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Kays, S.J. 2011. Phytoremediation of indoor air – Current state of the art. pp. 3-21, In: The Value Creation of Plants for Future Urban Agriculture, K.J. Kim (ed.), Nat. Inst. Hort. Herbal Science, RDA, Suwon, Korea.

Phytoremediation of Indoor Air – Current State of the Art Stanley J. Kays University of Georgia Athens, Georgia 30602-7273 USA

Phytoremediation Phytoremediation of indoor air utilizes plants to remove or neutralize environmental contaminants such as volatile organic compounds (VOCs) in the air of homes, offices and other enclosed buildings. Certain plant species, working in tandem with yet unidentified microorganisms in the root zone, have the ability to remove VOCs and purify the air. Hundreds of VOCs have been identified as indoor contaminants (ACGIH, 1995; EPA, 1989; Won et al., 2005). For example, the U.S. Environmental Protection Agency (EPA) reported detection of more than 900 VOCs in the air of public buildings (EPA, 1989). In a Finnish study, over 200 VOCs were identified in each of 26 homes (Kostiainen, 1995). An example of the types of volatiles that might be encountered is presented in Table 1 which lists the VOCs found in two houses surveyed in Athens, Georgia that had serious air quality problems. The volatiles in the first house were emanating from toxic drywall and in the second from insulation that had been blown into the air space within the outside walls. Indoor air in cities has been reported to be as much as 5 to 1000 times more polluted than exterior air (Brown et al., 1994; Godish, 1995; Kostianen, 1995; Brown, 1997; Ingrosso, 2002; Yang et al., 2004; Zabiegała, 2006). The chemicals are absorbed into human and animal bodies through inhalation and in some instances, through direct penetration of the skin (McDougal et al., 1990). While the initial work on phytoremediation of indoor air was done in the 1970s, it has not been until recently that interest in the subject has spread. Currently, the leading research programs are in South Korea. To date, a significant portion of the research has been directed toward identifying superior phytoremediation species of indoor plants. While the results have been very positive, the lack of adequate funding has impeded exploring the basic mechanisms operative and making the transition from the laboratory to real world homes and offices. As a consequence, what we currently know is vastly exceeded by what we do not, a situation that is evident from, for example, the very limited number of VOCs that have been tested. The public has displayed tremendous interest in the potential of phytoremediation and there is a growing awareness of the serious health issues arising from breathing polluted indoor air. Four popular books on the subject are currently available (Son, 2004; Son, 2009; Wolverton, 1996; Wolverton and Takenaka, 2010).

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History In the early 1970s, NASA began monitoring the atmosphere inside spacecraft during manned Skylab missions. Since the spacecraft is a tightly sealed space, volatiles given off from materials and humans began to build up once the chamber was closed. During Skylab III, over 300 compounds were found in the air. It was evident from changes in the composition of the air that the quality deteriorated with time and that a means of removing undesirable volatiles was needed. Studies on a cross-section of methods of purifying the air within the spacecraft were undertaken and in 1984 the first, detailing the ability of indoor plants to remove VOCs in sealed chambers, was published (Wolverton et al., 1984). During this time, there was a growing body of research published on the role of VOCs in the declining air quality of homes, offices, and other buildings. The initial research on phytoremediation led to a relatively small number of subsequent studies on the potential of indoor plants to remove volatile pollutants. In nearly all instances, the research was done in closely controlled laboratory settings with the aim of subsequently testing species with superior phytoremediation potential in realworld settings to alleviate symptoms of “sick building syndrome” and in homes and offices where it is not evident that air quality has been compromised (i.e., the absence of distinct physical symptoms in the occupants). Plants Tested A cross-section of species have been assessed for their phytoremediation potential with most being indoor plants that are adapted to low light conditions. A partial list of plants is found in Table 2. While the assumption is that these plants will be used in homes and offices where the light intensity and quality differ markedly from sunlight, many of the phytoremediation tests have been conducted at light intensities that are appreciably higher than might be expected in homes. VOCs Tested Of the 900 VOCs listed as indoor pollutants by the EPA, only a very small crosssection have been tested for their ability to be removed by indoor plants. These include: acetone (Oyabu et al., 2003; Tani and Hewitt, 2009); benzene (Cornejo et al., 1999; Liu et al., 2007; Orwell et al., 2004; Tarran et al., 2007; Wolverton, 1986; Yang et al., 2009; Yoo et al., 2006); benzaldehyde (Tani and Hewitt, 2009); n-butyraldehyde (Tani and Hewitt, 2009); iso-butyraldehyde (Tani and Hewitt, 2009); crotonaldehyde (Tani and Hewitt, 2009); formaldehyde (Aydogan and Montagu, 2011; Chen et al., 2010; Kim et al., 2008; Kim et al., 2010; Oyabu et al., 2003; Sawada and Oyabu, 2008; Son et al., 2000; Wolverton et al., 1984; Wolverton, 1986; Xu et al., 2011); methacrolein (Tani and Hewitt, 2009); methyl ethyl ketone (Tani and Hewitt, 2009); diethyl ketone (Tani and Hewitt, 2009); methyl n-propyl ketone (Tani and Hewitt, 2009); methyl iso-propyl ketone (Tani and Hewitt, 2009); methyl isobutyl ketone (Tani and Hewitt, 2009); octane (Yang et al., 2009); pentane (Cornejo et al., 1999); α-pinene (Yang et al., 2009); propionaldehyde (Tani and Hewitt, 2009); toluene (Cornejo et al., 1999; Kim et al., 2011; Orwell et al., 2006; Sawada and Oyabu, 2008; Yang et al., 2009; Yoo et al., 2006);

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trichloroethylene (Wolverton, 1986; Yang et al., 2009); xylene (Cornejo et al., 1999; Orwell et al., 2004; Sawada and Oyabu, 2008; Wolverton, 1993). In some instances, assessment has been only cursory. The methods utilized in a number of the studies differ widely and the clarity and thoroughness of their description insufficient to make meaningful comparisons among studies. Likewise, the list of VOCs represents only a very small fraction of the number of volatiles encountered in the indoor air of homes and offices. Rate of VOC Removal Assessing indoor plants for phytoremediation efficiency involves comparing the purification capacity among species under standard conditions. As one might anticipate, there are distinct differences in removal rate among plant species. For example, comparing a cross-section of orchids, the formaldehyde removal efficiency of Sedirea japonicum (L. Linden & Rchb. f.) Garay & H.R. Sweet was the highest while Cymbidium sp. was the lowest of the species tested (Kim and Lee, 2008). Table 3 lists the highest and lowest rates of removal from a selection of phytoremediation research papers after conversion to a standard measure (e.g., µg m-3 m-2 h-1). The rate of removal varied substantially among experiments, initial VOC concentration, plant species, and the VOC in question (Table 3). Formaldehyde removal ranged from 95 to 18,582 µg mg-3 m-2 h-1, benzene from 1,281 to 44,843 µg mg-3 m-2 h-1, toluene from 22 to 928 µg mg-3 m-2 h-1 and hexane from 15,292 to 168,000 µg mg-3 m-2 h-1. It is doubtful, however, if valid comparisons can be made among experiments due to differences in methods. Concentrations, for example, ranged from 0.15 to 100 ppm and data from Wolverton et al. (1984) indicates a marked increase in removal rate between 14 and 37 ppm formaldehyde for the same species. The half-life (time required for 50% removal) is occasionally used as an indicator of the purification capacity of a plant and allows comparing the efficiency among species under standardized conditions (Kim et al., 2008; Orwell et al., 2006; Oyabu et al., 2003). In contrast, expression of VOC removal rate based on leaf area per unit time (µg m-3 m-2 h-1) is considered superior in that it allows comparing different experiments and plants of varying size, the latter being essential for determining the number of plants needed for specific indoor environments. Microorganisms It is now well established that microorganisms, in particular bacteria, in the media are a critical part of the phytoremediation response (Chun et al., 2010; Wolverton and Wolverton, 1993; Wood et al., 2002). Their role is important since they are more likely to be able to effectively metabolize the diverse range of chemical pollutants found in indoor air. The microbe populations are comprised of a number of organisms, the specific composition and/or gene expression of which are thought to be capable of shifting in response to the prevailing volatile composition. The ability to change adds tremendous flexibility to the phytoremediation response. It is important to note that at this time we know virtually nothing about the organisms involved: species/strains present, population dynamics, changes in gene expression in response to specific VOCs, sensitivity to VOCs,

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relationship to the plant and a seemingly endless list of other questions. The fact that certain microorganisms found in the growing media of potted-plants are involved in the removal of VOCs is demonstrated by the fact that when the plant(s) are removed from the media, the VOC concentration continues to decrease (Godish and Guindon, 1989; Wolverton et al., 1989; Wood et al., 2002) and plants held in the dark also remove VOCs (Orwell et al., 2004; Wolverton et al., 1984; Yoo et al., 2006). Media with plants removed formaldehyde faster than the media alone and media that formerly had plants, removed more formaldehyde than sterilized media. Media bacterial counts varied with the plant species from which they were isolated (Sansevieria trifasciata Prain. > Kalanchoe sp. > Ficus benjamina L. > Spathiphyllum sp.) (Wolverton and Wolverton, 1993). The addition of selected microbe populations to the media also increases the rate of VOC removal (Chun, et al., 2010). In addition, removal efficiency of the media increased (~7-16%) with increased VOC exposure frequency (Kil et al., 2008) suggesting an apparent stimulation of the organisms. Bacterial populations within pots of Howea forsteriana (C. Moore & F. Muell.) Becc., for example, could remove benzene and hexane even after the plant and roots were removed and a cultured isolated bacterial population applied to a sterile media (vermiculite) could likewise metabolize the two volatiles (Wood et al., 2002). Unused media (i.e., never having had plants) could also remove benzene with removal increasing after an initial lag period of around 5 days. Significant changes in the overall population of microbes (expressed as bacterial colony-forming units per g potting soil) in response to exposure to benzene were not found. Since the microbes may vary with the plant species growing in the media, Chun et al. (2010) isolated the bacterial populations from media in which 9 different plant species were growing. The ability of isolated bacteria populations to remove benzene and toluene varied with the VOC in question. When the populations growing on a culture medium were exposed to VOCs, there were significant differences in the rate of removal of the volatiles. Adding bacterial populations back to the media of Pachira aquatica Aubl., Ficus elastica Roxb. ex Home. and Spathiphyllum wallisii Regel, the isolate had a significant impact on the removal of benzene, toluene and xylene (Chun et al., 2010). The root-zone also eliminates a substantial amount of formaldehyde (Kim et al., 2008). VOC removal efficiency is known to vary with the microbe population present, the type and concentration of VOCs, plant species, potting media, and other factors. Plants excrete into the root zone significant amounts of carbon that stimulates the development of microorganisms in the rhizosphere (Kraffczyk et al., 1984; Schwab et al., 1998) and appears to be important in maintaining a viable population. The phyllosphere is also colonized by a diverse array of microorganisms (Mercier and Lindow, 2000). Therefore, rhizospheric and phyllospheric microorganisms, as well as stomate-mediated absorption, provide a means of biofiltration of VOCs from indoor air. It is evident that our understanding of rhizospheric and phyllospheric biology relative to the removal of VOCs is exceedingly limited and hinders the development of biological processes for indoor air VOC removal (Guieysse et al., 2008). A better understanding is essential for optimizing removal efficiency. Contribution of the Plant versus Microbes

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The root-zone eliminates a substantial amount of formaldehyde during both the day and night. The ratio of removal by aerial plant parts versus the root-zone was approximately 1:1 during the day and 1:11 at night (Kim et al., 2008). Wolverton and Wolverton (1993) found that the top to media ratio varied with the species of plant and the VOC in question. Dieffenbachia maculata (Lodd. et al.) G. Don 1 and Nephrolepis exaltata (L.) Schott had similar ratios (~1:1 aerial plant parts : root zone) for xylene while ratios for formaldehyde favored the root zone (37:63 Diffenbachia sp. to 40:60 Aglaonema sp.). While a number of soil microorganisms are capable of degrading toxic chemicals (Darlington et al., 2000; Wolverton et al., 1989), few that are directly associated with formaldehyde removal have been identified. VOC Stimulation of Phytoremediation Phytoremediation efficiency of many plant species increases with exposure to VOCs (Kil et al., 2008; Kim et al., 2011; Orwell, et al., 2004), however, the mechanism(s) controlling the response is not known. The increase in efficiency in response to toluene appears to be relatively widespread in the plant kingdom (Kim et al., 2011), though such changes in efficiency have only been demonstrated for a small number of VOCs to date. Changes in phytoremediation efficiency in response to toluene exposure (1.3 ppm) occurred quite rapidly (i.e., Nephrolepis exaltata (L.) Schott > Sanservieria trifasciata Prain) in the removing the VOCs and their removal efficiency varied with the volatile in question. The observed increases in efficiency could have been mediated through an effect on the microbe population and/or the plant itself through altered gene expression. They could also be due to a change in the population of microbes that effectively metabolize toluene and presumably derive a benefit from its presence. The rapid rate of increase in toluene removal efficiency is likely faster than could be accounted for by an increase in beneficial microbe populations (i.e., in some instances, up to a 6-fold increase in efficiency occurs). Regardless of the cause, increasing the removal efficiency of VOCs is advantageous to the phytoremediation process in general and a better understanding of 1

D. maculata is a synonym of Dieffenbachia seguine (Jacq.) Schott var. seguine.

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the mechanism(s) responsible for this increase may enable end-users to take full advantage of the response.

Enhancing Phytoremediation Efficiency There are a number of possible avenues for enhancing phytoremediation efficiency in plants. Pretreating the media with microorganisms selected for their ability to remove certain targeted VOCs is one possibility. Alternatively, since the VOCs encountered vary widely among buildings, it may be essential to enhance the rhizosphere with a cross-section of specific microorganism isolates. Another approach for increasing the phytoremediation potential of indoor plants is through transgenic technology. Two examples have been reported thus far for facilitating the removal of formaldehyde: 1) over expression of a glutathione-dependent HCHO dehydrogenase (FALDH) pathway found in plants (Achkor et al., 2003) and 2) the introduction of a bacterial ribulose monophosphate (RuMP) pathway (Chen et al., 2010). In the former, an enzyme for formaldehyde oxidaion, glutathione-dependent formaldehyde dehydrogenase, is over expressed. FALDH plants, however, remain sensitive to formaldehyde and the system requires the addition of glutathione as a cofactor and regeneration systems for the reduced gluthathione and NAD+. The latter system, however, utilizes a gene from a methylotroph, an microorganism that utilizes one carbon compounds (e.g., methane, formaldehyde) as its carbon source (Yurimoto et al., 2005; Kato et al., 2006; Yurimoto et al., 2009.). The RuMP pathway, like the CalvinBenson pathway, fixes the single carbon unit to ribulose phosphate. In each case fructose6-phosphate cycles back to ribulose phosphate through a series of rearrangement reactions. Therefore the CO2 fixation steps in the Calvin-Benson pathway are bypassed in the RuMP pathway by 3-hexulose-6-phosphate synthase (HPS) and 6-phospho-3hexuloisomerase (PHI) catalyzed reactions (Chen et al., 2010). Two superior constructs (rmpA and rmpB) were found and when regenerated Arabidopsis thaliana (L.) Heynh. plants were crossed, the AB7 hybrid displayed far greater insensitivity to high levels of formaldehyde that either parent or transgenic FALDH plants. Removal of formaldehyde by the RuMP transgenic plants was estimated to be enhanced by around 20%. While these first transgenic plants with enhanced phytoremediation potential are only capable of removing C1 VOCs, the potential for adapting this approach to other VOC metabolizing pathways is attractive. It is thought that transgenic house plants might be more acceptable to the general public than transgenic food plants (Chen et al., 2010) VOC Considerations A range of questions involving the interaction of VOCs with the plant, microbes, and other volatiles remain to be addressed. a. Fate of VOCs – Little is known about the fate of VOCs during phytoremediation. Giese et al. (1994) demonstrated that the leaves of spider plant Chlorophytum comosum (Thunb.) Jacques exposed to 7.1 [mu]L L-1 (8.5 mg m-3) gaseous [14C]-formaldehyde could absorb the volatile and metabolize it to carbon dioxide.

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Radioactivity was found to be incorporated into organic acids, amino acids, free sugars, and lipids as well as cell-wall components. Formaldehyde appears to be efficiently detoxified by oxidation and subsequent C1 metabolism. The volatile is also known to be removed by microorganisms in the media. The mechanism of uptake, degree of adsorption versus absorption, and plant/microbe species differences in processing for a number of critical VOCs await similar isotope experiments. b. VOC concentration effects and toxicity to the plant and microbes – The linearity of the phytoremediation response, upper and lower VOC concentration limits for phytoremediation, changes in removal efficiency with concentration, and the concentrations at which plant and microbe toxicity effects occur are not known. Toxicity can be determined by assessing the development of visual symptoms. Likewise, a crosssection of physiological responses (photosynthetic, respiratory and transpiration rates, stomatal conductance and intercellular CO2) have been measured before and after exposure to benzene (1.0 ppm), toluene (1.0 ppm) or both volatiles (0.5 ppm each) to assess possible deleterious effects to the plant (Yoo et al., 2006). There were significant differences in each of the parameters. For example, the photosynthetic rate decreased when exposed to either benzene or toluene and even more so when exposed to both simultaneously. While the treatments did not produce symptoms of physical damage, it is probable that at certain concentration × exposure duration combinations, damage to the plant and/or beneficial microbes will occur. c. Effect of multiple VOCs – When assessing removal by the aerial portion of the plant, the VOC removal efficiency of both benzene and toluene (0.5 ppm each) was reduced both during the day and the night by the presence of the other volatile (Yoo et al., 2006). The removal efficiency of Cissus rhambifolia Vahl. was the least effected of the 4 plant species tested while Syngonium podophyllum Schott was the most. Day and night rates of benzene removal by C. rhambifolia were reduced 27 and 18% respectively when toluene was present, while toluene removal was reduced 38 and 56% when benzene was present. While the rates will no doubt change markedly when the entire plant is exposed, the effect of one VOC on another is indicative of an interaction or competition among VOCs. Cornejo et al. (1999) found that benzene but not toluene was removed when both gasses were applied simultaneously (Kalanchoe blossfeldiana Poelln.). Yoo et al. (2006) in contrast found that most species could remove both gases, with toluene being removed more effectively than benzene (e.g., toluene was double that of benzene in Hedera helix L.). d. Synthesis of VOCs by the plant – Plants release a large number of VOCs into their environment and in some cases a considerable volume [e.g., 6 Tg y-1 of isoprene are produced by trees and shrubs (Guenther et al., 2006)]. Three primary pathways (isoprenoid, shikimic acid, and the oxidative cleavage and decarboxylation of various fatty acids) are responsible for the synthesis of many of the volatile compounds (Dudareva et al., 2004; Kays and Paull, 2004). House plants also emit VOCs, however, the rate of synthesis is relatively low such that they are not considered to represent a health problem. The fragrance of flowers and the aroma of an apple pie represent benign

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and generally pleasurefull VOCs. The volatiles emitted from 4 species of house plants (Chrysalidocarpus lutescens Wendl., Ficus benjamina L., Sansevieria trifasciata Prain, Spathiphyllum wallisii Regel) were identified by Yang et al., (2009). Included were (-)alloaromadendrene, butyl butyrate, caryophyllene, copaene, (+)-β-costol, α-cubebene, βcubebene, (+)-cycloisosativene, 3,4-dimethyl-2-hexanone, (E)-4,8-Dimethyl-1,3,7nonatriene, farnesal, α-farnesene, (3Z,6E)-α-farnesene, (E)-β-farnesene, (Z)-β-farnesene, E-farnesene epoxide, germacrene D, 1-hexanol, 2-heptanone, 3-hydroxy-2-butanone, 4hydroxy-4-methyl-2-pentanone, isopropyl myristate, D-limonene, linalool, (E)-linalool oxide, (Z)-linalool oxide, methyl 4-tert-butylbenzoate, methyl salicylate, 2-nonanone, (Z)-β-ocimene, 1-octanol, santalol, sesquirosefuran, 1-tetradecanol, and 3,3,5trimethylcyclohexanol. VOCs were also found to be emitted by the media + microbes, the plastic pot and pesticides that had been applied to the plants. The volatile profile differed markedly among the species tested and between day and night with the total concentration ranging from 61,465 pg 100 g-1 dwt h-1 (day)/42,958 pg 100 g-1 dwt h-1 (night) for S. wallisii to 427 pg 100 g-1 dwt h-1 (day)/130 pg 100 g-1 dwt h-1 (night) for S. trifasciata. Night time rates were lower, in part reflecting the greater diffusion resistance with the stomata closed. S. wallisii was in flower and emitted substantial amounts of αfarnesene which represented 90.3 % of the total pg of volatiles from the plant. In general, however, the levels of VOC synthesis were very low and those emitted did not appear to represent a health concern. Plant Considerations The precision by which one can determine the mechanisms operative during phytoremediation and the potential application of the results to homes and offices is dependent on the care and precision at which the experiments are conducted. Experimental protocol can be separated into three general topics: plant factors, treatment environment and considerations associated with the volatile(s) being tested. Plant factors – the age, size, health, condition, leaf area, fertilization program, growing medium, and water status of the plant(s) and the acclimatization method and duration. Treatment environment – temperature, O2 and CO2 concentrations, relative humidity, air exchange rate or frequency, type of system (closed versus flow through), length of time in the chamber and light intensity, quality, duration, and photoperiod. Volatile considerations – initial exposure concentration, method of introduction and quantification, equilibration time, and duration of exposure. Additional desirable information needed when reporting phytoremediation experiments include the analytical method used, least detectable quantity, source and purity of analytical standards, number of replications and statistical method utilized. The presentation of the data should be in a manner that allows comparison among experiments whenever applicable, (e.g., µg m-3 m-2 h-1). Essential Requisites for Widespread Adoption of Indoor Air Phytoremediation a. Development of an accurate analytical method for measuring the volatile status of the

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air in homes and offices that is economically acceptable to the public and is provided by a credible organization. From existing scientific studies, it is readily evident that a large number of homes and offices have VOC levels that potentially compromise the health of the occupants. The absence of a means for the public to determine the presence of a VOC problem is a major obstacle. For example, even though complaints of serious health problems were repeatedly voiced due to the volatile emissions from U.S. government trailers used as temporary housing after hurricane Katrina, it was 2.5 years before the CDC assessed the air quality and found excessively high levels of formaldehyde (Brunker, 2008), a highly toxic volatile thought to be a carcinogen. Likewise, contamination due to methamphetamine synthesis in clandestine laboratories typically results in the structures being sufficiently toxic to be uninhabitable even though the presence of pollutants is not necessarily readily apparent (Lim Abdullah and Miskelly, 2010). One striking technological deficiency is the absence of an accurate, affordable means of determining the VOC status of homes and offices. Currently the majority of commercial services are either prohibitively expensive for the average homeowner or lack sufficient analytical accuracy. Existing University Extension Service analytical laboratories represent an excellent possible source for such a service. Indoor air VOC composition is known to vary widely among structures. Plant species, likewise, vary in their ability to remove volatiles. As a consequence, knowledge of the building (e.g., volume, air exchange rate) and its volatile composition is essential for determining the appropriate species and number of plants of each to reduce the VOC concentrations to a safe level. b. Additional information on the toxicology of volatiles found in air of homes and offices. A major problem with interpreting the volatile composition of indoor air is that there is toxicology data for only a relatively small portion the volatiles found. Currently the CAS Registry identifies more than 56 million organic and inorganic substances with an additional 12,000 new substances added daily (CAS, 2011). In 1976, when congress passed the Toxic Substances Control Act (TSCA, 1976), there were 60,000 known chemicals in the US marketplace. Today, that number has grown to 80,000 chemicals (http://www.potomac riverkeeper.org/chemical-pollution) plus impurities and compounds formed via reactions occurring during fabrication of products. While there are exposure guidelines for some chemicals, the data is absent or incomplete for an exceedingly large number. The need for increased testing was recently made in a Chemical and Engineering News article by Erickson (2011) indicating “...EPA still has to deal with the tens of thousands of chemicals already in commerce. Only a few hundred of them have been assessed for their toxicity, and the EPA needs to prioritize which of the remaining ones should be evaluated.” The lack of adequate information is also indicated by order of magnitude differences among countries in the acceptable concentrations allowed in the air for some volatile compounds [e.g., the threshold limit value (TLV) for toluene in homes is 0.27 ppm in Korea (Korean Ministry of Environment, 2006), 0.07 ppm in Japan (Japanese

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Ministry of Health, Labour and Welfare, 2000), 20 ppm (time-weighted average) in the U.S. (ACGIH, 2008), and 100 ppm in Australia (NOHSC, 2001)]. c. Support for phytoremediation research Research on phytoremediation of indoor air has proceeded in spite of virtually no government sponsored funding outside of South Korea. The rate of progress has been exceedingly slow and critical deficiencies (e.g., fate of VOCs, assessing the effectiveness of plants in different types of buildings, maximizing the effectiveness of microorganisms in the media) represent research that is expensive and requires a team of scientists from a cross-section of disciplines. Better prioritization of grant funding and focusing more research dollars on projects that have the potential for a tremendous impact on the health and well-being of humans simply makes good sense. A better understanding of the biological processes operative in phytoremediation will allow maximizing the potential of plants and their associated microbes to remove volatile pollutants. While plants will not be the solution for indoor VOC problems in all structures (e.g., large structures), they represent an affordable solution to the majority of citizens especially with the current economic conditions. Conclusions While our understanding of the basic biology and chemistry of phytoremediation of indoor air remains extremely limited, the possible impact of this inexpensive means of air purification on the health and wellbeing of humans is potentially tremendous. Indoor plants not only create an aesthetically pleasing but potentially healthier environment for people worldwide that live and/or work in enclosed buildings. Facilitating research through additional funding is the key to maximizing the many positive advantages of this technology, assessing its real world potential, and if appropriate expediting its widespread use.

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Son, K.C., S.H. Lee, S.G. Seo and J.E. Song. 2000. Effects of foliage plants and potting soil on the absorption and adsorption of indoor air pollutants. J. Korean Soc. Hort. Sci. 41:305-310. Tani, A. and C.N. Hewitt. 2009. Uptake of aldehydes and ketones at typical indoor concentrations by houseplants. Environ Sci Technol. 43(21):8338-8343. Tarran, J., F. Torpy and M. Burchett. 2007. Use of living pot-plants to cleanse indoor air – research review. Proc. Sixth Intern. Conf. on Indoor Air Quality, Ventilation & Energy Conservation in Buildings – Sustainable Built Environment, Sendai, Japan. TSCA. 1976. Toxic Substances Control Act. U.S. Public Law 94-469. Wolverton, B.C. 1986. Houseplants, indoor air pollutants and allergic reactions, National Space Technology Laboratories, NASA, Stennis Space Center, Mississippi. Wolverton, B.C. 1996. How to Grow Fresh Air. 50 Houseplants that Purify Your Home or Office. Penguin Books. New York. Wolverton, B.C. and K. Takenaka. 2010. Plants – Why You Can’t Live Without Them. Roli Books, New Delhi. Wolverton, B.C., R.C. McDonald and E.A. Watkins, Jr. 1984. Foliage plants for removing indoor air pollution from energy-efficient homes. Econ. Bot. 38:224228. Wolverton, B.C., A. Johnson and K. Bounds, 1989. Interior landscape plants for indoor air pollution abatement. Final Rept., NASA, Stennis Space Center, Mississippi. Wolverton, B.C. and J.D. Wolverton. 1993. Plants and soil microorganism: Removal of formaldehyde, xylene, and ammonia from the indoor environment. J. Mississippi Acad. Sci. 38:11-15. Won, D., E. Lusztyk and C.Y. Shaw. 2005. Target VOC list. Final Rept., National Research Council Canada. Wood, R.A., R.L. Orwell, J. Tarran, F. Torpy and M. Burchett. 2002. Pottedplant/growth media interactions and capacities for removal of volatiles from indoor air. J. Hort. Sci. Biotechnol. 77:120-129. Xu,, Z., and L. Wang and H. Hou. 2011. Formaldehyde removal by potted plant-soil systems. J. Hazardous Materials. 192:314-318. Yang, D.S., S.V. Pennisi, K.C. Son and S.J. Kays. 2009. Screening indoor plants for volatile organic pollutant removal efficiency. HortScience 44:1377-1381. Yang, D.S., K.C. Son and S.J. Kays. 2009. Volatile organic compounds emanating from indoor ornamental plants. HortScience 44:396-400. Yang, X., J. Srebric, X. Li and G. He. 2004. Performance of three air distribution systems in VOC removal from an area source. Building Environ. 39:1289-1299. Yoo, M.H., Y.J. Kwon, K.C. Son and S.J. Kays. 2006. Efficacy of indoor plants for the removal of single and mixed volatile organic pollutants and physiological effects of the volatiles on the plants. J. Amer. Soc. Hort. Sci. 131:452-458. Yurimoto, H., N. Kato and Y. Sakai. 2005. Assimilation, dissimilation, and detoxification of formaldehyde, a central metabolic intermediate of methylotropic metabolism. Chem. Rec. 5:367-375. Yurimoto, H., N. Kato and Y. Sakai. 2009. Genomic organization and biochemistry of the rubulose monophosphate pathway and its application in biotechnology. Appl. Microbiol. Biotechnol. Biochem. 84:407-416.

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Zabiegała, B. 2006. Organic compounds in indoor environments. Polish J. Environ. Stud. 15: 383-393.

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Table 1. Volatile organic compounds found in two houses in Athens, Georgia. Aliphatic hydrocarbons 2-n-Butylacrolein 1* Decane 1, 2 2,3-Dimethylheptane 1 2,6-Dimethyloctane 1 2,6-Dimethylundecane 1 Dodecane 1 (E)-6-Dodecene 1 (Z)-5-Dodecene 1 3-Ethyl-2-methylheptane 1 1-Ethyl-3-methylcyclohexane (c,t) 1 (E)-1-Ethyl-4-methylcyclohexane 1 Heptadecane 1, 2 Hexadecane 1, 2 4-Methyldecane 1 4-Methyldodecane 1 3-Methylnonane 1 7-Methylpentadecane 1 3-Methyltetradecane 1 15-Methyltricyclo [6.5.2(13,1)0(7,15)] pentadeca1,3,5,7,9,11,13-heptene 2 2-Methyltridecane 1 4-Methyltridecane 1 5-Methyltridecane 1 Nonadecane 1 Nonane 1, 2 Aliphatic alcohols 1-Butanol 1 2-Butoxyethanol 1, 2 1-(2-Butoxyethoxy)ethanol 1 1-Butoxy-2-propanol 1 1,3-Dichloro-2-propanol 1 Dimethylsilanediol 1 2-(2-Ethoxyethoxy)ethanol 1 2-Ethyl-1-hexanol 1 1-Hexanol 1 Hexylene glycol 1 2-(Hexyloxy)ethanol 1 2-(2-Methoxyethoxy)ethanol 1 1-(2-Methoxy-1-methylethoxy)2-propanol 1 1-(2-Methoxypropoxy)-2propanol 1

2-Methylene cyclopentanol 1 3-Methyl-1-butanol 1 5-Methyl-1-hexanol 2 1-Phenyl-1,4-butanediol 2 2-Phenylisopropanol 1 1-Octanol 1 1-Pentanol 1, 2 1-Propoxy-2-propanol 1 Propylene glycol 1 Aliphatic aldehydes Decanal 1 (Z)-2-Decenal 1 Heptanal 1, 2 (E)-2-Heptenal 1 Hexanal 1, 2 (E)-2-Hexenal 1 2-Methyl-3-phenylpropanal 1 Nonanal 1 Octanal 1 (E)-2-Octenal 1 Pentanal 1 Aliphatic ketones Cyclohexanone 2 2-Decanone 1 Geranylacetone 1 2-Heptanone 1 2-Hexanone 1 6-Methyl-2-heptanone 1 6-Methyl-5-hepten-2-one 1 4-Methyl-2-pentanone 1 1-(4-Methylphenyl)ethanone 1 2-Nonanone 1 (+)-Nopinone 1 Aromatic compounds Acetophenone 1 p-Allylanisole 1, 2 Benzaldehyde 1 Benzyl acetate 1 Benzyl alcohol 1 Butylated hydroxytoluene 1 Decahydro-1,6dimethylnaphthalene 2 Decahydro-4,4,8,9,10pentamethylnaphthalene 1, 2

Decahydro-8a-ethyl-1,1,4a,6tetramethyl-naphthalene 1 1,2-Dichlorobenzene 2 1,4-Dichlorobenzene 2 1,3-Diethylbenzene 1 1,2-Diethylbenzene 2 3,4-Diethylbiphenyl 1 2,3-Dihydro-1,4,7-trimethyl-1Hindene 1 2,3-Dihydro-4-methyl-1H-indene 1

2,6-Di-tert-butyl-1,4benzoquinone 1 Esters Butyl acetate 1, 2 Butyl butyrate 1 2-Ethoxyethyl acetate 1 2-Ethyl-1-hexanol benzoate 1 Fenchyl acetate 1 1-Methoxy-2-propyl acetate 1 3-Methyl-1-butanol acetate 1 Methyl salicylate 1 Nonyl chloroformate 2 2-Pentyl acetate 1 Acids Acetic acid 1 Butanoic acid 1 2-Ethylhexanoic acid 1 Hexanoic acid 1 Terpenoids Borneol 1 Camphene 1 d-Camphor 1, 2 3-Carene 1 2-Carene 2 d-Carvone 1 N-containing compounds 2-Anthracenamine 1 Benzonitrile 1 Methylpyrazine 1 Pyrazine 1 N,S-containing compound Benzothiazole 1

______________________________________________________________________________________ * Numbers indicate in which house the chemical was present.

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Table 2. Plant species tested for their ability to remove selected VOCs. Plant Species Adiantum capillusveneris L. Aglaonema modestum Schott ex Engl. Aglaonema Schott Aloe vera (L.) Burm. f. Aloysia triphylla (L’Hér.) Britton Anthurium andreanum Linden Arachniodes aristata (G. Forst.) Tindale Araucaria heterophylla Franco Ardisia crenata Sims. Ardisia japonica (Thunb.) Blume Ardisia pusilla A. DC. Asparagus densiflorus (Kunth) Jessop ‘Sprengeri’ Aspidistra elatior Blume ‘Milky Way’ Asplenium nidus L. ‘Avis’ Begonia maculata Raddi Botrychium ternatum (Thunb.) Swartz. Brassaia arboricola Endl. Calathea makoyana E. Morr. Calathea roseopicta (Linden) Regal Camellia japonica L. Camellia sinensis Kuntz. Chamaecyparis obtusa Endl. Chlorophytum bichetii Baker Chlorophytum comosum (Thunb.) Jacq. ‘Fire Flash’ Chlorophytum elatum (Aiton) R. Br. var. vittatum Chlorophytum elatum (Aiton) R. Br. Chrysalidocarpus lutescens H. Wendl Chrysanthemum morifolium (Ramat.) Hemsl. Cinnamomum camphora (L.) J. Presl Cissus rhombifolia Vahl. Citrus medica var. sarcodactylis (Hoola van Nooten) Swingle Clivia miniata Regal Codiaeum variegatum (L.) Blume Coniogramme japonica (Thunb.) Diels

Reference Chemical c3 c3j3 h2 j3 d7 c3l1,2,5, 6 c3 c3 c3d7 d7 c3d7 l1,2,5, 6 l1,2,5, 6 c3 d7 c3 j3 c3 l1,2,5, 6 c3 c3 c3 c3 l1,2,5, 6 i3 j3 c3 a3 d7 m2,7 e2 c3 l1,2,5, 6 c3

Plant Species Reference Chemical Crassula portulacea Lam. e2 c3 Cupressus macrocarpa Hartweg ‘Gold Crest’ Cycas revoluta Thunb. c3 Cymbidium Sw. ‘Golden Elf’ e2 Cyrtomium caryotideum Nakai ‘Coreanum’ c3 Cyrtomium falcatum (L.f.) Presl. c3 Davallia mariesii Moore ex Baker c 3d 7 Dendranthema morifolium (Ramat.) Tzvelev e2 Dendropanax morbifera Nakai Lév. c3 Dieffenbachia sp. a3 Dieffenbachia amoena Hort. ex Gentil ‘Marianne’ c3 Dieffenbachia amoena Hort. ex Gentil ‘Tropic Snow’ e2 Dieffenbachia seguine (Jacq.) Schottz l1,2,5, 6 Dizygotheca elegantissima R. Vig. & G. c3 Dracaena sp. f2 Dracaena concinna Kunth c3 Dracaena deremensis Engl. k2,4 Dracaena deremensis Engl. ‘Variegata’ e2 Dracaena deremensis Engl. ‘Warneckii’ c3 Dracaena fragrans (L.) Ker-Gawl. l1,2,5, 6 Dracaena fragrans (L.) Ker-Gawl. ‘Massangeana’ c3j3 Dracaena marginata Lam. f2 Dryopteris nipponensis Koidz c3 Elaeocarpus sylvestris Hara ‘Ellipticus’ c3 Epipremnum aureum Bunt. a3c3f2l1,2,5, 6 Eugenia myrtifolia ‘Compacta’ c3 Eurya emarginata (Thunb.) Makino b3c3d7 Farfugium japonicum (L.) Kitam. b 3d 7 Fatsia japonica Decne. et Planch. b3c3b3 Ficus benjamina L. b3c3g3l1,2,5, 6 Ficus elastica Roxb. ex Horne. c3 Ficus elastica Roxb. ex Home. ‘Rubra’ l1,2,5, 6 Ficus microcarpa L. f. var. fuyuensis e2 Fittonia argyroneura Coem. l1,2,5, 6 Fittonia verschaffeltii (Lem.) Van Houtte d7

References: a Aydogan et al., 2011; b Kim et al, 2008; c Kim et al., 2010; d Kim et al., in press; e Lui et al., 2007; f Orwell et al., 2004; g Son et al., 2000; h Tarran et al 2007; i Wolverton et al., 1984; j Wolverton, 1986; k Wood et al., 2002; l Yang et al, 2009; mYoo et al., 2006. VOCs: α-pinene 1; benzene 2; formaldehyde 3; hexane 4; octane 5; TCE 6; toluene 7.

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Table 2. Plant species tested for their ability to remove selected VOCs.

Plant Species Reference Chemical Gardenia jasminoides Ellis c3 Guzmania sp. l1,2,5, 6 Haemaria discolor Lindl. c3 Hedera helix L. a3c3d7l1,2,5, 6m2,7 Hemigraphis alternata (Burm.f.) T. Anders ‘Exotica’ l1,2,5, 6 Howea belmoreana (C. Moore & F. Muell.) Becc. c3l1,2,5, 6 Howea forsteriana (C. Moore & F. Muell.) Becc. f2k2,4 Hoya carnosa (L.f.) R.Br. c3 Hoya carnosa (L.f.) R.Br. ‘Variegata’ e2,3,6, 7 Hydrangea macrophylla (Thunb.) Ser. e2 Ilex cornuta Lindl. & Paxton b3d7 Ilex crenata Thunb. c3 Jasminum polyanthum Franchet c3 Jasminum sambac (L.) Aiton c3 Laurus nobilis L. c3 Lavandula sp. c3 Ligustrum japonicum Thunb. c3d7 Maranta leuconeura E. Morren l1,2,5, 6 Melissa officinalis L. d7 Mentha piperita L. d7 Mentha piperita L. ‘Citrata’ d7 Mentha suaveolens Ehrh. d7 Mentha suaveolens Ehrh. ‘Applemint’ c3 Mentha suaveolens Ehrh. ‘Variegata’ d7 Microlepia strigosa (Thunb.) Presl. c3 Nandina domestica Thunb. c3 Nephrolepis exaltata (L.) Schott g3 Nephrolepis exaltata (L.) Schott ‘Bostoniensis’ e2 Osmunda japonica Thunb. c3 Pachira aquatica Aubl. c3g3 Pelargonium sp. c3 Pelargonium graveolens L’Her. ex Ait i4l1,2,5, 6 Peperomia clusiifolia (Jacq.) Hook c3 Peperomia clusiifolia (Jacq.) Hook ‘Variegata’ l1,2,5, 6 Peperomia obtusifolia (L.) A. Dietr. j3

Plant Species Philodendron domesticum G. S. Bunting Philodendron oxycardium Schott Philodendron scandens K. Koch & Sello ssp. oxycardium (Schott) G. S. Bunting Philodendron selloum C. Koch. Philodendron sp. ‘Sunlight’ Phoenix roebelenii O’Brien. Pinus densiflora Siebold & Zucc. Plectranthus tomentosus Benth. ex E. Mey. Polypodium formosanum Baker Polyscias balfouriana Bailey Polyscias fruticosa (L.) Harms Polystichum tripteron (Kunze.) Presl. Psidium guajava ‘Safeda’ Pteris dispar Kunze Pteris ensiformis Burm. ‘Victoriae’ Pteris multifida Poir. Quercus acuta Thunb. Quercus glauca Thunb. Raphiolepis umbellata Makino Rhapis excelsa Wendl. Rhapis humilis Blume Rhododendron fauriei Franch. Rosmarinus officinalis L. Saintpaulia ionantha H. Wendl Salvia elegans Vahl Sansevieria trifasciata Prain Schefflera arboricola (Hayata) Merr. Schefflera arboricola (Hayata) Merr. ‘Variegata’ Schefflera arboricola (Hayata) Merr. ‘Hong Kong’ Schefflera elegantissima (Veitch ex Masters) Lowry & Frodin Scindapsus aureus (Linden & André) G. S. Bunting Selaginella tamariscina Spring Serissa foetida (L.F) Lam.

Reference Chemical j3 j3 l1,2,5, 6 c 3j 3 d7 c3 d7 d7 c3 c3 l1,2,5, 6 c3 c3 c3 c3 c3 c3 c3 c3 c3 g3 d7 c 3d 7 c3 d7 c3j3l1,2,5, 6 g3 l1,2,5, 6 c3 d7l1,2,5, 6 g3i3j3 c3 c3

References: a Aydogan et al., 2011; b Kim et al, 2008; c Kim et al., 2010; d Kim et al., in press; e Lui et al., 2007; f Orwell et al., 2004; g Son et al., 2000; Tarran et al 2007; i Wolverton et al., 1984; j Wolverton, 1986; k Wood et al., 2002; l Yang et al, 2009; mYoo et al., 2006. VOCs: α-pinene 1; benzene 2; formaldehyde 3; hexane 4; octane 5; TCE 6; toluene 7.

h

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Table 2. Plant species tested for their ability to remove selected VOCs. Plant Species Reference Chemical Soleirolia soleirolii (Req.) Dandy d7 Spathiphyllum sp. ‘Petite’ f2 Spathiphyllum sp. ‘Sensation” f2 Spathiphyllum sp. ‘Supreme’ e2 Spathiphyllum patinii (R. Hogg) N. E. Br. g3 Spathiphyllum wallisii Regel c3k2,4l1,2,5, 6m2,7 Spathiphyllum wallisii Regel ‘Clevelandii’ j3 Stauntonia hexaphylla (Thunb.) Dence. c3 Syngonium podophyllum Schott c3i3l1,2,5, 6m2,7 Thelypteris acuminate (Houtt.) Morton c3 Thelypteris decursivepinnata Ching c3 Thelypteris torresiana (Gaudich.) Alston ‘Calvata’ c3 Tillandsia cyanea Linden ex C. Koch c3 Trachelospermum asiaticum Nakai c3 Tradescantia pallida (Rose) D.R. Hunt ‘Purpurea’ l1,2,5, 6 Tradescantia sillamontana Matuda j3 Viburnum awabuki K. Koch c3 Zamia pumila L. c3 Zamioculcas sp. h2 Zamioculcas zamiifolia (Lodd. et al.) Engl. c3

Plant Species

Reference Chemical

References: a Aydogan et al., 2011; b Kim et al, 2008; c Kim et al., 2010; d Kim et al., in press; e Lui et al., 2007; f Orwell et al., 2004; g Son et al., 2000; Tarran et al 2007; i Wolverton et al., 1984; j Wolverton, 1986; k Wood et al., 2002; l Yang et al, 2009; mYoo et al., 2006. VOCs: α-pinene 1; benzene 2; formaldehyde 3; hexane 4; octane 5; TCE 6; toluene 7.

h

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Table 3. Variation in phytoremediation rates among species and experiments. Chemical Initial Concentration Formaldehyde 14-37 ppm

Plant Species Syngonium podophyllum Schott Chlorophytum elatum (Aiton) R. Br.var. vittatum

22 ppm

Philodendron oxycardium Schott Philodendron domesticum G. S. Bunting

1.5 ppm

Ficus benjamina L. Schefflera arboricola (Hayata) Merr.

1.63 ppm

Chrysanthemum morifolium (Ramat.) Hemsl. Dieffenbachia sp.

2.0 ppm

Fatsia japonica Decne. et Planch. Ficus benjamina L.

2.0 ppm

Osmunda japonica Thunb. Dracaena deremensis Engl.

Toluene 1.3 ppm

Benzene 25 ppm

25 ppm 150 ppb (continuous flow) 25 ppm

Hexane 100 ppm

Rhododendrom fauriei Franch. Pittosporum tobira (Thunb.) W. T. Aiton

Removal Rate µg m-3 m-2 h-1 574

Citation Wolverton et al., 1984

2,920 832 95 18,582 8,313 270 309

Wolverton, 1986 Son et al., 2000

Aydogan et al., 2011

1,000 1,100

Kim et al., 2008

13,300 1,300

Kim et al., 2010

928 22

Kim et al., 2011

Howea forsteriana (C. Moore & F. Muell.) Becc. Spathiphyllum wallisii Regel

23,833 28,583

Wood et al., 2002

Dracaena marginata Lam. Spathiphyllum sp. ‘Sensation’

44,843 7,857

Orwell et al., 2004

Crassula portulacea Lam. Dracaena deremensis Engl.‘Variegata’

15,725 1,281

Lui et al., 2007

Aglaonema Schott Zamioculcas sp.

Howea forsteriana (C. Moore & F. Muell.) Becc. Dracaena deremensis Engl.

7,024 4,152

Tarran et al 2007

168,000 15,292

Wood et al., 2002

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