ai ha condition since this technique allows accurately 1 ith ity of 1 determining the absorption and translocation of Fo ystyrene pots with a capacity of approximately 1500 small amounts of herbicides in vlants such as diuron cm were used Each pot received 800 g of dry soil and water hexazinone sulfometuronmeth i Tedfilo et al 202 0 was added to reach field capacity Twentyfour hours after quinclorac an dtebuthiuron Men des et al 202 1a the soil reached saturation point each pot was sown with 20 Many phytoreme diation studies of various herbici des seeds of each specie that then were covered by 100 g of dry in contaminated soils have been carried out in several soil eee eee cer of the pot each rate was edaphoclimatic conditions and with a diversity of plant PON species H h prepared in a concentration of active ingredient per pecies However there is still a lack of studies that detect 4 1s application volume equivalent to the rate of 200 L ha The herbicides by analytical techniques in the soil and plants Thus this study aimed to select plant species to evaluate herbicide application was used a chamber with spray nozzle was 14 TTI11002 and the constant pressure of 2792 kPa for the phytoremediation of Ctebuthiuron by showy rattlepod Crotalaria spectabilis sorghum Sorghum bicolor The herbicide was applied at the appearance of the first 1 leaf until the emergence of the second pair of leaves radish Raphanus sativus peanut Arachis hypogaea and true wo every two days visual evaluations of the injury level were alfalfa Medicago sativa in soil performed according to a scale of 0 to 100 where 0 represents the absence of symptoms and 100 represents 2 Material and Methods death of the plant After injury level evaluations the pots were 21 Soil collection and preparation disassembled and from each plot three plants were To ensure that there was no previous contamination randomly collected Each plant measured by plant height with herbicides in the soil used in this study the soil was and root length and stored in paper bags The collected collected in native forests permanent preservation area plants were dried 72 h in an oven heated to 40 C and near PiracicabaSP Brazil at a minimum distance of 20m then weighed to determine the accumulated dry matter from the edge of a road For the data on percent reduction in dry matter A preliminary cleaning was performed eliminating plant height and root length Tukeys test p005 was leaves and pieces of plants from the soil surface and then performed to verify the difference between the treatments the layer from 0 to 10 cm deep was collected The collected The level injury data were expressed as mean and standard soil was airdried homogenized and passed through a 2 deviation n 3 All figures were plotted using Sigma Plot mm sieve and the physical and chemical properties were version 100 for Windows Systat Software Inc Point analyzed Table 1 Richmond CA USA 2 Adv Weed Sci httpsdoiorg1051694AdvWeedSci20234100002 Advances in Weed Science Plant selection and phytoremediation from herbicidecontaminated soil Table 1 Soil physical and chemical properties CaCL mg cm mmol dm gdm mmol dm 66 10 6 33 74 18 1 20 69 955 116 83 clay 406 150 444 exchange capacity SB saturation base Source Soil Laboratory Luiz de Queiroz College of Agriculture University of Sdo Paulo Piracicaba SP Brazil 222 Phytoremediation of CTebuthiuron in contaminated soil and dried in an oven for 72 h at 40 C The dried soil was Pots with a capacity of 2800 cm filled with 900 g of crumbled homogenized and ground Three samples of 02 g each were burned in a biological oxidizer RJ Harvey airdried soil were used Water was added to the trays of the ye ys Instrument Corporation OX500 Tappan NY USA at pots until it reached the soil surface by capillarity action am 900 C in porcelain dishes by 3 min to determine the After 24 h each pot received either 5 sorghum or 5 peanut Ls 4 7 14 radioactivity amount of Cherbicide mineralized to C seeds species selected in the first study and a layer of 100 14 CO The Ctebuthiuron concentration was determined g of dry soil was deposited over the seeds Lo eer using a Liquid Scintillation Spectrometry LSS for 15 The study was a randomized block design with a min with a TriCarb 2910 TR LSS counter PerkinElmer factorial scheme 2x3 with two plant species sorghum d t in th henological st devel t Waltham MA USA an peanut 1 ree paeno ogica Stages oF cevetopments After centrifugation to separate the soil the solution with three repetitions In addition a control treatment h diluted with distillated Th herbicide application was added for comparison of the rom the Pots was Guuted with cistivated water unree ne er PP P aliquots 10 mL each of this solution were taken from ot cr nn the oy il f th d th each pot To each sample 10 mL of the scintillator Given the sma Surlace area t pots an t solution Instagel plus was added and then measured handling of a radioactive product the herbicide application LSS was performed by adding 100 g of treaded dry soil A The phytoremediation was evaluated by absorption working solution containing 1747 kBq of Ctebuthiuron 4 translocation of Ctebuthiuron This study CUL specific activity 301 MBq mg radiochemical was qualitatively analyzed by autoradiography and purity 98 and technical product nonradiolabeled quantitatively by combustion of plant tissues Plants were was prepared to reach 600 g ai ha of herbicide rate washed pressed and dried in a forced circulation oven recommended in the field at 45 C for 120 h One triplicate in each plant was used Whenever necessary the reestablishment of the according to Mendes et al 2017 and Cruz et al 2021 on moisture in the pots occurred through the deposition of phosphorus film plates for 120 h and analyzed in a radio water in the trays to maintain soil moisture close to field scanner PerkinElmer Storage Phosphor System model capacity and avoid herbicide leaching Cyclone Plus Shelton WA USA When the plants reached the desired three stages of After drying the plants were removed and divided phenological development one pair of true leaves formed into leaves roots stems and cotyledon when this was 1 phenological stage 1 pair of branches 2 and still present to quantify the radioactivity in each part of beginning of flowering 3 for peanut and 3 leaf 1 the plant phenological stage 5 leaf 2 and fully extended 3 The samples were burned in a biological oxidizer flag leaf for sorghum The plants were removed from with three repetitions for each part of the plant The C the pots and placed on plastic trays A KCl 002 mol L CO released in the combustion was collected in a flask solution was used to wash the roots containing scintillator solution plus monoethanolamine The trays were left to stand for 24h for sedimentation and methanol The radioactivity contained in this flask was of the solution The soil solution was collected to quantify determined in aLSS the herbicide remaining and centrifuged Hitachi Radioactivity present in all parts of the plants was CF16RXII Hitachi Koki Co Ltd Indaiatuba SP Brazil considered as translocation because the initial herbicide in Teflon flasks at 4000 rpm for 15 min to remove the soil application was in the soil The data were expressed as suspension The sediment soil was returned to the trays mean n3 Adv Weed Sci httpsdoiorg1051694AdvWeedSci20234100002 3 Advances in Weed Science Conciani PA Mendes KF Sousa RN Ribeiro AP Pimpinato RF Tornisielo VL 3 Results and Discussion died and had 83 injury to radish treated with a rate of 500 g ha Pirest et al 2003a Corroborating this data 31 Plant selection for phytoremediation of tebuthiuron in in another study the injury levels of 95 at 15 DAA and contaminated soil At the rates of 300 and 600 g ha of tebuthiuron there was a small initial incidence of injury level 8 i 100 ne in sorghum compared to the control treatment no a Eo herbicide However after 10 days after emergence DAE Kk om there was a tendency in decreased injury symptoms and 80 at 20 DAE the injury did not differ from the control S i i treatment Figure 1 60 1 17 A study performed by Pires et al 2003a showed the effects of different rates of tebuthiuron in multiple species 8 40 A in which the authors also found a lower injury 25 in s i pearl millet Pennisetum glaucum treated with 500 g ha of 20 tebuthiuron at 60 days after application DAA LY At rates of 1200 2400 and 4800 g ha of tebuthiuron 0 ao the initial symptoms of injury in sorghum increased 0 2 4 6 8 1 12 14 16 18 20 over time reaching 80 with 1200 g ha and values Days After Emergence DAE 1 above 95 in rates of 2400 and 4800 g ha Figure 1 300 gha g 1007541expx77791245 R 099 p001 These results corroborate those of Pires et al 2003a 600 gha g 1000311expx68891222 R 099 p001 in which pearl millet plants had an injury level of 76 v rane Me Oe Oe eee Sere oemel Re nee a A g hat g 983691explx29400654 R 099 p001 compared to the control when treated with 1000 g ha M4800 g ha 9 98290texplx27120618 R 098 p001 of tebuthiuron and 100 with the rate of 2000 g hat at 60 DAA Even at the lowest rate of tebuthiuron 300 g ha all Figure 2 Injury level in showy rattlepod Crotalaria spectabilis showy rattlepod plants died at 12 DAE Figure 2 the same caused by the application of five rates of tebuthiuron with can be observed for alfalfa Figure 3 and radish Figure 4 evaluations at 2 4 6 8 10 12 14 16 18 and 20 days after respectively at 8and10 DAE At60 DAA showvrattlepod mengence DAE Vertical bars represent standard deviations P Y y P SD of means n 3 100 100 80 ei t Y 80 o 7 IL xz xX I 60 2 3 2 s 2 5 40 2 40 Ir a 20 i 20 as ate Se LLL Ee 0 0 0 2 4 6 8 1 1 14 16 18 20 0 2 4 6 8 0 172 4 18 20 Days After Emergence DAE Days After Emergence DAE 300 gha g 61661explx100100062 R 094 p001 300 g ha 982911explx34390814 R 099 p001 600 gha g 72091expx35670334 R 085 p001 600g ha g 989921expx38181041 R 099 p001 Vv 1200 gha g 845811expx106752136 R 099 p001 Vv 1200 g ha g 988711expx30340923 R 099 p001 4 2400 g ha g 988521expx101312218 R 099 p001 2400 g ha g 1000171explx29400654 R 099 p001 m 4800 g ha g 1018361expx86671879 R2 098 p001 m 4800 g hat Y 1000341expx01311054 R 039 p001 Figure 1 Injury level in sorghum Sorghum bicolor caused by Figure 3 Injury level in alfalfa Medicago sativa caused by the application of five rates of tebuthiuron with evaluations the application of five rates of tebuthiuron with evaluations at 2 4 6 8 10 12 14 16 18 and 20 days after emergence at 2 46 810 12 14 16 18 and 20 days after emergence DAE Vertical bars represent standard deviations SD of DAE Vertical bars represent standard deviations SD of means n 3 means n 3 4 Adv Weed Sci httpsdoiorg1051694AdvWeedSci20234100002 Advances in Weed Science Plant selection and phytoremediation from herbicidecontaminated soil 100 100 KE 80 ly 80 J j 60 fi S 60 g t Q 3 40 i j 3 40 r 4 20 20 ae 0 an 0 FF 0 2 4 6 8 10 12 14 16 18 20 0 2 4 6 8 10 12 14 16 18 20 Days After Emergence DAE Days After Emergence DAE 300 ghar g 1016851explx59551543 R 098 p001 300ghagg0 600g ha g 1010901explx64541118 R 099 p001 600 ghagy0 V 1200 g ha g 989991expx34261003 R 099 p001 1200 g ha g 35241expx112560805 R 081 p005 2400 g ha G 990101expx25201320 R 099 p001 2400 g ha G 274421expfx121332595 R 094 p001 4800 g ha G 992881expx02441883 R 096 p001 4800 g ha g 487851expx139654340 R 095 p001 Figure 4 Injury level in radish Raphanus sativus caused by Figure 5 Injury level in peanut Arachis hypogaea caused by the application of five rates of tebuthiuron with evaluations the application of five rates of tebuthiuron with evaluations at 2 46 8 10 12 14 16 18 and 20 days after emergence at 2 46 8 10 12 14 16 18 and 20 days after emergence DAE Vertical bars represent standard deviations SD of DAE Vertical bars represent standard deviations SD of means n 3 means n 3 100 plant death at 30 DAA were reported in radish It was observed that sorghum showed 62 and 72 with 500 g ha of this herbicide Pires et al 2003b reduction in dry matter 19 and 28 in plant height In peanuts with 300 and 600 g hat of tebuthiuron and 18 and 25 in root length at rates of 300 and there were no symptoms of injury however in the rate of 600 g ha of tebuthiuron respectively regardless of the 1200 gha slight symptoms 5 were observed between rates Table 2 Another study produced similar results 10 to 20 DAE Figure 5 In the two highest rates 2400 in which 44 reduction of dry matter of sorghum at and 4800 g ha of the herbicide there was a constant 50 DAA of sulfentrazone 500 g ha was observed increase in peanut injury over time At 20 DAE there were with a protoporphyrinogen oxidase PPO inhibitor injury levels of 30 and 40 respectively These results are Belo et al 2011 in agreement with Fernandes et al 2012 who reported Peanuts showed a 19 reduction in the dry matter at injury of 24 at 28 DAA in bean with a rate application of 300 g ha and 36 at 600 g ha which did not differ from 800 g ha Over time there was a decrease in symptoms the other rates In the variables above and root length with 18 injury at 56 DAA there were no differences between the evaluated rates in The reduction in dry matter plant height and roots of peanuts Table 2 five plants obtained after the application of different rates of tebuthiuron are shown in Table 2 With the increase of 32 Phytoremediation of CTebuthiuron in Contaminated Soil tebuthiuron rates all plants had decreased dry matter and reduced plant height and roots length when compared to There was a lower concentration of Ctebuthiuron control Table 2 4 in the water from the pots containing peanut Alfalfa and radish showed 100 of death due to compared to those with sorghum In addition there was their high sensitivity to the herbicide Showy rattlepod a higher percentage of the herbicide recovered 8 showed a reduction of 90 77 and 97 in dry matter in the 1 phenological stage one pair of true leaves plant height and root length respectively even at the formed for peanut and 3 leaf for sorghum of the plant lowest rate 300 g ha This result did not differ from compared to the others Table 3 showing the reduction radish and alfalfa in any of the variables evaluated for in the amount of herbicide available for plant absorption any of the rates Table 2 Similar results were observed in the soil solution in showy rattlepod Pires et al 2003a and in radish Peanut had a higher percentage of Ctebuthiuron Pires et al 2003b which showed 100 mortality when than sorghum in all phenological stages indicating greater applied to a rate of 500 g ha efficiency in herbicide absorption Table 3 Although there Adv Weed Sci httpsdoiorg1051694AdvWeedSci20234100002 5 Advances in Weed Science Conciani PA Mendes KF Sousa RN Ribeiro AP Pimpinato RF Tornisielo VL Table 2 Percent reduction in dry matter plant height and root length compared to the control treatment of five plant species cultivated in soil with five rates of tebuthiuron at 20 days after emergence DAE Sorghum 6231bA 7192 bA 8164 bB 1000 bC 1000 bC Showy rattlepod 9030 cA 1000 cA 1000 cA 1000 bA 1000 bA Alfalfa 1000 cA 1000 cA 1000 cA 1000 bA 1000 bA Radish 1000 cA 1000 cA 1000 cA 1000 bA 1000 bA Peanut 1938 aA 3593 ABC 4340 aC 2973 aB 3210 aB Sorghum 1889 aA 2756 aA 5706 bB 1000 bA 1000 bA Showy rattlepod 7697 bA 1000 bA 1000 cA 1000 bA 1000 bA Alfalfa 1000 bA 1000 bA 1000 cA 1000 bA 1000 bA Radish 1000 bA 1000 bA 1000 cA 1000 bA 1000 bA Peanut 2012 aA 2703 aA 1788 aA 1951 aA 1483 aA Sorghum 1785 aAB 2475 aB 852 aA 1000 bC 1000 bC Showy rattlepod 9735 bA 1000 bA 1000 bA 1000 bA 1000 bA Alfalfa 1000 bA 1000 bA 1000 bA 1000 bA 1000 bA Radish 1000 bA 1000 bA 1000 bA 1000 bA 1000 bA Peanut 711 aA 1029 aA 637 aA 1029 aA 392 aA Means followed by the same lowercase letter in the column and capital in the row do not differ by Tukeys test p005 was a considerable variation in the percentage of herbicide accumulation of tebuthiuron in the leaves within 24 h recovered there was no difference in the concentration of Demethylation was determined to be the primary Ctebuthiuron found in the analyzed plants throughout detoxification mechanism of this herbicide by eastern the phenological stages showing that there was herbicide redcedar loblolly pine and bur oak Quercus macrocarpa absorption by the plants McNeil et al 1984 Thus it can be affirmed that the root absorption of the The potential of showy rattlepod jack bean velvet 4Ctebuthiuron present in the soil and the translocation bean and white lupin in the soil phytoremediation of this herbicide for the two species occurred continuously treated with Cquinclorac and Ctebuthiuron was throughout the phenological stages Figure 6 studied and all species were reported to have the Over the evaluation time there was a decrease in the potential to remedy soils contaminated with both sharpness of the C in the autoradiography The decreases herbicides Mendes et al 2021a The same authors also is due to the percentage of radioactivity recovered from observed that the translocation of Ctebuthiuron was the herbicide in the plants remained constant while the greater in the old leaves than roots and young leaves concentration of radioactivity per gram of dry matter also the translocation of Cquinclorac synthetic auxin decreased as the plants grew Figure 6 This confirmed was higher in the young leaves compared to the old that there was no accumulation of the herbicide molecule leaves roots and cotyledons The same Ctebuthiuron in the plant Possibly the plants metabolized the herbicide behavior in was observed in our study as found by Johnsen 1992 in Utah junipers trees There was a reduction in the percentage of Juniperus osteosperma Loblolly pine Pinus taeda and Ctebuthiuron recovered in the soil over time for eastern redcedar Juniperus virginiana can prevent the both plants showing that peanuts and sorghum 6 Adv Weed Sci httpsdoiorg1051694AdvWeedSci20234100002 Advances in Weed Science Plant selection and phytoremediation from herbicidecontaminated soil a na cette Contin japonicas and corn Zea mays was above ground less than the different matrices about the initially rate applied 3 in the roots and less than 15 was in the nutrient 600 g ha in peanut Arachis hypogaea and sorghum solution Steinert Stritzke 1977 Generally tebuthiuron Sorghum bicolor in three phenological stages and its metabolites are found in plants however in low concentration Johnsen Morton 1991 In this study peanut at all phenological stages was more efficient in decreasing the amount of 4Ctebuthiuron with 69 43 and 24 in stages 1 24 Beguut a oe ee or and 37 In sorghum was recovered 98 86 and 55 of the herbicide initially applied respectively Table 3 Peanut Sorghum 870 655 450 658 and sorghum were able to phytoremediate however Mean 772 a 484b 329b peanut was more efficient in reducing contamination of cv 3678 tebuthiuron 76 from the soil than sorghum 45 at the 3 phenological stage Native microorganisms from sugarcanes rhizosphere had a synergistic bacterial pool able to produce 90 mg CO day upon the target tebuthiuron at 5 mmol g Lima et al 2022 Thus these authors clearly showed the microbial Peanut 083 v6 056 08S degradation of tebuthiuron in the rhizosphere soil Sorghum 006 030 039 025b It is evident that further studies are needed with Mean 0443 073a 0484 these species over the whole life cycle and to establish a cv 3958 comparison of the effect with uncultivated soils In order to demonstrate the maximum potential for herbicide phytoextractionphytodegradation by these species In peanut and sorghum there was a decrease in the total radioactivity recovered over the evaluation time confirming the degradation of the herbicide in Peanut cae aca eect e205 the soil which it was probably mineralized to CCO Sorghum 9842 8556 5551 7983 a Table 3 Under higher tebuthiuron concentrations Mean 8360a 6410b 3985 1000 g ha the mean CO evolution rate was higher cvs 4260 in the rhizospheric soil of jack bean followed by velvet bean and Georgia velvet bean Pires et al 2005b Accordingly when tebuthiuron was applied at 1000 g ha jack bean showed the best phytoremediation results Pires et al 2005a Peanut 7635 4694 2686 5005 b 4 Conclusions Sorghum 10720 9242 6041 8667 a Mean 91774 6968b 4363c Alfalfa radish and showy rattlepod were sensitive to the tebuthiuron presence in the soil not showing a a potential for phytoremediation of soil with residues One pair of true leaves formed 1 phenological stage 1 pair of branches of this herbicide Conversely sorghum and peanut 2 and beginning of flowering 3 for peanut and 3 leaf 1s phenological stage 5 leaf 2 and fully extended 3 flag leaf for sorghum Means were tolerant to tebuthiuron Peanut was able to followed by the same lowercase letter in the column and capital in the row phytoremediate 31 more herbicide from soil than do not differ by Tukeys test p005 sorghum at the 3 phenological stage even though the life cycle of the plants was not completed Thus both were efficient in the phytoextraction of tebuthiuron plants can be recommended in successionrotation phytodegradation metabolization by the plant with crops that have the tebuthiuron applied for pre andor rhizodegradation by the microorganisms emergence weed control This study is an important activity in the roots Seedlings of winged elm Ulmus contribution to new insights into herbicide physiology alata bur oak black walnut Juglans nigra eastern redcedar and loblolly pine also had root absorption a and leaf accumulation of Ctebuthiuron McNeil et al Authors contributions 1984 Less than 55 of the recovered activity of All authors read and agreed to the published 4Ctebuthiuron for species Japanese brome Bromus version of the manuscript PAC KFM and VLT Adv Weed Sci httpsdoiorg1051694AdvWeedSci20234100002 7 Advances in Weed Science Conciani PA Mendes KF Sousa RN Ribeiro AP Pimpinato RF Tornisielo VL det BLU Sorghum 1 ae ites ay meg ea Es a Pea cL cre eal Ne daniel Behe tet mn Gel Eich ay A se SNe sere wee i end a Re eng SS A ph ae ae ere oath cee eee Hae dears lth pec he OP ae ees reece a iz pe Oy 2 fa ee ba as oi Lore re aa Pa edie ee po et ee eee eg Sa nein viele ee ms ee tf 4 at Hy ie a ee oon SE ee he a Pee i ee a seek eee Beebe he eat egy ar joel cate sca ie ae ae Wear Te nee ae Le Are ae cs ee eR ts ae oe WC ey ieee ae ot ee Yc ae a de ae a eas on eS SS ety rate se ely s0 i yer lt he Adee oe ee ON RM Se eee ae es emer Se of NN ee ee See Ss WE ge RR ese ys oy ie i berets ey NE Nae pe eet 3 iad ny Ss ae rt a SE 4 eiaat Os Lor jt 7 2w mel I i i aa J H Th Figure 6 Visualization of phosphorescence images of autoradiography top and digital images bottom of peanut Arachis hypogaea and sorghum Sorghum bicolor with Ctebuthiuron application 600 g ha in three phenological stages One pair of true leaves formed 1 phenological stage 1 pair of branches 2 and beginning of flowering 3 for peanut and 3 leaf 1st phenological stage S leaf 2 and fully extended 3 flag leaf for sorghum The darker the gray the greater the radioactivity emitted by C or Acknowledgments conceptualization of the manuscript and development 9 of the methodology PAC and RFP data collection and The first author thanks Conselho Nacional de curation PAC and KEM data analysis PAC RNS and Desenvolvimento Cientifico e Tecnolégico CNPq for granting APR data interpretation VLT funding acquisition and the scholarship resources PAC and VLT project administration VLT supervision PAC KFM RNS APR and RFP writing the Fundin original draft of the manuscript PAC KFM RNS APR 9 and VLT writing review and editing This research received no external funding References Belo AF Coelho ATCP Ferreira LR Silva AA Santos JB Potential of in weeds and crops In Mendes KF Organizer Radioisotopes in weed plant species in the remediation of soil contaminated with sulfentra research Boca Raton CRC Press 2021 p 13058 zone Planta Daninha 201129482128 Portuguese Available from Faria AT Goncalves BFS Seraiva DT Souza ME Silva AA Silva DV httpsdoiorg101590SO010083582011000400012 yo Activity of rhizosphere soil microorganisms of sugarcane cultivars Bernardes MFF Maschio LR Oliveira MTVA Almeida EA Biochem after spraying of herbicides diuron tebuthiuron ametryn and diuron ical and genotoxic effects of a commercial formulation of the hexazinone Rev Caatinga 2018313593601 Available from herbicide tebuthiuron in Oreochromis niloticus of different siz httpsdoiorg101590198321252018v31n307rc nr renartocraey cr Ses Available from Fernandes CPC Braz AJBP Procopio SO Dan HA Braz GBP Barroso PSCoLorgr eee a ALL et al Selectivity of pre and postemergence herbicides registered Cruz RA Amaral GS Mendes KF RojanoDelgado AM Prado R Silva for use in sugarcane to common beans Rev Trop Cienc Agraria Biol MFGF Absorption translocation and metabolism studies of herbicides 201262821 Portuguese 8 Adv Weed Sci httpsdoiorg1051694AdvWeedSci20234100002 Advances in Weed Science Plant selection and phytoremediation from herbicidecontaminated soil Ferreira LC Moreira BRA Montagnolli RN Prado EP Viana RS Mercurio P Mueller JF Eaglesham G Flores F Negri AP Herbicide per Tomaz RS et al Green manure species for phytoremediation of soil sistence in seawater simulation experiments PLoS ONE 201510112 with tebuthiuron and vinasse Front Bioeng Biotechnol Jan 5 2021 Available from httpsdoiorg101371journalpone0136391 Available from httpsdoiorg103389fbioe2020613642 Paiva MCG Mendes KF Phytoremediation technique to herbi Guimardes ACD Paula DF Mendes KF Sousa RN Aratjo GR In cidespolluted soils In Mendes KF organizer Pesticides in agricul oue MH et al Can soil type interfere in sorptiondesorption mobil ture and environment Hooghly Book Publisher International 2021 ity leaching degradation and microbial activity of the Ctebuth p 4557 Available from httpsdoiorg109734bpimono97893 iuron herbicide J Hazard Mater Adv 20226 Available from 91882143CHS httpsdoiorg101016jh 2022100074 ps601019101016jnazadv20 000 Pires FR Procépio SO Santos JB Souza CM Dias RR Phytoremedi Johnsen TN Morton HL Longterm tebuthiuron content of grasses and ation evaluation of tebuthiuron using Crotalaria juncea as an indicator shribs on semiarid rangelands J Range Manag 199144324953 plant Rev Cienc Agron 200839224550 Portuguese Johnsen TN Observations potential longterm environmental im Pires FR Procdpio SO Souza CM Santos JB Silva GP Green manures pact of tebuthiuron and its metabolites in Utah juniper trees J Range in phytoremediation of soils contaminated with the herbicide tebuthi Manag 199245216770 uron Rev Caatinga 2006191927 Portuguese Lima EW Brunaldi BP Frias YA Moreira BRA Alves LS Lopes PRM A syn Pires FR Souza CM Cecon PR Santos JB Tétola MR Procépio ergistic bacterial pool decomposes tebuthiuron in soil Sci Rep 2022121 SO et al Rhizospheric activity of potentially phytoremedia 12 Available from httpsdoiorg101038s41598022131478 tive species for tebuthiuroncontaminated soil Rev Bras Cienc lo 2 29462734 Port Available f httpsdoi McNeil WK Stritzke JF Basler E Absorption translocation and deg Solo 2008b2946273 ortuguese Available from httpsdoi org101590S010006832005000400015 radation of tebuthiuron and hexazinone in woody species Weed Sci 198432673943 Available from httpsdoiorg101017 Pires FR Souza CM Silva AA Cecon PR Procdpio SO 0043174500059919 Santos JB et al Phytoremediation of tebuthiuroncontaminated Mendes KF Martins BAB Reis FC Dias ACR Tornisielo VL Methodol solls using species cultivated for green manure Planta Daninha 2005a2347117 Portuguese Available from httpsdoiorg101590 ogies to study the behavior of herbicides on plants and the soil using 010083582005000400020 radioisotopes Planta Daninha 201735121 Available from httpsdoi org101590S010083582017350100049 Pires FR Souza CM Silva AA Procépio SO Ferreira LR Phytoremediation of Mendes KF Maset BA Mielke KC Sousa RN Martins BAB Tornisielo VL herbicidepolluted soils Pianta Daninha 2003a21233541 Portuguese aa Available from httpsdoiorg101590SO10083582003000200020 Phytoremediation of quinclorac and tebuthiuronpolluted soil by green manure plants Int J Phytoremediation 2021a23547481 Available Pires FR Souza CM Silva AA Queiroz MELR Procépio SO Santos from httpsdoiorg1010801522651420201825329 JB et al Plant selection with potential for tebuthiuron phytodecon ination Planta Daninha 2 2134518 P Avail Mendes KF Régo APJ Takeshita V Tornisielo VL Water resource pol aeen on a j ane omnia sseabboabeaaboo rs e from sdoior lution by herbicide residues In Ince M Ince OK Ondrasek G organiz P hog ers Biochemical toxicology heavy metals and nanomaterials London Qian Y Matsumoto H Liu X Li S Liang X Liu Y et al Dissipation IntechOpen 2020access November 1 2022 p 116 Available from occurrence and risk assessment of a phenylurea herbicide tebuthi httpsdoiorg105772intechopen85159 uron in sugarcane and aquatic ecosystems in South China Environ Mendes KF Silva AA Mielke KC Classification selectivity and mech ree sOnoses Available from httpsdolorg101016 anisms of action of herbicides In Mendes KF Silva AA organizers enVvpor Weeds herbicides vol 2 SAo Paulo Oficina de Textos 2022 p 756 Steinert WG Stritzke JF Uptake and phytotoxicity of tebuthiuron Portuguese Weed Sci 19772553905 Available from httpsdoiorg101017 Mendes KF Wei MCF Furtado IF Takeshita V Pissolito JP Molin 0043174500033725 JP et al Spatial distribution of sorption and desorption process of Teofilo TMS Mendes KF Fernandes BCC Oliveira FS Silva TS Takeshita Cradiolabelled hexazinone and tebuthiuron in tropical soil Chemo Vet al Phytoextraction of diuron hexazinone and sulfometuronmethyl sphere 2021b2641 Available from httpsdoiorg101016jchemo from the soil by green manure species Chemosphere 2020256 Avail sphere2020128494 able from httpsdoiorg101016jchemosphere2020127059 Adv Weed Sci httpsdoiorg1051694AdvWeedSci20234100002 9
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RESEARCH ARTICLE formerly Planta Daninha SPECIAL TOPICS New Insights Peanut and sorghum are excellent phytoremediators of 14Ctebuthiuron in herbicidecontaminated soil Paulo A Conciania Kassio F Mendesb Rodrigo N de Sousac Andrew de P Ribeirob Rodrigo F Pimpinatoa Valdemar L Tornisieloa a Laboratory of Ecotoxicology Center for Nuclear Energy in Agriculture University of São Paulo Piracicaba SP Brazil b Department of Agronomy Federal University of Viçosa Viçosa MG Brazil c Department of Soil Science Luiz de Queiroz College of Agriculture Piracicaba SP Brazil Journal Information ISSN 26759462 Website httpawsjournalorg Journal of the Brazilian Weed Science Society How to cite Conciani PA Mendes KF Sousa RN Ribeiro AP Pimpinato RF Tornisielo VL Peanut and sorghum are excellent phytoremediators of 14Ctebuthiuron in herbicide contaminated soil Adv Weed Sci202341e020220068 httpsdoiorg1051694AdvWeedSci20234100002 Approved by Editor in Chief Carol Ann MallorySmith Associate Editor Marcos Yannicari Conflict of Interest The authors declare that there is no conflict of interest regarding the publication of this manuscript Received September 28 2022 Approved November 17 2022 Corresponding author kfmendesufvbr 1 This is an openaccess article distributed under the terms of the Creative Commons Attribution License which permits unrestricted use distribution and reproduction in any medium provided that the original author and source are credited 1 Introduction The contamination of the environment by pesticides including herbicides is a major global concern and can be considered a major obstacle to the development of sustainable agriculture Mendes et al 2020 There is social and scientific appeal for the minimization of environmental impacts caused by the use of herbicides in the large areas cultivated with sugarcane and the increase of areas treated with long residual effect herbicides such as tebuthiuron Tebuthiuron 15tertbutyl134thiadiazol2yl13dimethylurea is a systemic herbicide absorbed by roots and translocated in weeds widely used in sugarcane with a photosystem II PSII inhibitors mode of action of the urea chemical group Mendes et al 2022 This herbicide has a high leaching potential due to its high water solubility Sw 2500 mg L1 and low sorption sorption coefficient Kd 132 and 085 L Kg1 in clay and loamy sand soil respectively Guimarães et al 2022 A positive correlation among clay content soil organic matter SOM and tebuthiuron sorption was found by Mendes et al 2021 Also this herbicide has a high persistence in the soil 90 degradation time DT90 385 and 334 d Guimarães et al 2022 However bacteria can effectively degrade tebuthiuron in soil Lima et al 2022 and seawater Mercurio et al 2015 The application of herbicides with residual effects in the soil is essential for weed control in preemergence Nevertheless if the residual effect is greater than the cycle of the crop it can cause injury in the next crop rotationsuccession a process commonly known as carryover On the other hand tebuthiuron can have negative impacts on soil microorganisms Faria et al 2018 and water Bernardes et al 2014 In the sugarcane fieldsurrounding aquatic environment tebuthiuron distribution ranged from 0007 to 0022 mg L1 leading to a high risk at in aquatic ecosystems Qian et al 2017 as DNA damage in exposed small fish Oreochromis niloticus can occur Bernardes et al 2014 Then using strategies to remediate herbicides in contaminated soils is critical in agricultural systems Phytoremediation is one option to reduce the environment in soil contaminated by residual herbicides such as tebuthiuron Mendes et al 2021a and 2021b Abstract Background Phytoremediation is a technique used in soils contaminated with residual herbicides such as tebuthiuron However the herbicide presence in the soil and plant matrices are not generally quantified Objective This study aimed to select plant species to evaluate the phytoremediation of 14Ctebuthiuron by showy rattlepod Crotalaria spectabilis sorghum Sorghum bicolor radish Raphanus sativus peanut Arachis hypogaea and alfalfa Medicago sativa in herbicidecontaminated soil Methods The selection of the five herbicide phytoremediation plants was with the application of five rates of tebuthiuron 300 600 1200 2400 and 4800 g ai ha1 and compared to a control Peanuts and sorghum herbicidetolerant plants were sown in soil contaminated with tebuthiuron 600 g ai ha1 applied through a working solution containing 1747 kBq of 14Ctebuthiuron The total of herbicide was analyzed in the soil and plant at three phenological stages Results Showy rattlepod radish and alfalfa were sensitive to the herbicide even at the lowest application rate Sorghum was tolerant to the herbicide up to 600 g ha1 with the application of 1200 g ha1 there was 80 injury peanut was tolerant even at the highest rate 4800 g ha1 with only 40 injury Peanut and sorghum were able to phytoremediate the soil although peanut was more efficient in decreasing tebuthiuron contamination by 76 while sorghum reduced at by 45 at 3rd phenological stage Conclusions Thus both plants can be recommended in succession rotation with crops that had tebuthiuron applied from preemergence weed control Keywords Root absorption Rhizodegradation Radiolabeled herbicide Decontamination Crop Copyright 2022 Advances in Weed Science Conciani PA Mendes KF Sousa RN Ribeiro AP Pimpinato RF Tornisielo VL Results showed preliminary evidence of effective 22 Installation ofthe studies phytoremediation capacity by velvet bean Mucuna Two experiments were carried out for the development pruriens pearl millet Pennisetum glaucum and sunn of this study The first was to select five species of hemp Crotalaria juncea in tebuthiuron contaminatedsoil agronomic interest for phytoremediation at different Ferreira et al 2021 In the highest rate of tebuthiuron levels of soil imation by tebuthi Seeds f 1500 ha applied jack bean C ensiformis white evels of soil contamination by tebuthiuron Seeds from le tous i 1 mill t 2 ol the herbicide tolerant species that survived in the first upin Lupinus albus and pearl millet P glaucum were tud Ilected and d in th d stud the species with better phytoremediation effects Pires et ch the hvemedhstion o f cor hee aad ane al 2008 When the soil was treated with tebuthiuron at i P y db hi 8 d P d 1000 g ha jack bean followed by white lupin and velvet sot contaminate y tebut turon was determined The bean were the species that had better phytoremediation studies were conducted in a glass greenhouse for one year Pires et al 2006 However the phenological stages of During this period the averages observed for maximum the phytoremediation species and their association with 538C ne and average temperatures were 304 172 and rhizosphere microorganisms can directly interfere in the Fespecuvey amount of herbicide degraded The phytoremediation technique increases in 221 Plant selection for phytoremediation of tebuthiuron in complexity as researchers try to select species that present contaminated soil remediation capacity and other agronomic benefits to The experiment was set up in a randomized block farmers However phytoremediation is sustainable and desion j factorial sch 5x6 with th re effective less expensive and destructive when compared to Send f ac ea seneme m 1 nee i has eeds oO ve plant species showy rattlepod sorghum other soil decontamination processes and can be applied dish P d If y P oa d large areas Paiva Mendes 2021 radish peanut and alfalfa were grown in pots fille oe Then h techni tes of use of herbicides radiolabeled with soil sprayed simulated contamination by six rates ith Mc ti q ble t ty th tential of of tebuthiuron Ox 14x 12x x 2x and 4x in which x wi 1S Posstbie fo very ene porenna represents the maximum rate recommended for field phytoremediation of plant species at the laboratory re 1 fo application of the herbicide 1200 g ai ha condition since this technique allows accurately 1 ith ity of 1 determining the absorption and translocation of Fo ystyrene pots with a capacity of approximately 1500 small amounts of herbicides in vlants such as diuron cm were used Each pot received 800 g of dry soil and water hexazinone sulfometuronmeth i Tedfilo et al 202 0 was added to reach field capacity Twentyfour hours after quinclorac an dtebuthiuron Men des et al 202 1a the soil reached saturation point each pot was sown with 20 Many phytoreme diation studies of various herbici des seeds of each specie that then were covered by 100 g of dry in contaminated soils have been carried out in several soil eee eee cer of the pot each rate was edaphoclimatic conditions and with a diversity of plant PON species H h prepared in a concentration of active ingredient per pecies However there is still a lack of studies that detect 4 1s application volume equivalent to the rate of 200 L ha The herbicides by analytical techniques in the soil and plants Thus this study aimed to select plant species to evaluate herbicide application was used a chamber with spray nozzle was 14 TTI11002 and the constant pressure of 2792 kPa for the phytoremediation of Ctebuthiuron by showy rattlepod Crotalaria spectabilis sorghum Sorghum bicolor The herbicide was applied at the appearance of the first 1 leaf until the emergence of the second pair of leaves radish Raphanus sativus peanut Arachis hypogaea and true wo every two days visual evaluations of the injury level were alfalfa Medicago sativa in soil performed according to a scale of 0 to 100 where 0 represents the absence of symptoms and 100 represents 2 Material and Methods death of the plant After injury level evaluations the pots were 21 Soil collection and preparation disassembled and from each plot three plants were To ensure that there was no previous contamination randomly collected Each plant measured by plant height with herbicides in the soil used in this study the soil was and root length and stored in paper bags The collected collected in native forests permanent preservation area plants were dried 72 h in an oven heated to 40 C and near PiracicabaSP Brazil at a minimum distance of 20m then weighed to determine the accumulated dry matter from the edge of a road For the data on percent reduction in dry matter A preliminary cleaning was performed eliminating plant height and root length Tukeys test p005 was leaves and pieces of plants from the soil surface and then performed to verify the difference between the treatments the layer from 0 to 10 cm deep was collected The collected The level injury data were expressed as mean and standard soil was airdried homogenized and passed through a 2 deviation n 3 All figures were plotted using Sigma Plot mm sieve and the physical and chemical properties were version 100 for Windows Systat Software Inc Point analyzed Table 1 Richmond CA USA 2 Adv Weed Sci httpsdoiorg1051694AdvWeedSci20234100002 Advances in Weed Science Plant selection and phytoremediation from herbicidecontaminated soil Table 1 Soil physical and chemical properties CaCL mg cm mmol dm gdm mmol dm 66 10 6 33 74 18 1 20 69 955 116 83 clay 406 150 444 exchange capacity SB saturation base Source Soil Laboratory Luiz de Queiroz College of Agriculture University of Sdo Paulo Piracicaba SP Brazil 222 Phytoremediation of CTebuthiuron in contaminated soil and dried in an oven for 72 h at 40 C The dried soil was Pots with a capacity of 2800 cm filled with 900 g of crumbled homogenized and ground Three samples of 02 g each were burned in a biological oxidizer RJ Harvey airdried soil were used Water was added to the trays of the ye ys Instrument Corporation OX500 Tappan NY USA at pots until it reached the soil surface by capillarity action am 900 C in porcelain dishes by 3 min to determine the After 24 h each pot received either 5 sorghum or 5 peanut Ls 4 7 14 radioactivity amount of Cherbicide mineralized to C seeds species selected in the first study and a layer of 100 14 CO The Ctebuthiuron concentration was determined g of dry soil was deposited over the seeds Lo eer using a Liquid Scintillation Spectrometry LSS for 15 The study was a randomized block design with a min with a TriCarb 2910 TR LSS counter PerkinElmer factorial scheme 2x3 with two plant species sorghum d t in th henological st devel t Waltham MA USA an peanut 1 ree paeno ogica Stages oF cevetopments After centrifugation to separate the soil the solution with three repetitions In addition a control treatment h diluted with distillated Th herbicide application was added for comparison of the rom the Pots was Guuted with cistivated water unree ne er PP P aliquots 10 mL each of this solution were taken from ot cr nn the oy il f th d th each pot To each sample 10 mL of the scintillator Given the sma Surlace area t pots an t solution Instagel plus was added and then measured handling of a radioactive product the herbicide application LSS was performed by adding 100 g of treaded dry soil A The phytoremediation was evaluated by absorption working solution containing 1747 kBq of Ctebuthiuron 4 translocation of Ctebuthiuron This study CUL specific activity 301 MBq mg radiochemical was qualitatively analyzed by autoradiography and purity 98 and technical product nonradiolabeled quantitatively by combustion of plant tissues Plants were was prepared to reach 600 g ai ha of herbicide rate washed pressed and dried in a forced circulation oven recommended in the field at 45 C for 120 h One triplicate in each plant was used Whenever necessary the reestablishment of the according to Mendes et al 2017 and Cruz et al 2021 on moisture in the pots occurred through the deposition of phosphorus film plates for 120 h and analyzed in a radio water in the trays to maintain soil moisture close to field scanner PerkinElmer Storage Phosphor System model capacity and avoid herbicide leaching Cyclone Plus Shelton WA USA When the plants reached the desired three stages of After drying the plants were removed and divided phenological development one pair of true leaves formed into leaves roots stems and cotyledon when this was 1 phenological stage 1 pair of branches 2 and still present to quantify the radioactivity in each part of beginning of flowering 3 for peanut and 3 leaf 1 the plant phenological stage 5 leaf 2 and fully extended 3 The samples were burned in a biological oxidizer flag leaf for sorghum The plants were removed from with three repetitions for each part of the plant The C the pots and placed on plastic trays A KCl 002 mol L CO released in the combustion was collected in a flask solution was used to wash the roots containing scintillator solution plus monoethanolamine The trays were left to stand for 24h for sedimentation and methanol The radioactivity contained in this flask was of the solution The soil solution was collected to quantify determined in aLSS the herbicide remaining and centrifuged Hitachi Radioactivity present in all parts of the plants was CF16RXII Hitachi Koki Co Ltd Indaiatuba SP Brazil considered as translocation because the initial herbicide in Teflon flasks at 4000 rpm for 15 min to remove the soil application was in the soil The data were expressed as suspension The sediment soil was returned to the trays mean n3 Adv Weed Sci httpsdoiorg1051694AdvWeedSci20234100002 3 Advances in Weed Science Conciani PA Mendes KF Sousa RN Ribeiro AP Pimpinato RF Tornisielo VL 3 Results and Discussion died and had 83 injury to radish treated with a rate of 500 g ha Pirest et al 2003a Corroborating this data 31 Plant selection for phytoremediation of tebuthiuron in in another study the injury levels of 95 at 15 DAA and contaminated soil At the rates of 300 and 600 g ha of tebuthiuron there was a small initial incidence of injury level 8 i 100 ne in sorghum compared to the control treatment no a Eo herbicide However after 10 days after emergence DAE Kk om there was a tendency in decreased injury symptoms and 80 at 20 DAE the injury did not differ from the control S i i treatment Figure 1 60 1 17 A study performed by Pires et al 2003a showed the effects of different rates of tebuthiuron in multiple species 8 40 A in which the authors also found a lower injury 25 in s i pearl millet Pennisetum glaucum treated with 500 g ha of 20 tebuthiuron at 60 days after application DAA LY At rates of 1200 2400 and 4800 g ha of tebuthiuron 0 ao the initial symptoms of injury in sorghum increased 0 2 4 6 8 1 12 14 16 18 20 over time reaching 80 with 1200 g ha and values Days After Emergence DAE 1 above 95 in rates of 2400 and 4800 g ha Figure 1 300 gha g 1007541expx77791245 R 099 p001 These results corroborate those of Pires et al 2003a 600 gha g 1000311expx68891222 R 099 p001 in which pearl millet plants had an injury level of 76 v rane Me Oe Oe eee Sere oemel Re nee a A g hat g 983691explx29400654 R 099 p001 compared to the control when treated with 1000 g ha M4800 g ha 9 98290texplx27120618 R 098 p001 of tebuthiuron and 100 with the rate of 2000 g hat at 60 DAA Even at the lowest rate of tebuthiuron 300 g ha all Figure 2 Injury level in showy rattlepod Crotalaria spectabilis showy rattlepod plants died at 12 DAE Figure 2 the same caused by the application of five rates of tebuthiuron with can be observed for alfalfa Figure 3 and radish Figure 4 evaluations at 2 4 6 8 10 12 14 16 18 and 20 days after respectively at 8and10 DAE At60 DAA showvrattlepod mengence DAE Vertical bars represent standard deviations P Y y P SD of means n 3 100 100 80 ei t Y 80 o 7 IL xz xX I 60 2 3 2 s 2 5 40 2 40 Ir a 20 i 20 as ate Se LLL Ee 0 0 0 2 4 6 8 1 1 14 16 18 20 0 2 4 6 8 0 172 4 18 20 Days After Emergence DAE Days After Emergence DAE 300 gha g 61661explx100100062 R 094 p001 300 g ha 982911explx34390814 R 099 p001 600 gha g 72091expx35670334 R 085 p001 600g ha g 989921expx38181041 R 099 p001 Vv 1200 gha g 845811expx106752136 R 099 p001 Vv 1200 g ha g 988711expx30340923 R 099 p001 4 2400 g ha g 988521expx101312218 R 099 p001 2400 g ha g 1000171explx29400654 R 099 p001 m 4800 g ha g 1018361expx86671879 R2 098 p001 m 4800 g hat Y 1000341expx01311054 R 039 p001 Figure 1 Injury level in sorghum Sorghum bicolor caused by Figure 3 Injury level in alfalfa Medicago sativa caused by the application of five rates of tebuthiuron with evaluations the application of five rates of tebuthiuron with evaluations at 2 4 6 8 10 12 14 16 18 and 20 days after emergence at 2 46 810 12 14 16 18 and 20 days after emergence DAE Vertical bars represent standard deviations SD of DAE Vertical bars represent standard deviations SD of means n 3 means n 3 4 Adv Weed Sci httpsdoiorg1051694AdvWeedSci20234100002 Advances in Weed Science Plant selection and phytoremediation from herbicidecontaminated soil 100 100 KE 80 ly 80 J j 60 fi S 60 g t Q 3 40 i j 3 40 r 4 20 20 ae 0 an 0 FF 0 2 4 6 8 10 12 14 16 18 20 0 2 4 6 8 10 12 14 16 18 20 Days After Emergence DAE Days After Emergence DAE 300 ghar g 1016851explx59551543 R 098 p001 300ghagg0 600g ha g 1010901explx64541118 R 099 p001 600 ghagy0 V 1200 g ha g 989991expx34261003 R 099 p001 1200 g ha g 35241expx112560805 R 081 p005 2400 g ha G 990101expx25201320 R 099 p001 2400 g ha G 274421expfx121332595 R 094 p001 4800 g ha G 992881expx02441883 R 096 p001 4800 g ha g 487851expx139654340 R 095 p001 Figure 4 Injury level in radish Raphanus sativus caused by Figure 5 Injury level in peanut Arachis hypogaea caused by the application of five rates of tebuthiuron with evaluations the application of five rates of tebuthiuron with evaluations at 2 46 8 10 12 14 16 18 and 20 days after emergence at 2 46 8 10 12 14 16 18 and 20 days after emergence DAE Vertical bars represent standard deviations SD of DAE Vertical bars represent standard deviations SD of means n 3 means n 3 100 plant death at 30 DAA were reported in radish It was observed that sorghum showed 62 and 72 with 500 g ha of this herbicide Pires et al 2003b reduction in dry matter 19 and 28 in plant height In peanuts with 300 and 600 g hat of tebuthiuron and 18 and 25 in root length at rates of 300 and there were no symptoms of injury however in the rate of 600 g ha of tebuthiuron respectively regardless of the 1200 gha slight symptoms 5 were observed between rates Table 2 Another study produced similar results 10 to 20 DAE Figure 5 In the two highest rates 2400 in which 44 reduction of dry matter of sorghum at and 4800 g ha of the herbicide there was a constant 50 DAA of sulfentrazone 500 g ha was observed increase in peanut injury over time At 20 DAE there were with a protoporphyrinogen oxidase PPO inhibitor injury levels of 30 and 40 respectively These results are Belo et al 2011 in agreement with Fernandes et al 2012 who reported Peanuts showed a 19 reduction in the dry matter at injury of 24 at 28 DAA in bean with a rate application of 300 g ha and 36 at 600 g ha which did not differ from 800 g ha Over time there was a decrease in symptoms the other rates In the variables above and root length with 18 injury at 56 DAA there were no differences between the evaluated rates in The reduction in dry matter plant height and roots of peanuts Table 2 five plants obtained after the application of different rates of tebuthiuron are shown in Table 2 With the increase of 32 Phytoremediation of CTebuthiuron in Contaminated Soil tebuthiuron rates all plants had decreased dry matter and reduced plant height and roots length when compared to There was a lower concentration of Ctebuthiuron control Table 2 4 in the water from the pots containing peanut Alfalfa and radish showed 100 of death due to compared to those with sorghum In addition there was their high sensitivity to the herbicide Showy rattlepod a higher percentage of the herbicide recovered 8 showed a reduction of 90 77 and 97 in dry matter in the 1 phenological stage one pair of true leaves plant height and root length respectively even at the formed for peanut and 3 leaf for sorghum of the plant lowest rate 300 g ha This result did not differ from compared to the others Table 3 showing the reduction radish and alfalfa in any of the variables evaluated for in the amount of herbicide available for plant absorption any of the rates Table 2 Similar results were observed in the soil solution in showy rattlepod Pires et al 2003a and in radish Peanut had a higher percentage of Ctebuthiuron Pires et al 2003b which showed 100 mortality when than sorghum in all phenological stages indicating greater applied to a rate of 500 g ha efficiency in herbicide absorption Table 3 Although there Adv Weed Sci httpsdoiorg1051694AdvWeedSci20234100002 5 Advances in Weed Science Conciani PA Mendes KF Sousa RN Ribeiro AP Pimpinato RF Tornisielo VL Table 2 Percent reduction in dry matter plant height and root length compared to the control treatment of five plant species cultivated in soil with five rates of tebuthiuron at 20 days after emergence DAE Sorghum 6231bA 7192 bA 8164 bB 1000 bC 1000 bC Showy rattlepod 9030 cA 1000 cA 1000 cA 1000 bA 1000 bA Alfalfa 1000 cA 1000 cA 1000 cA 1000 bA 1000 bA Radish 1000 cA 1000 cA 1000 cA 1000 bA 1000 bA Peanut 1938 aA 3593 ABC 4340 aC 2973 aB 3210 aB Sorghum 1889 aA 2756 aA 5706 bB 1000 bA 1000 bA Showy rattlepod 7697 bA 1000 bA 1000 cA 1000 bA 1000 bA Alfalfa 1000 bA 1000 bA 1000 cA 1000 bA 1000 bA Radish 1000 bA 1000 bA 1000 cA 1000 bA 1000 bA Peanut 2012 aA 2703 aA 1788 aA 1951 aA 1483 aA Sorghum 1785 aAB 2475 aB 852 aA 1000 bC 1000 bC Showy rattlepod 9735 bA 1000 bA 1000 bA 1000 bA 1000 bA Alfalfa 1000 bA 1000 bA 1000 bA 1000 bA 1000 bA Radish 1000 bA 1000 bA 1000 bA 1000 bA 1000 bA Peanut 711 aA 1029 aA 637 aA 1029 aA 392 aA Means followed by the same lowercase letter in the column and capital in the row do not differ by Tukeys test p005 was a considerable variation in the percentage of herbicide accumulation of tebuthiuron in the leaves within 24 h recovered there was no difference in the concentration of Demethylation was determined to be the primary Ctebuthiuron found in the analyzed plants throughout detoxification mechanism of this herbicide by eastern the phenological stages showing that there was herbicide redcedar loblolly pine and bur oak Quercus macrocarpa absorption by the plants McNeil et al 1984 Thus it can be affirmed that the root absorption of the The potential of showy rattlepod jack bean velvet 4Ctebuthiuron present in the soil and the translocation bean and white lupin in the soil phytoremediation of this herbicide for the two species occurred continuously treated with Cquinclorac and Ctebuthiuron was throughout the phenological stages Figure 6 studied and all species were reported to have the Over the evaluation time there was a decrease in the potential to remedy soils contaminated with both sharpness of the C in the autoradiography The decreases herbicides Mendes et al 2021a The same authors also is due to the percentage of radioactivity recovered from observed that the translocation of Ctebuthiuron was the herbicide in the plants remained constant while the greater in the old leaves than roots and young leaves concentration of radioactivity per gram of dry matter also the translocation of Cquinclorac synthetic auxin decreased as the plants grew Figure 6 This confirmed was higher in the young leaves compared to the old that there was no accumulation of the herbicide molecule leaves roots and cotyledons The same Ctebuthiuron in the plant Possibly the plants metabolized the herbicide behavior in was observed in our study as found by Johnsen 1992 in Utah junipers trees There was a reduction in the percentage of Juniperus osteosperma Loblolly pine Pinus taeda and Ctebuthiuron recovered in the soil over time for eastern redcedar Juniperus virginiana can prevent the both plants showing that peanuts and sorghum 6 Adv Weed Sci httpsdoiorg1051694AdvWeedSci20234100002 Advances in Weed Science Plant selection and phytoremediation from herbicidecontaminated soil a na cette Contin japonicas and corn Zea mays was above ground less than the different matrices about the initially rate applied 3 in the roots and less than 15 was in the nutrient 600 g ha in peanut Arachis hypogaea and sorghum solution Steinert Stritzke 1977 Generally tebuthiuron Sorghum bicolor in three phenological stages and its metabolites are found in plants however in low concentration Johnsen Morton 1991 In this study peanut at all phenological stages was more efficient in decreasing the amount of 4Ctebuthiuron with 69 43 and 24 in stages 1 24 Beguut a oe ee or and 37 In sorghum was recovered 98 86 and 55 of the herbicide initially applied respectively Table 3 Peanut Sorghum 870 655 450 658 and sorghum were able to phytoremediate however Mean 772 a 484b 329b peanut was more efficient in reducing contamination of cv 3678 tebuthiuron 76 from the soil than sorghum 45 at the 3 phenological stage Native microorganisms from sugarcanes rhizosphere had a synergistic bacterial pool able to produce 90 mg CO day upon the target tebuthiuron at 5 mmol g Lima et al 2022 Thus these authors clearly showed the microbial Peanut 083 v6 056 08S degradation of tebuthiuron in the rhizosphere soil Sorghum 006 030 039 025b It is evident that further studies are needed with Mean 0443 073a 0484 these species over the whole life cycle and to establish a cv 3958 comparison of the effect with uncultivated soils In order to demonstrate the maximum potential for herbicide phytoextractionphytodegradation by these species In peanut and sorghum there was a decrease in the total radioactivity recovered over the evaluation time confirming the degradation of the herbicide in Peanut cae aca eect e205 the soil which it was probably mineralized to CCO Sorghum 9842 8556 5551 7983 a Table 3 Under higher tebuthiuron concentrations Mean 8360a 6410b 3985 1000 g ha the mean CO evolution rate was higher cvs 4260 in the rhizospheric soil of jack bean followed by velvet bean and Georgia velvet bean Pires et al 2005b Accordingly when tebuthiuron was applied at 1000 g ha jack bean showed the best phytoremediation results Pires et al 2005a Peanut 7635 4694 2686 5005 b 4 Conclusions Sorghum 10720 9242 6041 8667 a Mean 91774 6968b 4363c Alfalfa radish and showy rattlepod were sensitive to the tebuthiuron presence in the soil not showing a a potential for phytoremediation of soil with residues One pair of true leaves formed 1 phenological stage 1 pair of branches of this herbicide Conversely sorghum and peanut 2 and beginning of flowering 3 for peanut and 3 leaf 1s phenological stage 5 leaf 2 and fully extended 3 flag leaf for sorghum Means were tolerant to tebuthiuron Peanut was able to followed by the same lowercase letter in the column and capital in the row phytoremediate 31 more herbicide from soil than do not differ by Tukeys test p005 sorghum at the 3 phenological stage even though the life cycle of the plants was not completed Thus both were efficient in the phytoextraction of tebuthiuron plants can be recommended in successionrotation phytodegradation metabolization by the plant with crops that have the tebuthiuron applied for pre andor rhizodegradation by the microorganisms emergence weed control This study is an important activity in the roots Seedlings of winged elm Ulmus contribution to new insights into herbicide physiology alata bur oak black walnut Juglans nigra eastern redcedar and loblolly pine also had root absorption a and leaf accumulation of Ctebuthiuron McNeil et al Authors contributions 1984 Less than 55 of the recovered activity of All authors read and agreed to the published 4Ctebuthiuron for species Japanese brome Bromus version of the manuscript PAC KFM and VLT Adv Weed Sci httpsdoiorg1051694AdvWeedSci20234100002 7 Advances in Weed Science Conciani PA Mendes KF Sousa RN Ribeiro AP Pimpinato RF Tornisielo VL det BLU Sorghum 1 ae ites ay meg ea Es a Pea cL cre eal Ne daniel Behe tet mn Gel Eich ay A se SNe sere wee i end a Re eng SS A ph ae ae ere oath cee eee Hae dears lth pec he OP ae ees reece a iz pe Oy 2 fa ee ba as oi Lore re aa Pa edie ee po et ee eee eg Sa nein viele ee ms ee tf 4 at Hy ie a ee oon SE ee he a Pee i ee a seek eee Beebe he eat egy ar joel cate sca ie ae ae Wear Te nee ae Le Are ae cs ee eR ts ae oe WC ey ieee ae ot ee Yc ae a de ae a eas on eS SS ety rate se ely s0 i yer lt he Adee oe ee ON RM Se eee ae es emer Se of NN ee ee See Ss WE ge RR ese ys oy ie i berets ey NE Nae pe eet 3 iad ny Ss ae rt a SE 4 eiaat Os Lor jt 7 2w mel I i i aa J H Th Figure 6 Visualization of phosphorescence images of autoradiography top and digital images bottom of peanut Arachis hypogaea and sorghum Sorghum bicolor with Ctebuthiuron application 600 g ha in three phenological stages One pair of true leaves formed 1 phenological stage 1 pair of branches 2 and beginning of flowering 3 for peanut and 3 leaf 1st phenological stage S leaf 2 and fully extended 3 flag leaf for sorghum The darker the gray the greater the radioactivity emitted by C or Acknowledgments conceptualization of the manuscript and development 9 of the methodology PAC and RFP data collection and The first author thanks Conselho Nacional de curation PAC and KEM data analysis PAC RNS and Desenvolvimento Cientifico e Tecnolégico CNPq for granting APR data interpretation VLT funding acquisition and the scholarship resources PAC and VLT project administration VLT supervision PAC KFM RNS APR and RFP writing the Fundin original draft of the manuscript PAC KFM RNS APR 9 and VLT writing review and editing This research received no external funding References Belo AF Coelho ATCP Ferreira LR Silva AA Santos JB Potential of in weeds and crops In Mendes KF Organizer Radioisotopes in weed plant species in the remediation of soil contaminated with sulfentra research Boca Raton CRC Press 2021 p 13058 zone Planta Daninha 201129482128 Portuguese Available from Faria AT Goncalves BFS Seraiva DT Souza ME Silva AA Silva DV httpsdoiorg101590SO010083582011000400012 yo Activity of rhizosphere soil microorganisms of 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