Chemosphere 119 (2015) 662–667
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Foliar trichome-aided formaldehyde uptake in the epiphytic Tillandsia velutina and its response to formaldehyde pollution Peng Li a, Robert Pemberton b, Guiling Zheng a,⇑ a b
College of Resource and Environment, Qingdao Agricultural University, Qingdao 266109, China Florida Museum of Natural History, Gainesville, FL 32601, USA
h i g h l i g h t s Epiphytic Tillandsia plants were able to uptake a large amount of formaldehyde. Foliar trichomes of the leaves facilitated formaldehyde absorption in T. velutina. T. velutina absorbed formaldehyde more quickly in the first 2 h.
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Article history: Received 21 April 2014 Received in revised form 20 July 2014 Accepted 24 July 2014
Handling Editor: Caroline Gaus Keywords: Air plant Formaldehyde pollution Indoor air quality Phytoremediation
a b s t r a c t Epiphytic Tillandsia (Bromeliaceae) species have been found to be efficient biomonitors of atmospheric heavy metals and persistent organic pollutants, but have not been used to monitor or remove the primary indoor atmospheric pollutant formaldehyde (FA). The absorptive capacity of Tillandsia trichomes is wellestablished, but potential secondary effects of foliar trichomes on gas exchange remain unclear. Our study investigated whether Tillandsia species can absorb FA efficiently and if the leaf trichomes function to improve FA uptake, using Tillandsia velutina. Plants with intact trichomes, decreased FA concentration by 48.42% in 12 h from 1060 lg m3 to 546.67 lg m3, while FA concentration decreased only by 22.51% in the plants without trichomes. Moreover, the more trichomes removed from the leaves, the lower the capability of FA uptake per unit leaf area, which suggested that T. velutina was capable of absorbing a large amount of FA via the leaves and specialized trichomes facilitated the whole leaf tissue FA absorption. In addition, all plants exposed to FA were chloric, had a reduction in measured leaf chlorophyll, and an increment in permeability of plasma membranes. However, plants in which trichomes had been removed declined or increased more quickly than plants with intact trichomes, indicating Tillandsia leaf trichomes also give the leaves some protection against this toxin. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction Formaldehyde (FA), a high-volume chemical is ubiquitous in indoor environments due to both natural sources and anthropogenic activities. The capacity of plants to absorb and metabolize exogenous FA has promoted research on the efficiency of plants to remove FA in the atmosphere (Wolverton et al., 1984; Kim et al., 2008; Aydogan and Montoya, 2011; Wang et al., 2012). Plants have been shown to uptake air pollutants via their stomata during normal gas exchange (Schmitz et al., 2000) and various pollutants have been found to be sequestered or degraded, then transferred to other parts in the plant (Giese et al., 1994; Son et al., 2000). ⇑ Corresponding author. E-mail address: [emailprotected] (G. Zheng). http://dx.doi.org/10.1016/j.chemosphere.2014.07.079 0045-6535/Ó 2014 Elsevier Ltd. All rights reserved.
Epiphytic Tillandsia (Bromeliaceae) species, known as air plants, are very common in the American tropics (Benzing, 2000), and now cultivated worldwide, outdoors in warm regions and indoors in cold regions. Besides ornamental uses, Tillandsia species are also frequently used for biomonitoring of airborne trace metals because they absorb nutrients directly from the atmosphere by wet or dry deposition (Wannaz et al., 2006; Figueiredo et al., 2007; Vianna et al., 2011). Different species of Tillandsia have been used as biomonitors of many heavy metals, such as Hg, Pb, Cu, Zn, Co, Mn, and persistent organic pollutants PAH, PCB, PCDD and PCF in different countries (Brighigna et al., 1997; Calasans and Malm, 1997; Pignata et al., 2002; Cortés, 2004; Pereira et al., 2007). However, epiphytic Tillandsia species have not been used to monitor or remove the main indoor atmospheric pollutant FA. Stem and leaves of Tillandsia species are equipped with a dense foliar trichome cover. It has long been presumed that the foliar
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is due to the beautiful pink or red coloration that develops in the center of the rosette when the plant flowers, and also its seemingly magic ability to live in the air. In this study, T. velutina was selected for the study because its leaves are relatively broad and soft, making it easy to remove their trichomes. Foliar trichomes of T. velutina were hand removed to investigate the following hypotheses: (1) the epiphytic plant T. velutina can absorb FA efficiently; (2) foliar trichomes of T. velutina can improve FA uptake. 2. Materials and methods 2.1. Study species
Fig. 1. Leaf anatomy of Tillandsia species (from Benzing (2000)).
trichomes are a primary site of water and nutrient absorption from air moisture (Nowak and Martin, 1997; Ohrui et al., 2007). The most conspicuous feature of tillandsioid trichomes is an array of highly elongated cells known as the wing, which connects to the outermost series of shield cells (Fig. 1). The center of the shield is composed of central disc cells that are heavily cutinized on the distal surfaces but lack a cuticle on their lower surfaces where they connect to a series of living cells, known as the stalk (Benzing, 2000). The stalk cells form in essence a channel between the central disc cells and the mesophyll cells adjacent to the most proximal stalk cells or foot cells. The absorption of water and macronutrients by Tillandsia trichomes via stalk cells has been well documented and is undoubtedly a critical adaptation for plants inhabiting the epiphytic niche (Pierce et al., 2001; Benz and Martin, 2006; Papini et al., 2010). It has also been reported that foliar trichomes play an important role in absorbing pollutants. Filhoa et al. (2002) found that Hg was partly associated with atmospheric particles deposited upon the plant surface, but it was highly absorbed by the foliar trichomes and less absorbed by epidermal cells of T. usneoides. No Hg was detected in mesophyll parenchyma or in vascular system cells. When the plants of T. usneoides were soaked in the stable nuclide Cesium (133Cs) solutions, Cs was adsorbed on each type of cells in foliar trichomes, and the ratio of Cs in the internal disc cell was higher than that in ring cell and wing cell (Li et al., 2012). Although the absorptive capacity of Tillandsia trichomes has been well-established, potential secondary effects of foliar trichomes on gas exchange remain unclear and merit further investigation. Tillandsia velutina (Fig. 2A) is native to Mexico and Guatemala, but has been in the horticultural trade for a long time because it is one of the easily collectible plants from nature. Its popularity
T. velutina is now grown commercially on a wide scale, is inexpensive, sold by numerous vendors via the internet, and is perhaps the most commonly cultivated air plant in the world. The plants of T. velutina we chose for further experiment were grown under natural photoperiods in a greenhouse for 4 years. Day/night average temperatures were approximately 27/20 °C. Their leaf lengths were approximately 15–20 cm and root lengths about 4–5 cm. 2.2. Removal of foliar trichomes Fifteen T. velutina plants of similar size were randomly chosen for the trichomes removal study. They were divided into five groups in which 100%, 75%, 50%, 25% and 0% of the trichomes were removed, with three replicates per group. Foliar trichomes were removed with the adhesive tape method (Yamaura et al., 1992; Ohrui et al., 2007). The sticky side of adhesive tape was lightly pressed onto the adaxial and abaxial surfaces of a leaf five times each to remove trichomes. 2.3. Analysis of leave morphology of T. velutina To investigate the effect of FA on the leaf morphology of T. velutina, leaves with and without FA treatment were observed and photographed after 12 h when the experiment ended. Scanning electron microcopy (SEM) was used to examine potential effects of trichome removal on leaf surface morphology. Two mature leaves with and without trichomes were evaluated. Two mid-leaf sections from each leaf were fixed in 4% glutaraldehyde for 48 h, dehydrated with ethanol 30%, 50%, 70%, 80%, 90%, 100% (2 times) for 10 min respectively, coated with a 30 nm layer of gold palladium (Papini et al., 2010), then examined with SEM (Leica S440) at 20 kV. 2.4. Formaldehyde treatment and concentration measurement Following Wolverton et al. (1984), four clear glass chambers with dimensions of 60 cm3 and a wall thickness of 0.4 cm was used
Fig. 2. Plants of Tillandsia velutina: A. Before formaldehyde stress; B. after formaldehyde stress. Bar = 1 cm.
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the surface area of leaves was measured by a leaf area meter (WDY-500 A, measurement error is ±5 cm). In order to not remove many leaves of T. velutina, 3 sample leaves in the intermediate layer of one plant were taken and total 9 leaves were measured in each group. The surface area value for each plant was then multiplied by the number of the leaves. 3. Results and discussion 3.1. Leaf surface morphology
Fig. 3. Chamber used in the experiment.
in these experiments. One was for control and the other three for plant experiments. A 12 V DC fan inside the chamber promoted complete mixing of the air (Fig. 3). Window curtains were closed in the laboratory and incandescent lamps (full spectrum, wave lengths 380–780 nm) were on all the time to create similar light conditions. The room temperature was kept at 25 °C. Test plant was suspended in the middle of the chamber, in which a beaker with 1 ll FA solutions (40%) was placed, with a vertical string line attached to the top cover of the chambers with adhesive tape (Fig. 3). The formaldehyde levels in the chambers were measured every 2 h with a formaldehyde monitor (IST IQ350, USA) during a 12 h period (10:00–22:00). A hole was made in one side glass for the entry of the formaldehyde monitor probe (Fig. 3). A rubber stopper was used to plug the hole before measuring formaldehyde concentrations. The probe was inserted into the chamber through a port in the stopper, keeping from leakage. 2.5. Measurement of leaf chlorophyll content and the permeability of plasma membrane After treatments, leaves were harvested and ground into fine powder in liquid nitrogen, and leaf chlorophyll (Chl) was extracted with 95% ethanol. Chl content was measured as described previously (Strain et al., 1971) and expressed on a dry weight basis. The permeability of plasma membrane was determined by measuring leaf relative electronic conductivity with the conductivity meter (sensION + EC7, USA). Each treatment had three replicates.
T. velutina has velvety leaves due to its dense trichome covering on the leaves. Plants in the FA treatments exhibited a slight chlorosis and bleaching of the leaves (Fig. 2B), while no visible changes were observed in the leaves of the control plants (Fig. 2A), indicating a visible loss of Chl in leaves due to FA stress. The foliar trichomes of T. velutina are made up of many long, outermost wing cells, eight middle ring cells and four inner disc cells (Fig. 4A and C). After removal with adhesive tape, almost no trichome wings remained on the leaf surface (Fig 4B), ring cells and disc cells were also removed, so no distinct cell structure was remained on the leaf surface (Fig. 4D). In addition, epidermal cells could be found after trichome wings were removed. These epidermal cells had thick walls and were tightly packed. However, stomata were rare and not found to be open after removal of trichome wings (Fig. 4B). 3.2. Effect of trichomes removal on the normal physiological processes 3.2.1. Effect on permeability of the plasma membrane The permeability of the plasma membrane is the rate of passive diffusion of molecules through the membrane. Relative electronic conductivity is a measure of membrane permeability, with higher conductivity indicating an increment in permeability. The relative electrical conductivity was 48.88% ± 0.94 in the plants with trichomes, which was a little higher than in plants which the trichomes were removed (Table 1). Statistical analysis showed that conductivities among different treatments were not significantly different (One-way ANOVA analysis, F = 1.057, P = 0.427). This suggests that trichome removal had no significant effect on gas diffusion in the leaves. However, after FA stress, the relative electronic conductivity in every group increased (Table 1), which suggests that FA impacted gas exchange. In plants with all trichomes removed, their relative electronic conductivity increased from 44.05% to 66.86%, an average percentage increase of 22.8%. In contrast, the relative electronic conductivity of plants with trichomes increased from 46.88% to 52.81%, an average percentage increase of 5.93%. One-way ANOVA analysis found that plants with and without trichomes were significantly different (F = 33.035, P < 0.001), which indicated that foliar trichomes delayed the relative electronic conductivity increase.
2.6. Data analysis FA concentrations were expressed as micrograms per cubic meter (lg m3). Percent removal efficiency in each case was evaluated using the initial and final gas concentrations within the chamber and was calculated as:
ðC 0 C F Þ=C 0 100% The amount of FA removed per unit surface area of plant leaf was calculated as:
ðC 0 C F Þ=A where C0 is initial concentration (lg m3), CF is final concentration (lg m3), and A is total leaf area (cm2). To facilitate comparisons,
3.2.2. Effects on chlorophyll content Before FA stress, the total Chl content of plants with intact trichomes was significantly higher (0.89 ± 0.06 mg/g) than those plants without trichome wings or those with 3/4 of trichome wings removed. One-way ANOVA analysis showed the total Chl content among different treatments was also significantly different (F = 8.442, P = 0.003), indicates that trichome removal affects Chl content. This would be expected because some chlorophyll is in the trichome wing cells, and leaf pubescence has a significant effect on photosynthesis through increased light reflectance (Ehleringer, 1984). After FA stress, the Chl content of all plants decreased (Table 2), correspondent with the chlorosis in leaves (Fig. 2 B), which sug-
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Fig. 4. Leave surface of Tillandsia velutina with SEM: A. Leaf surface before trichomes removal; B. leaf surface after trichomes removal; C. trichome showing wing cells, ring cells and disc cells; D. trichome after wing cells removed. Bar = 100 lm in A and B, bar = 10 lm in C and D.
Table 1 Changes of relative electronic conductivity of Tillandsia velutina under formaldehyde stress. Treatments
Removal of all trichomes Removal of 3/4 trichomes Removal of 1/2 trichomes Removal of 1/4 trichomes No removal of trichomes
Relative electronic conductivity(% ± SD) Before formaldehyde stress
After formaldehyde stress
Percentage of increase
44.05 ± 3.82a 46.88 ± 7.59a 42.44 ± 4.98a 46.87 ± 3.02a 46.88 ± 0.94a
66.86 ± 2.32a 64.73 ± 2.55a 64.01 ± 8.34a 58.73 ± 5.41ab 52.81 ± 12.20b
22.80 ± 1.27a 17.85 ± 1.1ab 17.14 ± 1.62ab 17.29 ± 2.31ab 5.93 ± 0.94b
Notes: Different small letters mean significant difference among different treatments at 0.05 level.
Table 2 Changes of total Chlorophyll content of Tillandsia velutina under formaldehyde stress. Treatments
Removal of all trichomes Removal of 3/4 trichomes Removal of 1/2 trichomes Removal of 1/4 trichomes No removal of trichmoes
Chlorophyll content (mg g1 ± SD) Before formaldehyde stress
After formaldehyde stress
Percent decrease
0.59 ± 0.06a 0.67 ± 0.04a 0.73 ± 0.07ab 0.75 ± 0.04ab 0.89 ± 0.06b
0.38 ± 0.08a 0.58 ± 0.04ab 0.65 ± 0.07bc 0.68 ± 0.05bc 0.73 ± 0.06d
17.30 ± 5.04a 9.53 ± 1.473b 8.03 ± 7.33b 7.70 ± 3.30b 9.43 ± 5.52b
Notes: Different small letters mean significant difference among different treatments at 0.05 level.
gests that FA influences the formation of chlorophyll. However, the Chl content in plants with all trichomes removed declined quickly from 0.59 mg g1 to 0.38 mg g1, a 17.3% reduction. This is significantly higher than in plants with trichomes, indicating that the foliar trichomes protect chlorophyll loss caused by FA damage. FA is toxic to plants even at low concentrations. Li et al. (2002) demonstrated that exposure to 0.2–0.4 mM FA notably inhibited root elongation and growth of Arabidopsis. Recent studies showed that most leaves of Arabidopsis, tobacco and geranium became yellow and necrotic when exposed to a high concentration of gaseous FA (Chen et al., 2010; Song et al., 2010). Similarly, almost all of T. velutina leaves were bleached (Fig. 2 B) and Chl content and relative electronic conductivity decreased significantly after a 12 h exposure to FA (Tables 1 and 2). These observations suggest that
chlorosis and plasma membrane permeability were probably symptoms of severe FA stress. However, a dense trichome layer may function to protect underlying tissues from damage due to FA stress. Dense trichomes are known protect leaves from ultraviolet radiation, high visible irradiance and radioactivity (Karabourniotis and Bornman, 1999; Nagata et al., 1999). 3.3. Formaldehyde uptake The initial FA concentrations in different chambers were about 1000 lg m3, not significantly different between treatments (Table 3, One-way ANOVA analysis, F = 2.047, P = 0.143). The final FA concentrations after different treatments, however, changed significantly from 546.67 lg m3 to 943.33 lg m3 (One-way ANOVA analysis, F = 34.696, P < 0.001).
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Table 3 Characteristics of epiphyte Tillandsia velutina and formaldehyde absorption. Treatments
Initial FA concentration (lg m3)
Final FA concentration after 12 h (lg m3)
Percentage of removal efficiency (%)
Leaf area (cm2)
Ability of absorbing formaldehyde (lg m3 cm2)
Control Removal of all trichomes Removal of 3/4 trichomes Removal of 1/2 trichomes Removal of 1/4 trichomes No removal of trichomes
1053.33 ± 24.94a 1050.00 ± 24.49a 983.33 ± 26.25a 1030.00 ± 37.42a 1020.00 ± 37.42a 1060.00 ± 8.17a
943.33 ± 20.55a 848.67 ± 15.17b 623.33 ± 30.91c 656.67 ± 16.99c 646.67 ± 66.50c 546.67 ± 30.91c
10.44 ± 0.64a 22.51 ± 2.15b 36.61 ± 2.73c 36.16 ± 2.87c 36.73 ± 4.45c 48.42 ± 2.99d
– 848.67 ± 15.17a 910.67 ± 44.97a 900 ± 43.205a 856.67 ± 16.99a 853.333 ± 49.889a
– 0.28 ± 0.04a 0.40 ± 0.03ab 0.42 ± 0.06ab 0.44 ± 0.05b 0.60 ± 0.06c
Notes: Results represents means ± SD. Different small letters mean significant difference among different treatments at 0.05 level.
Formaldhyde concentrations (µg m-3)
1100
1000
900
800
700
600
500
2
4
6
8
10
12
14
Time after initial exposure (h) No trichome
1/4 trichome
1/2 trichome
3/4 trichome
All trichome
Fig. 5. Variation of formaldehyde concentrations in chambers after different degrees of trichome removal in Tillandsia velutina.
0.8
Formaldhyde removal (µg m-3 cm-2 )
FA concentration in control chambers (i.e. without plants) had initial concentration of 1053 lg m3 and final of 943 lg m3 after 12 h, a 10.3% decrease (Table 3). This was apparently due to leakage, absorption, and chemical reactions with the chamber surfaces. Aydogan and Montoya (2011) reported similar values of FA loss. In contrast, the FA concentration in chambers with plants, with and without trichomes decreased by at least 22.51%, significantly higher than the control plants (One-way ANOVA analysis, F = 42.988, P < 0.001). Changes of FA concentrations in the chambers with different plants were also significantly different (One-way ANOVA analysis, F = 17.2, P < 0.001). For plants with all trichomes, the FA concentration decreased by 48.42% from 1060 lg m3 to 546.67 lg m3. For plants with all trichomes removed, the FA concentration decreased from 1050 lg m3 to 848.67 lg m3, by 22.51%. For plants with part of the trichomes removed, the percentage of FA removal efficiency was around 36% (Table 3), and there were no significantly difference between groups. FA concentrations in the chambers with plants declined continuously within the first 8 h (Fig. 5). After that, the FA concentrations tended to be stable, or increased slightly in plants without trichomes or with half trichomes. The degree of decrease in FA concentrations in plants was related to amount of trichome tissue removed (intact 1/4 and 3/4) (Fig. 5). Interestingly, the changes in FA concentrations were not same early in the 8 h period. During the first 2 h, the concentration declined much more rapidly in all treatments (Fig. 5). Correspondingly, the capability of trichomes to lower formaldehyde concentration per unit leaf area increased continuously during the first 8 h (Fig. 6), due to the similar size (One-way ANOVA
0.7 0.6 0.5 0.4 0.3 0.2 0.1 0 0
2
4
6
8
10
12
14
Time after initial exposure (h) No trichome
1/4 trichome
1/2 trichome
3/4 trichome
All trichome
Fig. 6. Formaldehyde removal per unit leaf area in Tillandsia velutina.
analysis, F = 1.229, P = 0.359) of plants used. The more trichome wings removed, the lower the capability of removing formaldehyde per unit leaf area was (Fig. 6). Those plants with intact trichomes could adsorb FA 0.60 ± 0.06 lg m3 cm2, while those without trichomes adsorb FA only 0.28 ± 0.05 lg m3 cm2 (Table 3). One-way ANOVA analysis showed that control plants with intact trichomes was significantly different from those with trichomes removed (F = 11.973, P = 0.001). However, plants with all trichomes removed were not significantly different from those with 1/2 and 3/4 trichome removal although the value was lower than them, while different from plants with 1/4 trichomes removed (Table 3). The data demonstrated that the epiphytic T. velutina was capable of absorbing a large amount of FA via the leaves. Plants with intact trichomes, decreased the FA concentration by 48.42% in 12 h (Table 3), declining more rapidly during the first 2 h (Fig. 5). This removal efficiency was comparable to Scindapsus aureus and Syngonium podophyllum, which could remove 50% FA in 6 h and 61–67% FA in 24 h (Wolverton et al., 1984). However, FA concentration reduction by Chlorophytum elatum var. vittatum and other plant species declined rapidly in the first 6 h (Wolverton et al., 1984) compared to 2 h in T. velutina. Therefore, T. velutina absorbs FA more quickly than in other studied plants. The ability of Tillandsia species adsorbing water and nutrients through the leaves directly from the ambient air enables them to absorb air pollutants rapidly. Because of this ability Tillandsia species are used to monitor different heavy metals and organic pollutants (Brighigna et al., 1997; Calasans and Malm, 1997; Pignata et al., 2002; Cortés, 2004; Pereira et al., 2007). This adsorbing ability enables them to uptake air pollutants including FA effectively and rapidly. The present study demonstrates that the specialized trichomes densely covering Tillandsia leaves facilitate whole leaf tissue
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absorption of FA (Fig. 5). The FA-uptake capacity of plants is indeed dependent on the number of intact trichomes, as demonstrated the removal of trichomes experiments in this study (Fig. 6). Generally, exogenous FA is adsorbed by plants through stomata and cuticle, further permeation into the tissue can then alter metabolic processes within the leaf (Giese et al., 1994; Schmitz et al., 2000). However, in T. velutina the stomata are covered by the dense trichomes and the stomata were rarely open even after trichomes were removed (Fig. 4). Stomata open generally at night in plants with the crassulacean acid metabolism (CAM) (Martin, 1994). A 50% decrease in stomatal conductance was observed when Ficus benjamina was exposed to 0.05 ppm FA under realistic polluted indoor conditions (Schmitz et al., 2000). In T. velutina, stomatal density is lower, and length and width are much smaller than those of terrestrial plants plants, as well as in many other bromeliads (Martin, 1994). Therefore, the boundary layer formed by trichomes is but one component of the conductance or resistance pathway for gas diffusion. FA may be also diffused through partially open stomata and cuticle. The trichome stalk may be another diffusion pathway with less resistance and thus facilitate FA uptake throughout the day while stomata are closed. A positive correlation between maximum rates of CO2 uptake and leaf trichome cover was found to be statistically significant in 12 species of Tillandsia (Benz and Martin, 2006). The hydrophobic trichome layers and epicuticular wax may minimize absorbed FA loss to the external environment, as diffusion across this waxy layer must overcome a high level of resistance (Nobel, 1999). Therefore, leaf trichomes reduce absorbed FA loss from leaf tissues by serving as a physical barrier. Acknowledgements This study was funded by Qingdao Science and Technology Program (14-2-4-46-jch) and Doctoral Foundation of Qingdao Agricultural University (No. 1351). References Aydogan, A., Montoya, L.D., 2011. Formaldehyde removal by common indoor plant species and various growing media. Atmos. Environ. 45, 2675–2682. Benzing, D.H., 2000. Bromeliaceae: Profile of An Adaptive Radiation. Cambridge University Press. Benz, B.W., Martin, C.E., 2006. Foliar trichomes, boundary layers, and gas exchange in 12 species of epiphytic Tillandsia (Bromeliaceae). J. Plant Physiol. 163, 648– 656. Brighigna, L., Ravanelli, M., Minelli, A., Ercoli, L., 1997. The use of an epiphyte (Tillandsia capuy-medusae morren) as bioindicator of air pollution in CostaRica. Sci. Total Environ. 198, 175–180. Calasans, C.F., Malm, O., 1997. Elemental mercury contamination survey in a chloralkali plant by the use of transplanted Spanish moss, Tillandsia usneoides (L.). Sci. Total Environ. 208 (3), 165–177. Chen, L.M., Yurimoto, H., Li, K.Z., Orita, I., Akita, M., Kato, N., Sakai, Y., Izui, K., 2010. Assimilation of formaldehyde in transgenic plants due to the introduction of the bacterial ribulose monophosphate pathway genes. Biosci. Biotechnol. Biochem. 74, 627–635. Cortés, E., 2004. Investigation of air pollution in Chile using biomonitors. J. Radioanal. Nucl. Chem. 2629 (1), 269–276. Ehleringer, J., 1984. Ecology and ecophysiology of leaf pubescence in North American desert plants. In: Rodriguez, E., Healey, P.L., Mehta, I. (Eds.), Biology and Chemistry of Plant Trichomes. Plenum, New York, pp. 113–132. Figueiredo, A.M.G., Nogueira, C.A., Saiki, M., Milian, F.M., Domingos, M., 2007. Assessment of atmospheric metallic pollution in the metropolitan region of São
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