thesis on ornamental plant

Phytoremediation by ornamental plants: a beautiful and ecological alternative

Review Article
Published: 11 November 2021
Volume 29 , pages 3336–3354, ( 2022 )

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Camila Silva Rocha 1 ,
Daiane Cristina Rocha 1 ,
Leticia Yoshie Kochi 1 ,
Daniella Nogueira Moraes Carneiro 2 ,
Michele Valquíria dos Reis 3 &
Marcelo Pedrosa Gomes ORCID: orcid.org/0000-0001-9406-9815 1

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Phytoremediation is an eco-friendly and economical technology in which plants are used for the removal of contaminants presents in the urban and rural environment. One of the challenges of the technique is the proper destination of the biomass of plants. In this context, the use of ornamental plants in areas under contamination treatment improves landscape, serving as a tourist option and source of income with high added value. In addition to their high stress tolerance, rapid growth, high biomass production, and good root development, ornamental species are not intended for animal and human food consumption, avoiding the introduction of contaminants into the food web in addition to improving the environments with aesthetic value. Furthermore, ornamental plants provide multiple ecosystem services, and promote human well-being, while contributing to the conservation of biodiversity. In this review, we summarized the main uses of ornamental plants in phytoremediation of contaminated soil, air, and water. We discuss the potential use of ornamental plants in constructed buffer strips aiming to mitigate the contamination of agricultural lands occurring in the vicinity of sources of contaminants. Moreover, we underlie the ecological and health benefits of the use of ornamental plants in urban and rural landscape projects. This study is expected to draw attention to a promising decontamination technology combined with the beautification of urban and rural areas as well as a possible alternative source of income and diversification in horticultural production.

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This research was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Financial Code 001, and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil)—Financial Code 406190/2018–6. M.P. Gomes received research productivity scholarship from CNPq.

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Mid-Florida Research and Education Center and Department of Environmental Horticulture, Institute of Food and Agricultural Sciences, University of Florida, 2725 South Binion Road, Apopka, FL 32703, USA

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An efficient micropropagation protocol for an endangered ornamental tree species ( Magnolia sirindhorniae Noot. & Chalermglin) and assessment of genetic uniformity through DNA markers

Yuanyuan Cui 1 , 2 , 4 ,
Yanwen Deng 1 , 2 ,
Keyuan Zheng 1 , 2 ,
Xiaomin Hu 1 , 2 ,
Mulan Zhu 3 ,
Xiaomei Deng 1 , 2 &
Ruchun Xi 1 , 2

Scientific Reports volume 9 , Article number: 9634 ( 2019 ) Cite this article

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Plant breeding
Plant physiology

Magnolia sirindhorniae Noot. & Chalermglin is an endangered species with high ornamental and commercial value that needs to be urgently protected and judiciously commercialized. In this study, a protocol for efficient regeneration of this species is standardized. The lateral buds of the M. sirindhorniae plant were used as an explant. Half-strength Murashige and Skoog (MS) medium supplemented with 2.0 mg/L 6-benzyladenine (BA), 0.1 mg/L α-naphthaleneacetic acid (NAA), and 2.0 mg/L gibberellic acid (GA 3 ) was found to be the optimal medium for shoot induction. The maximum shoot multiplication rate (310%) was obtained on Douglas-fir cotyledon revised medium (DCR) fortified with 0.2 mg/L BA, 0.01 mg/L NAA, and additives. The half-strength DCR medium supplemented with 0.5 mg/L NAA and 0.5 mg/L indole-3-butyric acid (IBA) supported the maximum rate (85.0%) of in vitro root induction. After a simple acclimatization process, the survival rate of plantlets in a substrate mixture of sterile perlite and peat soil (1:3; v/v ) was 90.2%. DNA markers were used for assessment of genetic uniformity, confirming the genetic uniformity and stability of regenerated plants of M. sirindhorniae . Thus, the described protocol can safely be applied for large scale propagation of this imperative plant.

Efficient micropropagation of Thunbergia coccinea Wall. and genetic homogeneity assessment through RAPD and ISSR markers

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Establishment of an efficient in vitro propagation protocol for Sumac ( Rhus coriaria L.) and confirmation of the genetic homogeneity

Introduction.

Magnolias (Magnoliaceae) have long been popular and widely cultivated as ornamental plants, shrubs, and trees. The majority of magnolias are an evergreen species of tree with a graceful form and abundant blooms, typically grown in gardens. Furthermore, many magnolia species have been used in traditional medicine for centuries and many of them have great economic importance as natural sources of aroma and bioactive compounds 1 , 2 , 3 . Magnolia sirindhorniae Noot. & Chalermglin, discovered in a freshwater bog in Thailand in 2002, is a new species used in landscaping due to its fast growth, dense foliage, beautiful canopy, and fragrant flowers 4 . Moreover, M. sirindhorniae has a unique waterlogging resistance, which makes it perfect and promising for the regreening of the wetland parks. Like other magnolia plants, essential oils can be derived from the leaves and flowers of M. sirindhorniae 5 , 6 . However, due to the decline of its habitat, it was classified as ‘Endangered’ on the IUCN Red List 7 . In addition, it is difficult for M. sirindhorniae to reproduce by seeds due to the low percentage of fruit setting.

Plant tissue culture has made a significant contribution to the mass clonal propagation of ornamental and forest trees, providing a large number of superior clonal seedlings in a short time throughout the year 8 . Direct multiple shoot induction is the useful means of producing plantlets from young or mature trees with a lower risk of genetic instability than by the other regeneration routes, and it is a more reliable method for clonal propagation 9 , 10 . Many endangered magnolia species with high ornamental or commercial value, such as M. dealbata and M. punduana , have been protected and expanded by in vitro propagation 11 , 12 , 13 . However, only one root initiation study of M. sirindhorniae has been conducted in which root initiation (90%) was obtained on USK II medium (described by Chaidaroon, 2004) with 4.0 mg/L indole-3-butyric acid (IBA) after 24 days 14 . To date, no studies have reported a protocol for efficient regeneration of this important rare species. Therefore, we explored an efficient protocol for in vitro plant regeneration via shoot induction of M. sirindhorniae for the mass propagation of this precious magnolia plant.

Under the long-term in vitro process, various factors such as media composition and plant growth regulators may result in variations in regenerated plants 15 . Therefore, the genetic uniformity assessment of regenerated plants is of great importance. In recent years, random amplified polymorphic DNA (RAPD) and inter simple sequence repeat (ISSR) have successfully used for assessing the genetic fidelity of regenerated plantlets in many plant species 16 , 17 , 18 .

In the present study, the semi-lignified nodal segments of a 10-year-old M. sirindhorniae plant were used as the explants, followed by optimization of protocol for axillary bud induction, cluster bud proliferation, rooting, and acclimatization. The genetic uniformity of regenerated plants was assessed by RAPD and ISSR markers. This research will be of great help to preserve this important species.

Plant material and preparation of explants

The semi-lignified nodal segments were collected from Shen Zhou Magnolia Park (113°18′E, 23°06′N) in the South China Agricultural University (Fig. 1a ). After cleaning in a solution of 5% ( v/v ) liquid detergent, they were washed under running tap water for 1 hour. Further, they were cut into segments (2–5 cm) with one or two buds, then surface-sterilized with 75% ( v/v ) ethanol for 30 s, followed with 0.1% ( w/v ) mercuric chloride solution for 8–20 min. Afterwards, they were rinsed with sterile distilled water five times. After cutting off two ends, the sterilized explants were inoculated vertically on half-strength MS medium supplemented with different concentrations and combinations of plant growth regulators for shoot induction.

In vitro propagation of M. sirindhorniae using mature axillary node explants. ( a ) Mature tree; ( b ) Shoot bud initiation. ( c ) Multiple shoot bud regeneration. ( d,e ) Regenerated plantlets with well- developed roots. ( f,h ) Acclimatized plants.

Shoot bud initiation

Half-strength MS medium was chosen as the basal culture medium for shoot induction 25 , 26 . The effect of different concentrations of diverse plant growth regulators added to half-strength MS medium was compared. Orthogonal design was adopted and repeated three times; each treatment consisted of 10 explants. The concentrations were as follows: 6-benzyladenine (BA): 0.5, 1.0, 2.0 mg/L; α-naphthaleneacetic acid (NAA): 0, 0.05, 0.1 mg/L; gibberellic acid (GA 3 ):0, 1.0, 2.0 mg/L. Three levels of each of the three factors were examined in nine experimental runs (orthogonal array L 9 (3 4 )) 27 , 28 . After four weeks of incubation, the percentage of shoot induction, time taken for bud initiation (marked by separation layer on the edges of the petiole), and the growth state of the buds were recorded.

Shoot proliferation

Nodal segments (1–2 cm) were cut off and transferred into fresh half-strength MS medium supplemented with different concentrations of BA (0.1, 0.2, 0.4, and 0.6 mg/L) in combination with NAA (0.01, 0.02, 0.04, and 0.06 mg/L) individually in order to standardize the maximum rate of shoot multiplication; there were 16 treatments in total. In addition, six different basal culture media (MS, 1/2 MS, 3/4 MS, WPM, B5, and DCR) with the same plant growth regulators were compared during the phase of subculture, and the optimal medium was selected. After four weeks of incubation, the multiplication rate and number of new shoots per explant ( ≧ 0.5 cm) were recorded.

Individual shoots ( ≧ 1.2 cm height) were cut off and transferred into rooting media. Observations were recorded after every two days 29 , 30 . To optimize the best root induction medium, half-strength DCR medium was chosen as the rooting medium and was supplemented with different compositions and concentrations of the plant growth regulator: NAA (0.1–1.0 mg/L), IBA (0.1–1.0 mg/L), and cycocel CCC (0.1 and 0.5 mg/L. The percentage of root induction, root numbers, and the growth state of roots were observed and recorded after four weeks.

Acclimatization

Plantlets that were observed to have well-developed roots after four weeks were transferred to a greenhouse and kept for approximately 5–7 days. Afterwards, the plantlets were gently removed from the culture vessels and washed off the adhering medium. Subsequently, they were transplanted to plastic cups containing mixture of perlite and peat soil in a ratio of 1:3 ( v/v ), which had been disinfected with potassium permanganate solution (1000–1250 ppm). The survival rate was calculated after one month.

Assessment of genetic uniformity

For genetic fidelity studies, total genomic DNA was extracted from fresh leaves of 18 randomly selected acclimatized plants and their mother plant using the Cetyltrimethyl Ammonium Bromide (CTAB) method 31 . In addition, the total genomic DNA of another M. sirindhorniae plant developed from seed was also extracted as the negative control. The concentration of DNA was measured using a NanoDrop 2000 (Thermo Fischer Scientific, Waltham, MA, USA). For RAPD analysis, a total of 18 primers (TsingKe Biological Technology, Tianjin, China) were used according to previous reports 32 , 33 and initial experiments. The ISSR analysis was performed with three ISSR primers (TsingKe Biological Technology, Tianjin, China), which had been selected for genetic analysis of Magnolia in previous reports 34 , 35 .

DNA amplification for RAPD and ISSR markers was performed in a volume of 25 μL reaction mixture containing 2.0 μL of template DNA (50–60 ng), 12.5 μL of 2 × Taq Plus MasterMix (Beijing ComWin Biotech Co., Ltd., Beijing, China), 1.0 μL of 10 μM forward and reverse primer, and 8.5 μL ddH 2 O. RAPD amplification was performed in a thermal cycler (Bio-Rad, Hercules, CA, USA) programmed for initial denaturation at 94 °C for 5 min, followed by 40 cycles of denaturation at 94 °C for 45 s, annealing at 37 for 45 s, and extension at 72 °C for 90 s with a final extension at 72 °C for 10 min. ISSR amplification was performed in a thermal cycler (Bio-Rad) programmed for initial denaturation at 94 °C for 3 min, followed by 35 cycles of denaturation at 94 °C for 30 s, annealing at 54 for 30 s, and extension at 72 °C for 30 s with a final extension at 72 °C for 3 min. All the PCRs were repeated three times, using the same conditions to check the accuracy of the amplified products. Amplified products were electrophoresed in 1.5% agarose gel containing 0.25 μg/mL ethidium bromide (Invitrogen, Carlsbad, CA, USA) using 1x TAE (Tris Acetate EDTA) buffer. The size of the amplification products was estimated by 100 DNA ladder or 5000 bp DNA marker (Takara, Kyoto, Japan). The gels were photographed using the gel documentation system (Bio-Rad, Hercules, CA, USA), only clear and scorable DNA bands were considered.

Statistical analysis

Induction rate (%) = the number of induced explants/the number of total initial explants × 100%;

Multiplication rate (%) = the total number of buds ( ≧ 0.3 cm)/the number of initial buds on the subcultured explants × 100%;

Rooting rate (%) = the number of the rooted plantlets/the number of total shoots × 100%;

Average root numbers = the total number of roots/the number of rooted seedlings.

Each treatment consisted of 10 glass vessels with 4 plantlets, repeated in triplicate. SPSS software version 19.0 was used for the statistical analyses. The significance of differences among means was carried out using Duncan’s multiple range test at P ≤ 0.05 and P ≤ 0.01; The results were represented as mean ± standard error of three replicates.

Results and Discussion

Shoot bud induction.

The sterilized explants were inoculated into the shoot induction media and then initiated growth after 5–14 days, while petioles began to fall off and small green buds appeared (Table 1a ). The axillary bud induction phase was observed between 10–20 days. The higher the concentration of BA added, the earlier the buds sprouted. The range analysis shows that BA had the most influence on the induction rate (Table 1b ). The induction rate was only 68% in the case of low BA concentration and the lateral buds initiated late; additionally, the new buds were thin and delicate. The advantageous BA concentration is 2.0 mg/L, and the induction rate reached 79%. Previous studies also showed that BA induced the maximum response. The superiority of BA over other cytokinins was reported by Hashem, Bekircan and Hussain 36 , 37 , 38 . GA 3 contributes to the initiation and elongation of axillary buds as well as leaf expansion; the axillary buds began to grow after five days when GA 3 was added. Comprehensively considering growth and induction rate, half-strength MS medium supplemented with 2.0 mg/L BA, 0.1 mg/L NAA, and 1.0 mg/L GA 3 turned out to be a better medium for in vitro induction, as it supported maximum shoot bud induction (Fig. 1b ).

GA 3 has been shown to modulate the growth and development of plants, mainly by stimulating mitotic division and cell elongation 39 , 40 . The positive effects of GA 3 on bud break have been reported in the tissue culture of woody plant species 41 , 42 , 43 , 44 . However, adding the improper concentration of GA 3 has a negative effect. It was found that a high level of GA 3 effectively increased shoot length, whereas a lower concentration of GA 3 inhibited shoot growth in in vitro culture of potato 45 . GA 3 has been used to break dormancy and stimulate shoot elongation in different species of magnolias for a long time 46 , 47 , 48 . In the present study, GA 3 was found to be important for bud induction, effectively shortening the time of initiation and inducing stronger buds, which is consistent with previous reports 49 , 50 . However, some plants cultured in vitro did not undergo any significant growth stimulation with GA 3 51 . Furthermore, GA 3 at any concentration induced the formation of malformed plants in in vitro culture of Annona emarginata 52 . Therefore, GA 3 should be used conservatively in tissue culture. Different species have different responses to GA 3 , and even different genotypes of the same species have different responses to GA 3 .

Shoot bud proliferation

The basal medium is an important substrate for plant tissue culture. Due to the genetic, biological and ecological characteristics of various plants, the nutritional components required by various plants are not the same, and the requirements for the composition of the medium are also different. Therefore, choosing the right type of medium is crucial for the success of plant tissue culture 53 , 54 . Shoot buds from explants were subcultured on six media supplemented with 0.2 mg/L BA in combination with 0.01 mg/L NAA to screen the optimal medium. Among the six tested media (Table 2 ), the best shoot bud proliferation and elongation were observed on DCR medium, which proliferated to 2.92 times than the original after four weeks (Fig. 1c ). Although there was no significant difference observed in the multiplication rate and shoot numbers between MS, 1/2MS, WPM, and DCR media, the growth state of the buds was totally different. The bud clusters on the DCR medium were verdant green and thriving, showing no defoliation, vitrification, or callus.

Further, shoot buds were subcultured on DCR medium supplemented with different combinations of BA and NAA to screen for the optimal combination and concentration of BA and NAA (Table 3 ). Apparently, there was an increase in the multiplication rate with the increase of BA concentration under the same auxin level. On the contrary, it decreased both in the multiplication rate and shoot numbers with increasing NAA concentration under the same cytokinin level. Higher number of multiple shoots occurred on the media with high BA concentrations. Defoliation and vitrification occurred when NAA concentration reached 0.06 mg/L. It is known that plantlets do not grow well when the level of growth regulator is high. Cytokinin promoted the optimal proliferation at low concentrations Among the various combinations tested, the highest rate (299%) of multiplication was observed on the medium fortified with the combination of 0.6 mg/L BA and 0.01 mg/L NAA. However, the optimal growth state of the buds as well as the shoot length ( ≧ 0.5 cm) was found on the medium fortified with the combination of 0.2 mg/L BA and 0.01 or 0.02 mg/L NAA (Table 3 ). In conclusion, the latter two combinations were more suitable for shoot bud proliferation and elongation (Fig. 1c ).

Hyperhydricity is a physiological malformation that results in excessive hydration, yellowing, swelling, glassiness, and leaf curling, which directly affects propagation 55 . In the present study, M. sirindhorniae plantlets that were grown showed signs of being hyperhydrated when cultured on MS medium and 3/4 MS medium that contained high concentrations of nitrate, especially with higher BA (Tables 2 and 3 ). Hyperhydricity disappeared when the medium was changed and the concentration of plant growth regulators was reduced. It was reported that hyperhydricity was positively correlated with tissue nitrate content and cytokinin concentration 56 , 57 , which may explain why plantlets are hyperhydrated on MS medium or 3/4 MS medium. However, it is unlikely that the tissue nitrate level alone directly affects hyperhydricity. It was also reported that ventilation of culture vessels and using the proper gelling agent can relieve hyperhydricity; the use of gelrite resulted in almost four times higher hyperhydricity compared to agar-solidified medium 58 , 59 , 60 . Using a ventilated culture vessel was proven to be useful to relieve hyperhydricity for in vitro plantlets of M. sirindhorniae .

The inability to induce adventitious roots is often a limiting factor in conventional cuttings and tissue culture. In an earlier review, the plants in Magnoliaceae had difficulty with root formation 61 , 62 . It was reported that in vitro Magnoliaceae shoots had difficulty with rhizogenesis under the low concentration of plant growth regulators and only produced a large amount of calluses 63 . Therefore, CCC was specifically added to the rooting media for the purpose of reducing the generation of calluses 29 . However, the supplementation of the medium with CCC did not result in successful rooting. The maximum percentage of rooting (95.67%) with plentiful lateral roots and slight callus as well as the highest average root number of 1.87 was observed on half-strength DCR medium supplemented with 0.5 mg/L NAA and 0.5 mg/L IBA (Table 4 , Fig. 1d,e ). This rooting medium is more efficient compared with that used in previous research 14 . The percentage of rooting first increased and then declined with the increasing concentration of auxins, which was consistent with the in vitro rooting studies of other woody plants 12 , 13 , 64 . Besides, the quality of the subculture shoots evidently influenced rooting. As a consequence, it is important to obtain healthy normal shoots in the phase of multiplication culture.

The acclimatization of tissue cultured plants was the most difficult and labor-consuming step because the newly transplanted plantlets were highly susceptible to fungal diseases 65 . In the present study, the rooted plantlets were successfully transferred into plastic cups containing a perlite and peat soil mixture at a ratio of 1:3 followed by a series of effective protection measures. After being transplanted, the plantlets must be watered and then covered with plastic film and shading net to maintain high humidity. Additionally, it is necessary to spray the plantlets with a carbendazim solution to increase plant tolerance to environmental stresses. Ventilation and removal of fallen leaves and rotten seedling should be performed in a timely manner to prevent plant diseases and insect pests. The plastic film and shading net was removed after two weeks. The survival rate of plantlets reached 90.2% (Fig. 1f,g ). After lignification, they were transferred to the field. Regenerated plants grew well in the field and were phenotypically similar to the mother stock (Fig. 1h ).

Assessment of genetic uniformity of regenerated plants

Compared with the natural environment, in vitro culture is more complicated and stressful, which is more likely to cause genetic variation 66 . Therefore, it is necessary to assess the genetic uniformity of the regenerated plants before confirming the success of a micropropagation protocol. In the present study, a total of 174 bands were generated by RAPD and ISSR markers with an average of 8.3 bands per primer (Table 5 ). Eighteen RAPD primers generated 152 clear and scorable bands in total, ranging from 250 to 4000 bp. The number of bands generated by a single RAPD primer varied from 5 to 13 (Table 5 , Fig. 2 ). Three ISSR primers generated 22 clear and scorable bands in total, ranging from 250 to 5000 bp. The number of bands generated by a single ISSR primer varied from 6 to 9. Compared with the negative control, no polymorphic bands were detected between mother plant and regenerated plants, confirming the genetic uniformity and stability of regenerated plants of M. sirindhorniae (Table 5 , Fig. 3 ). Our results demonstrate that axillary shoot proliferation minimizes the chance of instability, consistent with previous reports 17 , 67 , 68 . This is the first report of genetically sustainable micropropagation in Magnolia plants.

RAPD profiles generated by PCR amplification with primer S10 ( a ), S30 ( b ). Lane M: Molecular marker (100 bp–5 Kb for S10; 100 bp–1.5 Kb for S30); Lane A: Mother plant; Lane 1–18: Regenerated plants; Lane B: Another M. sirindhorniae plant developed from seed (negative control).

ISSR profiles generated by PCR amplification with primer UBC842 ( a ), UBC855 ( b ). Lane M: Molecular marker (100 bp–5 Kb); Lane A: Mother plant; Lane 1–18: Regenerated plants; Lane B: Another M. sirindhorniae plant developed from seed (negative control).

Conclusions

The present report describes an efficient protocol for large-scale micropropagation from axillary nodal explants of M. sirindhorniae . Direct multiple shoot induction suppresses the risk of genetic instability. The maximum shoot bud induction (79.0%) occurred on 1/2 MS medium supplemented with 2.0 mg/L BA, 0.1 mg/L NAA, and 2.0 mg/L GA 3 . It turned out that DCR medium was the best basic medium for in vitro propagation of M. sirindhorniae , and the highest proliferation rate (310%) was obtained on DCR medium fortified with 0.2 mg/L BA and 0.01 mg/L NAA. Half-strength DCR medium supplemented with 0.5 mg/L NAA and 0.5 mg/L IBA was proven to be the best for rooting, and the highest rooting percent (nearly 96%) was achieved in spite of the fact that it is difficult for Magnoliaceae plants to root in plant tissue culture. The regenerated plantlets were well-acclimatized to the wild. RAPD and ISSR markers confirmed the genetic uniformity of regenerated plants. Hence, this protocol can be successfully used for the commercial multiplication of M. sirindhorniae .

Data Availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

This work was supported by the Forestry Public Welfare Industry Research of China [grant number 201404116], the Forestry Science and Technology Innovation of Guangdong Province [grant numbers 2014KJCX006 and 2017KJCX023], and the National Natural Science Foundation of China [grant number 31670601]. We would like to thank LetPub ( www.letpub.com ) for providing linguistic assistance during the preparation of this manuscript.

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Yuanyuan Cui, Yanwen Deng, Keyuan Zheng, Xiaomin Hu, Xiaomei Deng & Ruchun Xi

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Department of Fruit Tree Sciences, College of Horticulture, China Agricultural University, Beijing, 100193, China

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Y.C., X.D. and R.X. designed the experiments. Y.C. and Y.D. conducted the experiments and analyzed the results. Y.C., K.Z., X.H. and M.Z. prepared the manuscript. All authors have read and approved the manuscript for publication.

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Cui, Y., Deng, Y., Zheng, K. et al. An efficient micropropagation protocol for an endangered ornamental tree species ( Magnolia sirindhorniae Noot. & Chalermglin) and assessment of genetic uniformity through DNA markers. Sci Rep 9 , 9634 (2019). https://doi.org/10.1038/s41598-019-46050-w

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Research progress of chromosome doubling and 2 n gametes of ornamental plants.

1. Introduction

2. natural occurrence of polyploid cells, 3. artificial induction of polyploidy in ornamental plant, 3.1. physical induction polyploidy/mutation, 3.2. chemical induction polyploidy/mutation.

Species	Explant	Induction Method	Method	Concentration, Duration	Most Successful Conversion rate	Reference
Actinidia arguta	hardwood	Co γ-ray		Gy, 1 Gy·min	6.67% chimera	[ ]
Magnolia denudata	callus	γ-ray		2.475 × 10 C/kg	chimera	[ ]
Cymbidium hybridum	protocorm-like bodies	colchicine	co-culture	0.05% for 5 d	23.7%	[ ]
Cymbidium hybridum	young shoots	colchicine	immersion	0.05% for 24 h	28.2%	[ ]
Lilium davidii var. unicolor	bulb	colchicine	immersion	0.05% for 48 h	33.3%	[ ]
Asiatic Lilies	bulb	oryzalin	immersion	0.005% for 5 h	23%	[ ]
Phalaenopsis amabilis	cluster bud	colchicine	co-culture	0.05% for 10 d	3%	[ ]
Tagetes erecta	seeds	colchicine	immersion	0.1% for 6 h	100%	[ ]
Impatiens walleriana	seeds	colchicine	immersion	0.05% for 48 h	1.5%	[ ]
Gladiolus grandiflorus	corms	colchicine	immersion	0.2% for 24 h	18%	[ ]
Chrysanthemum carinatum	apical buds	colchicine	absorbent cotton wrapping	0.2% for 6 h/d, 3 d	2.08%	[ ]
Clematis heracleifolia	apical buds	colchicine	spraying	0.2% for 2 d	80%	[ ]
Agastache foeniculum	seeds, apical buds	colchicine	immersion	17.5 mM for 6 h	16%	[ ]
Agastache foeniculum	seeds, apical buds	oryzalin	immersion	50 μM for 12 h	14%	[ ]
Agastache foeniculum	seeds, apical buds	trifluralin	immersion	50 μM for 12 h	12%	[ ]
Hibiscus moscheutos	seedlings	colchicine	immersion	0.025% for 12 h	22.5%	[ ]
Dendrobium officinale	seeds	colchicine	co-culture	0.05% for 4 months	50%	[ ]
Dendrobium officinale	embryo	colchicine	immersion	0.3% for 36 h	40%	[ ]
Dendrobium officinale	protocorm-like bodies	colchicine	immersion	0.3% for 36 h	40%	[ ]
Dendrobium officinale	stems	colchicine	immersion	0.3% for 36 h	30%	[ ]
Neolamarckia cadamba	nodal segments	colchicine	immersion	0.3% for 48 h	20%	[ ]
Ziziphus jujuba	in vitro callus	colchicine + dimethylsulphoxide	absorbent cotton wrapping	0.05% + 1% for 50 d		[ ]
Buddleja lindleyana	seeds	colchicine	immersion	0.3% for 48 h	3%	[ ]

3.3. Others

4. sexual polyploidization, 4.1. 2n gametes, 4.2. others, 5. identification of ploidy, 6. conclusions and further prospects, author contributions, informed consent statement, data availability statement, conflicts of interest.

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Click here to enlarge figure

Species	Ploidy	Reference
Lilium lancifolium	2n = 3x	[ ]
Magnolia spp.	2n = 4x, 6x, 8x	[ ]
Lycoris spp.	2n = 3x, 4x	[ , ]
Narcissus spp.	2n = 3x	[ ]
Primula spp.	2n = 4x, 6x	[ ]
Chrysanthemum spp.	2n = 4x, 5x, 6x, 7x, 8x, 10x	[ ]
Habenaria aitchisonii	2n = 4x	[ ]
Phalaenopsis amabilis	2n = 4x	[ ]
Malus spp.	2n = 3x, 4x, 5x	[ ]
Styrax spp.	2n = 4x, 5x	[ , ]
Fragaria spp.	2n = 4x, 6x, 8x, 10x	[ ]
Oxalistuberosa	2n = 8x	[ ]
Zephyranthes grandiflora	2n = 8x	[ ]
Sequoia sempervirens	2n = 6x	[ ]
Paeonia mairei	2n = 4x	[ ]
Camellia reticulata	2n = 4x, 6x	[ ]
Rosa spp.	2n = 4x, 5x, 6x, 10x	[ , , ]
Hibiscus paramutabilis	2n = 4x	[ ]
Ilex theezans	2n = 4x	[ ]
Oenothera spp.	2n = 4x, 6x, 8x	[ ]
Deutzia spp.	2n = 4x	[ ]
Alnus spp.	2n = 4x, 6x, 8x, 16x	[ ]
Neolamarckia cadamba	2n = 4x	[ ]

Species	Explant	Induction Method	Method	Concentration, Duration	Result	Reference
Populus canescens	pollen	high temperature	detached heat treatment	38~41 °C for 3 and 6 h	42 triploids seedlings	[ ]
Populus canescens	pollen	colchicine	injection	0.5% for injection 11 times (2 h/time)	30.27% 2n pollen	[ ]
Populus tomentosa	pollen	colchicine	injection	0.5% for injection 3, 5, 7 times (2 h/time)	68 triploids seedlings	[ ]
Dimocarpus longan	pollen	colchicine	absorbent cotton wrapping	0.9% for 2 d	19.46% 2n pollen	[ ]
Dimocarpus longan	pollen	high temperature		38 °C for 10 d	5.7% 2n pollen	[ ]
Eucommia ulmoides	megasporogenesis	high temperature	bagging	42~48 °C for 2~6 h	23 triploids seedlings	[ ]
Lily	pollen	high temperature	greenhouse	30 °C for 4 h and 8 h	1~5% 2n pollen	[ ]
Eucalyptus urophylla	pollen	colchicine	injection	0.5% for 3 and 6 h	28.71% 2n pollen	[ ]
Phalaenopsis	pollen	colchicine	absorbent cotton wrapping	0.05% for 3 d	0.9~1.78% 2n pollen	[ ]
Tulipa	pollen	N O	high-pressure container	6 atm for 24 h	16~26.7% 2n pollen	[ ]
Phalaenopsis amabilis	pollen	N O	high-pressure container	48 h	35.6% triploids seedlings	[ ]
Populus	pollen	gibberellins	injection	10 μM for 7 times	21.37% 2n pollen	[ ]
Paeonia lactiflora	pollen	colchicine	injection	0.4% for 2 times	7.79~47.39% 2n pollen	[ ]

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Cui, L.; Liu, Z.; Yin, Y.; Zou, Y.; Faizan, M.; Alam, P.; Yu, F. Research Progress of Chromosome Doubling and 2 n Gametes of Ornamental Plants. Horticulturae 2023 , 9 , 752. https://doi.org/10.3390/horticulturae9070752

Cui L, Liu Z, Yin Y, Zou Y, Faizan M, Alam P, Yu F. Research Progress of Chromosome Doubling and 2 n Gametes of Ornamental Plants. Horticulturae . 2023; 9(7):752. https://doi.org/10.3390/horticulturae9070752

Cui, Luomin, Zemao Liu, Yunlong Yin, Yiping Zou, Mohammad Faizan, Pravej Alam, and Fangyuan Yu. 2023. "Research Progress of Chromosome Doubling and 2 n Gametes of Ornamental Plants" Horticulturae 9, no. 7: 752. https://doi.org/10.3390/horticulturae9070752

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The Spectacular Rise of Ornamental Plants

Aesthetic appeal may have played a role in the domestication of plants and animals, but the rise of pure ornamentals, that is, plants cultivated only for their aesthetic characteristics, is a much later development. Long after the emergence of urban civilization, ornamental and economic uses of plants seem not to have been distinguished. For example, the elegant gardens depicted in Egyptian tombs of the 18th Dynasty (ca. 1415 BCE) consisted, as far as we can tell, of multiple-use plants. Among those that have been identified are date palms, grapes, pomegranates, papyruses, and figs.

A few Egyptian tomb paintings show flowering plants that may have been pure ornamentals, but could just as well have been medicinals. Even blue water lilies, which are ubiquitous in Egyptian art, were more than symbolic and ornamental. The rhizomes of Nymphaea caerulea yield a powerful hallucinogen that the Egyptians probably used to make contact with the gods.

The earliest gardens that seem to have been intended primarily for pleasure were in Mesopotamia. The Gilgamesh epic, which refers to events in 2700 BCE, contains descriptions of what may have been ornamental gardens; however, the first unmistakable evidence of plants cultivated for pleasure is from Assyria. There, kings had hunting preserves and parklike tree plantations. Tiglath Pilesar I, who reigned about 1100 BCE, brought back cedars and box from lands he conquered. Other Assyrian kings left records of parks planted with palms, cypresses, and myrrh.

We do not know what these parks looked like. The first nonutilitarian gardens that can be loosely reconstructed date from the sixth century BCE. The Hanging Gardens of Babylon were created by Nebuchadnezzar, who, the story goes, built them for his Persian wife, who was homesick for the mountains of her childhood. Babylon was situated on a river plain. The terraced gardens, which covered three or four acres, were said to resemble a green mountain. The earliest records of the Hanging Gardens are by the Greek historians Diodorus and Strabo, but no remains have ever been found. However, remnants of Cyrus the Great’s (ca. 585-ca. 529 BCE) garden at Pasargadae still exist. It had trees and shrubs planted symmetrically in plots.

Records of Mesopotamian parks and gardens emphasize trees. Why trees rather than flowers? In the case of Cyrus the Great’s garden, only the remains of trees and shrubs have survived the centuries. Herbaceous plants, if they existed, have vanished. The Greeks, whose records we must rely on for much of our information about Mesopotamian gardens, were not horticulturally advanced, and may have been unduly impressed by the largest, most obvious plants. Still, trees were almost certainly important features of Mesopotamian gardens. Trees provide shade, a necessity in that part of the world, with its intense light and scorching heat.

The practice of cultivating plants for aesthetic pleasure seems to have arisen independently in four widely separated places: Mesopotamia, China, Mexico, and South America.

In addition to their utilitarian value, many trees are architecturally pleasing, and have symbolic and social significance. Like other agricultural peoples, the Mesopotamians cleared land for crops and cut trees for wood. Near towns and cities, groves left uncut may have gradually disappeared because cattle, sheep, and goats grazed and trampled seedlings, allowing no new trees to grow. When forests are reduced to memories, surviving remnants may take on new meanings. Groves can become emblematic of the past, and sacred. They can also become indicators of wealth and worldly power.

The same meanings do not necessarily accrue to smaller flowering plants. Agriculture and herding eliminate many kinds of small plants, but others spring up in their places, even when environments have drastically changed. As a result, ecological discontinuities between past and present can be less immediately obvious with herbaceous plants than with trees.

Agriculture and herding tend to impoverish environments biologically and to the senses. Pleasure gardens may be a reaction to the sensory and emotional impoverishment of overly instrumental, bleakly humanized environments. The Mesopotamian gardens for which we have plans were organized geometrically, which today may not seem the best remedy to visual poverty. However, for the ancients, geometric plantings would have recontextualized familiar plants and provided new experiences, among them a heightened sense of meaning and security. In Mesopotamia the geometric ordering of space was used to suggest an alternative to nature. Gardens, known as paradises, were walled spaces where divine order could be recreated. This order was mathematical.

We know that these mathematical spaces were sensuously enriched with displaced species and plant combinations unknown in the wild. There may also have been pruned, grafted, and trained plants. And, in time (after all, Mesopotamian civilization was more than 2,000 years old by the time of Homer), new varieties would have arisen in gardens, with or without encouragement from people.

From Mesopotamia the concept of the pure ornamental spread westward. Neither the Egyptians nor the Greeks seem to have added much to Mesopotamian and Persian ideas, although the Greeks, with their passion for the written word, left the first extensive records of ornamental plants.

The Romans enthusiastically took up ideas from the East. As early as the middle of the second century BCE Roman estates had pleasure gardens. During the time of the empire some of these gardens were geometric, probably modeled after Eastern originals, but others were informal, wild gardens. Ornamental plant materials included many kinds of trees and shrubs, as well as herbaceous perennials, including violets, narcissuses, convolvuluses, hyacinths, ferns, periwinkles, anemones, rockets, lilies, pimpernels, saffron, and ivies. Calendulas and poppies are the first annual ornamentals on record.

An extreme and oddly prescient Roman garden was the parklike adjunct to Nero’s Golden House, built after the Great Fire of 64 CE, which destroyed most of the city of Rome. The Golden House had a pillared arcade 3,000 feet long and a vestibule large enough to accommodate a 120-foot-high statue of the emperor. The historian Tacitus, Nero’s near contemporary, wrote that the real wonder of the Golden House was not its “customary and commonplace luxuries like gold and jewels, but lawns and lakes and faked rusticity.” There were artificial woodlands, waterfalls, and an enormous pool “like a sea,” along with ploughed fields, vineyard, pastures, and both wild and domesticated animals. Rome already had many gardens, but the Golden House was something new, a country villa set in the center of the city.

Nero inspired such loathing that after his death, the Golden House was dismantled and its countryside restored to city. The Golden House was a cruel and ill-fated expression of a deep human need better answered (if still inadequately) by urban parks, green belts, and other attempts to preserve or recreate countryside in the city.

The emergence of pure ornamentals in the West is poorly documented, but their early histories elsewhere are even more difficult to trace. The practice of cultivating plants for aesthetic pleasure seems to have arisen independently in at least four widely separated places: Mesopotamia, China, Mexico, and South America.

The Aztecs and other peoples of ancient Mexico had pleasure gardens, and by the time of the Spanish invasion, dahlias, zinnias, and two species of marigolds had been cultivated long enough to have become domesticated. Accounts of early Mexican pleasure gardens often emphasize fragrance. To enter the garden of Netzahualcoyotl, the poet king of Texcoco, was, as the king’s descendent Ixtilxochitl described, “like falling into a garden raining with aromatic tropical flowers.” Aztec poetry associates floral perfumes and drunkenness. Lyrics to an Aztec song read:

I inhale the perfume My soul becomes drunk. I so long for the place of beauty The place of flowers, the place of my fulfillment. That with flowers my soul is made drunk.

The association of flowers with drunkenness is probably a literary device, but conceivably may reflect actual experience. The peoples of Mesoamerica were masters of mindaltering substances. The Aztecs and others used the pollen of maguey (the century plant, Agave americana ) to produce dizziness. The flowers of at least one group of plants, the daturas, which figured prominently in Aztec medicine, have pollen and perfumes that cause intoxication.

The peoples of Mesoamerica were masters of mind-altering substances.

Out of curiosity, I placed a bouquet of daturas near my bed and breathed their scent as I fell asleep. I had no unusual dreams, so I tried again by bringing a datura relative into my studio, a potted brugmansia, a South American shamanic plant with hanging trumpet-shaped blossoms. The glorious fragrance gave me one of the worst headaches I have ever experienced. That ended my investigations into intoxicating perfumes.

We know very little about Inca pleasure gardens. The 16th-century Peruvian chronicler Garcilaso de la Vega, the son of an Inca princess and a conquistador, recorded that before the conquest, “all the royal palaces had gardens and orchards for the Inca’s [king’s] recreation. They were planted with all sorts of gay and beautiful trees, beds of flowers, and fine and sweet-smelling herbs.”Several other early accounts confirm the existence of Inca pleasure gardens, but as we might expect, the chroniclers were more interested in precious metals than in flowers. Consequently we know less about the ornamental plants that the Incas cultivated than about an assemblage of artificial plants fashioned out of gold and silver in the Temple of the Sun in Cusco. The assemblage included replicas of herbs, flowers, grains, and trees. Sculptures of useful plants, such as corn and quinoa, were mixed with flowers, lizards, and butterflies.

The idea of growing plants for pleasure may have made its way from Mesopotamia to China, but there is no strong evidence for this. More likely, shamans independently created the precursors to Chinese ornamental gardens. Shamanic gardens served ceremonial functions and contained plants valued for their powers to concentrate the vital powers of nature.

By the Warring States period (481–221 BCE), Chinese magicians and healers had evolved a kind of garden intended to entice spirits. Emperor Han Wu-ti (141–86 BCE) had two lakes built, each with replicas of the legendary islands of the immortals. The purpose of these artificial islands was to lure immortal beings and gain their secrets for the emperor.

Only an emperor could carry things so far. Already during Han Wu-ti’s reign parts of China were densely populated, arable land was in short supply, and a land use ethic had evolved that discouraged the acquisition of large estates for nonutilitarian purposes except by the emperor. The government confiscated huge game parks belonging to certain powerful officials and gave the land to the poor. Sometimes the government confiscated gardens as well. The Han Chinese evidently saw proto-ornamentals and the gardens where they grew as magical and healing in some circumstances, as status symbols in others, and in yet others as expressions of greed. Today there is a remarkably similar range of reactions to ornamentals and ornamental gardens in the West.

Literary evidence suggests that pure ornamentals existed by the Six Dynasties period (222-598 CE). Tao Yuan-ming (365-427 CE), who gave up a secure and high-paying government position because he felt that life was too short for the bowing and scraping necessary for such success, associated garden flowers with poetry and song. “I want not wealth. I want not power. Heaven is beyond my hopes. Then let me stroll through the bright hours as they pass, in my garden among my flowers.”

Camellias were first cultivated for oil, peonies for medicine, lotuses for food, and delphiniums as love potions and to control lice.

Many of today’s ornamentals began as multiple-use plants. Camellias were first cultivated for oil, peonies for medicine, lotuses for food, and delphiniums as love potions and to control lice. In the days before calendars, Japanese farmers brought into cultivation Iris ensata , the forerunner of today’s highly bred Japanese irises, because it bloomed at the time when rice had to be transplanted from seed beds to paddies.

The rose illustrates how circuitous the path to purely ornamental status can be. The Greeks and Egyptians grew roses as medicinal plants and for perfumes and wreaths. The ancients took wreaths quite seriously. They were worn as badges of honor and signs of rank, with proper use strictly enforced. Pliny tells of a man who was jailed for stepping out onto the balcony of his home wearing an inappropriate wreath of roses.

The first clear evidence of roses used as pure ornamentals is Roman. Murals at Pompeii show pleasure gardens with roses, and Pliny evaluated several different varieties for their aesthetic qualities. Yet even among the Romans roses may have been grown less for ornament than for use in wreaths, medicine, perfumes, or for their petals, which were scattered in the paths of dignitaries in the streets.

Flowers, especially roses, figured in Rome’s decay. Nero’s Golden House had rooms with paneled ceilings that slid open so that slaves, working overhead, could sprinkle guests with perfumes and petals. The highlight of Emperor Elagabalus’s brief reign was a party at which so many flowers were dumped on guests that several died of suffocation.

Because of associations with the bad old days, roses fell out of favor among Christians in Western Europe after the collapse of Rome. But roses continued to be cultivated for medicinal purposes and eventually became emblematic of the Virgin Mary, which restored the plant’s prestige. As late as the 18th century a third of all herbal remedies called for roses. Except for the vitamin C in remedies made from rose hips, the benefits were probably a matter of suggestion. Only in the last few centuries have most roses become purely ornamental.

In gardens, species that had never met in the wild were juxtaposed. Wind and insects did the hybridizing and gardeners did the selection. Well before the discovery of plant sexuality, some ornamentals had become remarkably refined. John Creech, former director of the U.S. National Arboretum and an authority on azaleas, wrote that “one can only be awed by the sophisticated level of azalea culture that existed [in seventeenth-century Japan]…. It is doubtful that there are any objectives pursued by modern azalea breeders that were not taken into consideration by the pioneer azalea developers, who produced selections that have not been duplicated since.” Seventeenth-century chrysanthemums, tulips, roses, and camellias displayed comparable accomplishments.

Taste in plants changes. Cyclamens with bizarre crests were popular in 18th-century Europe. Today these flowers are grown by only a few specialists. In Japan, petal-less azaleas consisting mostly of stamens were considered extremely elegant. Chinese and Japanese gardeners took chrysanthemums to heights of eccentricity, developing wilted-looking flowers and ones that resembled mops or shredded coconut.

Because of associations with the bad old days, roses fell out of favor among Christians in Western Europe after the collapse of Rome.

Different eras prefer different novelties. The Victorians were wildly enthusiastic about pelargoniums, newly arrived from South Africa, and fuchsias, from Central and South America. Kao Lin, a 15th-century Chinese cataloger of peonies, mentioned a cultivar named ‘Being Black Purple,’ which he compares to a black mallow, indicating an interest in black flowers. European fascination with black did not arise until two centuries later. Green flowers have never appealed to more than a minority. Kao Lin mentions peonies with green markings, but by his time, appreciation of green cymbidiums was already well established among the literati. In 17th-century Europe some tulips had green hearts or streaks, but it was not until the 18 th century that a few British florists began deliberately selecting for green auriculas.

Preferences for particular patterns and forms also vary greatly. Striped camellias were popular in Japan, and striped dianthuses and tulips became fashionable in Europe, but nothing comparable seems to have developed in China, where selfs were favored. The Ottoman Turks preferred tulips with slender, pointed petals, while Europeans preferred broad, rounded petals. Long-cultivated flowers such as peonies, roses, and chrysanthemums increased in size in both Europe and China, but as long ago as the 17th century Chu Ta respectfully painted modestly sized chrysanthemums. Europeans, Chinese, and Aztecs favored very full doubles, but in Japan many gardeners preferred semi-doubles or singles. Aesthetic preferences among plants bear comparison to those in painting and sculpture. Some preferences are widely shared, but many belong to particular times and places.

In light of the refinement of 18th-century ornamentals such as auriculas, tulips, and ranunculuses, why weren’t they recognized as art? More than two centuries earlier Shakespeare in “The Winter’s Tale” had reflected on a streaked gillyvor, or carnation, as representing “an art which does mend nature — change it rather — but the art itself is nature.” Here the word “art” means “skill” or “craft” rather than fine art. Still, Shakespeare apparently understood certain cultivated plants as shaped by human choices. This was a major step toward considering some plants as fine art, because Europeans believed that art was a distinctively human activity (assisted, perhaps, by divine inspiration.)

The idea that art is uniquely human is not universal. The Chinese, Japanese, and Koreans who practiced highly sophisticated ornamental horticulture, believed that art arose from nature, and attributed the aesthetic and philosophical qualities of art to natural objects. In China, scholars collected remarkable stones and gnarled roots and displayed them as sculpture. These found natural objects were associated with landscape painting, which, along with calligraphy, occupied the pinnacle of the visual arts.

Cultural conditions in the East would seem to have favored recognition of various plants, wild and domesticated, as art. But this did not happen. One reason may be that until very late in the dynastic period, flower painting was considered an inferior genre. Joseph Needham, who spent the greater part of his life studying Chinese culture, suggests a deeper reason why bio art did not emerge in dynastic China.

The single greatest obstacle in the West to recognizing plant breeding as an art was the belief that art and nature are separate.

In attempting to answer the question of why science arose in the West but not in China, Needham came to the conclusion that the West suffered from a “schizophrenia of the soul,” characterized by a sharp split between the physical world and the realms of the spirit. Split consciousness was, to Needham, a condition that drove intellectual and cultural developments in the West. Science arose because it promised to help bridge the divide between nature and spirit and overcome the disease of dualism. The Chinese, who did not suffer from schizophrenia of the soul, were not driven to develop science, and did not need to heal themselves through bio art.

In 1694 Rudolph Camerarius, a professor of natural philosophy at the University of Tübingen, proved that plants reproduce sexually. This made plant breeding possible and would eventually draw attention to the role that humans played in shaping new kinds. However, in itself, an understanding of plant sexuality did not lead to recognition of plants as fine art. Part of the reason was that for at least another century, plant sexuality remained controversial. Also, during this time ornamental plant breeding became associated with the lower classes. However, the single greatest obstacle in the West to recognizing plant breeding as an art was not class prejudice or the scandal of plant sexuality, but the belief that art and nature are separate.

This idea, which can be traced back to Mesopotamia, comes to us mostly through the Bible, which claims there is an unbridgeable chasm between human beings and the rest of life. According to the book of Genesis, God created humans separately from the beasts and in his own image, but plants and animals exist merely in their own, earthbound images. The implications are clear: Not only are humans more important to God than any other kind of life, we belong to a separate and higher category of being.

Humankind’s absolutely singular and privileged place in the universe became a key Christian tenet, reinforced by borrowings from Greek philosophy. Aesthetic theory echoed church doctrine by arguing that art arose from the human mind or spirit and was therefore outside nature and superior to it. “Artistic beauty,” wrote Hegel, “stands higher than nature. For the beauty of art is the beauty that is born… of the mind… God is more honored by what mind does or makes than by the productions or formations of nature” (italics Hegel’s).

Not all philosophers were so adamant. Kant thought that art and nature are separate but that the line between them is not always clear. In “Critique of Judgment” he distinguishes between the aesthetic qualities of nature and the aesthetic qualities of fine art, but identifies artistic genius with nature. In addition, he includes landscape gardening among the fine arts, which means that living plants can be components of art.

Kant did not go so far as to recognize particular ornamental plants as works of art. To have done so would have risked intellectual heresy. As if to reassure his peers that he was no flaming radical, he describes flowers as “free beauties of nature,” using roses as his prime examples.His choice of roses rather than water lilies, say, is telling. By Kant’s time more than 200 varieties of roses were being cultivated in Europe, many of them highly domesticated. Yet he identifies roses as neither wild nor cultivated. This is a striking omission for a claim that roses represent nature’s beauty. By lumping wild and domesticated roses together as exemplars of nature, Kant left undisturbed traditional beliefs that cultivated plants are works of God created when the world began and unchanged ever since. His conveniently generalized rose maintained crucial elements of the ancient dualism that separated man from nature and art from life. Challenge to that dualism was to come less from philosophy than from science, with a little help from the arts.

George Gessert is an artist whose work focuses on the overlap between art and genetics. His exhibits often involve plants he has hybridized or documentation of breeding projects. He is the author of “ Green Light Toward an Art of Evolution ,” from which this article is excerpted.

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Ornamental Plant Efficiency for Heavy Metals Phytoextraction from Contaminated Soils Amended with Organic Materials

Mahrous awad.

1 Department of Soils and Water, Faculty of Agriculture, Al-Azhar University, Assiut 71524, Egypt; moc.liamg@64tuissarebas

M. A. El-Desoky

2 Department of Soils and Water, Faculty of Agriculture, Assiut University, Assiut 71524, Egypt; [email protected]

3 Department of Soils and Water, Faculty of Agriculture, Aswan University, Aswan 81711, Egypt; [email protected]

4 Department of Botany and Plant Physiology, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Kamycka 129, 16500 Prague, Czech Republic; zc.uzc.fa@sebuk (J.K.); zc.uzc.fa@ykcilaks (M.S.); [email protected] (M.B.)

S. E. Abdel-Mawly

Subhan danish.

5 Department of Soil Science, Bahauddin Zakariya University, Multan 06110, Pakistan; moc.liamg@05869ds

Disna Ratnasekera

6 Department of Agricultural Biology, Faculty of Agriculture, University of Ruhuna, Peradeniya 20400, Sri Lanka; moc.liamg@arekesantaransid

Mohammad Sohidul Islam

7 Department of Agronomy, Hajee Mohammad Danesh Sience and Technology University, Dinajpur 5200, Bangladesh; moc.oohay@anahos_dihahs

Milan Skalicky

Marian brestic.

8 Department of Plant Physiology, Slovak University of Agriculture, Nitra, Tr. A. Hlinku 2, 94901 Nitra, Slovakia

Alaa Baazeem

9 Department of Biology, College of Science, Taif University, P.O. Box 11099, Taif 21944, Saudi Arabia; as.ude.ut@meezaabaa

Saqer S. Alotaibi

10 Department of Biotechnology, College of Science, Taif University, P.O. Box 11099, Taif 21944, Saudi Arabia; as.ude.ut@reqas

Talha Javed

11 College of Agriculture, Fujian Agriculture and Forestry University, Fuzhou 350002, China; nc.ude.ufaf@jahatm (T.J.); moc.liamg@82ribbahsbabur (R.S.)

Rubab Shabbir

12 Agriculture Department, The University of Swabi, Khyber Paktunkhwa 94640, Pakistan; kp.ude.ibawsou@dahafhahs

Muhammad Habib ur Rahman

13 Crop Science Group, Institute of Crop Science and Resource Conservation (INRES), University Bonn, 53115 Bonn, Germany; ed.nnob-inu@rubibahm

14 Department of Agronomy, MNS-University of Agriculture, Multan 60000, Pakistan

Ayman EL Sabagh

15 Department of Agronomy, Faculty of Agriculture, Kafrelsheikh University, Kafr El-Shaikh 33516, Egypt

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Accumulation of heavy metals (HMs) by ornamental plants (OPs) from contaminated agriculture soils is a unique technique that can efficiently reduce the metal load in the food chain. Amaranthus tricolor L. has attractive characteristics acquiring a higher growth rate and large biomass when grown at heavy metal contaminated soils. Site-specific detailed information is not available on the use of A. tricolor plant in metal phytoremediation from the polluted sites. The study aimed to enhance the uptake of HMs (Pb, Zn, and Cu) via amending poultry litter extract (PLE), vinasse sugarcane (VSC), and humic acid (HA) as natural mobilized organic materials compared to ethylene diamine tetraacetic acid (EDTA), as a common mobilized chemical agent by A. tricolor plant. The studied soils collected from Helwan, El-Gabal El-Asfar (Cairo Governorate), Arab El-Madabeg (Assiut Governorate), Egypt, and study have been conducted under pot condition. Our results revealed all organic materials in all studied soils, except EDTA in EL-Gabal El-Asfar soil, significantly increased the dry weight of the A. tricolor plant compared to the control treatment. The uptake of Pb and Zn significantly ( p > 0.05) increased due to applying all organic materials to the studied soils. HA application caused the highest uptake as shown in Pb concentration by more than 5 times in Helwan soil and EDTA by 65% in El-Gabal El-Asfar soil while VSC increased it by 110% in El-Madabeg soil. Also, an increase in Zn concentration due to EDTA application was 58, 42, and 56% for Helwan, El-Gabal El-Asfar, and El-Madabeg soil, respectively. In all studied soils, the application of organic materials increased the remediation factor (RF) than the control. El-Madabeg soil treated with vinasse sugarcane gave the highest RF values; 6.40, 3.26, and 4.02% for Pb, Zn, and Cu, respectively, than the control. Thus, we identified A. tricolor as a successful ornamental candidate that, along with organic mobilization amendments, most efficiently develop soil health, reduce metal toxicity, and recommend remediation of heavy metal-contaminated soils. Additionally, long-term application of organic mobilization amendments and continued growth of A . tricolor under field conditions could be recommended for future directions to confirm the results.

1. Introduction

Contaminated soils by heavy metals (HMs) are the global environmental problem caused by certain natural processors, including erosion, mineral weathering, volcano eruptions and anthropogenic activities such as industrialization, urbanization, agricultural practices (application of HMs-containing pesticides and fertilizers, sewage sludge, etc.) and casting minerals [ 1 , 2 , 3 , 4 , 5 , 6 ]. Their accumulation in agricultural soils could potentially increase the risk of entry into the food/feed chain, threatening human and animal health [ 7 , 8 ]. For cleaning-up of HM contamination, various practices and technologies such as adsorption, oxidation, reduction, precipitation [ 9 ], ion-exchange, coagulation-flocculation, electrochemical methods [ 10 ], leaching/acid extraction, and soil washing [ 11 ] have been adopted. However, such remedial methods are not economically viable, destructive to the agro-ecosystems, impractical for large quantities of hazardous waste [ 12 ]. Also, changing the metal mobility via immobilization or mobilization with soil amendments and green remediation has been recognized as a calm remediation tactic [ 13 ].

The use of plants for remediation of HM contaminations attracts special attention because of additional beneficial effects, including preventing erosion, improving soil quality, and maintaining healthy ecosystem functioning. Further, it is an economical and easily applicable eco-friendly and natural process, wherein no residual and toxic materials are left behind, preserve, maintain soil physical, chemical, and biological properties, and prevents HMs penetration into groundwater [ 14 ]. The phytoremediation should be a holistic approach to immobilize or lower the HM from the contaminated soil and restore the healthy soil characteristics to perform its normal functions. The success of this practice depends on the ability of the selected plant to produce rapid biomass and accumulate HMs within their tissues [ 15 , 16 ]. Plant mediating to absorb, transfer and accumulate hazardous contaminants using edible plants [ 17 ], non-edible plants including medicinal and aromatic species [ 18 , 19 ] along with trees, grasses, and ornamental plants [ 20 ] has been documented. Using edible crops is an inappropriate option because pollutants enter the food chain, threatening human and animal health [ 21 , 22 ].

As a suitable option, ornamental plants (OPs) may be of special interest because of their fast growth, viability, abundance, thus preferably chosen from the local environment. The characteristics to be considered when selecting an OP were well documented [ 23 ]. Among these species, Amaranthus tricolor , also known as red amaranth, which belongs to the Amaranthaceae family, originated in Asia would be one of the best candidates. It is the most common cultivated plant in Bangladesh as leafy vegetables [ 24 ]. Also, Ref. [ 25 ] identify the A. tricolor as the Cd hyperaccumulators. Moreover, these plants can clean up the contaminants, beautifying the environment, and pollutants without access to the food chain [ 24 , 26 ]. It tends to accumulate HMs in their non-food biomasses that significantly contribute to their economic and ecological values [ 22 , 27 ].

The factors affecting the amounts of metal that a plant absorbs those controlled by the concentration and speciation of the metal in the soil solution; the movement of metal from the bulk soil to the root surface; the transport of the metal from the root surface into the root, and its translocation from the root to the shoot [ 28 , 29 ]. Plants readily uptake HMs dissolved in soil solution in ionic or chelated, or complex forms [ 30 , 31 ]. Several organic and inorganic agents might effectively and specifically increase HMs solubility that could be accumulated by several plant species [ 32 ]. Ethylenediaminetetraacetic acid (EDTA), as a synthetic chelator, is used among the most common chelating agents to increase the plant uptake of metals cause environmental contamination by leaching HMs into groundwater bodies [ 7 ]. Further, low biomass of hyperaccumulation increased bioavailability of metals, and the persistence of metal-chelate complexes are major disadvantages of such mobilizing synthetic chelators [ 33 ].

As alternatives to synthetic chelators, widespread natural sources called biochelators, such as poultry litter extract (PLE), vinasse, and humic substances, could be used. Enhanced soil biological, chemical, and physical properties have been reported with increased soil fertility by applying such organic amendments [ 34 ]. The organic materials, including poultry litter, Vinasse, humic acid are by-products or industry wastes with various unique benefits related to soil quality and health [ 31 , 34 , 35 ]. Using such organic materials and different plant species to boost phytoextraction was previously reported [ 16 , 20 , 21 ]. For example, Ref. [ 36 ] pointed out that biochelators (humic acids) realized positive effects on the HMs uptake. They also found that adding humic acids (HA) to artificially contaminated soil increased the cadmium (Cd) uptake by tobacco plants. Moreover, the application of soil amendments such as biosolids and cow manure exhibited the enhanced uptake HMs in sunflower [ 16 ]. Exploring the phytoextraction potential of ornamental plants for remediation of polluted environments is considered an important strategy that could be highlighted in future research [ 11 , 14 ].

Particularly A . tricolor was reported to have specific interest amongst other ornamental plants as it has specific mechanisms to solubilize Cd adsorbed to soil particles while acquiring higher growth rate and large biomass when grown in heavy metal contaminated soils [ 25 ]. Hence, A. tricolor is a suitable model to explore metal transfer and phytoremediation of HMs grown in contaminated soils amended by different organic and inorganic materials. Most of the previous studies evaluate the performance of one or two organic or synthetic materials on contaminated soil, mostly using edible plants to assess their study. Our hypothesis that each material or metal may have specific behaviour depending on the soil characteristics or metal and the ability of the used biomaterial to make the metal more soluble. In our study, we considered the advantage of using three natural materials that are already present in a huge quantity, problematic in getting rid of them and imposing additional cost in waste management programs of the country. Therefore, the purpose of this study was to compare the performance of naturally occurring organic materials (poultry litter extract (PLE), vinasse sugarcane (VSC), and humic acid (HA)) with synthetic chelates (EDTA) in enhancing phytoextraction of lead (Pb), zinc (Zn) and copper (Cu) by A. tricolor plants in different naturally contaminated soils, and to assess the storing and removing of metals using ornamental plants and their ability to produce a large amount of biomass in a short time for such soil characteristics.

2. Materials and Methods

2.1. characterization of soil sites.

The surface soil layer (topsoil) (0–30 cm) was collected from three different locations in Egypt (Helwan and El-Gabal El-Asfar, Cairo Governorate, and El-Madabeg soil, Assiut governorate). The soils at selected sites are continuously contaminated by HMs from sewage (El-Gabal El-Asfar and El-Madabeg soils) and/or industrial (Helwan) wastewaters. The soils at these locations are receiving a continuous supply of heavy metals as domestic, such as the soils of El-Gabal El-Asfar (31°23′15″ E and 30°12′19″ N) and El-Madabeg (31°08′42″ E and 27°09′52″ N) for more than 50 years, and the Helwan soil (31°20′09″ E and 29°34′55″ N), which are very close to the army factories that receive their industrial waste in addition to human waste. The chosen soils varied in their texture between silty clay loam, loamy sand and sand, soil pH (8.11, 6.71 and 7.59) and organic matter (2.18, 5.70 and 2.80), respectively, for Helwan, El-Gabal El-Asfar and El-Madabeg soils ( Figure 1 ).

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An aerial map of Egypt showing the location of the Helwan ( a ) El-Gabal El-Asfar ( b ) and El-Madabeg ( c ) soils scene acquired from Google Earth. 2020.

The collected soil samples were air-dried, ground with a wooden roller, sieved to pass through a 2 mm sieve, and kept for experimental purposes. Available Pb, Zn and Cu were extracted from the soil samples using a 0.005 M of diethylene triamine pentaacetic acid (DTPA) solution buffered at pH 7.3 as described by [ 37 ]. A soil sample of 1 g was used to extract metal content using HNO 3 , H 2 O 2 , and HCl [ 38 ]. Certain physical properties, soil reaction (pH), soil salinity (EC), and soil organic matter of tested soils were measured according to [ 39 ] with three replicates for each and are presented in Table 1 .

Some chemical and physical properties of the studied soils.

Property	Soils
Property	Helwan	El-Gabal El-Asfar	El-Madabeg
Clay (%)	24.74	12.00	4.91
Silt (%)	17.32	12.64	7.35
Sand (%)	57.94	75.36	87.74
Texture	Silty clay loam	Loamy sand	Sand
CaCO (g/kg)	53.7	25.0	68.00
pH (1:2.5)	8.11	6.71	7.59
Organic matter (%)	2.18	5.70	2.80
EC (1:1 dS/m)	5.18	1.86	1.7
US.EPA-extractable metals (mg/kg)
Pb	45.60	247.20	86.10
Zn	202.90	585.30	139.10
Cu	36.10	191.20	38.30
Total metals (mg/kg)
Pb	56.80	261.00	95.00
Zn	216.00	618.00	165.00
Cu	55.00	195.00	45.00
DTPA-extractable metals (mg/kg)
Pb	2.70	45.51	6.16
Zn	11.91	5.63	4.10
Cu	3.21	3.75	6.07

2.2. Testing Organic Materials

Four organic materials were examined for their effects on HMs mobility and phytoextraction capacity by growing tested plants on contaminated soils. Ethylenediaminetetraacetic acid (EDTA) at 2 mM as a synthetic organic material, in addition to poultry litter extract (PLE) solution (75 g/L), vinasse sugarcane (VSC) 1:2 water ( V / V ), and humic acid (HA) at 0.025% solution as natural organic materials was assembled as treatments. The investigated levels of the organic materials were chosen as effective levels according to the leaching procedures. The poultry litter (PL) was collected from the poultry farm of Assiut University, Assiut Governorate. Vinasse sugarcane (VSC), a by-product of the sugar industry, was obtained from Abu-korkas Sugar Factory, El-Minya Governorate, Egypt. The humic acid (HA) solution was brought from the Agriculture Company for Recycling Agriculture Residues, El-Minya Governorate, Egypt. PLE, VSC, and HA samples were subjected to necessary chemical analysis (OM, pH, and EC). Other samples were digested using concentrated nitric and perchloric acids to determine their total Pb, Zn, and Cu contents using atomic absorption ( Table 2 ). The analysis of these organic materials was done in three replicates for each ( n = 3).

Some chemical properties of the examined organic materials.

Organic Material	Metals (mg kg )			EC (dS/m)	pH (1:2.5)	OM (%)
Organic Material	Pb	Zn	Cu	EC (dS/m)	pH (1:2.5)	OM (%)
Poultry litter extract (PLE)	0.51	0.22	0.15	4.20	7.66	2.25
Vinasse sugarcane (VSC)	0.39	4.18	1.15	14.70	4.45	5.11
Humic acid (HA)	0.12	0.34	0.10	25.90	12.90	3.10

2.3. Experimentation

A pot experiment under a greenhouse condition was conducted to study the ability of A. tricolor to accumulate Pb and Zn from contaminated soil. Plastic pots were filled with 2 kg of soil and two seedlings of A. tricolor (15-day-old) were grown in each pot. The pots were carefully watered to near field capacity by deionized water for two weeks. Four organic amendments were used in the current study (EDTA, PLE, VSC, and HA solutions). The pots were set up in a completely randomized design (CRD) and each treatment was replicated three times. At the end of the experiment (10 weeks from transplanting), plant samples were collected and cleaned first using tap water, followed by washing with distilled water. Then samples were oven-dried at 70 °C for 72 h, and the dry weight was recorded. The dried plant materials were ground using a mortar and pestle and kept for plant analysis with three replicates for each. Soil samples from each pot were air-dried, ground, and passed through a 2 mm sieve. Plant samples of 0.2 g were digested using concentrated acids of H 2 SO 4 and HClO 4 . The heavy metals: Pb, Zn, and Cu in the digests were determined using model 906 of GBC atomic absorption spectrophotometry (AA 800, Perkin Elmer Co., 14775 E Hinsdale Ave, Centennial, CO, USA) according to the method outlined by [ 38 ] method (3050).

In brief, one gram of a soil sample is transferred to a digestion vessel, 10 mL of 1:1 HNO 3 is added, mixed, and covered with a watch glass, heated to 95 ± 5 °C and refluxed for 10 to 15 min without boiling and allowed to cool. 5 mL of concentrated HNO 3 is repeated and refluxed for 30 min until no brown fumes are given. After the last step is completed and the sample is cooled, add 2 mL of water and 3 mL of 30% H 2 O 2 . One mL of 30% H 2 O 2 is added while warming until the minimal effervescence or until the total of 10 mL 30% H 2 O 2 (should not be exceeded). Then, reduce the volume to approximately 5 mL. After that, 10 mL of concentrated HCl is added to the sample digest, heated for 15 min. During this whole process, the sample should be covered with a watch glass. The digestate is filtered through a Whatman No. 41 filter paper; the filtrate is collected in a 100-mL volumetric flask and made to the volume. This method successively digests a soil sample with HNO 3 , H 2 O 2 and HCl acids to measure “total sorbed metals” by the acidic dissolution of clay, oxides, and carbonates and oxidation of organic matter; elements associated with silicates are not dissolved. All soil and plant sample measurements were performed in three replications.

2.4. Calculation of Remediation Factor

The percentage of remediation factor (RF) was calculated according to the equation [ 40 ]:

where, metal (shoot) is the concentration of metal in the shoot as milligram per gram, DW refers to the dry weight of shoot as gram per pot, and metal (soil) is the concentration of total soil Metal as milligram per kilogram.

2.5. Analysis of Data

One-way analysis of variance (ANOVA) and Duncan’s multiple range test was used to determine the statistical significance of the organic materials treatment effects on heavy metals uptake and plant development using CoStat software, and p < 0.05 was considered statistically significant. All the results are shown as mean values ( n = 3) ± Standard deviation (SD).

3.1. Effect of Organic Materials on Fresh and Dry Weight

The illustrated results in Figure 2 a,b showed the application effect of the investigated organic materials on the fresh and dry weight of A. tricolor plants. The incorporation of organic materials, except EDTA in El-Gabal El-Asfar soil, significantly increased the fresh and dry weight of the tested plants compared to the control treatment. The magnitude of increase varied according to the added organic materials and soil types. Among all organic materials, EDTA was the most effective material in Helwan soil. Meanwhile, the vinasse sugarcane (VSC) was the most effective one in El-Gabal El-Asfar and El-Madabeg soils. El-Gabal El-Asfar soil showed the highest dry matter of the A. tricolor plants than other soils. The highest increase of dry matter was observed in Helwan soil treated with EDTA followed by VSC that increased by about 4.13 and 3.97 times compared to the control treatment, respectively. Adding VSC to El-Gabal El-Asfar and El-Madabeg soils resulted in increasing dry matter of A. tricolor plants by 63.56 and 64.90%, respectively, compared to the control treatment. On the other hand, HA was the least effective in Helwan soil (18.18%), while the EDTA was the least effective in El-Madabeg soil (15.32%) compared to the control treatment.

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Fresh weight ( a ) and dry weight ( b ) of A. tricolor plants as affected by application of different organic materials.CK (control, No additions), EDTA (Ethylene diamine tetra acetic acid at 2 mM), PLE (poultry litter extract at 75 g/L), VSC (vinasse sugarcane 1:2 water) and HA (humic acid at 0.025%). Same letters were not significantly different at p < 0.05.

3.2. Lead (Pb) Uptake by A. tricolor Plants

In all studied soils, the investigated organic materials significantly ( p = 0.05) increased the Pb concentration in A. tricolor plants compared to the control treatment ( Table 3 ). The degree of the uptake varied depending upon the organic material and soil type. The organic material differed in its behaviour according to soil types. HA gave the highest increase in Pb concentration in plants grown in Helwan soil, followed by VSC. EDTA showed the highest value in the plants grown in El-Gabal El-Asfar soil, whereas VSC induced the highest amount in El-Madabeg soils.

Lead (Pb) concentrations (mg kg −1 ) in the shoots of A. tricolor grown in the contaminated soils amended with some organic materials.

Treatment	Helwan Soil	El-Gabal El-Asfar Soil	El-Madabeg Soil
CK	16.71 ± 0.27	96.47 ± 0.46	41.17 ± 1.08
EDTA	55.43 ± 1.74	132.69 ± 0.53	60.53 ± 0.86
PLE	77.18 ± 0.75	105.33 ± 0.38	63.41 ± 0.60
VSC	114.23 ± 1.06	88.04 ± 0.50	86.77 ± 0.33
HA	115.39 ± 0.57	98.53 ± 0.57	68.49 ± 0.11

CK (control), EDTA (Ethylene diamine tetraacetic acid at 2 mM), PLE (poultry litter extract at 75 g/L), VSC (vinasse sugarcane 1:2 water) and HA (humic acid at 0.025%). Same letters were not significantly different at p < 0.05.

Meanwhile, the highest Pb concentration was observed in El-Gabal El-Asfar soil, followed by Helwan soil and finally El-Madabeg soil. Application of HA and VSC caused an increase (5.83 and 5.90 times, respectively) in the Pb concentration in Helwan soil. In El-Gabal El-Asfar soil, the concentration of Pb increased by about 65 and 9% for EDTA and PLE treatments, respectively. At the same time, the application of VSC and HA in El-Madabeg soil raised the Pb concentration by about 110 and 66%, respectively.

3.3. Zinc (Zn) Uptake by A. tricolor Plants

The studied organic materials induced uptake of Zn in A. tricolor plants over the control ( Table 4 ). The increase in Zn concentration in plants varied according to both the organic materials and the soil types. EDTA was superior to rest treatments regarding the concentration of Zn uptake in plants in all studied soils. While VSC and PLE materials recorded the second-highest Zn in El-Gabal El-Asfar and El-Madabeg soils, respectively. Application of EDTA and HA in Helwan soil caused an increase in Zn concentration in A. tricolor plants by 7.74 and 24%, respectively. In the case of plants in El-Gabal El-Asfar soil, the concentration of Pb increased by 42.83 and 11.54% for EDTA and VSC treatments, respectively. While the application of EDTA and PLE raised the plant Pb concentration by 56.60 and 21.40%, respectively, in El-Madabeg soil. El-Gabal El-Asfar soil showed high shoot Zn concentration than the other two soils.

Zinc (Zn) concentrations (mg kg −1 ) in the shoots of A. tricolor grown in the contaminated soils amended with some organic materials.

Treatment	Helwan Soil	El-Gabal El-Asfar Soil	El-Madabeg Soil
CK	84.93± 1.90	129.97 ± 0.99	67.01 ± 0.53
EDTA	133.97± 1.13	185.64 ± 1.18	104.94 ± 0.93
PLE	98.27± 1.62	143.19 ± 1.10	81.35 ± 3.06
VSC	86.25± 0.77	144.97 ± 1.04	76.72 ± 1.71
HA	105.53± 0.77	144.55 ± 1.13	74.65 ±0.59

CK (control), EDTA (Ethylene diamine tetraacetic acid at 2 mM), PLE (poultry litter extract at 75 g/L), VSC (vinasse sugarcane 1:2 water) and HA (humic acid at 0.025%). The same letters were not significantly different at p < 0.05.

3.4. Copper (Cu) Uptake by A. tricolor Plants

The data presented in Table 5 showed that the organic materials significantly increased the uptake of Cu over the control. The increase in Cu uptake varied according to both the organic materials and the soil types. EDTA and HA were the most effective organic materials for increasing Cu concentration in the shoot in Helwan soil. Cu concentration in the shoot of A . tricolor plant increased to 32.53 and 32.71% for Helwan soil due to EDTA and HA, respectively. In the same context, EDTA was the most effective treatment in both El-Gabal El-Asfar and El-Madabeg soils. It caused an increase in the shoot Cu by 26.82 and 37.21% for El-Gabal El-Asfar and El-Madabeg soils, respectively. VSC recorded the second highest order in El-Gabal El-Asfar and El-Madabeg soil since it increased Cu by 31.15 and 15.11% over the control, respectively. On the other hand, PLE was the least effective organic material in enhancing amounts of Cu that were taken up by Amaranthus plants grown in El-Gabal El-Asfar and El-Madabeg soils.

Copper (Cu) concentrations (mg kg −1 ) in the shoots of A. tricolor grown in the contaminated soils amended with some organic materials.

Treatment	Helwan Soil	El-Gabal El-Asfar Soil	El-Madabeg Soil
CK	17.57 ± 0.57	26.74 ± 0.44	22.44 ± 0.57
EDTA	26.04 ± 0.71	36.54 ± 1.09	35.74 ± 0.86
PLE	24.68 ± 0.55	27.09 ± 1.88	23.02 ± 0.37
VSC	18.12 ± 0.25	35.07 ± 1.01	25.83 ± 1.51
HA	26.11 ± 0.46	29.35 ± 1.00	23.76 ± 3.28

3.5. Effect of Organic Materials on Pb, Zn, and Mn Phytoextraction by A. tricolor Plants

The total amount of metal removed from contaminated soils at the end of the remediation process is the only way to evaluate the effectiveness of the remediation process. The remediation factor (RF) was calculated to assess the ability of A. tricolor plants in Pb, Zn, and Mn phytoextraction. This parameter shows the level of metal removal from soil by the plant. In the case of Pb, the highest value of RF was recorded when A. tricolor plants treated with VSC in Helwan and El-Madabeg soil (5.8 and 6.40%, respectively), while the value was 2.7 under PLE treatment in El-Gabal El-Asfar soil ( Figure 3 ). However, the VSC gave the highest RF value of 1.68 and 3.26% for Zn in El-Gabal El-Asfar and El-Madabeg soil, respectively. Meanwhile, the highest value of RF (1.67%) was observed with EDTA in Helwan. Except for EDTA in El-Gabal El-Asfar soil, the lowest RF value of Pb and Zn was observed of A . tricolor plants grown on the control soils.

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The remediation factor (RF%) of Pb ( a ), Zn ( b ) and Cu ( c ) by A. tricolor as affected by the application of different organic materials. CK (control, No additions), EDTA (Ethylene diamine tetraacetic acid at 2 mM), PLE (poultry litter extract at 75 g/L), VSC (vinasse 1:2 water) and HA (humic acid at 0.025%). Same letters were not significantly different at p < 0.05.

4. Discussion

The dry biomass of plants increased in all tested organic materials compared to the control. The properties of biochar have a great impact on HM immobilization [ 41 ]. The increase in fresh and dry weight by applying the organic material could be explained by the fact that the presence of soil organic matter improves physical, chemical, and biological characteristics and the fertility of studied soils [ 30 , 31 ]. It was further supported by applying organic materials that showed enhanced soil fertility by improving soil physical, chemical, and biological properties, and biomass production of plant and uptake of heavy metals through altering the physiological and morphological characteristics [ 32 ]. EDTA was the most effective material in Helwan soil, while the Vinasse sugarcane (VSC) was the most effective one in El-Gabal and El-Madabeg soils. These results agreed with those obtained by [ 33 ], who postulated that organic amendments promoted switchgrass growth. It has been reported that the application of vinasse increased the yield of wheat [ 34 , 35 , 36 ]. Also, [ 28 ] revealed that some organic compounds in the soil increased both the fresh and dry yield of tomato plants.

Moreover, the enhanced uptake and accumulation of HMs such as Pb, Zn, and Ni in sunflower have been reported recently when adding biosolids and cow manure simultaneously [ 16 ]. Increasing the A. tricolor plants’ dry matter in El-Gabal El-Asfar soil may be due to the high organic matter content than other soils ( Table 1 ). Helwan soil has been characterized by high salt content, low organic matter ( Table 1 ) that probably caused stress on the plants grown on this soil compared to the other soils. In contrast, the direct adverse action of EDTA as salts on the dry weight of A. tricolor plants in El-Gabal El-Asfar soil might be decreased plant growth. As indirect action, increasing the bioavailability of soil HMs could negatively influence plant performance. So, the reversible effect of EDTA on the plant growth in El-Gabal El-Asfar soil may be due to increasing the bioavailability of the HMs in this soil that contains a high amount of metals. EDTA treatments reduced the shoot growth of sunflower and saltbush plants [ 8 , 37 ]. They reported that EDTA might chelate HMs that enable the plant to absorb many of them, leading to reduced dry matter. Also, this result is agreed with those obtained by [ 38 ], who indicated that the application of EDTA at a level of 5.0 mmol/kg soil or higher significantly decreased the plant growth (dry weight).

The phytoremediation action of plants mainly involves phytoextraction or phytostabilization strategies. The efficiency of plants to absorb and accumulate a large quantity of metal in their tissue in a short period defined as phytoextraction. The metal of the hyperaccumulator is defined as a plant that can accumulate 100 mg kg −1 in its tissues [ 14 ]. The obtained data indicated that the investigated materials increased metals uptake by A. tricolor plants in all studied soils. The plants grown on El-Gabal El-Asfar soil showed the highest values of Pb uptake than the other soils. This result may be due to its high metal content and/or low soil pH value that led to increased mobility and uptake compared to the others. Increasing the amounts of Pb taken up by plants in the studied soils could be arranged in the descending order of El-Gabal El-Asfar soil > El-Madabeg soil > Helwan that is compatible with their Pb content. On polluted soils, a strong association was observed mainly between heavy metal content in the soil and its content of plants [ 31 ]. EDTA treatment caused the highest Pb amount in El-Gabal El-Asfar soil and the highest Zn content in all studied soils. This may be because it chelates the metal in this soil with low acidity and contains a high Pb and Zn content. Application of chemical chelators such as triethylene glycol diamine tetraacetic acid (EGTA) and sodium dodecyl sulfate (SDS) was reported as promising materials to use in HMs accumulation in ornamental plants [ 30 , 42 , 43 , 44 ]. EDTA was reported to be superior in solubilizing soil Pb and Zn for root uptake and its translocation into the above-ground biomass due to its strong chemical affinity for metals [31). It is considered one of the strongest synthetic chelating agents for metals with more ability than the naturally occurring organic ligands [ 28 ]. The higher level of EDTA caused an increased uptake of Cd by 63% due to the formation of complexes with Cd, which increases its availability and roots to shoot translocation [ 8 ]. Similar results were found by [ 43 ]. HA led to the highest increment of Pb in Helwan soil. These results are consistent with those obtained by [ 43 , 45 ], who found that HA enhanced plant growth and improved root development led to an increase in the availability of metals. Also, Refs. [ 46 , 47 , 48 ] reported that the HA was effective in the evapotranspiration, gas exchange, and leaf uptake of nutrients. Nonetheless, VSC caused a greater increment of Pb (110%) in El-Madabeg soil. This increase may be due to the formation of soluble organometallic complexes via vinasse application and its ability to increase metal availability in soil by re-distributing them from unavailable to available forms and low pH ( Table 2 ). A similar result was obtained by [ 8 ], who indicated that the application of VSC at a rate of 30 mL kg −1 soil increased (42%) the availability of Cd compared to the untreated soil. The dissolved organic matter binds to metals and forms stable aqueous complexes with metals such as Pb, Cu, Zn, and Mn [ 49 ]. El-Gabal El-Asfar soil showed the highest shoot Zn concentration than the other two soils. These findings might be due to low pH values in both soils and VSC that encourage the plant’s mobility and uptake of metals.

In general, ornamental plants selected for phytoextraction should be fast-growing, deep-rooted, and easily propagated [ 14 ]. Plant depends on one or more of the many mechanics for its resistance and/or tolerance to metallic stress such as selective absorption metals, metal retention in roots, bind to metal-related compounds within the cell, retaining the metal in the cell wall, and regulating the metal concentration inside the cell through cellular mechanisms [ 50 ]. When the remediation factor (RF) value ranging between 1 and 10, the plant is considered an accumulator, and higher than ten plants is considered a hyperaccumulator [ 51 ]. The results showed that the ability of A. tricolor plants to accumulate Pb and Zn varied with soil type. A. tricolor , irrigated with Loom-dye effluent water, showed high accumulations of Pb, Cd, Cr, Fe, Mn, Zn, and Cu [ 52 ], inferring its efficacy of phytoextraction capacity. Wang et al. [ 53 ] reported that functional divergence between indigenous plant species A. tricolor and invasive alien species Amaranthus retroflexus L. and explored the strong competitive intensity in A. retroflexus over A. tricolor under HM stress, inferring the impact of successful invasion process and adaptation to ecological selection pressure.

The result indicated that the VSC gave the highest Pb (6.40%) and Zn (3.26%) removed from El-Madabeg soil. This result may be because VSC can improve soil structure and water holding capacity, promoting the growth of A. tricolor plants [8,30). High salt content, low pH (4.5), and the dissolved organics of VSC ( Table 2 ) could be the reasons behind its high efficiency in mobilizing soil metals. Although, the EDTA showed the highest amount of absorbed Zn than other treatments, and the removal of Zn in El-Gabal El-Asfar soil decreases the plant biomass. Both the direct adverse action of EDTA as salt and its role in the increasing soil HMs bioavailability could negatively influence the plant performance. So, the reversible effect of EDTA on the plant growth in El-Gabal El-Asfar soil may decrease the dry matter, resulting in the reduction of RF for Zn. Conclusively, the detailed understanding of detoxification mechanisms employed by each OP for location specificity, distribution, and deposition of HMs in the cellular compartments such as cell walls, vacuoles, and metabolically inactive tissues have great concern as which plays a vital role in decreasing the free HMs concentrations [ 54 ].

5. Conclusions

The use of OPs is an eco-friendly technique that tends to clean up and accumulates HMs from contaminated soils. The efficacy of phytoremediation depends upon soil characteristics, available microbial types, their population size, and the phytoextraction efficiency of the plant species. Our results inferred that the application of organic materials increases fresh and dry weight while the degree of increment varied depends on the organic materials and soil types. El-Gabal El-Asfar soil showed the highest dry matter of the A. tricolor plants than other soils. The application of organic materials on the studied soils significantly increased Pb, Zn, and Cu uptake by A. tricolor plants compared to the control treatment. The removed metal amount is affected by the type of organic materials and soil type. In general, VSC was the most effective material for removing tested metals, especially in Gabal El-Asfar and El-Madabeg soil, while EDTA was the best effective in Helwan soil. The A. tricolor plants had a good ability to remove Pb than Zn and Cu, which was more evident in El-Madabeg soil treated with VSC. The difference in the amount of each metal removed from the different soils confirms our hypothesis due to the variation of soil properties. The identification of plant traits that contributed to enhancing phytoremediation in OPs is critical in uplifting phytoextraction capacity. In addition, the research gaps of exploring site-specific performances of OPs in phytoextraction, interaction with different chelators and beneficial soil micro-organisms, development of genetically modified OPs with enhanced detoxifying capacities, the improved function of antioxidants in detoxifying HMs while uptaking through root and foliage are of particular need to be filled. Moreover, the in-depth studies on HM-induced health risks to the human being, mainly when handling OPs are further investigated to minimize health hazards. According to our current study, using ornamental plants to remove mineral pollutants such as lead, zinc and copper from contaminated soil is more advantageous to minimize human health hazards because they avoid direct intoxication that could happen through edible plants. Thus, attention needs to be paid to bioavailability and uptake mechanisms of HMs and detoxification pathways to improve phytoextraction capacity in OPs in future studies. Also, extensive field experiments are necessary, especially in polluted soils near industrial areas, using these materials, particularly VSC, which has unique properties, that can be available in huge quantities. The in-depth experiments on mechanisms in cellular level HMs uptake and accumulation, signalling, and molecular events in OPs leading to phytoextraction are limited and need to be further explored to understand.

Acknowledgments

The authors extend their appreciation to Taif University for funding current work by Taif University Researchers Supporting Project number (TURSP-2020/295), Taif University, Taif, Saudi Arabia.

Author Contributions

Conceptualization, M.A. and M.A.E.-D., A.G., S.E.A.-M.; methodology, M.A., M.A.E.-D., A.G., S.E.A.-M.; software, M.A., M.A.E.-D.; validation, M.A., M.A.E.-D.; formal analysis, M.A., S.E.A.-M.; investigation, M.A. and M.A.E.-D., A.G., S.E.A.-M.; data curation, A.B., A.E.S., M.A. and M.A.E.-D.; writing—original draft preparation, M.A., M.A.E.-D., A.G., S.E.A.-M.; writing—review and editing, S.F., S.S.A., M.S., S.D., D.R., M.S.I., J.K., M.H.u.R., T.J., R.S., A.B., M.S.I., A.E.S. and funding acquisition, A.B., M.S., M.B., J.K. and A.E.S. All authors have read and agreed to the published version of the manuscript.

This research was funded by the EU-Project “NutRisk Centre” (No. CZ.02.1.01/0.0/0.0/16_019/0000845) and by Taif University Researchers Supporting Project number (TURSP-2020/295), Taif University, Taif, Saudi Arabia.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Informed consent was obtained from all subjects involved in the study.

Data Availability Statement

Conflicts of interest.

The authors declare no conflict of interest. The funders had no role in the study’s design; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

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Phytoremediation by ornamental plants: a beautiful and ecological alternative

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The Spectacular Rise of Ornamental Plants

Ornamental Plant Efficiency for Heavy Metals Phytoextraction from Contaminated Soils Amended with Organic Materials

M. A. El-Desoky

S. E. Abdel-Mawly

Disna Ratnasekera

Mohammad Sohidul Islam

Milan Skalicky

Alaa Baazeem

Saqer S. Alotaibi

Talha Javed

Rubab Shabbir

Muhammad Habib ur Rahman

Ayman EL Sabagh

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1. Introduction