Tolerance of Hymenaea stigonocarpa Mart. ex Hayne. to glyphosate

doi:10.21203/rs.3.rs-2210951/v1

Download PDF

Article

Tolerance of Hymenaea stigonocarpa Mart. ex Hayne. to glyphosate

https://doi.org/10.21203/rs.3.rs-2210951/v1

This work is licensed under a CC BY 4.0 License

Version 1

posted

You are reading this latest preprint version

The objective of this work was to evaluate the glyphosate herbicide effect on Hymenaea stigonocarpa Mart. ex Hayne seedlings. A randomized block design with 5 replicates was used with an experimental unit composed of one H. stigonocarpa plant in 5L pots. The treatments were: 0 (control); 9.6; 240; 480; 960 g a. ha^− 1 of glyphosate. Evaluations were performed 24 hours and 60 days after application. Gas exchange, respiration, photosynthesis, visual, anatomical and histochemical evaluations were carried out with leaves from the middle third being collected, and the growth in relation to the two dates was measured and recorded. The growth analysis showed that the seedlings showed an increase in stem diameter, a decrease in leaf number and an increase in height. There were increases in photosynthetic, electron transport and transpiratory rates, and in the effective yield of photosystem II one day after the glyphosate application. The plants then showed a reduction in transpiratory rate and a reduction in Fv/Fm at 60 days after application. With these studies we can conclude that the Hymenaea stigonocarpa species is able to survive after contact with the glyphosate herbicide, with no visual and/or anatomical damage, along with positive increases in growth and physiological characteristics.

Biological sciences/Biological techniques

Biological sciences/Physiology

Biological sciences/Plant sciences

Photosynthesis

Herbicide

Leaf anatomy

Growth and development

Glyphosate is one of the most widely used herbicides in the world and has been marketed for over 35 years [1]. It is an herbicide which is widely used to control weeds to eliminate them at an early stage of development [2], acting on sensitive plants by blocking the enzyme activity, interrupting the activity of the plastid enzyme 5-enolpyruvylshikimate-3-phosphate synthesis (EPSPS) [3]. The shikimate route is interrupted by the herbicide and in turn the biosynthesis of the essential phenylalanine, tyrosine and tryptophan aromatic amino acids which are indispensable in protein synthesis, cell division and plant growth, and can lead to plant death [4, 5].

Research with herbicide drift enables evaluating the effects and selection of tolerant or bio-indicator species; phytotoxicity is a current problem and causes serious damage to non-target crop species [6]. One of the visible symptoms is chlorosis, and depending on the degree of intoxication it can lead to inuria. The symptoms depend on several factors such as the species, the development stage, the climate, the dose and the amount of active principles that reach the plant, and may benefit the morphological characteristics of the species [3, 7, 8, 9, 10]. Therefore, the use of herbicide in chemical control needs to be based on strict criteria, taking into account cost, efficiency, as well as environmental and human safety, and must be integrated into weed control [11, 12].

Photosynthesis can be affected by herbicides displaced from the application site by drift [10]. Glyphosate indirectly influences photosynthetic processes [13, 14, 15]. Another important tool that helps in detecting damage caused by contact with herbicides is anatomically evaluating the leaf, which determines uptake by the plant. This contributes to understanding the barrier that each species imposes to its penetration [16, 17]. In addition, micromorphological changes occur before visual damage [9].

The Cerrado is the second largest Brazilian domain and has been changing from the expansion of agricultural frontiers due to the increase in the demand for meat and grains for export, promoting a depletion of natural resources [18]. Such changes make the Cerrado one of the main tropical ecosystems, being a hotspot for the preservation of our planet’s biodiversity [19]. Native species start to occupy close environments with agricultural crops due to this change in the biome, in turn becoming subject to the action of herbicides and undergoing unwanted exposure caused by the action of the winds and physical proximity, which has caused damage to the environment [20].

Hymenaea stigonocarpa Mart. Ex Hayne is a large tree naturally occurring in the Cerrado domain. They have leaves with adaxial and abaxial epidermis covered by a very thick cuticle, and the presence of oil glands in a subepidermal location has also been observed [21]. These anatomical structures are involved in decreasing the effective amount of herbicide absorbed by plants. Glyphosate has little affinity for lipids, therefore epicuticular waxes with large amounts of non-polar compounds constitute a barrier to the penetration of this herbicide [22, 23, 24].

Based on similar results, it is possible to search for new planting technologies for the recovery of degraded areas, either to control weeds in cultivation or even to implement protection belts for existing native forest fragments in agricultural areas [25].

In view of the above, this work aims to evaluate the impact of the glyphosate herbicide on the leaf blade growth, physiology and anatomy of the H. stigonocarpa. species (jatoba), as well as to test the plant’s tolerance to the herbicide.

Experimental design and application of treatments

The experiment was carried out in an acclimatized greenhouse (temperature ~ 25.5°C and relative humidity ~ 74%) at the Instituto Federal Goiano, Rio Verde Campus, Brazil. H. stigonocarpa seedlings at 8 months were obtained from a commercial nursery, being replanted in 5 L pots, totaling 25 plants. The exsicata de H. stigonocarpa plants was deposited in the herbarium of the Rio Verde in Goiano Federal Institute under catalog number 10039.

The physicochemical characteristics of soil (dystrophic Red Oxisol) were: pH 5.12; 1.06 cmol_c dm^− 3 Ca; 0.48 cmol_c dm^− 3 Mg; 1.6 Ca + Mg, 0.05 cmol_c dm^− 3 Al; 2.1 H + Al, 0.33 cmol_c dm^− 3 K; and 128 mg dm K; 8.4 mg dm^− 3 S; 2.6 mg dm^− 3 P; and 48% clay, 12% silt and 40% sand. Irrigation was performed daily with a nutrient solution containing ammonium sulfate (100 mg L^− 1), monoammonium phosphate (150 mg L^− 1), potassium chloride (110 mg L^− 1), copper sulfate (58 mg L^− 1), boric acid (81 mg L^− 1) and zinc sulfate (173 mg L^− a) [26].

The experiment was carried out in a randomized block design in a 5 × 2 factorial scheme with five doses (0 (control), 96, 240, 480, 960 g ha^− 1) and two evaluation dates (1 and 60 days after application), with five replicates. The experimental unit was a pot containing one H. courbaril plant. The plants were then exposed to glyphosate doses (Roundup Transorb®, 480 g ha^− 1 of the acid equivalent) after ~ 60 days of acclimatization.

A control treatment was conducted in parallel without herbicide application, 0 (Control) 96, 240,480, and 960 g ha^− 1, which represent 10, 25, 50, and 100% of the recommended doses for 480 g ha^− 1 for control of tree species. Application was performed using a backpack sprayer with constant pressure maintained by compressed CO₂, equipped with a bar with four spray tips and a XRTeejet® series nozzle with a XR11002-VP fan. A total of 120 L ha^− 1 of spray solution was applied. The application was carried out at 8:00 am, wind speed at 1 m s^− 1, average temperature of 18.3°C and the relative humidity was 90%. The pots were transferred to the greenhouse after the treatments were applied.

Visible leaf symptoms

The fully expanded leaves were photographed with a semi-professional camera (Cyber-Shot SONY HX100V) for visual analysis of the leaves which best represented the treatment to be used to make the board [27].

Leaf morphoanatomical characterization

Leaf samples were collected 24 h and 60 days after the application of the herbicide for the morphoanatomical analysis. Leaf samples of 3 cm² were collected from the central region of the last fully expanded leaf from all replicates of each treatment of the H. stigonocarpa plants. The samples were initially fixed in Karnovsky solution for 24 h [28]. After this period, the plant material was pre-washed in phosphate buffer (0.1 M, pH 7.2) and dehydrated in an increasing ethyl series (30–100%), pre-infiltrated and infiltrated in historesin (Leica, Germany), according to the manufacturer’s recommendations.

The samples were then transversely sectioned at 5 µm thick in a rotating microtome (Model 1508 R, Logen Scientific, China) and the sections were stained with toluidine blue - polychromatic staining (0.05% 0.1 M phosphate buffer, pH 6.8). Images were obtained through an Olympus microscope (BX61, Tokyo, Japan) coupled with a DP-72 camera using the bright field option. Morphoanatomical observations of the epidermis were subsequently performed on the adaxial and abaxial surfaces, palisade and spongy parenchymas and mesophyll [29].

Histochemical test

Samples previously fixed in FAA70 and SFF were included in historesin. The sections were stained with ferric chloride for the reaction of phenolic compounds [30] and Lugol for detection of starch grains. The respective controls were simultaneously performed with the histochemical tests according to standard procedure.

Micromorphometric measurements

Micromorphometric measurements were obtained from the records of anatomical and histochemical images captured through an Olympus microscope (BX61, Tokyo, Japan) using the ImageJ software program (Image Processing and Analysis in Java, v. 1.47, USA). Measurements were made in ten observations per repetition 5 for each evaluated structure [31].

Evaluation of chlorophyll a fluorescence and gas exchange

Measurements were taken after 24 h and 60 days after herbicide application. Chlorophyll a fluorescence variable was evaluated using a portable LI-6800 infrared gas analyzer (IRGA) (Li-cor, Nebraska, USA). The minimum fluorescence analysis (F₀) was performed before dawn through excitation of the leaf tissues by low intensity modulated red light (003 µmol photons m^− 2 s^− 1). Next, saturation impulses of approximately 8000 µmol photons m^− 2 s^− 1 were applied for 0.8 s to obtain maximum fluorescence (F_m). From these values it was possible to determine the potential photochemical quantum yield of photosystem II (PSII: F_v/F_m = [F_m-F₀]/F_m). After exposing the leaves to light, minimum fluorescence (F₀) was obtained by: F₀ = F₀/[(F_m– F₀/F_m )+(F₀/F_m′)] [32].

Non-photochemical quenching (qN = [F_m-F₀] / [F_m-F_o] [33], and non-photochemical extinction coefficient (NPQ = [F_m-F_m’]/F_m) were determined. Apparent electron transport rate (ETR) was calculated as ETR = Φ FSII × PAR × 0.5 × 0.84 [34], where PAR represents photosynthetically active radiation (µmol m^− 2 s^− 1) in leaves, 0.5 is the fraction of excitation energy directed to PSII and 0.84 leaf absorbance [31]. The maximum efficiency of PSII photochemistry in adapted-light leaves (F_v’/F_m’ = [(F_m’–F_o’)/F_m’]), the quantum yield of the assimilation of CO² (ΦCO²), and the relationship between the (Φ_PSII) were calculated according to the methodology proposed by [35]. Gas exchange form in H. stigonocarpa plants were measured in the same leaf as the chlorophyll a fluorescence. The photosynthetic rate was measured in the same leaf using the LI-6800 system. The photosynthetic rates (A, µmol m^− 2s^− 1), stomatal conductance (gs, mol H₂O m^− 2s^− 1), transpiration rate (E, mmol m^− 2s^− 1) and the ratio between internal and external CO₂ concentration (C_i/C_a) were determined under constant photosynthetic photon flux density (PFFD, 1000 µmol m^− 2s^− 1) and CO₂ concentration (400 µmol mol^− 1 air), and environmental temperature (~ 25.5 C) and relative humidity (~ 74%). The evaluations were performed between 8:00 am and 11:00 am.

Morphological analysis

Morphological measurements began after applying glyphosate doses. H. stigonocarpa seedlings were measured monthly for plant height (PH, cm) considering the length of the main stem to the apex of the stem, and the stem diameter (SD, mm), which were measured with a millimeter ruler and digital caliper, respectively; the total number of expanded leaves (NL) [35]. Values obtained after 60 days after the application of the glyphosate doses were analyzed.

Statistical analysis

The results were submitted to Shapiro-Wilk’s normality tests and Bartlett’s test for homogeneous variances at 5% of significance. Next, the data underwent variance analysis (ANOVA) by the F-test, being adjusted to regression models at 5% significance level. The models were chosen for simplicity, biological significance and the coefficient of determination. Statistical analyzes were performed using the SISVAR statistical program and graphs were performed using Excel.

Visible leaf symptoms and morphoanatomical characterization

Visible damage to the leaf blade was not observed in any of the treatments (Fig. 1).

The evaluation of anatomical changes showed that the leaf epidermis of H. stigonocarpa is made up of isodiametric cells with flat or slightly convex anticline walls and amphi-stomatal leaves on the adaxial and abaxial surfaces. The mesophyll is, composed of one or two layers of palisade parenchyma, four to five layers of spongy parenchyma and secretory channels. The glyphosate doses did not cause changes in H. stigonocarpa during the analysis period (Fig. 2).

Histochemical test

The presence of starch grains in the mesophyll, adaxial epidermis and abaxial epidermis of H. stigonocarpa leaves was not observed in the histochemical tests, regardless of the glyphosate dose used in the study (Fig. 3).

The presence of phenolic compounds in the leaf cells of Hymenaea stigonocarpa was not observed in either the control treatment or in the treatments with glyphosate doses (Fig. 4).

Morphological analysis

When analyzing the relative growth rate for the H. stigonocarpa plants, it was possible to verify that the diameter presented a quadratic behavior, and all treatments were better than the control (Fig. 5A), whereas the relative growth of new leaves and the relative growth in height showed negative quadratic behavior (Fig. 5B-C).

The effects of glyphosate doses were not significant in the micromorphometric analyses by the F-test at 5% probability for the thickness of leaf tissues of H. stigonocarpa plants. The averages for the evaluated characteristics are presented below (Table 1).

Table 1

Leaf tissue thickness, F-test at 5% probability for *H. stigonocarpa* Mart. ex Hayne. seedlings 60 days after glyphosate application. (AdEp) adaxial epidermis. (AbEp) abaxial epidermis. (PP) palisade parenchyma. (SP) spongy parenchyma. (CutAd) adaxial cuticle. (CutAb) abaxial cuticle
Dose (g ha^− 1)	Leaf (µm)	EpAd (µm)	EpAb (µm)	PP (µm)	Sp (µm)	Mesofilo (µm)	CutAd (µm)	CutAb (µm)
0	197,942	18,205	15,966	72,709	89,408	162,538	4,432	4,476
9,6	190,423	15,572	13,880	62,629	92,383	156,323	4,327	4,346
240	187,893	17,859	14,424	61,674	91,780	155,280	4,482	4,48
480	190,650	17,608	15,550	60,023	97,129	156,010	4,566	4,586
960	174,924	18,083	17,003	44,906	94,928	138,994	4,489	4,489
Average	188,366	17,465	15,364	60,388	93,126	153,829	4,486	4,475

Evaluation of chlorophyll a fluorescence and gas exchange

Physiological analyzes of H. stigonocarpa seedlings one day after glyphosate application showed positive quadratic behavior for photosynthetic rate (Fig. 6A), electron transport rate (Fig. 6B), transpiration rate (Fig. 6C) and on the effective quantum yield of photosystem II. (Fig. 6D), except for transpiration rate, where there was an increase only up to dose 240; all glyphosate doses increased the values of the aforementioned characteristics in relation to the control.

The second physiological evaluation on H. stigonocarpa seedlings 60 days after application showed that the transpiration rate decreases with higher glyphosate doses (Fig. 7A) and the potential quantum yield of photosystem II showed a quadratic behavior, with the highest dose showing lower values compared to other treatments (Fig. 7B).

Glyphosate did not affect the morphology and anatomy of H. stigonocarpa leaves, regardless of herbicide doses and evaluation time. There are reports of weeds whose herbicide tolerance mechanism is due to low absorption and/or translocation of the herbicide to the action site [17, 24, 38, 39, 40], which is why it led us to believe that the wax layer or cuticle serves as a physical and hydrophobic barrier that hinders absorption via the leaves [41].

Glyphosate can present different responses in relation to morphological characteristics, being beneficial or inhibiting [42, 43]. In the case of H. stigonocarpa, glyphosate promoted stem thickening the diameter, which in turn is one of the characteristics whose analysis enables indicating the ability of a seedling to survive in the field and should be used as one of the best indicators of seedling quality and consequently survival in the field [44, 45]. Stem thickening is an important parameter to generate greater plant resistance and support the weight of leaves and fruits [46]. Species that have morphological characteristics which hinder glyphosate absorption causing the compound to only be absorbed in sub-doses may be related to “beneficial” changes; first, the occurrence of physiological changes such as photosynthetic rate, electron transport, transpiration and on the effective quantum yield of photosystem II stimulate the species to produce more photoassimilates [3]. The increase in these rates positively influences the plants, and this is all related to the degree of absorption; low doses have a hormesis effect as already reported in other forest species, and thus promote a positive effect of stem thickening [47, 48].

Defoliation can probably be related to lower plant height production, a fact which is intensified by the decrease in transpiration rate and potential quantum yield of photosystem II verified at 60 days after glyphosate application. Leaf abscission has already been related to a reduction in photosynthetic capacity [49, 50], and with an increase in the herbicide dose, the intoxication level increased, causing leaf abscission and consequently a reduction in leaves to perform photosynthesis and is related to the drop in the growth rate of H. stigonocarpa seedlings. Defoliation reduces the production of carbohydrates for plants, followed by a high demand for photoassimilates [51]. Thus, something similar is believed to have occurred with H. stigonocarpa from the Cerrado, in which the energy demand for plant growth was not met at the highest glyphosate doses.

It is known that the main symptoms of glyphosate appear hours after application and include chlorosis followed by necrosis, and become more accentuated according to the dose of the active ingredient in sensitive plants. However, these symptoms were absent during the analysis period and doses. Anatomical analyzes on leaves are important tools that help in the detection of damage caused by contact with herbicides, as these can determine absorption by the plant [16]. However, for this work, no anatomical damage was observed in the leaf structures evaluated. Glyphosate is rapidly absorbed and transported to meristematic tissues [52], and doses higher than 360 g e.a h^− 1 would be enough to kill the plant 21 days after glyphosate application, which did not occur with H. stignocarpa [53]. We can analyze the defense mechanism through anatomical evaluations, which contributes to understanding the barrier that each species imposes to its penetration [16]. In the case of H. stignocarpa, it was found that the main protection barrier is the thickness of the cuticle in the leaf, which minimizes how much of the active principle the plant absorbs.

According to a study [54], about 785,300 tons of products containing glyphosate were marketed worldwide in 2017. The results of histochemical tests were negative for detecting phenolic compounds and starches, and these results indicate that the species did not undergo oxidative stress [55]. No accumulation of starch grains was observed in H. stigonocarpa leaves, indicating that carbohydrate translocation was not impaired, as already observed in species exposed to various atmospheric pollutants [56].

Glyphosate is one of the most studied herbicides by the scientific community in recent years [57]. Glyphosate foliar phytotoxicity is related to absorption through the cuticle, in which case the removal of the wax layer due to herbicide application increases the chance of glyphosate absorption [58], which is why H. stigonocarp did not present visible or anatomical damage. Epicuticular wax is a very effective barrier against the foliar absorption of water-soluble herbicides, such as glyphosate [59]. For this reason, it may indicate that only sub-doses of glyphosate were absorbed by the plants, providing benefits to the studied plants.

Non-photochemical quenching was not affected by the glyphosate application, so the dissipation of non-radiative energy 24 hours and 60 days after the exposure of the seedlings to the herbicide was not affected. We know that non-photochemical quenching is involved in dissipating excess energy and regulating the photosystem II reaction center, which in turn is a photoprotection mechanism [60, 61]. The initial increase in the transpiration rate after 24 hours has already been pointed out as a defoliation compensation mechanism [62], which in turn could not be maintained during the 60 days as there was a progressive decrease, which may suggest that the plant’s capacity to absorb enough water to replace that consumed in the transpiration process was not sufficient, as has been shown by other authors [62, 63].

Glyphosate acts by inhibiting the activity of the 5-enolpyruvylshikimate-3 phosphate synthase (EPSPS) enzyme, which catalyzes the condensation of shikimic acid and pyruvic acid, preventing the synthesis of three aromatic amino acids (e.g., phenylalanine, tyrosine and tryptophan), negatively influencing plant growth [15]. This happened in treated plants which had their growth affected depending on the glyphosate dose, as many herbicides were created with the objective of regulating growth [3].

The plants are tolerant to glyphosate with regard to visible and anatomical damage, and the lowest herbicide doses had little effect on the physiological analyses, which resulted in higher growth rates for the seedlings; however, the presence of the glyphosate in the highest doses negatively affected the foliar apparatus of plants, in turn affecting their growth.

Acknowledgments

To the Federal Institute of Education, Science and Technology, Graduate Program in Agricultural Sciences Goiano Campus Rio Verde; Plant anatomy laboratories; plant physiology; To the Coordination for the Improvement of Higher Education Personnel (CAPES/FAPEG) for granting a scholarship and encouraging research.

Author contributions

GSF: conduct experiments and collected data, writing the draft manuscript and editing. LC: supervision, writing, review, and editing, project administration. AJ: supervision, review and editing. SCVF: supervision, conceptualization, analysed sample and data. STFF: formal analysis, visualization, review and editing. LLL: supervision and collected data. AMC: analysed sample and data. IOFS: analysed sample and data.

Data availability statement

Data may be made available by contacting the corresponding author.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflicts of interest.

Ethics Statement

This study did not use any animal. The cultivars were obtained in accordance with Brazilian legislation, following the regulation of Law Nº 9,456, of April 25, 1997.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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. Pesticide Biochemistry and Physiology, 115, 15-22. https://doi.org/10.1016/j.pestbp.2014.08.003
Monsanto Do Brasil (2018). Disponível em: http://www.monsanto.com.br/ Acesso em: 19 jan. 2019.
Zavariz A, Berryhill QTA, Guimarães ET, Pereira, FAC (2020). The use of glyphosate in coffee cultivation, an epistemological study. Brazilian Journal of Development , 6, 36046-36058. DOI: https://doi.org/10.34117/bjdv6n6-231
França AC, Freitas MAM, Fialho CMT, Silva AA, Reis MR, Galon L, Victoria Filho R (2010). Growth of Arabica coffee cultivars submitted to glyphosate doses. Planta Daninha, 28, 599-607 https://doi.org/10.1590/S0100-83582010000300017
Ferreira SD, Exteckoetter V, Gibbert AM, Barbosa JA, Costa NV. (2018). Biological cycle of susceptible and glyphosate-resistant sourgrass biotypes in two growth periods. Planta Daninha, 36. https://doi.org/10.1590/S0100-83582018360100077
Oliveira APAD, Crispim Filho AJ, Santos VRS, Costa AC, Silva KLF (2021). Physiological and morphoanatomic responses of Bowdichia virgilioides kunth. (Fabaceae) to glyphosate. Revista Árvore, 45. https://doi.org/10.1590/1806-908820210000028
Rigoli RP, Fontana LC, Figueredo SS, Noldin JA (2008). Response of Beetroot (Beta vulgaris) and Carrot (Daucus carota) to Simulated Glyphosate and Clomazone Drift. Planta Daninha, 26, 451-456.
Pereira MRR, Rodrigues ACP, Costa NV da, Martins D, Klar AE, Silva MR da (2010). Efeito da deriva de glifosato sobre algumas características fisiológicas em plantas de eucalipto. INTESCIENCIA, 35.
Tuffi Santos LD, Sant’anna-Santos BF, Meira RMSA, Ferreira FA, TibuSCio RAST, Silva ECF (2009). Micromorfologia foliar na análise da fitotoxidez por glifosato em Eucalyptus grandis. Planta Daninha, 27, 711-720.
Machado AFL, Ferreira LR, Santos LDT, Ferreira FA, Viana RG, Machado MS, Freitas FCL (2010). Photosynthetic Efficiency and Water Use in Eucalyptus Plants Sprayed with Glyphosate. Planta Daninha, 28, 319-327.
Bianchi MA, Rissardi MA, Vargas L (2014). Manejo de plantas danunhas em cereais de inverno. In Manejo de Plantas Daninhas nas Culturas Agricolas. São Carlos: RiMa editora, 68-79.
Pereira DN, Moro D, Flores R (2019). Environmental education in initial teacher education: an experience report based on pesticides. Brazilian Journal of Development , 5, 25874-25888. DOI: https://doi.org/10.34117/bjdv5n11-239
Wagner JF, Merotto Junior (2014). Physiological and nutritional evaluation of soybean resistant to glyphosate in comparison with near isogenic lines. Ciência Rural, 44. https://doi.org/10.1590/S0103-84782014000300002
Gomes MP et al. (2017). Glyphosate-dependent inhibition of photosynthesis in willow. Frontiers in Plant Science, 65. https://doi.org/10.3389/fpls.2017.00207
Meloni DA, Martínez CA (2021). Physiological responses of Eucalyptus camaldulensis (Dehnh.) to simulated glyphosate drift. Biofix Scientific Journal, 6, 46-53. http://dx.doi.org/10.5380/biofix.v6i1.77236
Costa NV, Martins D, Rodella RA, Rodrigues-Costa ACP (2011). Anatomical leaf changes in Eichhornia crassipes due to herbicides application. Planta Daninha, 29, 17-23. https://doi.org/10.1590/S0100-83582011000100003
Cunha JPARD, Alves GS, Marques RS (2017). Surface tension, hydrogen potential and electrical conductivity of phytosanitary product and adjuvant mixtures1. Revista Ciência Agronômica, 48, 261-270. https://doi.org/10.5935/1806-6690.20170030
MMA - Ministério do Meio Ambiente (2009). Relatório Técnico de Monitoramento do Desmatamento no Bioma Cerrado, 2002 a 2008: Dados Revisados.
Atwoli L et al. (2021). Call for emergency action to limit global temperature rise, restore biodiversity and protect health. https://doi.org/10.1093/nutrit/nuab067
Yamashita OM et al. (2013) Deriva simulada de herbicidas em mudas de Coffea canephora. Scientia Agraria Paranaensis – SAP Mal. Cdo. Rondon, 12, 148-156. DOI: https://doi.org/10.18188/sap.v12i2.5680
de Castro RS, Gonçalves AR, dos Santos BFR, de Campos TMP, Chaves LJ (2021). Phenotypic variability of fruits and seeds in natural populations of Hymenaea stigonocarpa (Mart. Ex Hayne). Pesquisa Agropecuária Tropical, 51. Disponível em: https://www.revistas.ufg.br/pat/article/view/67292. Accessed: 30 nov. 2021. https://doi.org/10.1590/1983-40632021v5167292
Machado AFL, Ferreira LR, Santos LDT, Santos JB, Ferreira FA, Viana RG (2009). Absorption, Translocation and Radicular Glyphosate Exudation in Eucalyptus sp. Clones. Planta Daninha, 27, 549-554.
Gandini EMM, Santos JB, Gandini AMM, Santanna RC, Silva DV da (2014). Selectivity of Herbicide and Rhizospheric Microbial Activity on Hymenaea corbaril L. Seedlings, 45, 2235-2246, https://doi.org/10.1080/00103624.2014.931415
Galvão RF, Ecco M, Riffel RC, Barbosa AP. (2021). Use of different adjuvants in the application of fungicide in soybean crop. Research, Society and Development. https://doi.org/10.33448/rsd-v10i10.18469
Carlos L, Venturin N, Macedo RLG, Higashikawa EM, Garcias MB, Farias EdeS. (2014) Growth and mineral nutrition in seedlings of pequi subjected to nutrient deprivation. Forest Science. v. 24, p. 13-21, 2014. https://doi.org/10.5902/1980509813318
Botelho RA, Pinheiro A, Silva L, Silva SPM, Souza MD, Oliveira OE (2017). Diversity of ants (Hymenoptera: Formicidae) in jatoba tree fruits Hymenaea courbaril L. (Fabaceae) in the municipality of santo antônio do leverger, mato grosso. Biodiversidade, 16, 202.
Camper ND. Research methods in weed science. 3rd ed. Champaign: Southern Weed Science Society, 1986. 486p.
Kanovsky MJ. A formaldehyde glutaraldehyde fixative of high osmolality for use in electron microscopy. Journal of Cell Biology, v.27, p.137-138, 1965.
O'Brien TP, Feder N, McCully ME. (1964) Polychromatic staining of plant cell walls by toluidine blue O O. Protoplasma, 59, 368–373. https://doi.org/10.1007/BF01248568
Furr M, Mahlberg PG (1981). Histochemical analysis of lacticifers and glandular trichomes in Cannabis sativa. J Nat. Prod, 44, 153-159.
Cruz CD. (2001) Programa GENES - Versão Windows. Aplicativo Computacional em Genética e Estatística. Editora UFV, Viçosa. 648p.
Oxborough K, & Baker NR (1997). Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components–calculation of qP and Fv-/Fm-; without measuring Fo. Photosynthesis research, 54, 135-142.
Lichtenthaler HK, Buschamann C, Knapp M (2005). How to correctly determine the different chlorophyll fluorescence parameters and the chlorophyll fluorescence decrease ratio RFd of leaves with the PAM fluorometer. Photosynthetica 43, 379–393. https://doi.org/10.1007/s11099-005-0062-6
Bilger W, Schreiber 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.
Laisk A, & Loreto F (1996). Determining photosynthetic parameters from leaf CO2 exchange and chlorophyll fluorescence (ribulose-1, 5-bisphosphate carboxylase/oxygenase specificity factor, dark respiration in the light, excitation distribution between photosystems, alternative electron transport rate, and mesophyll diffusion resistance. Plant Physiology, 110, 903-912.
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence – a practical guide. J. Exp. Bot, 345, 659-668. Doi.org/10.1093/jexbot/51.345.659
Delarmelina WM, Caldeira MVW, Faria JCT, Gonçalves EO, Rocha RLF (2014). Different Substrates for the Production of Sesbania virgata Seedlings. Floresta e Ambiente, 21, 224-233. http://dx.doi.org/10.4322/floram.2014.027
Székács A, Darvas B (2012). Forty years with glifosato. In: M.N. Hasaneen, editor, Herbicides-properties, synthesis and control of weeds. InTech, 247–284 . doi: 424–43310.5772/32491
Alcántara R, Fernadez P, Smeda RJ, Alves PL, Prado R (2016). Response of Eleusine indica and Paspalum distichum to glifosato following repeated use in citrus groves. Crop Protection, 79, 1-7. https://doi.org/10.5039/agraria.v9i4a4731
Decaro ST (2019). The importance of the right adjuvant for greater efficiency in application technology UNESP/SP: Equipe Mais Soja. Accessed: 11 mar https://maissoja.com.br/a-importancia-do-adjuvante-certo-para-maior-eficiencia-na-tecnologia-de- aplicacao/#:~:text=Por%20defini%C3%%20A7%C3%20%A3o%2C%20considera%2Dse%20adjuvante,do%20fungic
ida%2C%20herbicida%20ou%20inseticida.&text=Neste%20cen%C3%A1rio%20%C3%A9%20i%20mprescind%C3
%ADvel%20o,utilizada%20no%20preparo%20da%20calda%3E.
dos Santos CM, da Silva AA, Trazzi PA (2021). Trifluralin inhibitory potential on mycorrhization and plant development-a literature review. Brazilian Journal of Development, 7, 22122-22133. DOI: https://doi.org/10.34117/bjdv7n3-090
Pereira MRR, Souza GSF, Fonseca ED, Martins D (2015). Glyphosate reduced rates on the development of native tree species. Bioscience Journal, 31, 326-332.
de Faria GS et al. (2022). Tolerance of Hymenaea courbaril L. to glyphosate. Ecotoxicology, 31, 168-177. https://doi.org/10.1007/s10646-021-02499-y
Sturion JA (1981). Influência do recipiente e do método de semeadura na formação de mudas de Mimosa scabrella Bentham. Boletim de Pesquisa Florestal, Colombo, 69-88.
Daniel O, Vitorito CT, Alovisi AA, Massochin L, Tokura AM, Reispinheiro E, de Souza E (1997). Crescimento de mudas de Acacia mangium willd em resposta a aplicação de diferentes fontes de fosforo. Revista árvore-Sociedade de Investigações Florestais Viçosa-Brasil, 21, 323-327.
Oka JM (2017). Growth and nutrient accumulation in Pimenteira-de-cheiro (Capsicum chinense Jacquin) cv. Universidade Federal do Amazonas, Manaus.
Yamashita OM, Silva GB, Rondon Neto RM, Campos OR, Peres WM (2017). Interference of glyphosate underdoses in the development of young nim plants. Nativa, Sinop, 5, 163-168. Pesquisas Agrárias e Ambientais DOI: 10.31413/nativa.v5i3.4193
Bertoncelli DJ, Alves GAC, Furlan FF, Freiria GH, Bazzo JHB, Faria RT (2018). Effect of Glyphosate in vitro culture of Cattleya nobilior Rchb. F Cattleya nobilior Rchb. F. Revista Ceres, 65, 165-73. https://doi.org/10.1590/0034-737X201865020008
Binotto B, Antoniazzi AP, Neumann GM, Sausen TL, Budke JC (2016). Tolerance of Cedrela fissilis vell. seedlings to different lenghts and intensities of flooding. Ciência Florestal, 26, 1339- 1348. https://doi.org/10.5902/1980509825153
da Cunha Codognoto L, Conde TT, Faria GA, Maltoni KL (2020). Sublethal doses of glyphosate in combination with leaf manganese in marandu grass production. Archivos de zootecnia, 69, 294-299.
Srisook W, Lm C, Oh E, Yi k, kim S, Park KS, Song KJ (2015). Effect of Artificial Defoliation on Cane Regrowth and Fruit Development in ‘Jecy Gold’ Kiwifruit. Hort. Environ. Biotechnol., 56, 22-26. http://doi.org/10.1007/s13580-015-0119-9
Brito IPFS, Tripaldi L, Carbonari CA, Velini ED (2017). ‘Hormetic effects of glyphosate on plants’, Pest Management Science, 1, 1064-1070. https://doi.org/10.1002/ps.4523
Moraes CP, Tropaldi L, Brito IPFS, Carbonari CA, Velini ED (2019). Determination of control dose of Urochloa decumbens by the glyphosate application, Revista Brasileira de Herbicidas, 18, 1-6. https://doi.org/10.7824/rbh.v18i1.6184
ZION MARKET RESEARCH. Glyphosate Market For Conventional Crops And Genetically Modified Crop Applications: Global Market Perspective, Comprehensive Analysis And Forecast, 2017 – 2024. https://www.zionmarketresearch.com/report/glyphosate-market Accessad in 12 Março. 2022.
Louback E, Pereira TAR, Souza SR, Oliveira JA, Silva LC (2016). Vegetation damage in the vicinity of an aluminum smelter in Brasil. Ecol. Indic. 64, 193-203. https://doi.org/10.1016/j.ecolind.2016.02.044
Rodrigues AA, Filho SCV, Mendes GC, Müller C, Rodrigues DA, Mendes, GC, Rehna LS, Costa AC, Vital RG, Sales JF (2018). Sapindus saponaria bioindicator potential concerning potassium fluoride exposure by simulated rainfall: Anatomical and physiological traits. Ecological Indicators. 89, 552-558. https://doi.org/10.1016/j.ecolind.2018.02.043
Duke SO (2018). The history and current status of glifosato. Pest Management Science, 74, 1027-1034, https://doi.org/10.1002/ps.4652
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. Revista Brasileira de Ciências Agrárias, 9, 550-555. https://doi.org/10.5039/agraria.v9i4a4731
Yilmaz G, Dane F (2012). Phytotoxicity Induced by Herbicide and Surfactant on stomata and epicuticular wax of Wheat. Romanian Biotechnological Letters, 17, 7757-7765.
Gomes MP et al (2016). Differential effects of glyphosate and aminomethylphosphonic acid (AMPA) on photosynthesis and chlorophyll metabolism in willow plants. Pesticide Biochemistry and Physiology, 13, 65-70. https://doi.org/10.1016/j.pestbp.2015.11.010
Yan H, Wu L, Filardo F, Yang X, Zhao X, Fu D (2017). Sinais químicos e hidráulicos regulam o comportamento estomático e a atividade fotossintética do milho durante a seca progressiva. Acta Phisiologiae Plantarum, 39, 125. http://dox.doi.org/10.1007/s11738-017-2418-5
Jucá ACC, Castro GLS, Sousa DP, Conceição SS, Ribeiro RC, Lins PMP, Carvalho LLB, Carvalho LLB, Batista TFV (2020). Crescimento e fotossíntese de dois materiais genéticos do coqueiro submetidos a desfolha artificial. Revista Ibero Americana de Ciências Ambientais, 11, 63-71. DOI: http://doi.org/10.6008/CBPC2179-6858.2020.001.0007
Silva FG, Dutra WF, Dutra AF, De oliveira IM, Filgueiras LMB, Melo AS (2015). Gas exchange and chlorophyll fluorescence of eggplant grown under different irrigation depths. Brazilian Journal of Agricultural and Environmental Engineering, 19, 946-952. https://doi.org/10.1590/1807-1929/agriambi.v19n10p946-952

No competing interests reported.

Download PDF

Version 1

posted

You are reading this latest preprint version

Tolerance of Hymenaea stigonocarpa Mart. ex Hayne. to glyphosate

Status:

Version 1

Abstract

Figures

Introduction

Material And Methods

Experimental design and application of treatments

Visible leaf symptoms

Leaf morphoanatomical characterization

Histochemical test

Micromorphometric measurements

Evaluation of chlorophyll a fluorescence and gas exchange

Morphological analysis

Statistical analysis

Results

Visible leaf symptoms and morphoanatomical characterization

Histochemical test

Morphological analysis

Evaluation of chlorophyll a fluorescence and gas exchange

Discussion

Conclusion

Declarations

References

Additional Declarations

Status:

Version 1