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Dipteryx alata, a tree native to the Brazilian Cerrado, is sensitive to the herbicide nicosulfuron

Abstract

The expansion of land use for agricultural interests and the excessive use of herbicides are among the causes of biodiversity losses in the Brazilian Cerrado biome. Therefore, we aimed to test the hypothesis that Dipteryx alata Vogel, a common species in this biome, is sensitive to nicosulfuron because of its high phytotoxicity. We evaluated physiological, biochemical and morphological responses in D. alata plants exposed to increasing doses of the herbicide. Young plants were transplanted to 10 L pots containing substrate composed of soil and sand (2:1) after fertilization. After an acclimation period, the following doses of nicosulfuron were applied: 0 (control), 6, 12, 24, 48, and 60 g a.e. ha−1. The experiment was conducted in a randomized block design factorial scheme with six doses of nicosulfuron, three evaluation times, and five replicates per treatment. The effects of the herbicide were assessed by measuring gas exchange, chlorophyll a fluorescence, photosynthetic pigments, membrane permeability, antioxidant enzymes and acetolactate synthase. Nicosulfuron altered the photosynthetic machinery and enzymatic metabolism of D. alata. Reductions in physiological traits, increased catalase and ascorbate peroxidase activities, enhanced malondialdehyde concentrations rate of electrolyte leakage and decreased acetolactate synthase activity in response to nicosulfuron all suggest that D. alata is sensitive to this herbicide.

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References

  1. Agostinetto D, Perboni LT, Langaro AC, Gommes J, Fraga DS, Franco JJ (2016) Changes in photosynthesis and oxidate stress in wheat plants submmited to herbicides application. Planta Daninha 34:1–9. https://doi.org/10.1590/S0100-83582016340100001

  2. Anderson D, Prasad K, Stewart R (1995) Changes in isozyme profiles of catalase, peroxidase and glutathione reductase during acclimation to chilling in mesocotyls of maize seedlings. Plant Physiol 109:1247–1257. https://doi.org/10.1104/pp.109.4.1247

  3. Armendáriz O, Gil-Monreal M, Zulet A, Zabalza A, Royuela M (2016) Both foliar and residual applications of herbicides that inhibit amino acid biosynthesis induce alternative respiration and aerobic fermentation in pea roots. Plant Biol 18:382–390. https://doi.org/10.1111/plb.12412

  4. Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287. https://doi.org/10.1016/0003-2697(71)90370-8

  5. Bilger W, Björkman O (1990) Role of xanthophyll cycle in photoprotection elucidated by measurements of light induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth Res 25:73–185. https://doi.org/10.1007/BF00033159

  6. Bilger W, Schereiber U, Bock M (1995) Determination of the quantum efficiency of photosystem II and of non-photochemical quenching of chlorophyll fluorescence in the field. Oecologia 102:425–432. https://doi.org/10.1007/BF00341354

  7. Bohnenblust EW, Vaudo AD, Egan JF, Mortensen DA, Tooker JF (2016) Effects of the herbicide dicamba on nontarget plants and pollinator visitation. Environ Toxicol Chem 35:144–151. https://doi.org/10.1002/etc.3169

  8. Bradford MN (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3

  9. Carbonera D, Gerotto C, Posocco B, Giacometti GM, Morosinotto T (2012) NPQ activation reduces chlorophyll triplet state formation in the moss Phycomitrella patens. Biochim Biophys Acta 1817:1608–1615. https://doi.org/10.1016/j.bbabio.2012.05.007

  10. Carvalho RA, Cianciaruso MV, Trindade-Filho J, Sagnori MD, Loyola RD (2010) Drafting a blueprint for functional and phylogenetic diversity conservation in the Brazilian Cerrado. Nat Conserv 8:171–176. https://doi.org/10.4322/natcon.00802011

  11. Cavalieri SDI, Silva FML, Velini ED, ARIV SãoJosé, Ulloa SM, Datta A, Cavalieri JD, Knezevic SZ (2012) Selectivity of nicosulfuron at three popcorn growth stages. Planta Daninha 30:377–386. https://doi.org/10.1590/S0100-83582012000200017

  12. Chagas RM, Silveira JAG, Ribeiro RV, Vitorrelo VA, Carrer H (2008) Photochemical damage and comparative performance of superoxide dismutase and ascorbate peroxidase in sugarcane leaves exposure to paraquat-induced oxidative stress. Pest Biochem Physiol 80:181–188. https://doi.org/10.1016/j.pestbp.2007.11.006

  13. Chaleff RS, Mauvais CJ (1984) Acetolactate synthase is the site of action of two sulfonylurea herbicides in higher plants. Science 224:1443–1445. https://doi.org/10.1126/science.224.4656.1443

  14. Daud MK, Quiling H, Lei M, Ali B, Zhu SJ (2015) Ultrastructural, metabolic and proteomic changes in leaves of upland cotton in response to cadmium stress. Chemosphere 120:309–320. https://doi.org/10.1016/j.chemosphere.2014.07.060

  15. Dayan FE, Zaccaro MLM (2012) Chlorophyll fluorescence as a marker for herbicide mechanisms of action. Pestic Biochem Physiol 102:189–197. https://doi.org/10.1016/j.pestbp.2012.01.005

  16. Debona D, Rodrigues FA, Rios JA, Nascimento KJT (2012) Biochemical changes in the leaves of wheat plants infected by Pyricularia oryzae. Phytopathology 102:1121–1129. https://doi.org/10.1094/PHYTO-06-12-0125-R

  17. Del Longo OT, González CA, Pastori GM, Trippi VS (1993) Antioxidant defenses under hyperoxygenic and hyperosmotic conditions in leaves of two lines of maize with differential sensitivity to drought. Plant Cell Physiol 34:1023–1028. https://doi.org/10.1093/oxfordjournals.pcp.a078515

  18. Diehl KE, Taylor SL, Simpson DM, Stoller EW (1995) Effect of soil organic matter on the interaction between nicosulfuron and terbufos in corn (Zea mays). Weed Sci 4:306–311. https://doi.org/10.1017/S0043174500081224

  19. Egan JF, Bohnenblust E, Goslee S, Mortensen D, Tooker J (2014) Herbicide drift can affect plant and arthropod communities. Agric Ecosyst Environ 185:77–87. https://doi.org/10.1016/j.agee.2013.12.017

  20. Forlani G, Nielsen E, Landi P, Tuberosa R (1991) Chlorsulfuron tolerance and acetolactate synthase activity in corn (Zea mays L.) inbred lines. Weed Sci 39:553–557. https://doi.org/10.1017/S0043174500088366

  21. Franco AC, Rossatto DR, Silva LCR, Ferreira CS (2014) Cerrado vegetation and global change: the role of functional types, resource availability and disturbance in regulating plant community responses to rising CO2 levels and climate warming. Theor Exp Plant Physiol 26:19–38. https://doi.org/10.1007/s40626-014-0002-6

  22. Galmés J, Aranjuelo I, Medrano H, Flexas J (2013) Variation in Rubisco content and activity under variable climatic factors. Photosynth Res 117:73–90. https://doi.org/10.1007/s11120-013-9861-y

  23. Gaston S, Ribas-Carbo M, Busquets S, Berry JA, Zabalza A, Royuela M (2003) Changes in mitochondrial electron partitioning in response to herbicides inhibiting branched-chain amino acid biosynthesis in soybean. Plant Physiol 133:1351–1359. https://doi.org/10.1104/pp.103.027805

  24. Gay C, Gebicki JM (2000) A critical evolution of the effect of sorbitol on the ferric-xylenol orange hydroperoxide assay. Anal Biochem 284:217–220. https://doi.org/10.1006/abio.2000.4696

  25. Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92. https://doi.org/10.1016/S0304-4165(89)80016-9

  26. Giannopolitis CN, Ries SK (1977) Superoxide dismutases I. Occurrence in higher plants. Plant Physiol 59:309–314. https://doi.org/10.1104/pp.59.2.309

  27. Gilmoré AM, Hazlett TL, Govindjee (1995) Xanthophyll cycle-dependent quenching of photosystem II chlorophyll a fluorescence: formation of a quenching complex with a short fluorescence lifetime. Proc Natl Acad Sci 92:2273–2277

  28. Hauben M, Haesendonckx B, Standaert E, Van Der Kelen K, Azmi A, Akpo H, Van Breusegem F, Guisez Y, Bots M, Lambert B, Laga B, De Block M (2009) Energy use efficiency is characterized by an epigenetic component that can be directed through artificial selection to increase yield. Proc Natl Acad Sci 106:20109–20114. https://doi.org/10.1073/pnas.0908755106

  29. Havir EA, Mc Hale NA (1987) Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. Plant Physiol 84:450–455. https://doi.org/10.1104/pp.84.2.450

  30. Hodges DM (1999) Improving the thiobarbituric acidreactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611. https://doi.org/10.1007/s004250050524

  31. Jamers A, De Coen W (2010) Effect assessment of the herbicide paraquat on a green alga using differential gene expression and biochemical biomarkers. Environ Toxicol Chem 29:893–901. https://doi.org/10.1002/etc.102

  32. Kuo MC, Kao CH (2003) Aluminum effects on lipid peroxidation and antioxidative enzyme activities in rice leaves. Biol Plant 46:149–152. https://doi.org/10.1023/A:1022356322373

  33. Langaro AC, Agostinetto D, Oliveira C, Silva JDG, Bruno MS (2016) Biochemical and physiological changes in rice plants due to the application of herbicides. Planta Daninha 34:277–289. https://doi.org/10.1590/S0100-83582016340200009

  34. Lima DA, Müller C, Costa AC, Batista PF, Dalvi VC, Domingos M (2017) Morphoanatomical and physiological changes in Bauhinia variegata L. as indicators of herbicide diuron action. Ecotoxicol Environ Saf 141:242–250. https://doi.org/10.1016/j.ecoenv.2017.03.038

  35. Lu GH, Ji Y, Zhang HZ, Wua H, Qin J, Wang C (2010) Active biomonitoring of complex pollution in Taihu lake with Carassius auratus. Chemosphere 79:588–594. https://doi.org/10.1016/j.chemosphere.2010.01.053

  36. Marris E (2005) The forgotten ecosystem. Nature 437:944–945. https://doi.org/10.1038/437944a

  37. MMA—Ministry of the Environment (2012) Biome monitoring report Cerrado 2009–2010: technical cooperation for deforestation monitoring in Brazilian biomes by satellite. CID Ambiental, Brasília, http://www.mma.gov.br/estruturas/sbf_chm_rbbio/_arquivos/relatoriofinal_cerrado_2010_final_72_1.pdf. Accessed Jan 2019

  38. Moura LMF, Costa AC, Müller C, Silva-Filho RO, Almeida GM, Vital RG, Castro JN, Teixeira MB (2018) Drought tolerance in potential oilseed plants for biofuel production. Aust J Crop Sci 12:289–298. https://doi.org/10.21475/ajcs.18.12.02.pne836

  39. Muhitch MJ (1988) Acetolactate synthase activity in developing maize (Zea mays L.) kernls. Plant Physiol 86:23–27. https://doi.org/10.1104/pp.86.1.23

  40. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232

  41. Olesen CFN, Cedergreen N (2010) Glyphosate uncouples gas exchange and chlorophyll fluorescence. Pest Manag Sci 66:536–542. https://doi.org/10.1002/ps.1904

  42. Oliveira L, Silva-Jr AC, Gonçalves CG, Pereira MRR, Martins D (2019) Selectivity of herbicides to native tree species in Brazil. Planta Daninha 37:e019188510. https://doi.org/10.1590/s0100-83582019370100086

  43. Pellegrini E (2014) PSII photochemistry is the primary target of oxidative stress imposed by ozone in Tilia americana. Urban For Urban Green 13:94–102. https://doi.org/10.1016/j.ufug.2013.10.006

  44. Ronen R, Galun M (1984) Pigment extraction from lichens with dimethyl sulfoxide (DMSO) and estimation of chlorophyll degradation. Environ Exp Bot 24:239–245. https://doi.org/10.1016/0098-8472(84)90004-2

  45. Scherbakova A, Kacperska-Palacz A (1980) Modification of stress tolerance by dehydration pretreatment in winter rape hypocotyls. Physiol Plant 48:560–563. https://doi.org/10.1111/j.1399-3054.1980.tb03304.x

  46. Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012:217037. https://doi.org/10.1155/2012/217037

  47. Siqueira APS, Castro CFS, Silveira EV, Lourenço MFC (2016) Chemical quality of Baru almond (Dipteryx alata oil). Cienc Rural 46:1865–1867. https://doi.org/10.1590/0103-8478cr20150468

  48. Strand DD, Livingston AK, Satoh-Cruz M, Froehlich JE, Maurino VG, Kramer DM (2015) Activation of cyclic electron flow by hydrogen peroxide in vivo. Proc Natl Acad Sci 112:5539–5544. https://doi.org/10.1073/pnas.1418223112

  49. Takahashi S, Murata N (2005) Interruption of the Calvin cycle inhibits the repair of Photosystem II from photodamage. Biochim Biophys Acta 1708:352–361. https://doi.org/10.1016/j.bbabio.2005.04.003

  50. Walters RG (2005) Towards an understanding of photosynthetic acclimation. J Exp Bot 56:435–447. https://doi.org/10.1093/jxb/eri060

  51. Wang J, Cheung M, Rassooli L, Amirsadeghi S, Vanlerberghe GC (2014) Plant respiration in a high CO2 world: how will alternative oxidase respond to future atmospheric and climatic conditions? Can J Plant Sci 94:1091–1101. https://doi.org/10.4141/cjps2013-176

  52. Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313. https://doi.org/10.1016/S0176-1617(11)81192-2

  53. Yuan X, Zhang L, Ning N, Wen Y, Dong S, Yin M, Guo M, Wang B, Feng L, Guo P (2014) Photosynthetic physiological response of Radix Isatidis (Isatis indigotica Fort.) seedlings to nicosulfuron. PLoS ONE 9:105310. https://doi.org/10.1371/journal.pone.0105310

  54. Zabalza A, Orcaray L, Gaston S, Royuela M (2004) Carbohydrate accumulation in leaves of plants treated with the herbicide chlorsulfuron or imazethapyr is due to a decrease in sink strength. J Agric Food Chem 52:7601–7606. https://doi.org/10.1021/jf0486996

  55. Zulet A, Gil-Monreal M, Villamor JG, Zabalza A, Van der Hoorn RAL (2013) Proteolytic pathways induced by herbicides that inhibit amino acid biosynthesis. PLoS ONE 8:e73847. https://doi.org/10.1371/journal.pone.0073847

  56. Zulet A, Gil-Monreal M, Zabalza A, Van Dongen JT, Royuela M (2015) Fermentation and alternative oxidase contribute to the action of amino acid biosynthesis-inhibiting herbicides. J Plant Physiol 175:102–112. https://doi.org/10.1016/j.jplph.2014.12.004

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Acknowledgements

The authors thank the National Council for Scientific and Technological Development (CNPq, grants no. 551456/2010-8 and 552689/2011-4) and the Goiano Federal Institute of Education, Science and Technology, Rio Verde campus (IFGoiano-RV, grants no. DPPG 052/2015) for providing financial support. The current study was also supported by SISBIOTA-BRASIL Program (grants no. 563335/2010; CNPQ and 2010/52319-2; the São Paulo Research Foundation/FAPESP). FBS, PFBC, RBV, CAM and CM are grateful to the Coordination for the Improvement of Higher Education Personnel (CAPES) and KJTN for the Goiás Research Foundation (FAPEG) for scholarships.

Author contributions

FBS, CAM, and ACC designed the study. FBS, RGV, and PFB conducted the experiments and performed the physiological measurements. FBS, PFB, and KJTN performed the biochemical analysis. FBS, CM, ACC and CAM analyzed and discussed the data. FBS and CM wrote the manuscript with contributions from CAM, AJ and MD. All authors read and approved the manuscript.

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Correspondence to Alan Carlos Costa.

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Silva, F.B., Costa, A.C., Müller, C. et al. Dipteryx alata, a tree native to the Brazilian Cerrado, is sensitive to the herbicide nicosulfuron. Ecotoxicology 29, 217–225 (2020). https://doi.org/10.1007/s10646-019-02154-7

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Keywords

  • Chlorophyll a fluorescence
  • Herbicide
  • Oxidative stress
  • Photosynthesis