Modulation of Urochloa brizantha development when phytoremediating lead-contaminated tropical soils: a photosynthetic approach

doi:10.21203/rs.3.rs-8137681/v1

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Modulation of Urochloa brizantha development when phytoremediating lead-contaminated tropical soils: a photosynthetic approach

https://doi.org/10.21203/rs.3.rs-8137681/v1

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The accumulation of heavy metals (HMs) in soils is a serious risk to the environment. Lead (Pb) has been a risk to human health and natural resources since the Industrial Revolution. The use of grasses for phytoremediation of HMs is a viable and promising alternative. We evaluated the tolerance of Urochloa brizantha in simulated phytoremediation of Pb in samples of two tropical soils: a clayey Oxisol and a sandy Entisol. To verify how the grass overcomes the stress generated by exposure to Pb, the levels of photosynthetic pigments and chlorophyll a fluorescence were quantified, as well as carbon fixation by CO₂ assimilation variables and carbo-protein compounds of primary metabolism. The readily available Pb content was higher in Entisol. Oxisol, due to its high Pb adsorption, had less effect on grasses at low Pb concentrations. Only the highest Pb concentration affected photochemistry and C fixation. Biomass was reduced only at higher concentrations, suggesting tolerance at low and medium doses when overall plant development was assessed. In terms of CO₂ assimilation variables, U. brizantha modulated the photosynthetic apparatus to maintain development and effective biomass accumulation even at high and very high Pb concentrations.

Brachiaria

tropical grass

phytostabilization

stress tolerance

plasticity

modulation

The environmental anthropization generated by humanity is recurrent and imminent. Actions that mitigate and remedy degradation and pollution status are the main strategies for maintaining a more sustainable development that is less harmful to the environment (Twardowska et al., 2007). Among the main agents of environmental degradation, environmental pollution stands out, as it poses a significant risk to human health and food safety (Macedo et al., 2022). Technological development generates large amounts of waste throughout its production chain, from the primary chain, in the generation of inputs such as agriculture and mining, to the final product for the consumer, before going through processing and industry (Almeida et al., 2013). In addition to the waste generated during the process, there is also solid waste and disposal after use and consumption.

Pollution by chemical and organic elements occurs all the time. Chemical pollution, unlike organic pollution, hardly has any efficient decomposer organisms in the environment (Okoye et al., 2022). This makes it challenging to manage the restoration and remediation of environments polluted by chemical elements, commonly referred to as potentially toxic elements (PTEs) (Okoye et al., 2022; Nieder & Benbi, 2024). Free PTEs in the environment can be harmful to human health and the environment. In general, most chemical elements in high concentrations have potential toxicity, but PTEs in even lower concentrations are dangerous and harmful, especially xenobiotic elements, such as some heavy metals (MPs) like lead, cadmium and mercury, for example, which are highly incompatible with biological life (Štefanac et al., 2021; Nieder & Benbi, 2024).

Lead (Pb) has been widely used in various industrial-technological sectors since the Industrial Revolution, such as in the manufacture of batteries, paints, pigments, fuel additives, and metal alloys (Eichler et al., 2015). Obtaining lead ore and separating it generates a large amount of highly toxic waste, and during the smelting process, it contaminates an entire area with a radius of up to 5 miles (Chen et al., 2016). Since exposure to lead is mainly through inhaling contaminated dust and ingesting contaminated water and food, the whole process of the Pb production chain is a potential pollutant and requires remediation measures (Levin et al., 2021). Lead contamination is currently a significant global problem, with an estimated 300 million tons of lead having been exposed to the environment over the last five millennia, especially in the last five centuries (Paoliello, 2001).

Remediation of contaminated areas can be carried out using physical, chemical, and biological techniques. Physical strategies are usually quite costly and risky, followed by chemical strategies which, in addition to being unattractive, can cause other types of contamination due to the chemical reagents that would remediate or neutralize the PTEs in the environment (Liu et al., 2018). Currently, biological techniques for soil and water remediation have shown great potential for large-scale applications, particularly in bioremediation. This is because numerous studies have been conducted in recent decades on biological agents, such as plants and microorganisms capable of enhancing the degradation of PTEs in the environment and/or their removal by some biological mechanisms of these organisms (Bhanse et al., 2022; Azhar et al., 2022).

A primary current tool of these biological strategies is phytoremediation, which consists of using plants that can grow through the phytotoxicity of PTEs; as in the case of Pb, the plant will tolerate the Pb-toxicity, will grow in the contaminated soil, and during its cycle will phytoaccumulate, phytoextract and phytostabilize the Pb ions present in the soil (Etim, 2012; Liu et al., 2024). In addition, the roots optimize the microbial community in the soil, where the rhizosphere area becomes an active agent for degrading or stabilizing Pb ions, and some plant species can emit exudates capable of enhancing these activities (Gavrilescu, 2022; Breton-Deval et al., 2022).

Some species have been used in Pb phytoremediation techniques, but many do not show potential, despite developing under Pb phytotoxicity; they do not have the capacity to bioaccumulate PTE, nor to optimize secondary interactions such as phytostabilization (Pasricha et al., 2021; Sladkovska et al., 2022). Plants that, in addition to tolerating the abiotic stress generated, can absorb and accumulate metal ions are hyperaccumulators, and in the case of HMs, they have been called metallophyte species (Fernández-Fernández et al., 2008; Fernando et al., 2018; Liu et al., 2022). Examples applied to Pb are vetiver grass (Vetiveria zizanioides) (Yoga & Tangahu, 2022), pigeonpea (Canavalia ensiformis) (Pereira et al., 2010), sunflower (Helianthus annuus) (Yoga & Tangahu, 2022), and castor bean (Ricinus communis) (Bauddh et al., 2015), used in the phytoremediation of lead-contaminated soils.

More recent studies have pointed out some tropical grasses as potential HMs-hyperaccumulators, common in the phytoremediation of soils with cadmium (Cd) and nickel (Ni) (Rabêlo et al., 2021). Potentialities have also been noted for Pb in species of the genus Penisetum, Megathyrsus, and Urochloa (Das et al., 2017; Rabêlo et al., 2021; Farnezi et al., 2022), especially species that have C4 metabolism. However, the efficiency of bioremediation by the plant does not depend solely on its characteristics and potential; it can vary due to other factors, such as soil conditions and the concentration of lead present (Butcher, 2009). The chemical composition, pH, texture, and the presence of other contaminants in the soil can affect the ability of grasses to absorb HMs (Rabêlo et al., 2021). In addition, at very high concentrations, some plants may be unable to absorb and accumulate lead efficiently, leading to less effective bioremediation (Egendorf et al., 2020).

Seeking to fill gaps and look for trends in phytoremediation by grasses (Rabêlo et al., 2021; Sladkovska et al., 2022), we investigated the phytoremediation of Pb by a cosmopolitan grass, Urochloa brizantha Hochst. ex A.Rich. cv. Marandú, using two contaminated soils, one with a clayey texture and the other with sandy texture. We also varied the Pb concentrations according to the guideline values proposed by the Brazilian Environmental Resolution (Brazil, 2023). This study aims to deepen our understanding of how the grass species resists Pb phytotoxicity in the soil by analyzing plant development in its physiological and metabolic aspects, thus being able to optimize the management of the species during the phytoremediation technique.

Our main questions to outline the study were: i) Do physiological and metabolic strategies occur for the species to develop in the face of abiotic stress generated by Pb? ii) Will soils of contrasting textures provide different levels of Pb-availability and toxicity? So, a controlled contamination trial of contrasting textured soils with different Pb concentrations was conducted, after which U. brizantha grasses were grown to phytoremediate the soils. In this way, this study model can be analysed to understand photosynthesis, metabolism, growth, and Pb-bioaccumulation in the face of Pb contamination levels in soils with different textures.

Lead contamination was induced using two soils with contrasting textures. After contamination, a phytoremediation test was carried out with Uroclhoa brizantha to evaluate its full development and relate it to the Pb contamination remediation status of each soil. All experimental phases were conducted in a greenhouse with a top cover of agro-plastic and sides protected by an anti-aphid screen, two concrete benches (0.9 x 1.2 x 6 m), located in Diamantina, state of Minas Gerais, Brazil.

2.1. Soil collection

The soil samples used were collected from the surface layer (0–20 cm) by the trench method in the municipality of Diamantina - MG (18°15′ S, 43°36′ W, 1250 m MSL). Two soils were used, a clayey and a sandy, being Xanthic Hapludox (XH) and a Typic Quartzipsamment (TQ), representing two orders of the twelve in Soil Taxonomy (Oxisol and Entisol) (Soil Survey Staff, 2022). The soil samples were sieved (2 mm) and dried on a bench in the greenhouse. Subsequently, a composite sample was taken from each soil, and chemical and granulometric analyses were performed following the methodologies described by Teixeira et al. (2017). The XH and TQ soils (oxisol and entisol) have contrasting granulometry; XH contains 40% clay and 49% sand, and TQ only 15% clay and 82% sand (Table 1). Other characteristics differed, such as the organic matter (OM) content, which was higher in XH, as well as lower nutrient and cation values (Table 1).

Table 1

Chemical and granulometric properties of the Xanthic Hapludox (XH) and Typic Quartzipsamment (TQ).
Soil	pH	P	K	Ca²⁺	Mg²⁺	Al³⁺	H + Al	ECC¹	CEC_ef	CEC²
Soil	H₂O	mg dm^− 3		cmol_c dm^− 3
XH	4.8	2.5	80	0.6	0.25	0.4	2.4	1	1.5	3.5
TQ	5.0	1.4	20	0.4	0.04	0.1	1.8	0.5	0.6	2
Soil	V%³	m%⁴	OM⁵	Cu	Fe	Mg	Zn	Sand	Clay	Silt
Soil	%		g kg^− 1	mg dm^− 3				g kg^− 1
XH	32	29	17	2	136	48	3	490	401	109
TQ	22	17	10	< 1	158	1	2	823	152	25
¹Sum exchangeable cation content; ²Cation exchange capacity at pH 7.0; ³Base saturation index; ⁴Aluminum saturation index; ⁵Organic matter. Methods: pH - Soil:water 1:2.5; P and K - Mehlich 1 extractor; Ca, Mg and Al - KCl 1 mol L^− 1. extractor; Granulometric properties - Pipette method.

2.2. Botanical material

The tropical grass used in the experiment was Urochloa brizantha (Hochst.) Stapf cv. Marandú. Specimens were grown in beds, and the botanical material was checked with specimens from national herbaria (specimens: CEPEC00034647, MBML048705, IBGE00048970) (BFG, 2018). Popularly known as braquiaria, marandú or brachiarão, U. brizantha is a perennial grass with a cespitose growth habit and a robust stature, from 1.5 to 2.0 m in height, with prostrate initial stems, but producing predominantly erect tillers. It has very short and curved rhizomes, the leaves are prominent and yellowish-green in colour, it requires medium to good fertility and is resistant to pasture leafhoppers, has tolerance to cold, drought and fire, and can produce more than 20 t ha-1 of dry mass (Nunes et al., 1984; Benett et al., 2008).

2.3. Soil fertilization and contamination

We induced a soil contamination following the processes: liming > fertilization > Pb contamination. Each pot was filled with a plastic bag and 4 kg of dry soil. A dolomitic limestone was added with a Effective Calcium Carbonate Equivalent (ECCE) of 90% containing 380 g kg^− 1 of CaO and 125 g kg^− 1 of MgO, in order to raise the base saturation to 45%, homogenized and moistened to 60% of the maximum water retention capacity (WRC) as recommended by Farnezi (2022). The soil samples were incubated for 30 days, then dried over time and sieved.

We repeated the process with the planting fertilizer, applying 100 mg N (NH₄H₂PO₄); 150 mg K (KCl); 50 mg S (NH₄)₂SO₄; 1 mg B (H₃BO₃), 5 mg Fe (FeSO₄.7H₂O-EDTA), 4 mg Mn (MnCl₂) and 4 mg Zn (ZnCl₂), and P was with (NH₄)H₂PO₄ and KH₂PO₄ at a dose of 200 mg for TQ and 350 mg for XH, all in mg kg^− 1 of soil. The soil was homogenized, incubated at 60% WRC for 15 days, then dried and sieved. All acidity correction and fertilization followed the recommendations of Alvarez and Ribeiro (1999) for tropical grasses.

Soil contamination followed the guidelines of the Brazilian Environment Council, as outlined in Resolution No. 420 of December 28, 2009, which sets out criteria and guideline values for soil quality in terms of the presence of chemical substances (Brazil, 2009). The resolution establishes that for each chemical agent in the soil, there are background, prevention, and intervention values, which represent the concentrations of critical levels in the area and are estimated based on the economic activity carried out in the soil, whether agricultural, residential, or industrial. The concentrations were 72 mg kg^− 1 (prevention), 150 mg kg^− 1 (agricultural intervention), 300 mg kg^− 1 (residential intervention), and 900 mg kg^− 1 (industrial intervention). The Pb was applied as lead chloride P.A. (PbCl₂), homogenized to the soil in the appropriate concentrations; the soil was moistened to 60% WRC and incubated for 15 days, according to Farnezi et al. (2022).

2.4. Experimental design and conduct

The experiment was conducted in a completely randomized design using a 2 x 5 factorial scheme (two soils and five Pb concentrations + control (no Pb added)), making up 12 treatments with six replications, where each pot (with two plants) was a sampling unit. The design was laid out on a bench, and the pots were randomized every 15 days.

Ten seeds were sown per pot. Seedling emergence began on the 13th day, with the two largest seedlings remaining. Five days after thinning, the first nitrogen fertilizer was applied, and 30 mg of N (urea) per kg of soil was applied every 15 days, with a total of four applications. Soil humidity was kept at 60% WRC, and each pot was manually irrigated three times a week on alternate days using tap water. The weight of each pot was measured weekly to adjust the irrigation rate according to the soil and plant transpiration. After thinning, the period of vegetative development of the grasses was 90 days.

2.5 Photochemistry - Chlorophyll a fluorescence, photosynthetic pigments, relative water content (RWC), and specific leaf area (SLA)

The physiological analyses were divided into non-destructive (IRGA and MINI-PAM) and semi-destructive (those using plant parts). For the physiological measurements, the last fully developed leaf was considered (fully expanded and with a deep green colour). The values were estimated by reading one leaf on each plant, in the middle third of the leaf. The physiological measurements were taken in the morning between 8:00 am and 11:00 am.

Chlorophyll a fluorescence was assessed using a pulse-modulated fluorometer (MINI-PAM, Heinz Walz, Effeltrich, Germany). The first assay measured the maximum quantum yield of photosystem II (F_v/F_m), determined after dark adaptation for 30 min (Genty and Baker, 1989). The second test was rapid light curves to determine the photosynthetic capacity of plants under contrasting light regimes in response to saturated light intensity. These were carried out by increasing the actinic light intensity (0-1800 µmol m^− 2s^− 1) divided into eight intervals of 30 s each, obtaining minimum (F₀) and maximum (F_m) fluorescence values in the light-adapted state for each light intensity, the difference between the two being the variable fluorescence (F_v). This then estimates the effective quantum yield of PSII (ФPSII) and the apparent electron transport rate (ETR) (Genty et al., 1989; Schreiber et al., 1995). The quantum yield of photochemical energy conversion in PSII (YII) according to Klughammer and Schreiber (2008).

Contents of photosynthetic pigments were determined using a colorimetric method after obtaining the leaf extract using an acetone solution. The same leaves used for the non-destructive analysis were collected, placed in plastic bags, and taken to the laboratory in a closed box containing ice. A 1 cm² fragment was removed and placed in amber vials containing 80% acetone. With the help of a mortar, the samples were macerated in the acetone solution until a green extract was formed. The extracts were centrifuged in a tube to decant the solid fragments, the supernatant was analysed in a UV-Vis spectrophotometer (Digital spectrophotometer Biospectro, 200–1000 nm, Brazil) at wavelengths of 470, 646, and 663 nm in absorbance light, and the concentrations of chlorophyll a (Chla), chlorophyll b (Chlb), and carotenoids (Car) measured in equations proposed by Lichtenthaler and Wellburn (1983).

RWC and SLA were measured on the same leaves. Two 1 cm² leaf fragments, one from each plant, were collected, and the fresh mass (FM) was measured, after which the fragment was turgid in distilled water and saturated for 48 h; the turgid mass (TM) was measured. The fragments were dried in an oven until the mass weight was stable, and finally, the dry mass (DM) was obtained. The equation proposed by Turner (1981) was used for the RWC: RWC = (FM - DM) / (TM - DM), which expresses the relative water content of the leaf in percentage (%). The SLA was calculated by dividing the area of the leaf fragment by its own DM, expressed in cm² g^− 1 (Witkowski and Lamont, 1991). At the end, after removing the necessary fragments, the rest of each leaf (more than 90%) was decayed in a microwave oven for 1 min to stop leaf metabolism, then dried in an oven, ground in a Willey mill (0.5 mm sieve), and set aside to analyse the compounds of primary metabolism.

2.6 Carbon fixation - CO₂ assimilation, carbohydrate, protein, carbon (C), and nitrogen (N) content

CO₂ assimilation was assessed using an Infrared Gas Absorption Analyzer - IRGA (ADC Bioscientific model LCpro-SD, Hoddesdon, England). Photosynthesis (A), transpiration (E), stomatal conductance (gs), CO₂ consumed (ΔC), internal carbon (Ci), and water use efficiency (WUE) were determined following the recommendations of Dalastra et al. (2014).

For the carbohydrate content and CHN analyses, the leaves were powdered in a mortar and pestle so that the leaf particles were less than 500 micrometers and passed through a fine sieve (0.5 mm sieve). The carbohydrate content was obtained using a colorimetric method after a phenol-sulphuric reaction (Chow and Landhãusser, 2004), which measured total soluble sugar (TSS), water-soluble polysaccharide (WSP), and starch content, expressed in mg of carbohydrate per gram of DM. The C, N, H, and protein contents were determined by dry combustion in a CHNS/O Elemental Analyser (LECO, Truspec Micro, Michigan, USA).

2.7 Biomass

The aerial part was collected by cutting at the base of the grass clump with pruning shears. The leaf blades (leaves) and stalks (pseudoculm) were separated and stored in a Kraft paper bag. Using a probe (20 mm diameter x 30 cm length), samples were taken from the soil profile in each pot at three points. The samples from each treatment were homogenized to form a composite sample, dried, sieved through a 1 mm mesh, and stored in a plastic bag. At the end, the soil was carefully broken up to remove the roots; the roots were washed in running water until all traces of soil were removed, then washed in a neutral detergent solution (0.5%) and rinsed with distilled water.

The base of the thatch was separated from the root system and stored separately in a Kraft paper bag. The biomass was placed in a hot air circulation oven at 50ºC until it reached a constant weight and, once dry, all the parts of the grasses were weighed separately. In the end, the leaf dry mass (LDM), stem dry mass (SDM), stem-base dry mass (SBDM), where the sum of the three masses measures the aerial dry mass (ADM), root dry mass (RDM), and the ratio of aerial mass to root mass (AP/RP) were all expressed in grams of dry mass.

2.8 Statistical analysis

Exploratory principal component analysis (PCA) was carried out using the R package FactoMineR version 2.4 (Lê et al., 2008) and we specified a correlation matrix as the variables did not have the same scales (Abdi and Williams, 2010), reducing the dimensionality of the data sets and assessing associations between variables, pointing out the most contributory ones. For better visualization and interpretation, the data set was subdivided into three groups of variables: i) Photochemistry (photosynthetic pigment content and chlorophyll a fluorescence variables); ii) Carbon fixation (CO₂ assimilation variables, relative leaf water content and primary leaf metabolism); and iii) Biomass (dry biomass and specific leaf area).

Subsequently, linear models (LMs) were developed to investigate the effects of the different Pb concentrations in the two soils. The R-package DHARMa version 0.4.6 (Hartig, 2022) was used to check the normality and homoscedasticity of the data. The R-package car version 3.1.1 (Fox and Weisberg, 2019) was used to perform the type II analysis of variance. When significant, a post-hoc analysis was carried out using the Tukey test to split the concentration and, where necessary, the interaction, using the R-package emmeans version 1.10.1 (Lenth, 2024). To calculate averages and perform contrast comparisons, the R-package multicomp version 1.4.25 (Hothorn, Bretz and Westfall, 2008) was used to apply the comparison method, differentiating the treatments from each other. The values adjusted by the model were transformed back using the R-package ggeffects version 1.1.5 (Lüdecke, 2018). All analyses were carried out in the R integrated statistical development environment version 4.2.2 (R Core Team 2022) with a significance level of 0.05.

3.1. Principal component analysis

3.1.1. Photochemistry

The PC1 axis contributed 34.51% to explaining the variation, and PC2 19.72%, a total of 54.23% (Fig. 1). The most contributory variables in PC1 were F_v, ФPSII and YII and for PC2 Chlb, total chlorophyll (TChl), and Chla/Chlb. The photosynthetic pigment variables Chlb, TChl and Chla were positively correlated, and the Car/TChl and Chla/Chlb ratios were negatively correlated. F0 was negatively correlated with the other chlorophyll a fluorescence variables. F_v/F_m and q_p were strongly correlated, as were ФPSII, YII and ETR, where the sub-axes overlapped. NPQ and Car had the smallest contributions to explaining the variation in the set of data measuring photochemistry.

3.1.2 Carbon fixation

The PC1 axis contributed 33.93% to explaining the variation, and PC2 22.26%, a sum of 56.19% (Fig. 2). The most contributory variables in PC1 were A, ΔC, and Ci, and for PC2 were E, protein, and N. N and protein contents are highly correlated, and showed a negative correlation with TSS and that with C/N, with TSS and C/N being highly correlated. With the exception of Ci, which is negatively correlated with these, the other CO₂ assimilation variables are highly correlated. C and RWC tend to correlate, but RWC, WSP, and starch had the smallest contributions to explaining the variation in the set of data measuring C fixation.

3.2.3 Biomass

The PC1 axis contributed 78.46% to explaining the variation, and PC2 9.8%, a total of 88.26% (Fig. 3). The most contributory variables in PC1 were TDM, ADM, and SDM, and for PC2 were AP/RP, SBDM, and RDM. All the biomass variables correlated strongly, with SLA correlating negatively, along with AP/RP.

3.2. Linear models

3.2.1. Photochemistry

Chla was reduced at Pb concentrations of 300 and 900 mg kg^− 1, and remained similar to the control at 72 and 150 mg kg^− 1 (Fig. 4A). On the other hand, Chlb and Chla/Chlb did not differ (Fig. 4B and C). Car differed between concentrations with a similar pattern to Chla (Fig. 4A and D). TChl was most reduced at 900 mg kg^− 1, while 72 mg kg^− 1 induced higher TChl values, even compared to the control. Synergistically, there was a difference between the soils, where entisol had higher levels compared to oxisol (Fig. 4E). Car/TChl did not differ among the treatments (Fig. 4F).

The F_v/F_m was lowest at Pb concentrations of 900 mg kg^− 1, and the other concentrations had similar averages. However, there was a difference between the soils, with lower averages in the entisol concentrations, with extremely low values in the 72 mg kg^− 1 concentration compared to the others and the control. The interaction between soil and Pb concentration was significant, with F_v/F_m values close to 300 and 900 mg kg^− 1. Antagonistically, 72 and 150 mg kg^− 1 had higher F_v/F_m in oxisol, and for the same concentrations, very low values in entisol (Fig. 4G). YII showed higher values in oxisol Pb concentrations than in entisol (Fig. 4H).

F₀ had the lowest values at 72 mg kg^− 1, and entisol was the soil with the highest average Pb concentrations. There was an interaction between the factors, as 72 and 180 mg kg^− 1 in oxisol were the lowest values, and the highest value was 72 mg kg⁻1 in entisol, followed by 900 mg kg^− 1 for both soils (Fig. 4I). F_m showed a reduction at 72 mg kg^− 1 and differences between soils, with oxisol having the highest average values (Fig. 4J). ETR did not differ between Pb concentrations, but it did differ between soils, with oxisol having the highest values (Fig. 4K). NPQ did not differ in any of the factors, while q_p differed in all of them, with lower values in entisol, especially at concentrations of 72 and 180 mg kg^− 1, and higher values in oxisol at the same Pb concentrations, highlighting the difference between soils and the interaction between the factors (Fig. 4L and M). ФPSII differed between soils, with higher values in oxisol (Fig. 4N).

3.2.1. Carbon fixation

RWC was highest at 72 mg kg^− 1 and lowest at 900 mg kg^− 1 (Fig. 5A). The g_s showed no difference (Fig. 5B). ΔC had a higher value at 72 mg kg^− 1 followed by a lower value at 300 mg kg^− 1, which rose again at 900 mg kg^− 1 (Fig. 5C). C_i and E did not differ in any of the factors and concentrations (Fig. 5D and F). The A showed differences and a similar pattern of distribution of means to ΔC (Fig. 5C and G). WUE and TSS did not differ between Pb concentrations, only in soils, with higher values in oxisols (Fig. 5H and I). WSP, on the other hand, had the highest levels in entisol, with the 900 mg kg^− 1 concentration having the highest averages (Fig. 5J). The starch content was highest in the Pb 900 mg kg^− 1 concentration, with the entisol having the highest values. There was an interaction between factors in which the highest content occurred in entisol at 900 mg kg^− 1 and the lowest in oxisol in the control treatment (Fig. 5K).

Protein was highest at 900 mg kg^− 1, there was a difference between the soils with the highest values in the entisol, the interaction being evidenced by the highest value in the entisol at 900 mg kg^− 1 and the lowest in the oxisol at 300 mg kg^− 1 (Fig. 5L). The C content was lowest at 900 mg kg^− 1 compared to the others. Entisol had the highest values (Fig. 5M). Antagonistically, N was higher at 900 mg kg^− 1 with higher Pb concentrations in entisol, there was an interaction, and the distribution of averages was similar to that of protein (Fig. 5L and N). H values did not differ in Pb concentrations, but did differ between soils with higher values in entisol (Fig. 5O). The C/N ratio was lowest at 900 mg kg^− 1 followed by 300 mg kg^− 1, the oxisol had the highest averages, and there was an interaction, with the lowest values in the entisol at 900 mg kg^− 1 and the highest in the oxisol at 180 mg kg^− 1.

3.3.3. Biomass

LDM was most reduced at 900 mg kg^− 1 followed by 300 mg kg^− 1 with the highest average mass in the control treatment, oxisol showed the highest average values (Fig. 6A). SLA had a large increase at 900 mg kg^− 1 and entisol was the one with the highest values (Fig. 6B). SDM had a reduction at 900 mg kg^− 1 followed by 300 mg kg^− 1, the control and 72 mg kg^− 1 were higher, and oxisol was the soil with the highest mass (Fig. 6C). SBDM showed a similar pattern to SDM, but as oxisol had better growth, 72 and 180 mg kg^− 1 had higher values (Fig. 6D). Thus, ADM followed the distribution of treatment averages similar to the other three masses of the parts that make it up, in which oxisol evidently showed the greatest accumulation of masses (Fig. 6E).

In RDM, the control treatment started with the highest average in entisol, which reversed at the first Pb concentration, leaving oxisol with the highest values. The lowest mass was at 900 mg kg^− 1, and the other concentrations did not differ (Fig. 6F). TDM followed a similar pattern of average points to the other biomass metrics (Fig. 6G). The AP/RP ratio did not differ between the Pb concentrations, with the exception of 900 mg kg^− 1, which had higher values (Fig. 6H).

4.1 Photochemistry

The photochemical phase is fundamental in C4 plants because it is an essential part of photosynthesis in which radiation from sunlight is used in chemical reactions, through which plants convert light energy into chemical energy. In this sense, photosynthetic pigments (chlorophyll a, chlorophyll b, and carotenoids) are important for the efficiency of the process; they absorb sunlight so that plants can carry out photosynthesis. Photosynthetic pigments absorb only specific wavelengths of visible light, a set of wavelengths absorbed by a pigment is its absorption spectrum. The type, quantity, and incorporation of carotenoids depend on the quality and quantity of sunlight radiated.

In this study, the environmental conditions were controlled and randomized, and all individuals received the same light radiation. This leads us to believe that the differences in photosynthetic pigments and chlorophyll a fluorescence are due to the abiotic stress generated by Pb, and the absence of these Pb stress symptoms due to the tolerance of U. brizantha. The fact that the chlorophyll a and b contents did not differ shows that despite the influence of high Pb concentrations such as 300 and 900 mg kg^− 1 affecting some growth and development variables, which will be discussed later, the chlorophyll content was maintained, which is a strategy to maintain efficiency in capturing light energy for the chemosynthesis of carbon compounds.

Ezhili et al. (2012) showed that concentrations of between 100 and 400 mg L^− 1 in the irrigation of Vetiveria zizanioides did not interfere with the synthesis of chlorophyll a and b, with a reduction only at 600 mg L^− 1. Similar results were found in Paspalum distichum grown in soils containing Pb (Bhattacharya et al., 2010). Ezhili et al. (2012) also found an increase in carotenoid content at higher Pb concentrations, the opposite of our study, in which U. brizantha showed a reduction at a concentration of 900 mg kg^− 1.

In general, HMs interact with the photosynthetic apparatus at various levels of organization, mainly affecting the synthesis of photosynthetic pigments, in which the organization of chlorophyll can interfere with the organization of pigment-protein complexes that are essential for optimal PSII function (Rai et al., 2016). One harmful rearrangement that occurs is the replacement of the Mg²⁺ ion by some toxic metal ion, which will influence the Chl content in plants, as the Mg in chlorophyll is replaced by Cu, Zn, Cd, Hg, Pb, or Ni (Kupper et al., 1996). Another change in functionality is that Pb alters the lipid composition of thylakoid membranes (Rai et al., 2016), in addition to a greater amount of starch grains in the chloroplasts of plants affected by Pb (Khan et al., 2018). In Hordeum vulgare leaves cultivated in the presence of Pb, there was a significant decrease in the number of thylakoids per granum and invaginations of the organelle membrane in the form of a covering of cytoplasmic material (Legocka et al., 2015).

The F_v/F_m fluctuated greatly between Pb concentrations and between soils. As the intervention values have a wide range between 300 and 900 mg kg^− 1, the chlorophyll fluorescence response to Pb toxicity differed between the last concentration and the others, which have different exponential ranges in each soil. Rice grown in a nutrient solution contaminated with Pb exhibited a reduction in F_v/F_m as the Pb concentration in the solution increased (Li et al., 2012), and the same was noted when soil Pb increased in the C4 grass Miscanthus floridulus (Qin et al., 2023). In our study, there was no immediate reduction in the values of F_v/F_m in oxisol; at lower Pb concentrations of 72 and 180 mg Kg^− 1, the values increased compared to the control, with a reduction at higher concentrations. In entisol, however, the values drop drastically at the first Pb concentration, followed by a gradual increase in the others, to the point where the concentration of 900 mg Kg^− 1 returns to the same level as the control.

Except for F₀, all chlorophyll fluorescence variables had higher values in the oxisol compared to the entisol. This may have several explanatory relationships, the main one of which we believe is the physicochemical properties of the entisol, which enhance the adsorption of Pb in the soil and reduce its bioavailable content in the nutrient solution, such as higher CTC, higher clay and OM content (Huang et al., 2020), OM being closely related to the optimization of chlorophyll synthesis and its fluorescence.

F_m gradually decreased with increasing Pb concentration, but F₀ showed a complex interaction, in which, unlike the other fluorescence variables, entisol had higher values at initial concentrations, while oxisol had higher values at high Pb concentrations. U. brizantha clearly shows different aspects of chlorophyll fluorescence depending on the physical-chemical aspects of the soil in which it grows in Pb phytoremediation. q_p in some plants increases as a protective mechanism to increase the efficiency of light use so that photosynthesis can be kept high, avoiding photo-oxidative damage (Ye et al., 2013). As the light conditions in our study were the same in all cases, we can interpret that the increase in q_p in oxisol with low Pb concentrations is a strategy to optimize photosynthesis.

HM, such as Cd and Pb, can reduce q_p, indicating damage to PSII and a lower efficiency in the use of light for photosynthesis, resulting in greater dissipation of energy as heat or non-photosynthetic fluorescence (Singh et al., 2016). However, indices such as NPQ and ETR, as well as variables that express fluorescence in the system itself (ΦPSII), did not differ at any Pb concentration. ETR remaining high indicates that the plant is efficiently converting light energy into chemical energy through the electron transport chain, which is essential for the production of ATP and NADPH, and subsequent C fixation, with ΦPSII being directly proportional to the efficiency of photosynthesis and correlated with ETR (Maxwell and Johnson, 2000; Baker, 2008; Mukherjee et al., 2016).

Species of the genus Urchloa (formerly Brachiaria) were used to evaluate the action of herbicides on the photosynthesis of U. ruziziensis and U. decumbens, both capable of regenerating their photosynthetic apparatus at medium concentrations (Silveira et al., 2017). Although the active compounds of the herbicides are not Pb-based, the comparison with Pb stress can be established through common effects, such as the production of reactive oxygen species (ROS), which lead to oxidative stress; both herbicides and HM trigger oxidative damage to lipids, proteins, and DNA. Furthermore, both can compromise crucial physiological processes, such as photosynthesis and energy metabolism, due to the accumulation of cellular damage (Délye et al., 2005; Sharma and Dietz, 2006; Duke and Powles, 2008). Thus, it is evident that U. Brizantha ends up modulating aspects related to photosynthetic pigments and chlorophyll a fluorescence, which will later reflect on the assimilation of carbon and products of primary metabolism.

4.2 Carbon fixation

The RWC was similar to the control treatment in almost all Pb concentrations, with a reduction of 900 mg kg^− 1. Synergistically, WUE showed no differences between treatments or soils, which corroborates some photochemical variables. This is because the main abiotic stresses affecting these variables are light and water stress (Flexas and Medrano, 2002; Mathur et al., 2014). These conditions were mitigated and remained consistent throughout the experiment thanks to the greenhouse's environmental controls and lighting. Thus, the stress generated by toxicity was the main agent of change and differences, and the absence of differences between factors, expresses tolerance of U. Brizantha to Pb stress.

More than environmental factors, the complexity of the soil-plant system, and especially how the environmental condition associated with the stress agent (Pb, in our case), will also influence the secondary metabolism of the grass to the impact of Pb stress, which goes beyond the initial tolerance based on the production of primary metabolites, such as those directly linked to CO₂ assimilation. Secondary metabolism plays a critical role in the plant's response to abiotic Pb stresses, such as phytohormones, phenolic compounds and antioxidants, produced in response to adverse conditions, with the presence of HM, and these compounds can function as an adaptive defense strategy, helping plants to mitigate the conflicts contracted by stress (Aguirre-Becerra et al., 2021).

The infrared CO₂ assimilation measurement variables demonstrated that U. Brizantha used modulation of its photosynthetic apparatus to tolerate Pb stress. E, A, C_i and even g_s did not show differences between treatments or between soils, only Δ^C showed a higher value at the lowest Pb concentration of 72 mg kg^− 1. Regardless of development, most variables indicate that the plant maintained CO₂ consumption, related to the high WUE index. The efficiency of the grass went beyond maintaining good light capture, but also in water resources for the photosynthetic apparatus, linked to both this, good rates of assimilated CO₂. Khan et al. (2018) saw that, unlike what we observed in CO₂ assimilation in U. brizantha, U. mutica had a reduction in A, E, and g_s indices as exposure to Pb increased.

Rabêlo et al. (2020) found results in the same direction studying Brachiaria decumbens in soils contaminated with cadmium (Cd), where CO₂ assimilation was also not affected, due to the protection provided by good levels of reduced glutathione (GSH) and phytochelatins (PCs) with greater synthesis in the aerial part than in the roots. Similar to the results obtained here, Rabêlo et al. (2020) notes that B. decumbens developed in low, medium, and high concentrations of copper (Cu), with CO₂ assimilation only being reduced at very high concentrations; the low concentration (30 mg kg^− 1) being higher than the copper fertilizer dose required for the forage crop Urochloa spp. High CO₂ assimilated per unit of transpired water is generally attributed to obtaining partial stomatal closure, with a decrease in transpiration, which leads to lower forage yield of the grass (Rao et al., 2011), the opposite being a sign of tolerance, in the present Pb stress conditions, U. brizantha resisted the stress generated by modulating the photosynthetic system.

Efficiency in CO₂ assimilation reflects more optimised synthesis of secondary metabolic compounds. The main ones in this study were: TSS was similar between Pb concentrations and the control, while WSP was higher at a Pb concentration of 900 mg kg^− 1. Starch content also showed this trend, with more abrupt values observed in the Entisol. A previous study on U. ruziziensis in Pb-contaminated soils revealed an increase in metallothionein (MT) and phytochelatin (PC) production; these compounds play a crucial role in eliminating reactive oxygen species (ROS) and maintaining Pb ion homeostasis, thereby influencing stress responses (Huang et al., 2018; Martins et al., 2023). This is confirmed in studies with Arabidopsis, which allowed the identification of the entire set of MT genes, linked to the understanding of the regulation of FQ biosynthesis and MT gene expression, corroborating the roles of these proteins in the detoxification and homeostasis of HMs (Cobbett and Goldsbrough, 2002).

A correlation between CO₂ assimilation and N metabolism in the leaf is evident as the N content increased in the highest Pb concentration, and there was also a reduction in the C/N ratio, as well as the C content itself with Pb at 900 mg kg^− 1. In dry-season tolerance to oxidative stress in C4 perennial prairie grasses, N-induced retranslocation may serve to protect plant N from loss by herbivory, fire, and volatilization during periods when soil N uptake and carbon assimilation are limited by water availability (Heckathorn and DeLucia, 1994). In fact, visually, we noticed that in U. brizantha the leaves of the lower third of the clump tended to yellow over time and senesce. Further studies may separate these two parts of the leaf biomass, having a functional leaf mass and a senesced leaf mass. Thus, the ratio of these two masses is an indicator of resistance or susceptibility in the case of Urochloa brizantha.

4.3 Biomass

The biomass yield of U. brizantha in Pb phytoremediation corroborates what was mentioned above in terms of photochemistry and CO₂ assimilation. Several factors related to photosynthesis are modulated so that the specimen tolerates Pb stress in the phytoremediation process in its study. U. mutica showed a greater degree of tolerance to high concentrations of Pb, because metal stress inhibited ROS activity but increased general catalase activity, reflecting maintenance of biomass accumulation (Khan et al., 2018). In a genetic study of U. ruzizienzis, Martins et al. (2023) identified proteins associated with the auxin efflux, and that the effects of auxin depend on concentration, being produced mainly in meristematic and specific regions (Blakeslee et al., 2005). In this case, transport is facilitated by influx and efflux transporter proteins, providing essential directional and positional cues for several developmental processes, including vascular differentiation, apical dominance, organ development, and adjacent growth (Grieneisen et al., 2007).

Generally, the biomass was drastically reduced at 900 mg kg^− 1, with smaller plants, visually dwarfish in all specimens of this treatment in the entisol. In the oxisol, although some were at least visually developed, others were extremely small. In the other concentrations, although the biomass in entisol plants reduced with increasing Pb concentration, in oxisol, it had a higher LDM at 72 and 180 mg kg^− 1, and at 180 mg kg^− 1 the mass was similar to the control. Other researchers have reported similar results, in which simulating Pb phytoremediation with U. decumbens and U. brizantha, the relative growth was similar to the control at 40 and 80 mg kg^− 1, but started to decrease at the highest treatment, 240 mg kg^− 1 (Farnezi et al., 2022).

Only a Pb concentration of 900 mg kg^− 1 affected CO₂ assimilation and primary metabolism, maintaining the contents of carbohydrates, proteins, C, and N, all at Pb concentrations of 0 to 180–300 mg kg^− 1 of soil. The biomass development of 90 days at Pb concentrations is promising for applied phytoremediation.

The increase or maintenance of biomass content is highly correlated with the rates of phytoextraction and phytostabilization throughout and at the end of the phytoremediation process of soils contaminated with Pb. Pb phytotoxicity to U. brizantha was greater in the sandy entisol with low OM contents than in the clayey oxisol with higher OM contents. U. brizantha showed modulation in photosynthetic aspects, leading to comprehensive plant development in concentrations between 72–300 mg Pb in kg^− 1 soil.

Phytoremediation of Pb-contaminated soil with U. brizantha cultivation is promising. Physiological modulations occur, maintaining optimized plant development, even in the face of Pb stress and oxidative damage. The modulation of energy capture by the photochemical phase is evidenced by the maintenance the photosynthetic pigment synthesis and the quality of chlorophyll a fluorescence.

Acknowledgements

To the National Council for Scientific and Technological Development (CNPq) for funding (process # 141821/2020-5). To the Federal University of Jequitinhonha and Mucuri Valley’s, Brazil, for the facilities used to conduct the experiment.

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Modulation of Urochloa brizantha development when phytoremediating lead-contaminated tropical soils: a photosynthetic approach

Status:

Version 1

Abstract

Figures

1. Introduction

2. Material and methods

2.1. Soil collection

2.2. Botanical material

2.3. Soil fertilization and contamination

2.4. Experimental design and conduct

2.6 Carbon fixation - CO₂ assimilation, carbohydrate, protein, carbon (C), and nitrogen (N) content

2.7 Biomass

2.8 Statistical analysis

3. Results

3.1. Principal component analysis

3.1.1. Photochemistry

3.1.2 Carbon fixation

3.2.3 Biomass

3.2. Linear models

3.2.1. Photochemistry

3.2.1. Carbon fixation

3.3.3. Biomass

4. Discussion

4.1 Photochemistry

4.2 Carbon fixation

4.3 Biomass

5. Conclusions

Declarations

Acknowledgements

References

Status:

Version 1

Modulation of Urochloa brizantha development when phytoremediating lead-contaminated tropical soils: a photosynthetic approach

Status:

Version 1

Abstract

Figures

1. Introduction

2. Material and methods

2.1. Soil collection

2.2. Botanical material

2.3. Soil fertilization and contamination

2.4. Experimental design and conduct

2.6 Carbon fixation - CO2 assimilation, carbohydrate, protein, carbon (C), and nitrogen (N) content

2.7 Biomass

2.8 Statistical analysis

3. Results

3.1. Principal component analysis

3.1.1. Photochemistry

3.1.2 Carbon fixation

3.2.3 Biomass

3.2. Linear models

3.2.1. Photochemistry

3.2.1. Carbon fixation

3.3.3. Biomass

4. Discussion

4.1 Photochemistry

4.2 Carbon fixation

4.3 Biomass

5. Conclusions

Declarations

Acknowledgements

References

Status:

Version 1

2.6 Carbon fixation - CO₂ assimilation, carbohydrate, protein, carbon (C), and nitrogen (N) content