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Morphophysiological indicators of the glyphosate action on Brazilian savanna plants: a multivariate analysis

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Abstract

Native plants from the Brazilian savanna (the Cerrado) are exposed to agrochemicals widely used in the crops around them. However, there are few studies on the toxicity of herbicides on the vegetation of this biome. Thus, the objective of this study was to identify and establish morphological and physiological indicators of glyphosate effects on two native Cerrado plants. Independent experiments were carried out for the species Pouteria torta and Alibertia edulis, exposing them to four glyphosate doses (0, 200, 400, and 800 g a.e. ha−1). The photosynthetic process and the morphoanatomy in developing leaf (F1) and full-expanded leaf (F3), at different days after herbicide application (DAA) were evaluated. Physiological indicators of glyphosate toxicity in P. torta, such as decreases in photosynthetic rate, in chlorophylls, and in the efficiency of photosystem II were identified. Increments of carotenoids and heat dissipation (NPQ) were common responses to glyphosate in both plants. Reduction in photochemical efficiency in A. edulis was more pronounced in older leaves. Multivariate analysis confirmed the physiological data and the contrasting response of plants to the herbicide. The damages on the foliar surface in P. torta are anatomical indicators of glyphosate toxicity. The susceptibility of P. torta makes it a phyto-indicator for the passive biomonitoring of the glyphosate effects on Cerrado vegetation. There were no changes in the micromorphology of the leaf surface in A. edulis. This plant showed tolerance to the glyphosate through morphological barriers in leaves, which reduced the absorption of the herbicide.

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References

  • Alves RM, Inacio EM, Monquero PA, Meneghin SP, Hirata A (2014) Leaf-surface characterization and the effects of the herbicide saflufenacil on the leaves of weeds. Rev Bras Ciênc Agra 9:550–555

    Google Scholar 

  • Areington CA, Varghese B (2017) The utility of biochemical, physiological and morphological biomarkers of leaf sulfate levels in establishing Brachylaena discolor leaves as a bioindicator of SO2 pollution. Plant Physiol Biochem 118:295–305

    Article  CAS  PubMed  Google Scholar 

  • Batista PF, Costa AC, Megguer CA, Lima JS, Silva FB, Guimarães DS, Nascimento KJT (2018) Pouteria torta: a native species of the Brazilian Cerrado as a bioindicator of glyphosate action. Braz J Biol 78:296–305

    Article  CAS  PubMed  Google Scholar 

  • Batlle-Bayer L, Batjes NH, Bindraban PS (2010) Changes in organic carbon stocks upon land use conversion in the Brazilian Cerrado: a review. Agric Ecosyst Environ 137:47–58

    Article  CAS  Google Scholar 

  • Bielczynski LW, Łącki MK, Hoefnagels I, Gambin A, Croce R (2017) Leaf and plant age affects photosynthetic performance and photoprotective capacity. Plant Physiol 175:1634–1648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boutin C, Strandberg B, Carpenter D, Mathiassen SK, Thomas PJ (2014) Herbicide impact on non-target plant reproduction: what are the toxicological and ecological implications? Environ Pollut 185:295–306

    Article  CAS  PubMed  Google Scholar 

  • Cruz CD, Regazzi AJ, Carneiro PCS (2012) Modelos biométricos aplicados ao melhoramento genético. Ed. UFV, Viçosa, p 508

  • Damasco G, Fontes C, Françoso R, Haidar R (2018) The cerrado biome: a forgotten biodiversity hotspot. Front Young Mind 6:1–9

    Google Scholar 

  • D’Avignon DA, Xia G (2018) In vivo NMR investigations of glyphosate influences on plant metabolism. J Magn Reson 292:59–72

    Article  CAS  PubMed  Google Scholar 

  • De la Cruz RA, Barro F, Domínguez-Valenzuela JÁ, De Prado R (2016) Physiological, morphological and biochemical studies of glyphosate tolerance in Mexican Cologania (Cologania broussonetii (Balb.) DC.). Plant Physiol Biochem 98:72–80

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Adams WW (2018) An integrative approach to photoinhibition and photoprotection of photosynthesis. Environ Exp Bot 154:1–3

    Article  CAS  Google Scholar 

  • Egan JF, Bohnenblust E, Goslee S, Mortenssen D, Tooker J (2014) Herbicide drift can affect plant and communities. Agric Ecosyst Environ 185:77–87

    Article  CAS  Google Scholar 

  • Fadin DA, Tornisielo VL, Barroso AAM, Ramos S, Dos Reis FC, Monquero PA (2018) Absorption and translocation of glyphosate in Spermacoce verticillata and alternative herbicide control. Weed Res 58:389–396

    Article  CAS  Google Scholar 

  • Feng X, Yu C, Chen Y, Peng J, Ye L, Shen T, He Y (2018) Non-destructive determination of shikimic acid concentration in transgenic maize exhibiting glyphosate tolerance using chlorophyll fluorescence and hyperspectral imaging. Front Plant Sci 9:468

    Article  PubMed  PubMed Central  Google Scholar 

  • Fernández-Moreno PT, Alcantara-de la Cruz R, Cruz-Hipólito HE, Rojano-Delgado AM, Travlos I, De Prado R (2016) Non-target site tolerance mechanisms describe tolerance to glyphosate in Avena sterilis. Front Plant Sci 7:1220

    Article  PubMed  PubMed Central  Google Scholar 

  • Florencia FM, Torres C, Bracamonte E, Galetto L (2017) Effects of the herbicide glyphosate on non-target plant native species from Chaco forest (Argentina). Ecotox Environ Saf 144:360–368

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Françoso RD, Brandão R, Nogueira CC, Salmona YB, Machado RB, Colli GR (2015) Habitat loss and the effectiveness of protected areas in the Cerrado Biodiversity Hotspot. Natureza & Conservação 13:35–40

    Article  Google Scholar 

  • Freitas-Silva L, de Araújo TO, Nunes-Nesi A, Ribeiro C, Costa AC, da Silva LC (2020) Evaluation of morphological and metabolic responses to glyphosate exposure in two neotropical plant species. Ecol Indic 113:106246

    Article  CAS  Google Scholar 

  • Gomes MP, Smedbol E, Chalifour A, Hénault-Ethier L, Labrecque M, Lepage L, Juneau P (2014) Alteration of plant physiology by glyphosate and its by-product aminomethylphosphonic acid: an overview. J Exp Bot 65:4691–4703

    Article  CAS  PubMed  Google Scholar 

  • Gomes MP, Manac’h SG, Maccario S, Labrecque M, Lucotte M, Juneau P (2016) Differential effects of glyphosate and aminomethylphosphonic acid (AMPA) on photosynthesis and chlorophyll metabolism in willow plants. Pestic Biochem Physiol 130:65–70

    Article  CAS  PubMed  Google Scholar 

  • Gomes MP, Manac’h L, Sarah G, Hénault-Ethier L, Labrecque M, Lucotte M, Juneau P (2017) Glyphosate-dependent inhibition of photosynthesis in willow. Front Plant Sci 8:207

    Article  PubMed  PubMed Central  Google Scholar 

  • Gorelova SV, Frontasyeva MV (2017) The use of higher plants in biomonitoring and environmental bioremediation. In: Ansari A, Gill S, Gill R, Lanza G, Newman L (eds) Phytoremediation. Springer, Cham, pp 103–155

    Chapter  Google Scholar 

  • Hajri H, Mhadhebi R, Ghorbel A, Armstrong J, Salem-Fnayou AB (2016) Physiological and leaf ultrastructural characteristics of perennial ryegrass (Lolium perenne L.) biotypes from Tunisia under sulfonylurea herbicide application. Sci Hortic 207:28–32

    Article  CAS  Google Scholar 

  • Huang Z, Liu Y, Zhang C, Jiang C, Huang H, Wei S (2019) Molecular basis of natural tolerance to glyphosate in Convolvulus arvensis. Sci Rep 9:1–10

    CAS  Google Scholar 

  • Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27:137–138

    Google Scholar 

  • Kleinman Z, Rubin B (2017) Non-target-site glyphosate resistance in Conyza bonariensis is based on modified subcellular distribution of the herbicide. Pest Manag Sci 73:246–253

    Article  CAS  PubMed  Google Scholar 

  • Krenchinski FH, Albrecht LP, Albrecht AJP, Cesco VJS, Rodrigues DM, Portz RL, Zobiole LHS (2017) Glyphosate affects chlorophyll, photosynthesis and water use of four Intacta RR2 soybean cultivars. Acta Physiol Plant 39:63

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Mateos-Naranjo E, Perez-Martin A (2013) Effects of sub-lethal glyphosate concentrations on growth and photosynthetic performance of non-target species Bolboschoenus maritimus. Chemosphere 93:2631–2638

    Article  CAS  PubMed  Google Scholar 

  • Murtaza B, Naeem F, Shahid M, Abbas G, Shah NS, Amjad M, Murtaza G (2019) A multivariate analysis of physiological and antioxidant responses and health hazards of wheat under cadmium and lead stress. Environ Sci Pollut Res 26:362–370

    Article  CAS  Google Scholar 

  • Natasha SM, Farooq ABU, Rabbani F, Khalid S, Dumat C (2020) Risk assessment and biophysiochemical responses of spinach to foliar application of lead oxide nanoparticles: a multivariate analysis. Chemosphere 245:125605

    Article  CAS  PubMed  Google Scholar 

  • Olesen CF, Cedergreen N (2010) Glyphosate uncouples gas exchange and chlorophyll fluorescence. Pest Manag Sci 66:536–542

    Article  CAS  PubMed  Google Scholar 

  • Olszyk D, Pfleeger T, Shiroyama T, Blakeley- Smith M, Lee EH, Plocher M (2017) Plant reproduction is altered by simulated herbicide drift to constructed plant communities. Environ Toxicol Chem 36:2799–2813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Orcaray L, Zulet A, Zabalza A, Royuela M (2012) Impairment of carbon metabolism induced by the herbicide glyphosate. J Plant Physiol 169:27–33

    Article  CAS  PubMed  Google Scholar 

  • Pan L, Yu Q, Han H, Mao L, Nyporko A, Fan L, Powles S (2019) Aldo-keto reductase metabolizes glyphosate and confers glyphosate resistance in Echinochloa colona. Plant Physiol 181:1519–1534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perotti VE, Larran AS, Palmieri VE, Martinatto AK, Permingeat HR (2020) Herbicide resistant weeds: a call to integrate conventional agricultural practices, molecular biology knowledge and new technologies. Plant Sci 290:110255

    Article  CAS  PubMed  Google Scholar 

  • Radwan DEM, Fayez KA (2016) Photosynthesis, antioxidant status and gas-exchange are altered by glyphosate application in peanut leaves. Photosynthetica 54:307

    Article  CAS  Google Scholar 

  • Rao RC (1952) Advanced statistical methods in biometric research. Wiley, New York

    Google Scholar 

  • Rezende-Silva SL, Costa AC, Dyszy FH, Batista PF, Crispim-Filho AJ, Nascimento KJT, da Silva AA (2019) Pouteria torta is a remarkable native plant for biomonitoring the glyphosate effects on Cerrado vegetation. Ecol Indic 102:497–506

    Article  CAS  Google Scholar 

  • Santos JS, Pontes MS, Grillo R, Fiorucci AR, Arruda GJ, Santiago EF (2020) Physiological mechanisms and phytoremediation potential of the macrophyte Salvinia biloba towards a commercial formulation and an analytical standard of glyphosate. Chemosphere 259:127417

    Article  CAS  Google Scholar 

  • Schrübbers LC, Valverde BE, Sørensen JC, Cedergreen N (2014) Glyphosate spray drift in Coffea arabica—sensitivity of coffee plants and possible use of shikimic acid as a biomarker for glyphosate exposure. Pestic Biochem Physiol 115:15–22

    Article  PubMed  CAS  Google Scholar 

  • Schrübbers LC, Valverde BE, Strobel BW, Cedergreen N (2016) Glyphosate accumulation, translocation, and biological effects in Coffea arabica after single and multiple exposures. Eur J Agron 74:133–143

    Article  CAS  Google Scholar 

  • Shahid M, Shamshad S, Farooq ABU, Rafiq M, Khalid S, Dumat C, Niazi NK (2019) Comparative effect of organic amendments on physio-biochemical traits of young and old bean leaves grown under cadmium stress: a multivariate analysis. Environ Sci Pollut Res 26:11579–11590

    Article  CAS  Google Scholar 

  • Silva CA, Simeoni LA, Silveira D (2009) Genus Pouteria: chemistry and biological activity. Rev Bras Farmacogn 19:501–509

    Article  CAS  Google Scholar 

  • Silva F, Costa A, Pereira AR, Megguer C (2014) Chlorophyll fluorescence as an indicator of cellular damage by glyphosate herbicide in Raphanus sativus L. plants. Am J Plant Sci 5:2509–2519

    Article  CAS  Google Scholar 

  • Silva FB, Costa AC, Müller C, Nascimento KT, Batista PF, Vital RG, Domingos M (2020) Dipteryx alata, a tree native to the Brazilian Cerrado, is sensitive to the herbicide nicosulfuron. Ecotoxicology 29:217–225

    Article  CAS  PubMed  Google Scholar 

  • Singh D (1981) The relative importance of characters affecting genetic divergence. Indian J Genet Plant Breed 41:237–245

    Google Scholar 

  • Soares C, Pereira R, Martins M, Tamagnini P, Serôdio J, Moutinho-Pereira J, Fidalgo F (2020) Glyphosate-dependent effects on photosynthesis of Solanum lycopersicum L.—an ecophysiological, ultrastructural and molecular approach. J Hazard Mat 5;398:122871. https://doi.org/10.1016/j.jhazmat.2020.122871

  • Strassburg BB, Brooks T, Feltran-Barbieri R, Iribarrem A (2017) Moment of truth for the Cerrado hotspot. Nat Ecol Evol 3:1–99

    Google Scholar 

  • Valli M, Young MCM, Bolzani VS (2016) The invisible beauty of the biodiversity: the Rubiaceae taxon. Rev Virtual Quim 8:296–310

    Article  Google Scholar 

  • Vila-Aiub MM, Yu Q, Powles SB (2019) Do plants pay a fitness cost to be resistant to glyphosate? New Phytol 223:532–547

    Article  CAS  PubMed  Google Scholar 

  • Wellburn AR (1997) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 44:307–313

    Google Scholar 

  • Wood LJ (2019) The presence of glyphosate in forest plants with different life strategies one year after application. Can J for Res 49:586–594

    Article  CAS  Google Scholar 

  • Yanniccari M, Istilart C, Giménez DO, Castro AM (2012) Glyphosate resistance in perennial ryegrass (Lolium perenne L.) from Argentina. Crop Prot 32:12–16

    Article  CAS  Google Scholar 

  • Yilmaz G, Dane F (2012) Phytotoxicity induced by herbicide and surfactant on stomata and epicuticular wax of wheat. Rom Biotech Lett 17:7757–7765

    CAS  Google Scholar 

  • Zulet-González A, Barco-Antoñanzas M, Gil-Monreal M, Royuela M, Zabalza A (2020) Increased glyphosate-induced gene expression in the shikimate pathway is abolished in the presence of aromatic amino acids and mimicked by shikimate. Front Plant Sci 11:459

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq, the Programa SISBIOTA-BRASIL, the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-CAPES, the Fundação de Amparo à Pesquisa do Estado de Goiás (FAPEG), and the Instituto Federal Goiano-Campus Rio Verde for providing financial support to this work. SLRS, AJCF, GMA, AAS (Grant number 88882.317497/2019-01) and KJTN are grateful to the CAPES, and PFB (Grant number 154958/2018-2) to the CNPq for scholarships. The authors would like thank also the Instituto de Botânica de São Paulo/Anatomy Research Center for the partnership in this study.

Funding

This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq (Grant numbers 551456/2010-8, 552689/2011-4); Directorate of Research and Graduate Studies of the Instituto Federal Goiano-Campus Rio Verde (Grant number 052/2015); and Sistema Nacional de Pesquisa em Biodiversidade (SISBIOTA-BRASIL Program) [Grant numbers 563335/2010-CNPq, 523192/2010-FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo)].

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Lopes Rezende-Silva, S., Costa, A.C., Nunes Vaz Pedroso, A. et al. Morphophysiological indicators of the glyphosate action on Brazilian savanna plants: a multivariate analysis. Acta Physiol Plant 44, 73 (2022). https://doi.org/10.1007/s11738-022-03409-3

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  • DOI: https://doi.org/10.1007/s11738-022-03409-3

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