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Zinc oxide and silver effects on the growth, pigment content and genetic stability of chrysanthemums propagated by the node culture method

Alicja Tymoszuk
Alicja Tymoszuk
, 
Urszula Szałaj
Urszula Szałaj
, 
Jacek Wojnarowicz
Jacek Wojnarowicz
, 
Jolanta Kowalska
Jolanta Kowalska
, 
Małgorzata Antkowiak
Małgorzata Antkowiak
 and 
Dariusz Kulus
Dariusz Kulus
   | Apr 28, 2024
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Article Category: ORIGINAL ARTICLE
Published Online: Apr 28, 2024
Page range: -
Received: Oct 31, 2023
Accepted: Jan 16, 2024
DOI: https://doi.org/10.2478/fhort-2024-0003
Keywords
© 2024 Alicja Tymoszuk et al., published by Sciendo
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.

Figure 1.

Sample pictures of Chrysanthemum × morifolium ‘UBG’ (A) and ‘UPG’ (B) shoot and root systems (C, D) developed from node explants cultured in vitro for 10 weeks on the modified MS medium, depending on the ZnO SMPs/ZnO NPs/ZnO + Ag NPs treatment; bar = 1 cm. MS, Murashige and Skoog; NPs, nanoparticles; SMPs, submicron particles; UBG, ‘UTP Burgundy Gold’; UPG, ‘UTP Pinky Gold’.
Sample pictures of Chrysanthemum × morifolium ‘UBG’ (A) and ‘UPG’ (B) shoot and root systems (C, D) developed from node explants cultured in vitro for 10 weeks on the modified MS medium, depending on the ZnO SMPs/ZnO NPs/ZnO + Ag NPs treatment; bar = 1 cm. MS, Murashige and Skoog; NPs, nanoparticles; SMPs, submicron particles; UBG, ‘UTP Burgundy Gold’; UPG, ‘UTP Pinky Gold’.

Figure 2.

Leaf architecture parameters of Chrysanthemum × morifolium ‘UBG’ plantlets developed from node explants cultured in vitro on the modified MS medium, depending on the ZnO SMPs/ZnO NPs/ZnO + Ag NPs treatment. Means ± SD on graphs for each parameter analysed followed by the same letter do not differ significantly at p ≤ 0.05 (Fisher’s test). MS, Murashige and Skoog; NPs, nanoparticles; SD, standard deviation; SMPs, submicron particles; UBG, ‘UTP Burgundy Gold’.
Leaf architecture parameters of Chrysanthemum × morifolium ‘UBG’ plantlets developed from node explants cultured in vitro on the modified MS medium, depending on the ZnO SMPs/ZnO NPs/ZnO + Ag NPs treatment. Means ± SD on graphs for each parameter analysed followed by the same letter do not differ significantly at p ≤ 0.05 (Fisher’s test). MS, Murashige and Skoog; NPs, nanoparticles; SD, standard deviation; SMPs, submicron particles; UBG, ‘UTP Burgundy Gold’.

Figure 3.

Leaf architecture parameters of Chrysanthemum × morifolium ‘UPG’ plantlets developed from node explants cultured in vitro on the modified MS medium, depending on the ZnO SMPs/ZnO NPs/ZnO + Ag NPs treatment. Means ± SD on graphs for each parameter analysed followed by the same letter do not differ significantly at p ≤ 0.05 (Fisher’s test). MS, Murashige and Skoog; NPs, nanoparticles; SD, standard deviation; SMPs, submicron particles; UPG, ‘UTP Pinky Gold’.
Leaf architecture parameters of Chrysanthemum × morifolium ‘UPG’ plantlets developed from node explants cultured in vitro on the modified MS medium, depending on the ZnO SMPs/ZnO NPs/ZnO + Ag NPs treatment. Means ± SD on graphs for each parameter analysed followed by the same letter do not differ significantly at p ≤ 0.05 (Fisher’s test). MS, Murashige and Skoog; NPs, nanoparticles; SD, standard deviation; SMPs, submicron particles; UPG, ‘UTP Pinky Gold’.

Figure 4.

Root system architecture of Chrysanthemum × morifolium ‘UBG’ plantlets developed from node explants cultured in vitro on the modified MS medium, depending on the ZnO SMPs/ZnO NPs/ZnO + Ag NPs treatment. Means ± SD on graphs for each parameter analysed followed by the same letter do not differ significantly at p ≤ 0.05 (Fisher’s test). MS, Murashige and Skoog; NPs, nanoparticles; SD, standard deviation; SMPs, submicron particles; UBG, ‘UTP Burgundy Gold’.
Root system architecture of Chrysanthemum × morifolium ‘UBG’ plantlets developed from node explants cultured in vitro on the modified MS medium, depending on the ZnO SMPs/ZnO NPs/ZnO + Ag NPs treatment. Means ± SD on graphs for each parameter analysed followed by the same letter do not differ significantly at p ≤ 0.05 (Fisher’s test). MS, Murashige and Skoog; NPs, nanoparticles; SD, standard deviation; SMPs, submicron particles; UBG, ‘UTP Burgundy Gold’.

Figure 5.

Root system architecture of Chrysanthemum × morifolium ‘UPG’ plantlets developed from node explants cultured in vitro on the modified MS medium, depending on the ZnO SMPs/ZnO NPs/ZnO + Ag NPs treatment. Means ± SD on graphs for each parameter analysed followed by the same letter do not differ significantly at p ≤ 0.05 (Fisher’s test). MS, Murashige and Skoog; NPs, nanoparticles; SD, standard deviation; SMPs, submicron particles; UPG, ‘UTP Pinky Gold’.
Root system architecture of Chrysanthemum × morifolium ‘UPG’ plantlets developed from node explants cultured in vitro on the modified MS medium, depending on the ZnO SMPs/ZnO NPs/ZnO + Ag NPs treatment. Means ± SD on graphs for each parameter analysed followed by the same letter do not differ significantly at p ≤ 0.05 (Fisher’s test). MS, Murashige and Skoog; NPs, nanoparticles; SD, standard deviation; SMPs, submicron particles; UPG, ‘UTP Pinky Gold’.

Figure 6.

Example of RAPD (A) and SCoT (B) band profiles of the control and 400 mg · L−1 ZnO SMPs/ZnO NPs/ZnO + Ag NPs-treated plantlets of Chrysanthemum × morifolium ‘UBG’ and ‘UPG’ received as a result of electrophoresis of the DNA amplification products obtained with the R2 (RAPD) and S4 (SCoT) primers. Outermost lanes (wm) are DNA bp weight markers. NPs, nanoparticles; RAPD, randomly amplified polymorphic DNA; SCoT, start codon targeted polymorphism; SMPs, submicron particles; UBG, ‘UTP Burgundy Gold’; UPG, ‘UTP Pinky Gold’.
Example of RAPD (A) and SCoT (B) band profiles of the control and 400 mg · L−1 ZnO SMPs/ZnO NPs/ZnO + Ag NPs-treated plantlets of Chrysanthemum × morifolium ‘UBG’ and ‘UPG’ received as a result of electrophoresis of the DNA amplification products obtained with the R2 (RAPD) and S4 (SCoT) primers. Outermost lanes (wm) are DNA bp weight markers. NPs, nanoparticles; RAPD, randomly amplified polymorphic DNA; SCoT, start codon targeted polymorphism; SMPs, submicron particles; UBG, ‘UTP Burgundy Gold’; UPG, ‘UTP Pinky Gold’.

Supplementary Figure S1.

X-ray diffraction patterns of samples.
X-ray diffraction patterns of samples.

Supplementary Figure S2.

SEM images of samples: (A, B) ZnO SMPs; (C, D) ZnO NPs (1.5% H2O); (E, F) ZnO NPs (6% H2O); (G, H) ZnO + 0.1% Ag NPs (1.5% H2O); (I, J) ZnO + 0.1% Ag NPs (6% H2O); (K, L) ZnO + 1% Ag NPs (1.5% H2O); (M, N) ZnO + 1% Ag NPs (6% H2O) images taken with the immersion lens detector. NPs, nanoparticles; SMPs, submicron particles.
SEM images of samples: (A, B) ZnO SMPs; (C, D) ZnO NPs (1.5% H2O); (E, F) ZnO NPs (6% H2O); (G, H) ZnO + 0.1% Ag NPs (1.5% H2O); (I, J) ZnO + 0.1% Ag NPs (6% H2O); (K, L) ZnO + 1% Ag NPs (1.5% H2O); (M, N) ZnO + 1% Ag NPs (6% H2O) images taken with the immersion lens detector. NPs, nanoparticles; SMPs, submicron particles.

Supplementary Figure S3.

Chrysanthemum × morifolium ‘UBG’ and ‘UPG’ shoot and root systems developed from node explants cultured in vitro for 10 weeks on the modified MS medium, depending on the ZnO SMPs/ZnO NPs/ZnO + Ag NPs treatment; bar = 1 cm. MS, Murashige and Skoog; NPs, nanoparticles; SMPs, submicron particles; UBG, ‘UTP Burgundy Gold’; UPG, ‘UTP Pinky Gold’.
Chrysanthemum × morifolium ‘UBG’ and ‘UPG’ shoot and root systems developed from node explants cultured in vitro for 10 weeks on the modified MS medium, depending on the ZnO SMPs/ZnO NPs/ZnO + Ag NPs treatment; bar = 1 cm. MS, Murashige and Skoog; NPs, nanoparticles; SMPs, submicron particles; UBG, ‘UTP Burgundy Gold’; UPG, ‘UTP Pinky Gold’.

Supplementary Figure S4.

RAPD and SCoT band profiles of the control and 400 mg · L−1 ZnO SMPs/ZnO NPs/ ZnO + Ag NPs-treated plantlets of Chrysanthemum × morifolium ‘UBG’ and ‘UPG’. Outermost lanes (wm) are DNA bp weight markers. NPs, nanoparticles; RAPD, randomly amplified polymorphic DNA; SCoT, start codon targeted polymorphism; SMPs, submicron particles; UBG, ‘UTP Burgundy Gold’; UPG, ‘UTP Pinky Gold’.
RAPD and SCoT band profiles of the control and 400 mg · L−1 ZnO SMPs/ZnO NPs/ ZnO + Ag NPs-treated plantlets of Chrysanthemum × morifolium ‘UBG’ and ‘UPG’. Outermost lanes (wm) are DNA bp weight markers. NPs, nanoparticles; RAPD, randomly amplified polymorphic DNA; SCoT, start codon targeted polymorphism; SMPs, submicron particles; UBG, ‘UTP Burgundy Gold’; UPG, ‘UTP Pinky Gold’.

Molecular products obtained from Chrysanthemum × morifolium ‘UBG’ and ‘UPG’ control and 400 mg · L−1 ZnO SMPs/ZnO NPs/ZnO + Ag NPs-treated plantlets analysed with RAPD (R 1–5) and SCoT (S 1–5) marker systems

Primer code Primer sequence 5’ → 3’ Reference Cultivar No. of bands Band sizes (bp) No. of loci No. of genotypes
Total mono poly spec
RAPD
R1 GGG AAT TCG G Lema-Rumińska et al. (2004) UBG 192 367–1,478 6 6 0 0 1
UPG 192 355–1,500 6 6 0 0 1
R2 GAC CGC TTG T UBG 160 564–1,207 5 5 0 0 1
UPG 320 195–2,418 10 10 0 0 1
R3 GCT GCC TCA GG Shibata et al. (1998) UBG 192 432–2,094 6 6 0 0 1
UPG 192 414–2,020 6 6 0 0 1
R4 TAC CCA GGA GCG Wolf (1996) UBG 160 500–1,807 5 5 0 0 1
UPG 160 500–1,910 5 5 0 0 1
R5 CAA TCG CCG T UBG 160 534–1,449 5 5 0 0 1
UPG 160 579–1,430 5 5 0 0 1
Σ UBG 864 27 27 0 0 1
UPG 1,024 32 32 0 0 1
Mean from a single primer UBG 172.8 5.4 5.4 0 0 -
UPG 204.8 6.4 6.4 0 0 -
SCoT
S1 CAA TGG CTA CCA CCT Collard and Mackill (2009) UBG 352 425–1,762 11 11 0 0 1
UPG 416 374–1,730 13 13 0 0 1
S2 CAA TGG CTA CCA CGT UBG 256 531–1,757 8 8 0 0 1
UPG 256 531–1,758 8 8 0 0 1
S3 ACG ACA TGG CGA CCA ACG UBG 352 509–1,888 11 11 0 0 1
UPG 288 400–1,989 9 9 0 0 1
S4 ACG ACA TGG CGA CCA TCG UBG 416 409–2,036 13 13 0 0 1
UPG 416 409–2,037 13 13 0 0 1
S5 ACC ATG GCT ACC GTC UBG 320 416–2,988 10 10 0 0 1
UPG 256 329–1,824 8 8 0 0 1
Σ UBG 1,696 53 53 0 0 1
UPG 1,632 51 51 0 0 1
Mean from a single primer UBG 339.2 10.6 10.6 0 0 -
UPG 326.4 10.2 10.2 0 0 -

Composition of the precursor solution used for synthesis

Sample name Ethylene glycol volume (mL) Weight of zinc acetate dihydrate (g) Weight of silver acetate anhydrous (g) Final water content of the precursor solution (weight %)
ZnO NPs (1.5% H2O) 0 1.5
ZnO NPs (6% H2O) 6
ZnO + 0.1% Ag NPs (1.5% H2O) 525 35 g 0.0266 1.5
ZnO + 0.1% Ag NPs (6% H2O) 0.0266 6
ZnO + 1% Ag NPs (1.5% H2O) 0.2689 1.5
ZnO + 1% Ag NPs (6% H2O) 0.2689 6

Content and ratios of chlorophylls and carotenoids in Chrysanthemum × morifolium ‘UPG’ plantlets developed from node explants cultured in vitro on the modified MS medium, depending on the ZnO SMPs/ZnO NPs/ZnO + Ag NPs treatment.

Treatment Chlorophyll a content (mg · g−1 FW) Chlorophyll b content (mg · g−1 FW) Chlorophyll a/b ratio Chlorophyll (a ± b) content (mg · g−1 FW) Carotenoid content (mg · g−1 FW) Chlorophyll/carotenoid ratio
Control 1.46 ± 0.06 a 0.51 ± 0.02 a–c 2.86 ± 0.06 a 1.97 ± 0.08 a 0.29 ± 0.01 ab 6.79 ± 0.07 ef
100 mg · L−1 ZnO SMPs 1.03 ± 0.04 fg 0.42 ± 0.03 d–f 2.45 ± 0.11 d–g 1.45 ± 0.07 d–f 0.23 ± 0.01 c–f 6.30 ± 0.26 ik
200 mg · L−1 ZnO SMPs 1.08 ± 0.15 e–g 0.45 ± 0.05 c–f 2.40 ± 0.06 f–h 1.53 ± 0.20 c–f 0.21 ± 0.03 d–g 7.29 ± 0.48 bc
400 mg · L−1 ZnO SMPs 1.03 ± 0.16 fg 0.42 ± 0.08 d–f 2.45 ± 0.08 d–g 1.45 ± 0.24 d–f 0.21 ± 0.04 d–g 6.91 ± 0.12 d–f
100 mg · L−1 ZnO NPs (1.5% H2O) 1.16 ± 0.19 c–f 0.47 ± 0.06 b–e 2.47 ± 0.09 c–f 1.63 ± 0.26 b–d 0.24 ± 0.04 c–e 6.79 ± 0.30 ef
200 mg · L−1 ZnO NPs (1.5% H2O) 0.97 ± 0.29 g 0.40 ± 0.12 ef 2.42 ± 0.02 e–g 1.37 ± 0.42 ef 0.18 ± 0.06 g 7.61 ± 0.36 a
400 mg · L−1 ZnO NPs (1.5% H2O) 1.26 ± 0.03 b–d 0.50 ± 0.03 a–c 2.52 ± 0.11 b–d 1.76 ± 0.07 a–c 0.26 ± 0.01 bc 6.77 ± 0.15 e–g
100 mg · L−1 ZnO NPs (6% H2O) 1.40 ± 0.13 ab 0.53 ± 0.04 ab 2.64 ± 0.07 b 1.93 ± 0.17 a 0.30 ± 0.03 a 6.43 ± 0.29 hi
200 mg · L−1 ZnO NPs (6% H2O) 1.14 ± 0.32 c–g 0.46 ± 0.09 c–e 2.48 ± 0.23 c–e 1.60 ± 0.42 bc 0.25 ± 0.07 c–d 6.40 ± 0.17 hj
400 mg · L−1 ZnO NPs (6% H2O) 1.17 ± 0.20 c–f 0.45 ± 0.07 c–f 2.60 ± 0.08 bc 1.62 ± 0.26 b–d 0.24 ± 0.04 c–e 6.75 ± 0.06 e–g
100 mg · L−1 ZnO + 0.1% Ag NPs (1.5% H2O) 1.19 ± 0.09 c–f 0.48 ± 0.03 a–d 2.48 ± 0.08 c–e 1.67 ± 0.12 b–d 0.24 ± 0.01 c–e 6.96 ± 0.34 de
200 mg · L−1 ZnO + 0.1% Ag NPs (1.5% H2O) 1.09 ± 0.05 d–g 0.48 ± 0.01 a–d 2.27 ± 0.06 i 1.57 ± 0.06 c–f 0.24 ± 0.02 c–e 6.54 ± 0.23 e–h
400 mg · L−1 ZnO + 0.1% Ag NPs (1.5% H2O) 1.16 ± 0.09 c–f 0.49 ± 0.03 a–c 2.37 ± 0.08 g–i 1.65 ± 0.11 b–d 0.22 ± 0.02 d–g 7.50 ± 0.19 ab
100 mg · L−1 ZnO + 0.1% Ag NPs (6% H2O) 1.09 ± 0.18 d–g 0.46 ± 0.08 c–f 2.37 ± 0.06 g–i 1.55 ± 0.26 c–f 0.25 ± 0.04 c–d 6.20 ± 0.08 jk
200 mg · L−1 ZnO + 0.1% Ag NPs (6% H2O) 1.15 ± 0.15 c–f 0.48 ± 0.05 a–d 2.40 ± 0.07 f–h 1.63 ± 0.20 b–d 0.24 ± 0.03 c–e 6.79 ± 0.04 ef
400 mg · L−1 ZnO + 0.1% Ag NPs (6% H2O) 1.30 ± 0.07 a–c 0.54 ± 0.04 a 2.41 ± 0.06 e–g 1.84 ± 0.11 ab 0.26 ± 0.01 bc 7.08 ± 0.24 de
100 mg · L−1 ZnO + 1% Ag NPs (1.5% H2O) 1.02 ± 0.27 fg 0.42 ± 0.12 d–f 2.43 ± 0.08 e–g 1.44 ± 0.39 d–f 0.20 ± 0.05 e–g 7.20 ± 0.32 cd
200 mg · L−1 ZnO + 1% Ag NPs (1.5% H2O) 1.25 ± 0.11 b–e 0.51 ± 0.03 a–c 2.45 ± 0.15 d–g 1.76 ± 0.14 a–c 0.27 ± 0.02 a–c 6.52 ± 0.21 f–h
400 mg · L−1 ZnO + 1% Ag NPs (1.5% H2O) 1.02 ± 0.12 fg 0.45 ± 0.04 c–f 2.27 ± 0.09 i 1.47 ± 0.16 d–f 0.19 ± 0.03 f–g 7.74 ± 0.27 a
100 mg · L−1 ZnO + 1% Ag NPs (6% H2O) 1.03 ± 0.07 fg 0.45 ± 0.03 c–f 2.29 ± 0.09 hi 1.48 ± 0.10 d–f 0.24 ± 0.02 c–e 6.17 ± 0.10 k
200 mg · L−1 ZnO + 1% Ag NPs (6% H2O) 1.11 ± 0.11 d–g 0.44 ± 0.03 c–f 2.52 ± 0.06 b–d 1.55 ± 0.14 c–f 0.24 ± 0.02 c–e 6.46 ± 0.03 gi
400 mg · L−1 ZnO + 1% Ag NPs (6% H2O) 0.96 ± 0.07 g 0.39 ± 0.03 f 2.46 ± 0.02 c–g 1.35 ± 0.10 f 0.18 ± 0.01 g 7.50 ± 0.16 ab

Biometric parameters of Chrysanthemum × morifolium ‘UBG’ plantlets developed from node explants cultured in vitro on the modified MS medium, depending on the ZnO SMPs/ZnO NPs/ZnO + Ag NPs treatment.

Treatment Number of leaves Micropropagation coefficient Shoot length (cm) Shoot FW (mg) Shoot DW (mg) Root system FW (mg) Root system DW (mg)
Control 14.75 ± 0.50 h 12.00 ± 0.82 i 5.20 ± 0.70 g 318.52 ± 128.04 d 34.10 ± 12.39 e 14.85 ± 9.12 c 1.12 ± 0.48 g
100 mg · L−1 ZnO SMPs 24.25 ± 1.89 b–e 21.50 ± 1.73 b–f 9.60 ± 1.70 ab 916.72 ± 390.89 a–c 122.80 ± 53.97 a 94.80 ± 58.17 ab 7.48 ± 3.97 a–d
200 mg · L−1 ZnO SMPs 22.50 ± 1.00 b–f 19.75 ± 0.96 c–h 9.00 ± 1.93 a–c 868.42 ± 338.87 a–c 91.75 ± 44.85 a–e 94.12 ± 44.37 ab 7.00 ± 3.13 a–e
400 mg · L−1 ZnO SMPs 25.25 ± 2.87 a–d 22.25 ± 2.87 b–e 10.25 ± 1.95 a 1,002.95 ± 389.36 a 120.58 ± 52.61 ab 107.10 ± 74.91 ab 8.00 ± 2.98 a–c
100 mg · L−1 ZnO NPs (1.5% H2O) 22.50 ± 1.73 b–f 20.00 ± 1.41 c–h 8.40 ± 1.77 a–d 531.70 ± 149.45 a–d 61.52 ± 21.16 b–e 44.08 ± 27.16 ab 2.32 ± 1.38 fg
200 mg · L−1 ZnO NPs (1.5% H2O) 18.50 ± 3.79 gh 16.50 ± 3.11 h 6.80 ± 1.35 c–g 598.95 ± 136.25 a–d 57.32 ± 12.32 c–e 90.28 ± 49.57 ab 4.62 ± 2.33 b–g
400 mg · L−1 ZnO NPs (1.5% H2O) 19.25 ± 0.96 fg 16.50 ± 1.29 h 5.32 ± 0.64 fg 467.12 ± 222.54 cd 47.28 ± 17.01 de 52.85 ± 21.40 ab 2.98 ± 1.61 e–g
100 mg · L−1 ZnO NPs (6% H2O) 28.75 ± 2.75 a 26.00 ± 2.58 a 8.62 ± 1.68 a–d 885.00 ± 378.42 a–c 104.15 ± 61.28 a–d 54.20 ± 21.37 ab 4.18 ± 2.82 b–g
200 mg · L−1 ZnO NPs (6% H2O) 22.00 ± 0.82 c–g 20.00 ± 0.82 c–h 6.40 ± 1.75 d–g 594.45 ± 214.63 a–d 59.82 ± 22.95 c–e 66.62 ± 27.71 ab 3.38 ± 1.23 d–g
400 mg · L−1 ZnO NPs (6% H2O) 25.75 ± 4.57 a–c 23.25 ± 4.03 a–c 7.48 ± 2.09 b–f 886.85 ± 525.24 a–c 99.62 ± 56.87 a–d 133.65 ± 79.22 a 7.25 ± 3.57 a–e
100 mg · L−1 ZnO + 0.1% Ag NPs (1.5% H2O) 26.00 ± 3.92 ab 24.00 ± 3.92 ab 8.98 ± 2.35 a–c 848.98 ± 418.51 a–c 107.55 ± 60.71 a–c 71.10 ± 29.22 ab 6.35 ± 2.15 a–f
200 mg · L−1 ZnO + 0.1% Ag NPs (1.5% H2O) 24.75 ± 3.30 b–e 22.50 ± 3.11 a–e 8.00 ± 1.06 a–d 699.28 ± 299.83 a–d 88.62 ± 39.66 a–e 61.50 ± 35.19 ab 4.88 ± 2.64 a–g
400 mg · L−1 ZnO + 0.1% Ag NPs (1.5% H2O) 19.50 ± 2.38 fg 17.00 ± 2.58 gh 5.25 ± 1.44 e–g 503.45 ± 253.84 b–d 60.68 ± 24.29 c–e 98.58 ± 52.69 ab 4.70 ± 2.21 b–g
100 mg · L−1 ZnO + 0.1% Ag NPs (6% H2O) 21.50 ± 3.70 d–g 19.50 ± 3.70 d–h 8.28 ± 2.21 a–d 822.58 ± 629.57 a–c 94.30 ± 61.92 a–d 48.22 ± 24.81 ab 2.55 ± 1.37 fg
200 mg · L−1 ZnO + 0.1% Ag NPs (6% H2O) 22.75 ± 2.22 b–f 20.25 ± 2.50 c–g 9.40 ± 1.15 ab 699.20 ± 213.92 a–d 73.52 ± 13.02 a–e 78.00 ± 31.07 ab 4.52 ± 2.71 b–g
400 mg · L−1 ZnO + 0.1% Ag NPs (6% H2O) 22.75 ± 2.36 b–f 20.25 ± 2.63 c–g 8.40 ± 1.87 a–d 798.75 ± 459.66 a–d 86.70 ± 35.42 a–e 146.67 ± 131.02 a 8.32 ± 2.11 ab
100 mg · L−1 ZnO + 1% Ag NPs (1.5% H2O) 21.25 ± 2.22 e–g 18.75 ± 1.71 e–h 9.38 ± 0.95 ab 849.22 ± 322.33 a–c 96.32 ± 35.65 a–d 67.18 ± 33.93 ab 3.78 ± 1.60 c–g
200 mg · L−1 ZnO + 1% Ag NPs (1.5% H2O) 21.50 ± 2.08 d–g 18.75 ± 2.50 e–h 7.88 ± 0.83 b–d 643.65 ± 229.90 a–d 68.72 ± 19.61 a–e 129.20 ± 53.27 a 8.15 ± 2.53 ab
400 mg · L−1 ZnO + 1% Ag NPs (1.5% H2O) 20.00 ± 1.83 fg 18.00 ± 1.83 f–h 8.00 ± 1.01 a–d 788.32 ± 228.25 a–d 81.00 ± 26.56 a–e 105.08 ± 42.26 ab 7.10 ± 3.03 a–e
100 mg · L−1 ZnO + 1% Ag NPs (6% H2O) 19.00 ± 2.94 fg 16.50 ± 2.65 h 6.58 ± 0.91 d–g 528.92 ± 268.54 a–d 49.15 ± 22.13 c–e 97.10 ± 40.77 ab 5.62 ± 1.70 a–f
200 mg · L−1 ZnO + 1% Ag NPs (6% H2O) 21.50 ± 4.36 d–g 19.00 ± 4.08 d–h 9.58 ± 2.00 ab 987.92 ± 370.32 ab 99.85 ± 38.98 a–d 143.60 ± 45.49 a 9.20 ± 3.23 a
400 mg · L−1 ZnO + 1% Ag NPs (6% H2O) 19.50 ± 2.65 fg 17.25 ± 2.22 gh 7.60 ± 1.88 b–e 724.85 ± 535.35 a–d 71.80 ± 45.90 a–e 62.32 ± 31.34 ab 4.33 ± 3.57 b–g

Content and ratios of chlorophylls and carotenoids in Chrysanthemum × morifolium ‘UBG’ plantlets developed from node explants cultured in vitro on the modified MS medium, depending on the ZnO SMPs/ZnO NPs/ZnO + Ag NPs treatment.

Treatment Chlorophyll a content (mg · g−1 FW) Chlorophyll b content (mg · g−1 FW) Chlorophyll a/b ratio Chlorophyll (a + b) content (mg · g−1 FW) Carotenoid content (mg · g−1 FW) Chlorophyll/carotenoid ratio
Control 1.13 ± 0.16 ab 0.43 ± 0.07 a–d 2.63 ± 0.05 bc 1.56 ± 0.23 ab 0.25 ± 0.03 ab 6.24 ± 0.18 c–f
100 mg · L−1 ZnO SMPs 1.08 ± 0.25 a–c 0.44 ± 0.09 a–c 2.45 ± 0.09 e–i 1.52 ± 0.34 a–c 0.22 ± 0.06 b–e 6.91 ± 0.41 b
200 mg · L−1 ZnO SMPs 0.95 ± 0.15 c–g 0.39 ± 0.03 c–f 2.44 ± 0.23 f–i 1.34 ± 0.18 c–f 0.21 ± 0.02 c–f 6.38 ± 0.27 c–f
400 mg · L−1 ZnO SMPs 0.83 ± 0.08 g–i 0.30 ± 0.03 j 2.77 ± 0.08 a 1.13 ± 0.11 g–i 0.17 ± 0.02 gh 6.65 ± 0.25 bc
100 mg · L−1 ZnO NPs (1.5% H2O) 0.83 ± 0.10 g–i 0.33 ± 0.04 g–j 2.51 ± 0.04 d–h 1.16 ± 0.14 f–i 0.17 ± 0.02 gh 6.82 ± 0.26 b
200 mg · L−1 ZnO NPs (1.5% H2O) 0.63 ± 0.03 j 0.25 ± 0.02 k 2.52 ± 0.07 c–h 0.88 ± 0.05 j 0.12 ± 0.01 i 7.33 ± 0.07 a
400 mg · L−1 ZnO NPs (1.5% H2O) 1.20 ± 0.06 a 0.46 ± 0.03 a 2.61 ± 0.05 b–e 1.66 ± 0.09 a 0.26 ± 0.02 a 6.38 ± 0.26 c–f
100 mg · L−1 ZnO NPs (6% H2O) 0.91 ± 0.06 e–h 0.35 ± 0.02 e–i 2.60 ± 0.06 b–f 1.26 ± 0.07 d–h 0.18 ± 0.01 f–h 7.00 ± 0.06 ab
200 mg · L−1 ZnO NPs (6% H2O) 0.89 ± 0.10 f–i 0.34 ± 0.03 f–j 2.62 ± 0.10 b–d 1.23 ± 0.13 e–i 0.22 ± 0.05 b–e 5.60 ± 1.66 f
400 mg · L−1 ZnO NPs (6% H2O) 0.86 ± 0.07 f–i 0.32 ± 0.04 h–j 2.69 ± 0.10 a–c 1.18 ± 0.11 e–i 0.18 ± 0.02 f–h 6.56 ± 0.11 b–d
100 mg · L−1 ZnO + 0.1% Ag NPs (1.5% H2O) 1.04 ± 0.03 b–d 0.40 ± 0.01 b–e 2.60 ± 0.10 b–f 1.44 ± 0.03 b–d 0.24 ± 0.02 a–c 6.00 ± 0.34 d–f
200 mg · L−1 ZnO + 0.1% Ag NPs (1.5% H2O) 0.88 ± 0.17 f–i 0.36 ± 0.05 e–i 2.44 ± 0.28 f–i 1.24 ± 0.21 e–h 0.19 ± 0.03 e–h 6.53 ± 0.11 b–d
400 mg · L−1 ZnO + 0.1% Ag NPs (1.5% H2O) 0.92 ± 0.11 d–h 0.38 ± 0.07 d–g 2.63 ± 0.14 bc 1.30 ± 0.18 d–g 0.22 ± 0.03 b–e 5.91 ± 0.11 ef
100 mg · L−1 ZnO + 0.1% Ag NPs (6% H2O) 1.03 ± 0.07 b–e 0.40 ± 0.04 b–e 2.58 ± 0.13 b–g 1.43 ± 0.11 b–d 0.23 ± 0.01 a–d 6.22 ± 0.36 d–f
200 mg · L−1 ZnO + 0.1% Ag NPs (6% H2O) 0.79 ± 0.12 h–i 0.31 ± 0.05 ij 2.55 ± 0.06 b–g 1.10 ± 0.17 hi 0.17 ± 0.03 gh 6.47 ± 0.29 b–e
400 mg · L−1 ZnO + 0.1% Ag NPs (6% H2O) 0.98 ± 0.03 c–g 0.39 ± 0.02 c–f 2.72 ± 0.04 ab 1.37 ± 0.05 c–e 0.22 ± 0.02 b–e 6.23 ± 0.24 c–f
100 mg · L−1 ZnO + 1% Ag NPs (1.5% H2O) 0.99 ± 0.06 c–f 0.38 ± 0.03 d–g 2.61 ± 0.10 b–e 1.37 ± 0.09 c–e 0.22 ± 0.01 b–e 6.23 ± 0.24 c–f
200 mg · L−1 ZnO + 1% Ag NPs (1.5% H2O) 1.07 ± 0.06 a–c 0.45 ± 0.03 ab 2.38 ± 0.04 hi 1.52 ± 0.08 a–c 0.22 ± 0.02 b–e 6.91 ± 0.20 b
400 mg · L−1 ZnO + 1% Ag NPs (1.5% H2O) 0.76 ± 0.03 ij 0.29 ± 0.02 jk 2.62 ± 0.14 b–d 1.05 ± 0.04 i 0.16 ± 0.01 h 6.56 ± 0.18 b–f
100 mg · L−1 ZnO + 1% Ag NPs (6% H2O) 0.92 ± 0.23 d–h 0.36 ± 0.08 e–i 2.56 ± 0.15 b–g 1.28 ± 0.31 d–h 0.21 ± 0.06 c–f 6.10 ± 0.47 d–f
200 mg · L−1 ZnO + 1% Ag NPs (6% H2O) 0.92 ± 0.08 d–h 0.38 ± 0.02 d–g 2.42 ± 0.12 g–i 1.30 ± 0.10 d–g 0.20 ± 0.02 d–g 6.50 ± 0.22 b–d
400 mg · L−1 ZnO + 1% Ag NPs (6% H2O) 0.85 ± 0.15 f–i 0.37 ± 0.08 e–h 2.30 ± 0.12 i 1.22 ± 0.22 e–i 0.20 ± 0.04 d–g 6.10 ± 0.19 d–f

Characteristics of samples

Sample name Skeleton density, ρs ± σ (g · cm−3) SSA, as (m2 · g−1) Average particle size from SSA BET, d ± σ (nm) Average crystallite size, Scherrer equation, d ± σ (nm)
ZnO SMPs 5.59 ± 0.03 4.5 240 ± 30 124 ± 11
ZnO NPs (1.5% H2O) 5.09 ± 0.06 48.4 25 ± 2 31 ± 8
ZnO NPs (6% H2O) 5.38 ± 0.05 17.2 65 ± 6 40 ± 10
ZnO + 0.1% Ag NPs (1.5% H2O) 5.16 ± 0.07 40.0 29 ± 2 17 ± 5 (ZnO)
31 ± 10 (Ag)
ZnO + 0.1% Ag NPs (6% H2O) 5.37 ± 0.06 14.2 79 ± 2 39 ± 12 (ZnO)
31 ± 10 (Ag)
ZnO + 1% Ag NPs (1.5% H2O) 5.05 ± 0.05 44.4 27 ± 2 22 ± 3 (ZnO)
45 ± 20 (Ag)
ZnO + 1% Ag NPs (6% H2O) 5.31 ± 0.09 21.4 53 ± 2 35 ± 5 (ZnO)
31 ± 15 (Ag)

Biometric parameters of Chrysanthemum × morifolium ‘UPG’ plantlets developed from node explants cultured in vitro on the modified MS medium, depending on the ZnO SMPs/ZnO NPs/ZnO + Ag NPs treatment.

Treatment Number of leaves Micropropagation coefficient Shoot length (cm) Shoot FW (mg) Shoot DW (mg) Root system FW (mg) Root system DW (mg)
Control 14.75 ± 1.50 e 11.75 ± 1.50 f 3.37 ± 0.97 e 183.88 ± 101.51 c 30.15 ± 9.71 b 14.22 ± 3.42 c 1.82 ± 1.44 d
100 mg · L−1 ZnO SMPs 18.50 ± 1.00 b–d 15.50 ± 1.00 c–e 8.42 ± 1.69 a–d 621.52 ± 246.24 a–c 76.82 ± 21.71 ab 97.58 ± 43.42 b 6.90 ± 4.00 bd
200 mg · L−1 ZnO SMPs 17.75 ± 0.96 cd 14.75 ± 0.96 e 6.55 ± 2.38 cd 525.30 ± 281.34 a–c 59.50 ± 25.42 ab 130.28 ± 45.46 b 5.28 ± 2.97 cd
400 mg · L−1 ZnO SMPs 19.75 ± 1.50 a–d 16.75 ± 1.50 b–e 6.85 ± 0.47 cd 610.65 ± 54.16 a–c 68.82 ± 9.47 ab 219.28 ± 82.43 b 9.15 ± 4.19 a–c
100 mg · L−1 ZnO NPs (1.5% H2O) 18.75 ± 0.96 b–d 15.75 ± 0.96 c–e 6.50 ± 2.43 cd 479.82 ± 182.32 bc 58.68 ± 21.99 ab 102.65 ± 66.78 b 5.08 ± 1.42 cd
200 mg · L−1 ZnO NPs (1.5% H2O) 19.00 ± 0.82 b–d 17.75 ± 2.36 a–c 7.12 ± 1.66 b–d 508.12 ± 195.29 a–c 67.40 ± 25.50 ab 122.02 ± 50.14 b 6.72 ± 2.26 cd
400 mg · L−1 ZnO NPs (1.5% H2O) 20.25 ± 2.50 a–c 17.25 ± 2.50 a–e 7.58 ± 2.88 a–d 665.65 ± 271.19 ab 82.82 ± 29.18 ab 91.95 ± 53.37 b 6.08 ± 3.47 cd
100 mg · L−1 ZnO NPs (6% H2O) 19.00 ± 1.41 b–d 16.00 ± 1.41 c–e 6.30 ± 1.89 de 543.68 ± 247.53 a–c 60.38 ± 26.87 ab 161.10 ± 77.52 b 7.35 ± 5.83 a–d
200 mg · L−1 ZnO NPs (6% H2O) 19.75 ± 0.96 a–d 16.75 ± 0.96 b–e 7.85 ± 0.79 a–d 665.58 ± 207.59 ab 84.38 ± 32.54 ab 168.35 ± 46.40 b 7.92 ± 2.66 a–c
400 mg · L−1 ZnO NPs (6% H2O) 18.50 ± 1.29 b–d 15.50 ± 1.29 c–e 6.42 ± 1.50 cd 511.45 ± 164.74 a–c 51.02 ± 14.96 ab 184.92 ± 81.48 b 6.95 ± 4.82 bd
100 mg · L−1 ZnO + 0.1% Ag NPs (1.5% H2O) 20.50 ± 0.58 ab 17.75 ± 0.96 a–c 7.28 ± 1.22 a–d 753.18 ± 305.43 ab 74.85 ± 36.24 ab 101.58 ± 50.87 b 5.98 ± 2.69 cd
200 mg · L−1 ZnO + 0.1% Ag NPs (1.5% H2O) 18.75 ± 0.50 b–d 15.75 ± 0.50 c–e 6.82 ± 1.25 cd 545.70 ± 131.47 a–c 61.08 ± 15.74 ab 229.28 ± 86.24 b 9.90 ± 4.08 a–c
400 mg · L−1 ZnO + 0.1% Ag NPs (1.5% H2O) 19.75 ± 0.96 a–d 16.75 ± 0.96 b–e 7.08 ± 1.28 bd 678.05 ± 265.25 ab 77.95 ± 26.21 ab 186.42 ± 75.81 b 9.85 ± 4.45 a–c
100 mg · L−1 ZnO + 0.1% Ag NPs (6% H2O) 20.50 ± 1.00 ab 17.50 ± 1.00 a–d 8.75 ± 1.13 a–d 755.55 ± 350.31 ab 85.68 ± 32.51 ab 140.40 ± 49.83 b 7.80 ± 3.77 a–c
200 mg · L−1 ZnO + 0.1% Ag NPs (6% H2O) 22.25 ± 1.89 a 19.50 ± 1.73 a 8.82 ± 1.08 a–c 858.52 ± 283.60 ab 99.28 ± 38.17 a 210.38 ± 64.28 b 12.98 ± 1.17 a
400 mg · L−1 ZnO + 0.1% Ag NPs (6% H2O) 20.75 ± 2.63 ab 17.75 ± 2.63 a–c 8.82 ± 1.11 a–c 746.30 ± 342.36 ab 83.68 ± 35.37 ab 482.35 ± 145.86 a 9.35 ± 4.15 a–c
100 mg · L−1 ZnO + 1% Ag NPs (1.5% H2O) 19.50 ± 3.11 b–d 17.25 ± 3.20 a–e 8.75 ± 1.37 a–d 618.72 ± 238.85 a–c 86.40 ± 39.95 ab 135.98 ± 69.05 b 8.22 ± 2.35 a–c
200 mg · L−1 ZnO + 1% Ag NPs (1.5% H2O) 18.50 ± 1.29 b–d 15.75 ± 0.96 c–e 8.80 ± 1.70 a–c 691.82 ± 299.58 ab 77.88 ± 37.48 ab 150.38 ± 58.97 b 8.92 ± 1.29 a–c
400 mg · L−1 ZnO + 1% Ag NPs (1.5% H2O) 19.00 ± 1.41 b–d 16.50 ± 1.00 b–e 9.48 ± 2.30 ab 764.60 ± 356.38 ab 78.62 ± 34.05 ab 137.82 ± 37.44 b 7.92 ± 1.30 a–c
100 mg · L−1 ZnO + 1% Ag NPs (6% H2O) 19.25 ± 3.77 b–d 17.25 ± 3.77 a–e 8.68 ± 3.04 a–d 687.50 ± 265.24 ab 81.50 ± 36.31 ab 104.40 ± 51.14 b 5.95 ± 5.35 cd
200 mg · L−1 ZnO + 1% Ag NPs (6% H2O) 20.50 ± 1.91 ab 18.75 ± 1.50 ab 9.72 ± 1.32 a 946.78 ± 134.07 a 406.50 ± 21.20 a 231.98 ± 133.63 b 12.62 ± 3.99 ab
400 mg · L−1 ZnO + 1% Ag NPs (6% H2O) 17.25 ± 2.99 de 15.00 ± 2.58 de 7.05 ± 2.36 b–d 733.92 ± 454.71 ab 74.20 ± 36.72 ab 146.40 ± 62.51 b 9.75 ± 4.49 a–c

Results of the analysis of the chemical composition of the sample

Sample name Actual dopant content (mol%) Nominal composition (mol%) Weight content of ZnO and Ag in 100 mg of sample (mg)
Zinc Silver Zinc Silver ZnO Ag
ZnO + 0.1% Ag NPs (1.5% H2O) 99.91 ± 0.04 0.09 ± 0.04 99.9 0.1 99.881 0.119
ZnO + 0.1% Ag NPs (6% H2O) 99.85 ± 0.06 0.15 ± 0.06 99.9 0.1 99.801 0.199
ZnO + 1% Ag NPs (1.5% H2O) 99.05 ± 0.20 0.95 ± 0.20 99.00 1.00 98.745 1.255
ZnO + 1% Ag NPs (6% H2O) 98.95 ± 0.20 1.05 ± 0.20 99.00 1.00 98.613 1.387
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