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Opinion

Plants for Sustainable Improvement of Indoor


Air Quality
Federico Brilli,1,* Silvano Fares,2 Andrea Ghirardo,3 Pieter de Visser,4 Vicent Calatayud,5
Amalia Muñoz,5 Isabella Annesi-Maesano,6 Federico Sebastiani,1 Alessandro Alivernini,2
Vincenzo Varriale,7 and Flavio Menghini7

Indoor pollution poses a serious threat to human health. Plants represent a Highlights
sustainable but underexploited solution to enhance indoor air quality. However, In modern energy-saving airtight con-
structions, the concentration of air pol-
the current selection of plants suitable for indoors fails to consider the physio-
lutants can build up to dangerous
logical processes and mechanisms involved in phytoremediation. Therefore, levels, posing a serious threat to
the capacity of plants to remove indoor air pollutants through stomatal uptake human health.

(absorption) and non-stomatal deposition (adsorption) remains largely Plants can efficiently remove pollutants
unknown. Moreover, the effects of the indoor plant-associated microbiome and improve indoor air quality,
still need to be fully analyzed. Here, we discuss how a combination of the although the stomatal and non-stoma-
tal processes driving phytoremediation
enhanced phytoremediation capacity of plants together with cutting-edge air- are poorly understood and not yet
cleaning and smart sensor technologies can improve indoor life while reducing properly quantified.
energy consumption.
Indoor plants are typically selected on
the basis of their aesthetic features
Living in Modern ‘Sick’ Buildings: Development of Plant-Based Biosystems rather than physiological requirements
‘To Cure’ Indoor Air reflecting their capacity to remove air
Residential and commercial buildings consume approximately 30% of total global energy [1]. pollutants.
In recent years, incentives to improve energy efficiency have facilitated the development of
thermally insulated buildings, which require less energy for heating, ventilating, and air-
conditioning (HVAC) systems. However, potentially toxic gases and particular matter (PM)
can be released by a variety of indoor sources and activities of occupants, including
furnishings, paints, varnishes, waxes, carpets, solvents, cleaning supplies, office equipment 1
National Research Council of Italy -
such as copiers and printers, gas cooktops, and cigarettes [2]. Air pollutants common to Institute for Sustainable Plant
Protection (CNR-IPSP), Via Madonna
different indoor environments include carbon monoxide and dioxide (CO and CO2), volatile del Piano 10, 50019 Sesto Fiorentino,
organic compounds (VOCs; e.g., formaldehyde and benzene), nitrogen oxides (NO and Firenze, Italy
2
NO2), and polycyclic aromatic hydrocarbons (PAHs) [3]. Since people in industrialized Council of Agricultural Research and
Economics (CREA), Research Centre
countries spend more than 80% of their lives indoors, the build-up of air pollutant concen- for Forestry and Wood, Viale Santa
trations to dangerous levels, especially in modern energy-saving but air-tight constructions, Margherita 80, 52100, Arezzo, Italy
3
represents one of the priority concerns for human health today [4]. In fact, continuous Research Unit Environmental
Simulation, Institute of Biochemical
exposure to air pollutants, the concentration of which indoors can even be higher than Plant Pathology, Helmholtz Zentrum
outdoors, may cause respiratory and cardiovascular diseases eventually contributing to the München, Ingolstädter Landstraße 1,
so-called ‘sick building syndrome’ (SBS; see Glossary) and ‘building-related illnesses’ D-85764 Neuherberg, Germany
4
Business Unit Greenhouse
(BRI). One of the major concerns regards formaldehyde, a widespread hazardous air Horticulture, Wageningen Research,
pollutant that is released over the long-term from aging furniture and pressed-wood prod- Droevendaalsesteeg 4, 6708 PB
ucts, and that is likely to have carcinogenic effects in humans [5]. Plants can absorb and Wageningen, The Netherlands
5
Fundación CEAM, c/Charles R.
catabolize almost any airborne pollutant, although this phytoremediation capacity has been Darwin 14, Parque Tecnológico,
poorly applied indoors. To date, plants selected for indoor environments have appealing 46980 Paterna, Valencia, Spain
6
aesthetic features, and their associated microbiome has been greatly overlooked. Here, we EPAR, IPLESP Université Pierre et
Marie and INSERM, Medical School
outline how the development of computerized self-sufficient biosystems, which combine the Saint-Antoine, 27 rue Chaligny, 75012
best-performing indoor plant species with new air-cleaning and sensor technologies, will Paris, France

Trends in Plant Science, June 2018, Vol. 23, No. 6 https://doi.org/10.1016/j.tplants.2018.03.004 507
© 2018 Elsevier Ltd. All rights reserved.
7
represent a cost-effective solution to radically improve the quality of life of people living in CityOasis Ltd, Office 7, 35–37
Ludgate Hill, London, EC4M 7JN, UK
‘smart’ and more sustainable buildings.

Plants Can Ameliorate Indoor Air Pollution in a Natural and Sustainable Way *Correspondence:
Plants can improve indoor air quality (IAQ) by simultaneously taking up CO2 and releasing O2 federico.brilli@ipsp.cnr.it (F. Brilli).

through light-dependent photosynthesis, and increase air humidity by water vapor transpired
from leaves through microscopic leaf pores, namely stomata [6]. The capacity of leaves to
exchange gases and, thus, to take up any pollutants from indoor air, is limited by physical
constraints related to stomatal and mesophyll resistance (Figure 1). Plants actively modulate
stomata apertures in response to variable environmental conditions (i.e., light availability or air
humidity) through a complex signaling network of hormones (i.e., abscisic acid, ABA) that are
exchanged between roots and shoots [7]. In addition, indoor air pollutants can passively
collect on the external surfaces of the complete root–soil system of the plant and, thus, be
effectively removed. Processes driving ‘non-stomatal’ adsorption not only depend on the
total area, anatomical features, morphological traits, and chemical properties of the plant
surface, but are also related to the characteristics of the soil substrate [8]. In particular, the
capacity of the leaf surface to remove air pollutants is influenced by the presence, shape, and
density of trichomes [9]. More specifically, the amount of cuticular wax and the lipid composi-
tion of the membrane of epidermis cells coating the plant surfaces have an important role in the
adsorption of pollutants, especially lipophilic VOCs, such as benzene, following deposition [10].

Pioneer studies conducted by NASA during the 1980s successfully demonstrated that plants are
able to remove airborne pollutants [11], although these findings were based on a simplistic
experimental approach [12]. Recently, more accurate experimentation simulating the long-term
exposure of foliage to typical indoor concentrations of air pollutants [13] highlighted that stomatal
(dependent) absorption is 30–100 times higher than the amount passively adsorbed through
non-stomatal deposition [14]. These results further suggest that, after entering the plant leaf, some
pollutants are metabolically degraded and/or translocated to shoots and roots [15]. Plants have
enzymes able to catalyze the degradation of pollutants, such as the oxidation of formaldehyde [16]
or the hydroxylation and cleavage of the aromatic rings of benzene and toluene [17]. Airborne
pollutants absorbed through leaf stomatal uptake can undergo transformation following enzy-
matic oxidation and conversion into different bioproducts via conjugation with plant endogenous
compounds (i.e., sugars, amino acid, organic acids, and peptides). After being catabolized, the
assimilated pollutants might be either re-expelled (re-emission into the air or ejection via root
exudates) or further metabolized to be finally used as both carbon and energy sources [17]. Plant
enzymatic mechanisms of scavenging and detoxification maintain a decreasing concentration
gradient of pollutants between the air and the interior of the leaves, allowing a steady and
continuous uptake when stomata are open. However, only a few of the enzymes responsible
for the metabolic transformation of airborne pollutants are currently recognized [18] and the fate of
many other toxic gaseous compounds inside plants remains unknown.

Therefore, although there is clear evidence that plants can improve IAQ, real applications have
been hampered by our limited understanding of the processes affecting stomatal uptake and
the factors influencing the size of the non-stomatal sink for air pollutant absorption (see
Outstanding Questions).

How to Select Indoor Plants: The Need to Define New Strategies


So far, plants used indoors have been selected on the basis of the preferences of consumers,
who typically favor aesthetic features, good survival, and low maintenance needs. Most
ornamental plants currently grown indoors are broadleaf evergreen species from the

508 Trends in Plant Science, June 2018, Vol. 23, No. 6


Glossary
Air-cleaning technologies: an
ensemble of mainly electrochemical-
and gas adsorption-based
technologies used to clean indoor
air; includes electro-filters, UV lights,
photocatalytic materials, fuel cells,
and catalyzers.
Air phytoremediation: the use of
plants to remove airborne pollutants.
It is plant species specific, being a
function of several genetic,
physiological, anatomical, and
morphological parameters, and
microbe–plant interactions. It is
carried out by plants via the stomata,
leaf surfaces, soil, and microbes.
Building-related illness (BRI):
includes allergic reactions or
infections accompanied by clinically
defined symptoms (i.e., cough, fever,
and muscle aches) that can be
attributed directly to indoor airborne
pollutants.
Decision support systems (DSS):
software designed to set and
regulate air-cleaning biosystems by
suggesting the most appropriate
plant species, optimal number and
positioning according to the
requirements desired for a certain
indoor environment (i.e., temperature,
air humidity, or level of pollutants).
Indoor air pollutants: carbon
monoxide and dioxide (CO and CO2),
nitrogen oxides (NO and NO2), ozone
(O3), VOCs (e.g., formaldehyde,
acetaldehyde, benzene, toluene,
xylene, acrolein, and styrene), PAHs.
Surface-assisted reacons secondary organic aerosols (SOA),
VOC O3, –OH VOC Transformaon of air pollutants (possible formaon of secondary products) and atmospheric oxidants (O3, OH,
Non-stomatal adsorpon: and NO3 radicals).
Upper epidermis
Passive accumulaon into the leaf surface epidermis (i.e., waxes)
Non-stomatal adsorption:
Palisade layer Acve removal by the microbes inhabing the surfaces accumulation of air pollutants onto
both the leaf surface layers (e.g., wax
deposition) and the soil surrounding
Spongy layer Stomatal absorpon:
the plants following degradation by
Acve removal through detoxifying enzymes
the microbial communities inhabiting
the phyllosphere and the
rhizosphere.
Lower epidermis
Emissions Plant-based ‘biosystems’:
Storma
Guard cell Constuve (depending on the both enzymac acvity and substrate availability)
Inducible by stress condions association of the best-performing
VOC VOC
indoor plant species with air-cleaning
technologies to maximize the
sequestration of air pollutants.
Figure 1. The Use of Computerized Self-Sufficient Biosystems Comprising Plants Combined with New Air- Plant microbiome: originally defined
Cleaning Technologies to Improve the Air Quality and Human Well-Being in Various Indoor Environments. as the collection of the genomes
The lower panel provides details of the various processes potentially involved in the interaction between indoor volatile belonging to the whole microbiota
organic compounds (VOCs) and the plant foliage. Micrograph modified from Kimball’s Biology Pages © John W. Kimball. associated with plants (including
microorganisms present on the
rhizosphere, phyllosphere, or within
endophytic compartments), this term

Trends in Plant Science, June 2018, Vol. 23, No. 6 509


understory of warm tropical and subtropical climates; to thrive under dense forest canopies, is now also often used to refer to the
such plants have optimized their leaf photosynthetic performances under low-light intensities microbial community itself (such as
bacteria, fungi, and viruses).
[19]. However, adaptation to shade implies the presence of large leaf surface areas and Sick building syndrome (SBS):
reduction of stomatal apertures [20], which both favor the deposition of pollutants on plant includes a condition, typically marked
surfaces rather than uptake by the leaves. The suboptimal quality and intensity of light that by headaches and respiratory
usually occurs indoors limit stomatal opening, which, in turn, restrains the flux of pollutants that problems, that impairs people’s
health and comfort and that appears
could enter the leaves and be removed by plant enzymes. to be linked directly to the amount of
time spent indoors; no specific illness
Besides the ability to survive in the light-limited conditions provided by traditional illuminating or cause of disease can be identified.
Stomatal absorption: a route of air
systems and to acclimate to frost-free environments, unambiguous recommendations to drive the
pollutant uptake through a leaf
selection of suitable indoor plants are lacking. Therefore, scientific criteria should be outlined followed by active processes of
urgently to screen the optimal-performing plant species in indoor environments on the basis of the biochemical degradation,
morphological (i.e., leaf shape, size, and hairiness), anatomical (i.e., composition of epidermis and detoxification via enzymes, and
possible conversion into different
mesophyll layers, and stomatal density and size) and physiological (i.e., CO2 assimilation rate and
bioproducts either within the plant or
activity of detoxifying enzymes) properties that reflect the capacity of the plant to phytoremediate air. in the rhizosphere.
Wireless network sensors (WNS):
A comprehensive understanding of the plant biochemical processes involved in the degrada- a system comprising spatially
distributed autonomous low-cost
tion of indoor air pollutants could be achieved through the combined application of advanced sensors that monitors, in real-time,
‘omics technologies (genomics, proteomics, and metabolomics). A readout of the metabolic both the physical characteristics (i.e.,
state of the plant provided by ‘omics profiling allows us to characterize and quantify large pools light, air temperature, and humidity)
of molecules and, thus, help identify physiological functions underlying the catabolism of air and the quality of air (i.e., level of
pollutants) and continuously
pollutants by plants. The discovery of the major metabolic pathways, genes, and enzymes communicates with logging stations,
involved in air phytoremediation will enable the determination of biomarkers for screening such as personal computers and
(and, thus, ‘phenotyping’) the most appropriate plant species for improving IAQ. In the near smartphones.
future, the number of species used to phytoremediate indoor air could be widened by editing
the genome of plants through precise and targeted DNA modifications aimed at overexpressing
or inserting genes encoding detoxification enzymes.

The Microbiomes of Indoor Plants Remain Unexplored


Plants do not ever stand alone. Populations of microorganisms (bacteria and fungi) are
ubiquitously associated with plants both belowground (i.e., in the soil rhizosphere) and above-
ground [i.e., on the leaf surfaces (phyllosphere], where they can reach an impressive concen-
tration of 106–107 microbial cells cm 2 [21]. The plant microbiome can actively participate in
the removal of airborne pollutants through non-stomatal adsorption [22]. However, the contri-
bution of different microbial species inhabiting the leaf surfaces and the plant root system to
removing air pollutants from various indoor environments is not yet established. Plants select
different microbial species on both leaves and roots depending on genetic features and
environmental conditions [23]. The introduction of microbiomes associated with various plant
species into indoor environments, already inhabited by different population of microbes [24],
may improve the removal of indoor air pollutants, but gives rise to concerns about their effects
on human health, including allergies and lung inflammation.

(Re)assessing and Modeling Indoor Air Phytoremediation


Plant species suitable for cleaning indoor air should simultaneously demonstrate high physio-
logical performance when exposed to limiting environmental conditions (i.e., low-light intensi-
ties or suboptimal growth temperatures) while being able to effectively lower the levels of
harmful air pollutants. The potential of plants to improve IAQ can only be approximated because
quantitative assessments mostly rely on the percent decays of heavily-concentrated air
pollutants measured in small chambers enclosing plants under static conditions [25]. More
sophisticated predictive models that are able to reproduce the ability of the plant to

510 Trends in Plant Science, June 2018, Vol. 23, No. 6


phytoremediate indoor air should be developed on the process-based mechanisms of the Outstanding Questions
dynamic stomatal- and non-stomatal removal of pollutants. Therefore, an accurate experi- How much should we worry about
mental approach is required to quantify, over time, the flux of indoor pollutants sequestrated by indoor air pollution?

the foliage (i.e., the amount of pollutants per unit time and leaf area) and the whole plant under
Why have plants not yet been fully
highly controlled environmental conditions. exploited as a sustainable and cost-
effective solution to improve indoor air
In addition, when introduced indoors, plants can become a source of pollution. In fact, some quality?
plant species, having scented leaves or flowers, release biogenic VOCs (mostly isoprenoids)
How much can plants effectively lower
that can react with ozone and other oxidants, such as hydroxyl (-OH) and nitrate (NO3) radicals
the level of harmful airborne pollutants
[26], in indoor air. Ozone-initiated oxidation [27] leads to the production of highly reactive indoors by?
secondary gas-phase pollutants (i.e., hyperoxides, aldehydes, and carbonyls) that can be more
harmful than their precursors [28] and contribute to the formation of indoor particles [29,30], What are the physiological functions,
with potential adverse effects on human health. As a consequence, the overall capacity of metabolic pathways, genes, and
enzymes involved in degradation of
plant–microbe systems to phytoremediate air should be tested in realistic scenarios simulating
indoor air pollutants by plants?
the chemistry, transport and deposition rates of pollutants under the low mixing (stagnant) air
conditions that occur indoors. What are the unambiguous and scien-
tific criteria needed to drive the selec-
Integrating Plants with Air-Cleaning Technologies: A Win–Win Strategy for tion of the most appropriate plant
species for indoor air
the Energy-Efficient Improvement of IAQ phytoremediation?
Existing air-cleaning technologies that integrate heating, ventilation, air conditioning with electro-
filters, ultraviolet (UV) lights, photocatalytic materials, fuel cells, and catalyzers are promising tools to Does the introduction of plants and
improve IAQ. However, the application of these commercial air-cleaning systems is often limited by their associated microbes indoor rep-
the high costs associated with frequent maintenance and their significant energy consumption. In resent a risk to human health?

future buildings, improving IAQ could become more cost-effective and sustainable thanks to the use
How can a biological system compris-
of ‘biosystems’ that combine air-cleaning technologies with the most optimally performing indoor ing highly performing plants species
plants (Figure 1). The introduction of sensor-controlled LED lighting, fertilization and ventilation and selected microbiomes be inte-
systems can reduce energy requirements to provide optimal conditions for plant growth and grated with a network of sensors con-
enhance indoor air phytoremediation. In particular, the use of a targeted spectrum of light provided trolled air-conditioning technologies to
reduce energy consumption in future
by LED illumination will simultaneously improve the efficiency of photosynthetic CO2 assimilation buildings while improving life indoor?
and stimulate stomata opening, thus increasing the sink strength of foliage for airborne pollutants
[31]. The development of such biosystems would enable the engineering of indoor environments
through the real-time monitoring of air quality retrieved from low-cost wireless network sensors
(WNS) communicating with logging stations, such as personal computers and smartphones. In
addition, user-friendly software will serve as a decision support system (DSS) to plan and
efficiently regulate the air-cleaning biosystem by suggesting the most suitable plant species, the
optimal number of plants, positioning and the environmental requirements that would maximize air
phytoremediation accordingly to both pollutant levels and the physical characteristics of the interior
spaces (i.e., volume, temperature, and relative humidity). However, new ‘green’ indoor environ-
ments could be designed only by pursuing an inter- and multidisciplinary approach that integrates
innovative technologies with a deep understanding of the air phytoremediation capacity of plants
and their associated microbiome, thoroughly assessed and modeled to improve human well-being.

Concluding Remarks and Future Perspectives


The ability of plants to phytoremediate indoor air pollutants has been overlooked for too long.
The selection of plants suitable for indoor phytoremediation should follow unambiguous
scientific criteria that reflect their capacity to sequestrate airborne pollutants, instead of only
taking into consideration their aesthetic features. The capacity of indoor plants to remove air
pollutants needs to be quantitatively assessed in realistic scenarios and modeled on the
process-based mechanisms of both (stomatal) uptake and (non-stomatal) deposition. How-
ever, some crucial points must be addressed when planning indoor phytoremediation: (i) the

Trends in Plant Science, June 2018, Vol. 23, No. 6 511


production of secondary gas-phase pollutants triggered by emission of plant biogenic VOCs
may negatively impact the IAQ; and (ii) the microbiome associated with indoor plants needs to
be managed to realize the benefits of removing pollutants without any risk to human health.

The possibility to integrate smart sensor networks and computerized technologies for air
cleaning with highly performing indoor plant species provides the opportunity to improve
indoor life while also reducing energy consumption. The development of ecosustainable,
cost-effective (and possibly self-sufficient) plant-based biosystems able to enhance IAQ
will positively affect both human society and the housing industry in an unprecedented fashion
that could lead to a postmodern version of ecoarchitecture. If this was to happen, society as a
whole would experience a paradigm shift in the way in which dwellings and indoor spaces are
perceived and designed since plants, that have so far been used only as a decorative tool,
would become a key player in everyone’s life.

Acknowledgments
We thank Srikanta Dani who has helped us design Figure 1. Some parts of the figure were imported from Vecteezy.

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