Roses in the City Environment: A Heavy Metals Case Study

Abstract

Kutno is a picturesque city in central Poland, known for extensive rose breeding worldwide. Soil samples and rose petals were collected from 13 locations in the city and characterized by diverse environments. This allowed determining the response of plants to changing cultivation conditions. Rose petals have found a wide range of applications. They are used in the food, pharmaceutical and cosmetic industries. The aim of the research was to assess the contents of Cu, Zn, Cd, Ni, Pb and Cr in soils and their accumulation in rose petals. Samples were subjected to the microwave mineralization process using a mixture of concentrated HCl and HNO₃. The metal contents in the soil and roses were determined by HR-CS-AAS and ICP-OES, respectively. Roses are usually cultivated in soils with a limited mobile fraction of heavy metals. In these unfavorable conditions, flower petals can absorb heavy metals substantially. Petals of roses cultivated for cosmetic, pharmaceutical or food purposes should be tested for heavy metal content. This study indicates that toxic metals are blocked at the root zone, and their transport to the above-ground parts is severely hampered. Nevertheless, metals related to the photo-synthesis process (Zn, Cu) are more intensively taken up by roses, while the uptake of toxic metals is partially inhibited.

1. Introduction

Kutno is an ancient city located in the central part of Poland. It is world known for extensive rose breeding. The planting area covers approximately 7.800 square meters, with numerous sites situated either in parks or road lanes, which are close to major traffic routes [1,2]. Kutno is an important communication hub of either national or international importance. It is surrounded by typical agricultural areas. The city is situated on a ground moraine altered by terminal moraine, river and stream valleys. This landscape is dominated by a flat or slightly undulating Earth form. Additionally, the area of Kutno is affected by the Ochnia River proglacial valley. The city extends 101–107 m above the sea level, with a slope from the northwest to the southeast. The maximum slope is about 6%. However, the majority of the city is fairly flat, with slopes not exceeding 4%. The investigated area is located far from the waste disposals or mining areas. In Kutno, according to the soil agronomic classification, light clays predominate, and all investigated soils are of natural origin [3,4,5].

The rose bushes are subjected to careful seasonal maintenance, which includes flower pruning. On the global flower market, roses are commonly regarded as “queens of flowers”. They are perennial flowering plants, with over 20,000 varieties cultivated worldwide [6]. Over the centuries, rose petals have been highly valued for their scent, color, health and distinguished cosmetic properties. They are finding applications in a plethora of life activities. In particular, rose petals have been used in many countries as an ingredient of dishes and drinks [7]. They are the basis for rose jams, syrups and flavored waters and teas. Thanks to their moisturizing, antioxidant and anti-inflammatory properties, rose petals are valued in the cosmetics industry. The rose petal tea is a useful medication for digestive problems [8]. The essential oil is mainly applied for non-edible purposes, such as the production of soaps and detergents and the preparation of insect repellents, cosmetics and perfumes. Roses are grown all over the world due to either their natural beauty or wide range of uses [9]. Moreover, the use of certain rose species for the phytoremediation of heavy metals in soil was also reported [10]. Nevertheless, reliable data on the content of heavy metals in roses are quite scarce indeed. In particular, Ramil et al. [11] determined contents of several heavy metals in rose petals, supplemented with organic and inorganic fertilizers. Unfortunately, they did not defined the rose species. Copper contents ranged from 10 to 204 µg·kg⁻¹, zinc from 1.38 to 1.58 µg·g⁻¹, cadmium from 0 to 2.25 µg·kg⁻¹, nickel from 35 to 193 µg·kg⁻¹, and lead was not detected. Metal levels depended heavily on the fertilizer applied. Dos Santos et al. [12] determined the content of macro- and microelements in rose petals of different colors. Cadmium and chromium were not detected. The concentration of copper ranged from 0.085 to 3.36, zinc from 2.38 to 5.17 and nickel from 0.04 to 0.2 µg·g⁻¹. Additionally, Li Jung et al. [13] analyzed heavy metal contents in several soil and rose samples. All sampling sites were selected away from identified polluting sources. The following metal contents were determined: Cd 0–0.01; Cr 0–8.14; Cu 0.059–8.92; Ni 0–9.94; Pb 0–0.4, Zn 0.094–16.4 µg·g⁻¹. The major outcome of this work is that the uptake of heavy metal from the soil into the roses was significantly influenced by the physicochemical properties of the soil; cultivation conditions, including the use of fertilizers; and the environment around the plants.

The continuous development of industry and technology fosters the use of chemicals in agriculture and contributes to increasing pollution of the natural environment. Especially, heavy metals pose a continuous threat to agricultural and municipal soils worldwide. The latter are also used for food production in garden and allotment areas, which are of particular importance in Poland. A growing number of people who prefer living in a suburban environment instead of densely populated cities prompts small-scale homemade food and flowers production. Kutno is a representative example of a medium-size town with substantial industrial capacity, located in a green, human-friendly area. According to the literature data, the main stream of heavy metals contaminating soil and roadside vegetation follows industrial activity and transport [14,15,16]. Petrol and diesel engines are widely used in the automotive transportation sector worldwide and are reported to be the main sources of atmospheric air pollutants in major cities. Heavy metals like zinc, cadmium and copper are reported to come from brake and tires wear [17]. Zinc oxide and zinc sulfide added as a component compound in the manufacturing of car tires during the vulcanization process contribute to zinc as a heavy metal during tire wear on roads [18].

In limited doses, many heavy metals are essential elements for plants but can be quite dangerous when they approach toxicity levels [19]. In general, metal contamination of urban soils is currently not regulated by the European Environment Agency [20]. The applicable standards regarding soil contamination and assessment of their quality apply only to agricultural areas [21,22,23]. However, it should be remembered that the bioavailability of metals to plants depends on many factors, including on the physicochemical properties of the soil, soil pH and organic matter content [24,25].

It is well documented that heavy metals as present in the soil from urban areas, especially grasslands, come mostly from industry, road traffic and solid-fuel combustion [26,27,28]. The bioavailability of metals to plants depends on many factors, including on the physicochemical properties of the soil, soil pH and organic matter content.

Plants have developed a number of mechanisms for the efficient uptake, transfer and storage of nutrients. Different parts of plants show different levels of tolerance to the accumulation of heavy metals [29]. Metals can be taken up and transferred using specific protein carriers. Their transport is facilitated by water and realized through either apoplastic or symplastic pathways [30]. On the entry to the roots, water penetrates the epidermis and goes inside, through the cortex and endoderm, towards the xylem. In the endoderm, the apoplastic mechanism is blocked by suberin, which hampers this water pathway and activates the symplast avenue. This water movement is mostly facilitated by pressure generated by transpiration through the Cohesion–Tension (C-T) mechanism [31]. Notably, abiotic factors, like heavy metals, can disrupt this flow at a number of points and interfere with the water transport pathways [32,33,34].

The primary goal of this study was to assess contents of Cu, Zn, Cd, Ni, Pb and Cr in soils and their accumulation in rose petals, with the major aim the influence of cultivation conditions. Obviously, the latter may affect the quality of relevant food and cosmetic products. Copper belongs to the group of micronutrients and in soil is strongly bound by organic matter components and clay minerals. In soil, it forms sulfates, sulfides and carbonates, with a very limited soluble fraction available to plants. Copper is a vital component of enzymes and proteins involved in photosynthesis and nitrogen metabolism [35,36]. On the contrary, zinc is a very mobile element in the soil easily absorbed by plants. Moreover, it is an important cofactor of several enzymes involved in plant photosynthesis, ribosome formation and the permeability of cell membranes. Nickel is recently regarded as an essential micronutrient characterized by high migratory properties. It is a cofactor of ureases, which are key enzymes involved in plant nitrogen metabolism [37]. Chromium and lead are toxic metals of limited mobility and phytoaccumulation, which are mostly taken up by plants via passive mechanisms. They inflict disturbances in photosynthesis and affect cell divisions. On the other hand, cadmium is a mobile metal and can readily be transferred to the upper, green parts of plant. In the soil environment, it is prone to complexing by chelating organic species. It hampers photosynthesis, disrupts cell membranes and affects DNA structures [35,38].

2. Materials and Methods

Rose petals and soils samples were collected in June 2023 from thirteen major locations in the city of Kutno (Figure 1 and Figure S1). Soil samples were taken according to the procedure as in PN-ISO 10381-4:2007, from the plant root zone (0–25 cm) [39]. Selected soil and plant sampling points were chosen to be representative for rose cultivation in urban areas subjected to significant anthropopreasure. Additionally, city park areas situated away from communication routes were considered for comparison. In particular, samples were taken from areas with heavy traffic—such as roundabouts (points 4–6), streets with heavy traffic (points 8–10, 12) and streets with medium traffic (points 1, 11, 13)—as well as green areas, such as parks in the city center (point 2) and on the outskirts of the city (point 3) and a square (point 7).

2.1. The Soil Samples Analysis

All soil samples were subsequently dried in a well-ventilated place, sifted through a 2 mm stainless steel sieve and finally stored in plastic bags. The soil pH of soil was measured by the potentiometric method in 1 mol/dm³ potassium chloride solution (Merck, Darmstadt, Germany) [40]. Organic matter content in soil was determined by the gravimetric method [41,42]. The bioavailable forms of metals in soil were determined in 1 mol L⁻¹ hydrochloric acid (Merck, Darmstadt, Germany) extracts [43]. The total metal content in soil was measured in samples mineralized using the Anton Paar Multiwave 3000 closed system instrument (Graz, Austria). The mixture of concentrated HNO₃ (6 mL) (Merck, Darmstadt, Germany) and HCl (2 mL) (Merck, Darmstadt, Germany) was applied (0.5000 g of soil). Metal concentrations were measured by the HR-CS-AAS technique. The reliability of the analytical procedures was checked using the certified reference material Light Sandy Soil 7001 (Analytica Co. Ltd., Prague, Czech Republic) (Table S1).

2.2. The Roses Petals Samples Analysis

2.2.1. Determination of Heavy Metals in Roses Petals

The rose petals were left to dry in a well-ventilated room for two weeks to a constant weight, grounded and homogenized. The dried plants (0.5 g sample) were subjected to microwave mineralization in concentrated HNO₃ (6 mL) and HCl (1 mL) acid solutions using the Anton Paar Multiwave 3000 closed system instrument. Metal contents were determined by the ICP-OES technique. Respective metal nitrates (Me(NO₃)₂, Merck, Darmstadt, Germany) were used for calibration curve determinations. The reliability of the analytical procedures was checked using the certified reference material INCT-MPH-2, containing a mixture of selected Polish herbs (Institute of Nuclear Chemistry and Technology, Warsaw, Poland) (Table S2) [44].

2.2.2. Determination of Chlorophyll Content in Roses Petals

The index of chlorophyll was measured in roses petals using the Konica Minolta SPAD-502 Plus, Tokyo, Japan.

2.3. Digital Maps Preparation

All maps were computed with the Esri ArcGIS Pro 3.2.2. software (Esri Polska sp. z o.o., Warsaw, Poland). The basemaps used are as implemented in the software. Additional auxiliary maps have been downloaded from the website https://mapy.geoportal.gov.pl/imap/Imgp_2.html (accessed on 24 April 2025).

2.4. Statistical Analysis

All the analytical measurements were performed in five replications. Single-factor analysis of variance (ANOVA) was performed. The arithmetic mean values are shown in tables ± standard deviation. All parameters were determined in parallel for five independent samples. Bartlett’s and Hartley’s tests were applied to check the equality of variance (STATISTICA 10 PL package). Normality of the data sets was evaluated using the Shapiro–Wilk test.

3. Results

The locations of soils and rose petals sampling in the city of Kutno are presented in Figure 1. All investigated soils were mineral, with pH ranging from neutral and slightly alkaline (

Table 1. Analysis of soil samples taken from selected locations (Figure 1) in Kutno.

Location Number	pH Average Value	Organic Matter [%]
1	7.59	3.51
2	7.06	4.22
3	7.48	4.03
4	7.64	3.18
5	7.39	3.96
6	7.48	4.11
7	7.62	4.87
8	7.61	3.42
9	7.37	4.57
10	7.55	3.77
11	7.55	4.20
12	7.06	4.48
13	6.82	3.13

). The bioavailable and total metals contents are shown on maps, as summarized in Figure 2.

The highest metals concentrations were observed at points 6 and 8. The lowest percentage of bioavailable metal forms in the soil as related to its total content was observed for chromium (7–10%), cadmium and nickel (11–15%). On the other hand, the highest values were determined for copper (61–66%) and zinc (52–67%). Only moderate mobility was observed for lead (38%).

Table 2. Heavy metal contents in rose petals grown in Kutno city area. The number of samples n = 5; probability level p = 0.05.

Location Number	Variety	Metal Content of Rose Petals μg·g−1
		Cu	Zn	Cd	Ni	Pb	Cr
1	Gebrüder Grim	5.24 ± 0.37	27.0 ± 1.5	<0.0020	0.68 ± 0.03	0.26 ± 0.01	0.11 ± 0.002
2	Artemis	3.93 ± 0.18	18.2 ± 0.9	0.0281 ± 0.0006	0.78 ± 0.05	0.78 ± 0.05	0.33 ± 0.04
	Apache	4.08 ± 0.15	15.1 ± 0.6	0.0123 ± 0.0003	0.39 ± 0.04	0.21 ± 0.03	0.068 ± 0.004
	Charmant	5.94 ± 0.15	13.5 ± 0.3	0.0025 ± 0.0001	0.43 ± 0.05	0.36 ± 0.05	0.14 ± 0.02
	Cherry Girl	4.88 ± 0.11	19.4 ± 0.4	<0.0020	0.12 ± 0.02	0.35 ± 0.03	0.054 ± 0.002
	Gebrüder Grim	6.28 ± 0.29	22.4 ± 0.5	<0.0020	0.52 ± 0.03	0.30 ± 0.01	0.017 ± 0.003
	Bad Birnbach	5.97 ± 0.16	13.3 ± 0.7	<0.0020	0.39 ± 0.05	0.11 ± 0.03	0.059 ± 0.005
	Orient Express	3.21 ± 0.21	17.2 ± 0.4	0.0023 ± 0.0001	0.56 ± 0.04	0.31 ± 0.03	0.21 ± 0.02
	Rosa rugosa “Hansa”	4.76 ± 0.12	20.1 ± 0.5	0.0050 ± 0.0001	0.31 ± 0.03	<0.0023	0.022 ± 0.002
	Diamant	4.49 ± 0.20	11.7 ± 0.2	0.0024 ± 0.0001	0.21 ± 0.01	<0.0023	0.038 ± 0.002
	Lady Kutno	8.07 ± 0.46	31.7 ± 1.1	<0.0020	1.21 ± 0.02	0.39 ± 0.02	0.025 ± 0.003
3	Nina	6.84 ± 0.30	22.5 ± 0.6	0.012 ± 0.0002	0.43 ± 0.03	0.36 ± 0.02	0.12 ± 0.01
	Queen Elizabeth	2.30 ± 0.10	13.8 ± 0.3	<0.0020	0.056 ± 0.001	0.35 ± 0.02	0.011 ± 0.001
4	Apache	4.91 ± 0.20	12.4 ± 0.3	0.0049 ± 0.0001	0.80 ± 0.04	0.017 ± 0.001	0.14 ± 0.01
	Bad Birnbach	6.02 ± 0.17	15.4 ± 0.8	0.0025 ± 0.0001	0.35 ± 0.04	0.15 ± 0.02	0.12 ± 0.02
5	Artemis	3.47 ± 0.12	13.8 ± 0.2	0.0071 ± 0.001	0.23 ± 0.01	1.03 ± 0.02	0.094 ± 0.002
6	Marathon	7.02 ± 0.43	20.2 ± 0.4	0.0050 ± 0.0001	1.04 ± 0.05	0.91 ± 0.05	0.23 ± 0.01
7	Nina	3.35 ± 0.13	15.9 ± 0.3	<0.0020	0.37 ± 0.02	0.017 ± 0.001	0.098 ± 0.005
	Queen Elizabeth	3.99 ± 0.08	14.6 ± 0.2	0.0025 ± 0.0001	0.042 ± 0.001	0.24 ± 0.01	0.023 ± 0.001
8	Cherry Girl	5.89 ± 0.19	14.2 ± 0.3	0.0073 ± 0.0001	0.41 ± 0.03	0.39 ± 0.02	0.24 ± 0.02
	Diamant	6.09 ± 0.31	16.8 ± 0.4	0.0049 ± 0.0001	0.28 ± 0.01	0.54 ± 0.03	0.37 ± 0.01
	Rosa rugosa “Hansa”	6.53 ± 0.37	17.2 ± 0.4	0.0025 ± 0.0001	0.15 ± 0.01	0.11 ± 0.008	0.020 ± 0.001
	Orient Express	8.06 ± 0.61	19.4 ± 0.5	0.0024 ± 0.0001	0.37 ± 0.02	0.23 ± 0.01	0.17± 0.01
9	Marathon	3.94 ± 0.11	16.7 ± 0.3	0.0025 ± 0.0001	0.43 ± 0.03	0.39 ± 0.02	0.32 ± 0.02
	Charmant	6.13 ± 0.18	14.9 ± 0.3	<0.0020	0.25 ± 0.01	0.17 ± 0.007	0.097 ± 0.006
10	Gebrüder Grim	8.28 ± 0.24	27.0 ± 0.5	0.0049 ± 0.0001	0.35 ± 0.02	0.56 ± 0.03	0.084 ± 0.007
	Bad Birnbach	3.37 ± 0.35	13.9 ± 0.8	0.0025 ± 0.0001	0.55 ± 0.06	0.12 ± 0.03	0.10 ± 0.02
	Lady Kutno	8.79 ± 0.45	28.0 ± 1.7	0.0023 ± 0.0001	1.21 ± 0.03	0.038 ± 0.002	0.10 ± 0.03
11	Bad Birnbach	6.10 ± 0.36	14.7 ± 0.7	0.0025 ± 0.0001	0.41 ± 0.03	0.099 ± 0.01	0.084 ± 0.010
12	Gebrüder Grim	6.04 ± 0.15	15.5 ± 0.3	0.0025 ± 0.0001	0.23 ± 0.01	0.60 ± 0.04	0.056 ± 0.006
13	Lady Kutno	3.75 ± 0.32	18.8 ± 0.4	<0.0020	0.13 ± 0.02	<0.0023	<0.0030

shows the metal contents in rose petals samples according to the location.

Three species of roses, namely, Gebrüder Grim, Bad Birnbach and Lady Kutno, grew in different places in the city of Kutno. They were located both close to traffic and in parks. In order to show the possible influence of the place of growth, the metal content in the petals of these species was compared. The metals uptake by rose petals was assessed by one-way ANOVA at the 0.95 probability level (

Table 3. One-way ANOVA for copper, zinc, nickel, lead and chromium contents in petals of three rose species across location (For Bad Birnbach, location 2, 4, 10, 11; F_cryt = 3.2389. For Gebrüder Grim, location 1, 2, 10, 12; Fcryt = 3.2389. For Lady Kutno, location 2, 10, 13; F_cryt = 3.8853).

	Cu	Zn	Ni	Pb	Cr
Bad Birnbach	F = 111.3649 p = 6.22 × 10−11	F = 4.8588 p = 1.37 × 10−2	F = 12.6996 p = 1.68 × 10−4	F = 2.5637 p = 9.11 × 10−2	F = 12.3475 p = 1.96 × 10−4
Gebrüder Grim	F = 105.7409 p = 9.23 × 10−11	F = 284.2421 p = 4.38 × 10−14	F = 73.3449 p = 1.44 × 10−9	F = 78.0890 p = 9.05 × 10−10	F = 89.6899 p = 3.20 × 10−10
Lady Kutno	F = 210.7356 p = 4.50 × 10−10	F = 130.8882 p = 7.09 × 10−9	F = 3124.50 p = 4.96 × 10−17	F = 2685.15 p = 1.23 × 10−16	F = 51.0783 p = 1.35 × 10−6

). The null hypothesis supported by these calculations was whether the location of a given rose species affects the migration of metals from the soil to the petals. These calculations showed that the location of growth can contribute to the uptake of metals by roses.

In addition, one-way Anova analysis was used to estimate the uptake of metals by rose petals of different species (

Table 4. One-way ANOVA for copper, zinc, nickel, lead and chromium contents across rose petals of Gebrüder Grim, Artemis, Apache, Charmant, Cherry Girl, Gebrüder Grim, Bad Birnbach, Orient Express, Rosa rugosa “Hansa”, Diamant, Lady Kutno in location 2; F_cryt = 2.1240.

Cu	Zn	Ni	Pb	Cr
F = 186.0752 p = 9.38 × 10−30	F = 285.5443 p = 2.16 × 10−33	F = 263.7759 p = 1.03 × 10−32	F = 183.1288 p = 1.28 × 10−29	F = 143.6139 p = 1.42 × 10−27

). The null hypothesis was whether there are differences in the uptake of heavy metals by rose petals of different species growing in one location.

The highest concentrations of lead and chromium were observed in the Artemis (locations 2 and 5) and Marathon (locations 6 and 9) varieties. The Lady Kutno variety is characterized by the highest content of Cu, Zn and Ni (locations 2 and 10). It is worth noting that site 2 is located in the park. Higher metal contents in rose petals are not related to high content of these elements in the soil. However, the park is located on a significant slope of the terrain, which may result in the above differences.

The Queen Elizabeth variety was characterized by the lowest content of the tested metals (locations 3 and 5). Figure 3, Figure 4 and Figure 5 present the metal contents in individual rose species depending on the place of their collection. For the Gebrüder Grim variety (Figure 3), relatively constant copper contents (6.04–8.23 μg·g⁻¹) in petals, regardless the place of growth, were observed. Similarly, no clear relationship was determined for zinc and nickel contents. The highest lead concentrations were observed at locations 10 and 12, which are located in the vicinity of two major traffic routes. The Bad Birnbach variety (Figure 4) did not show significant relationships between the content of copper and zinc and the place of plant growth. The highest nickel content was found in rose petals collected from location 10. The lead and chromium contents were quite similar in all locations. The highest concentrations were found in samples collected from locations 4 and 10, i.e., places in the city center. The cadmium content in all samples of this variety is at the limit of analytical quantification and ranges from 0 to 0.0025 μg·g⁻¹. Figure 5 shows metal concentrations in the Lady Kutno variety. The contents of copper, zinc, nickel and lead changed depending on the particular location. The highest metal content was found in sample 2 and the lowest in sample 13. The cadmium content, as in the previous samples, was below the limit of quantification (0.0063 μg·mL⁻¹).

In this work, we applied the generally accepted bioaccumulation factor (BAF) to rose petals instead of leaves and named it BAFp. We calculated BAFp, a factor that we defined as the ratio of the metal content in rose petals to its content in the soil. Series of those coefficients stated in an ordered way (

Table 5. Bioaccumulation factor (p) for rose petals in different locations.

Location Number	Rose Variety	BAF(p) Factors
1	Gebrüder Grim	Cu > Zn > Ni > Cr > Pb > Cd
2	Artemis	Cu > Zn > Ni > Cd > Cr > Pb
	Apache	Cu > Zn > Ni > Cd > Cr > Pb
	Charmant	Cu > Zn > Ni > Cr > Pb > Cd
	Cherry Girl	Cu > Zn > Ni > Cr > Pb > Cd
	Gebrüder Grim	Cu > Zn > Ni > Pb > Cr > Cd
	Bad Birnbach	Cu > Zn > Ni > Cr > Pb > Cd
	Orient Express	Cu > Zn > Ni > Cr > Pb > Cd
	Rosa rugosa “Hansa”	Cu > Zn > Ni > Cd > Cr > Pb
	Diamant	Cu > Zn > Ni > Cr > Cd > Pb
	Lady Kutno	Cu > Zn > Ni > Pb > Cr > Cd
3	Nina	Cu > Zn > Ni > Pb > Cr > Cd
	Queen Elizabeth	Zn > Cu > Pb >Ni > Cr > Cd
4	Apache	Cu > Zn > Ni > Cr > Cd > Pb
	Bad Birnbach	Cu > Zn > Ni > Cr > Cd > Pb
5	Artemis	Cu > Zn > Ni > Pb > Cr > Cd
6	Marathon	Ni > Cu > Zn > Cr > Pb > Cd
7	Nina	Zn > Cu > Ni > Cr > Pb > Cd
	Queen Elizabeth	Zn > Cu > Ni > Cr > Pb > Cd
8	Cherry Girl	Cu > Zn > Ni > Cr > Cd > Pb
	Diamant	Cu > Cr > Zn > Ni > Pb > Cd
	Rosa rugosa “Hansa”	Cu > Zn > Ni > Cr > Pb = Cd
	Orient Express	Cu > Zn > Ni > Cr > Pb > Cd
9	Marathon	Cu > Ni > Zn > Cr > Pb > Cd
	Charmant	Cu > Zn > Ni > Cr > Pb > Cd
10	Gebrüder Grim	Cu > Zn > Ni > Cr > Pb > Cd
	Bad Birnbach	Cu > Zn > Ni > Cr > Cd > Pb
	Lady Kutno	Cu > Zn > Ni > Cr > Cd > Pb
11	Bad Birnbach	Cu > Zn > Ni > Cr > Cd > Pb
12	Gebrüder Grim	Cu > Zn > Ni > Pb > Cr > Cd
13	Lady Kutno	Cu > Zn > Ni > Cr > Cd = Pb

and

Table 6. Bioaccumulation factors BAF(p) calculated for Gebrüder Grim, Bad Birnbach and Lady Kutno rose petals. Elements are shown in decreasing order of particular factor. Each value is the average of the data from five replicates.

Location Number	Bioaccumulation Factor (p)
Gebrüder Grim
1	Cu > Zn > Ni > Cr > Pb > Cd
2	Cu > Zn > Ni > Pb > Cr > Cd
10	Cu > Zn > Ni > Cr > Pb > Cd
12	Cu > Zn > Ni > Pb > Cr > Cd
Bad Birnbach
2	Cu > Zn > Ni > Cr > Pb > Cd
4	Cu > Zn > Ni > Cr > Pb > Cd
10	Cu > Zn > Ni > Cr > Cd > Pb
11	Cu > Zn > Ni > Cr > Cd > Pb
Lady Kutno
2	Cu > Zn > Ni > Pb > Cr > Cd
10	Cu > Zn > Ni > Cr > Cd > Pb
11	Cu > Zn > Ni > Cr > Cd > Pb

) provide useful information on metals migrations and associated interactions, which may affect plant tissues. In all analyzed rose varieties, BAFp coefficients calculated for Cu, Zn and Ni occupy the same position in the series, regardless of the place of plant growth. Minor changes were observed for Cr, Pb and Cd.

4. Discussion

Soil degradation prompted by growing urbanization is becoming an important environmental issue. The resulting waste accumulation and contamination with chemical and radioactive substances significantly deteriorates soil conditions [45]. In particular, substantial amounts of pollutants enter urban soils as a result of waste accumulation, transport (wear and tear of parts, emissions from fuel combustion) and industrial facilities (technological chains of production) [46]. Concrete and asphalt pavements, typical for urban areas, limit the penetration of water and air into the soil and make an additional negative contribution to the degradation of soil resources [47,48].

The total copper content in the analyzed area ranged from 9.78 to 27.3 µg·g⁻¹, while the bioavailable form was 4.50–18.0 µg·g⁻¹. According to the commonly accepted review of Kabata-Pendias [35], the average content in agriculturally used soils is 1–140 µg·g⁻¹. The total zinc content in soil ranged from 43.5 to 156 µg·g⁻¹, and the bioavailable form 23.5–81.3 µg·g⁻¹. Kabata-Pendias [35] shows that the average zinc content in soils is within the limits 30–125 µg·g⁻¹, while the permissible value is 250–300 µg·g⁻¹. In the studied area of the city, the total cadmium content in the soil ranged from 1.90 to 3.10, and the bioavailable forms 0.21–0.47 µg·g⁻¹. These values are within the permissible cadmium content in soil, which is 3–5 µg·g⁻¹. The total nickel content in the analyzed area ranged from 14.2 to 19.9 µg·g⁻¹, while the bioavailable form was 1.50–3.00 µg·g⁻¹. According to Kabata-Pendias [35], the average permissible nickel content in soil is 100 µg·g⁻¹. The total content in the soil determined for lead is 25–58.7 µg·g⁻¹ (bioavailable forms 9.6–33 µg·g⁻¹) and for chromium 13.7–29.3 µg·g⁻¹ (bioavailable forms 0.91–2.91 µg·g⁻¹). These values do not exceed the permissible standards for lead of 100 µg·g⁻¹ and chromium of 150 µg·g⁻¹. Analyzing the above data, we can conclude that the permissible standards were not exceeded in the studied area with respect to the determined metals [49].

Roses are a very important ornamental plant, cultivated as either cut flowers or gardening plants [50,51]. The object of our investigations was the petals of selected rose species. We analyzed the content of metals in well-opened rose flowers. We made every effort to collect petals from plants after pollination.

The copper content in rose petals ranged from 2.30 µg·g⁻¹ (Queen Elizabeth, location 3) to 8.79 µg·g⁻¹ (Lady Kutno, location 10). According to Kabata-Pendias [35], the copper content in garden plants is usually below 4–5 µg·g⁻¹, with the average content in above-ground parts ranging from 5 to 20 µg·g⁻¹. Therefore, those values were not exceeded over all analyzed petals.

Our results showed significant dependance between particular rose species and their availability to zinc uptake and accumulation. This phenomenon was initially described by Khoshgoftarmanesh et al. [52] for rose leaves and was presumably attributed to the dilution effect resulting from the increase in shoot dry matter weight. Notable, the zinc content in rose petals from location 2 ranged from 11.7 µg·g⁻¹ (Diamant) to 31.7 µg·g⁻¹ (Lady Kutno). However, in location 8, a similar pattern was not observed. This may indicate the vital influence of soil parameters on the uptake of this metal.

Cadmium concentrations in rose petals were very close to the detection limit, ranging in value from 0 to 0.0281 µg·g⁻¹, and therefore, they are not shown in Figure 3 and Figure 4.

The nickel content in rose petals ranged from 0.0415 µg·g⁻¹ (Queen Elizabeth, location 7) to 1.21 µg·g⁻¹ (Lady Kutno, locations 2 and 10) and the lead content from 0 (Diamant, location 2, and Lady Kutno, location 13) to 1.03 µg·g⁻¹ (Artemis, location 5). Nickel contents in plants range from 0.15 to 8.2 µg·g⁻¹. The toxic concentration depends on the sensitivity or resistance of the plants and ranges from 10 to 100 µg·g⁻¹. The uptake of lead by plants is a passive process and proportional to the presence of available lead in the soil. The amount of lead in plants ranges from 0.4 to 3.6 µg·g⁻¹. The critical value is above 30 ppm. The chromium content in food plants ranges from 0.02 to 1.0 µg·g⁻¹. It is generally assumed that for very sensitive plants, chromium is harmful at a concentration of 2 µg·g⁻¹, and for medium sensitive plants, above 20 µg·g⁻¹. None of the analyzed rose petals exceeded the limit values for the determined elements. The Lady Kutno rose species was the most sensitive to changing growing conditions. Chromium levels in rose petals adopted values ranging from 0.0025 µg·g⁻¹ (Lady Kutno, location 13) to 0.3725 µg·g⁻¹ (Diamant, location 8). An increase in lead content (location 8), along with an enhanced level of bioavailable forms of this element in the soil (30.7 µg·g⁻¹), was observed for the Diamant rose species. However, a similar situation was not detected at location 2, where other elements present in the soil environment influence the uptake of lead by roses.

The investigated plant material was characterized by a bioaccumulation factor (Table S3). The BAF value was higher than the one for copper, as determined in Lady Kutno rose petals at location 2 only (BAFp = 1.26). High values of this parameter indicate a well-developed system of transporting copper to above-ground parts. It is surprising that the place of growth of Lady Kutno (location 2) is not characterized by the highest copper content in the soil (6.40 µg·g⁻¹) in comparison to other locations. The accumulation of heavy metals in the plant increases along with the concentration of the assimilable form of the metal in the soil. However, the bioavailability of metals depends on the physicochemical properties of the soil and the presence of microorganisms that are inhabitants of the rhizosphere. Copper plays important roles in photosynthetic and respiratory electron transport chains, cell wall metabolism, oxidative stress protection and biogenesis of the molybdenum cofactor [53]. Therefore, plants developed efficient ways for extracting copper from soils with limited copper concentrations, which is reflected by the high BAFs of that metal. Our results clearly indicate that the presence of other elements in the soil is also extremely important for the way metals are uptaken and transported by plants.

The phenomenon of flower opening consists of both petal cell division and cell expansion, and they greatly affect petal growth and development. Many research studies indicate that petal growth associated with flower opening is mainly attributable to cell expansion, and the accumulation of osmosis is required [54,55,56]. Soluble carbohydrates, which act as osmotica and substrates for both respiration and cell wall synthesis for cell expansion, accumulate in the petal cells of many flowers, including roses [57]. The sugar accumulation in petal cells is pivotal for reducing petal water potential promotion of water influx, which is vital for cell enlargement and flower opening [51,58,59]. Flowers develop from florally determined meristems, which in turn proliferate to form the floral organs, including sepals, petals, stamens and carpels. During those morphological changes, each part of a floral organ shows a distinct pattern of color change that is specific to each plant species [60]. Metals penetrate rose petals during their formation and growth phase, along with the transport of water. After pollination, the flowers receive a signal to stop turgor, and the process of flower death begins. In this research, we collected rose flowers during the peak blooming phase but before the withering phase. All roses were grown in soils with a neutral or slightly alkaline reaction, which prompted a low content of bioavailable forms of metals in the soil. These circumstances reduced the impact of metals on the plant development.

The root system of roses is well developed, which increases their resistance to short periods of drought. However, during intensive growth, especially when the plants are preparing to flower and developing buds, their water requirements increase significantly. Water is essential for the transport of nutrients and plays a key role in the photosynthesis process and maintaining turgor, or the right cell tension. Hydration plays a fundamental role in the health and flowering of roses, affecting all aspects of their physiology. Flowering is one of the most water-intensive stages in the life cycle of a rose. Each flower bud requires a sufficient amount of water to develop and open properly. Water shortages during this crucial period can lead to weakened buds, their drying out and even premature drop. As a result, the plants can produce fewer and significantly reduced-quality flowers.

Chlorophyll plays a significant role in the photosynthesis process and is necessary for collecting light and transmitting energy. However, the petals of many flowering plants contain chlorophyll at the early stages of development only. In the mature petals, the chlorophyll content is very limited indeed. On the contrary, other pigments like anthocyanins, carotenoids and betalains are being accumulated [61,62]. The loss of chlorophyll during petal development is an important feature of flowering plants. It allows flowers to be visually distinguished from the surrounding leaves and attracts pollinators [60]. Chlorophyll is closely associated with the chlorophyll-binding proteins of photosystem I (PSI) and II (PSII) complexes [63,64] and accumulates in tissues where PSI and PSII are produced. It is well known that the flowers of most plant species consist of non-photosynthetic tissues or those with residual photosynthetic activity [65,66]. However, the mechanism behind that phenomenon has not been thoroughly investigated as yet. In our future work, we would like to explain this phenomenon and describe how it can be facilitated in rose cultivation and development.

5. Conclusions

Our investigations have shown that, despite the marvelous beauty of their petals, rose plants should be treated thoroughly as a complete organism, with special attention paid to their growing conditions and environment. Roses are usually cultivated in soils with a limited mobile fraction of heavy metals. However, even in these unfavorable conditions, flower petals can absorb heavy metals substantially. Therefore, petals of roses cultivated for cosmetic, pharmaceutical or food purposes should be tested for heavy metal content. The analyzed area located within the municipality of Kutno was characterized by diverse heavy metal contents. Especially, the highest heavy metal levels were determined in soil samples collected from points close to heavy traffic areas (6, 8 points). In particular, we have shown a significant relationship between the content of metals in rose petals and their level in soil. Metal ions transport in plants is facilitated by water flow, which in turn is stimulated by photosynthesis. We did not detect chlorophyll content in well-developed rose petals, which indicates that photosynthesis was limited to the early stage of petal formation in roses only. In well-developed petals, water transport is inhibited after pollination [67]. Our studies indicate that toxic metals can be blocked at the root zone, and thus, their transport to the above-ground parts is severely hampered [25,68,69]. Nevertheless, metals related to the photosynthesis process (Zn, Cu) are more likely to be taken up by roses, while the uptake of toxic metals is partially inhibited.