Atmospheric particle pollution is among the greatest challenges faced in urban areas. One of the most dangerous pollutants in the air is particulate matter (PM) (OECD 2012; WHO 2020), which is microscopic particles of different composition and origin (Han et al. 2020; Weuve et al. 2012). In the northern part of the Indian subcontinent, the most common PM is mineral dust from the Thar Desert, around half of which is large PM (50 %) (Gobbi et al. 2000; Sarkar et al. 2019). These particles are also known to be rich in nitrates that a photo-induced “re-noxification” process converts into NOx (Ndour et al. 2009). Nevertheless, in this region, the most problematic and dangerous PM is generated by human activity in the form of energy production, vehicular transportation and construction (Chernysheva et al. 2018). It comprises a mixture of trace elements, black carbon, dibenzofurans, polychlorinated biphenyls (PCBs) and polycyclic aromatic hydrocarbons (Alghamdi 2016; Łukowski et al. 2018). PM of all types is often suspended in the air for weeks and travels great distances, even between continents (Lin et al. 2014).
PM can enter the human body via the respiratory tract and is harmful to human health (Jędrychowski et al. 2015). Long-term exposure to airborne PM causes severe respiratory disorders, such as breathing difficulties, worsening asthma symptoms and chronic bronchitis, as well as diseases that affect all segments of the community such as cardiopulmonary diseases and lung cancer (Hsu et al. 2015; Kim et al. 2015; Saravia et al. 2013). Outdoor air pollution, mainly PM2.5 (PM particles less than 2.5 µm) caused 4.2 million premature deaths worldwide in 2016 (WHO 2017). After Bangladesh, India is the country with the most polluted air. New data reveal that air pollution shortens the average Indian lifespan by 5.2 years and average PM concentration in the country has risen by approximately 42 % since 1998 (Greenstone and Fan 2020). Today, almost the entire Indian population is exposed to levels of PM that exceed WHO guidelines (WHO 2020).
Plants, especially trees and shrubs, play an important role in the adsorption and reduction of PM concentrations in the air (Łukowski et al. 2020; Popek et al. 2015; Pugh et al. 2012). They are effective at accumulating PM on the surface of leaves, stems and bark, while being eco-friendly and in line with public needs (Popek et al. 2017). However, the ability to capture PM on leaves is strongly linked to the characteristics of the species (Jouraeva et al. 2002; Sæbø et al. 2012). Plant shape and porosity (Leonard et al. 2016), leaf surface morphology, the complexity of the layer of cuticular waxes, the arrangement of stomata and the presence of trichomes on leaves (Dzierżanowski et al. 2011; Haynes et al. 2019; Prusty et al., 2005) are very important. Urban greenery is able to remove significant amounts of pollutants from the air in cities (Kroeger et al. 2018; Pugh et al. 2012; Vailshery et al. 2013; Yang et al. 2005), and therefore air phytoremediation is becoming increasingly popular worldwide, especially as it does not involve any tangible costs (Paton-Walsh et al. 2019).
Unfortunately, the accumulated PM has a negative impact on plants, including trees and shrubs (Li et al. 2019; Mina et al. 2018; Popek et al. 2018a; Siqueira-Silva et al. 2016; Singh et al. 2019; Zhou et al. 2018). The PM aerosols can exert climatic effects by absorption and scattering of solar radiation, and cloud condensation nuclei activity (Luo et al. 2019). PM accumulated on the surface of foliage changes its optical properties due to the absorption/reflection of photosynthetic active radiation (PAR) or clogging/damage to stomata (Li et al. 2019; Singh et al. 2019). Jin et al. (2021) report that PM adsorbed on leaves is usually concentrated in the stomata or the corrugated areas around the stomata, and PM up to 2 µm can enter or block the stomata. As a result, gas exchange and the intensity of photosynthesis and transpiration are much less efficient (Li et al. 2019; Mina et al. 2018; Popek et al., 2018b). The PM may include toxic substances, such as heavy metals (HM) or organic pollutants, which can penetrate from the leaf surface to the inner plant tissues (Luo et al. 2019; Przybysz et al. 2019). There are growing reports that PM induces oxidative stress (Ghorbanli et al. 2007; Mudway et al. 2020; Piacentini et al. 2019). Prolonged exposure to higher concentrations of PM may cause different morphoanatomical (decreased plant biomass and height, disturbance in plant development, leaf chlorosis and necrosis, leaf thickness alteration, modification of the structure and chemical composition of waxes, cell turgor loss and cellular collapse) and physiological (decreased photosynthetic pigments and leaf water content, increased leaf temperature, nutritional alteration in leaflets, and early leaf senescence and abscission) alterations in foliage (Mina et al. 2018; Siqueira-Silva et al. 2016; Zhou et al. 2018). In addition, PM can change the pH and chemical composition of the soil and indirectly affect plant performance (Luo et al. 2019; Piacentini et al. 2019; Siqueira-Silva et al. 2016).
Plants growing in an environment with a polluted atmosphere are characterised by various modifications that enable them to survive in difficult growing conditions. Changes may relate to the frequency, density, location and size of the stomata (Gostin 2009; Kiyomizu et al. 2019). In order to protect gas exchange from the adverse effects of PM, smaller stomata are located on the abaxial side of the leaf (Gostin 2009; Li et al. 2019). Some species increase mesophyll thickness at sites with high pollution, which may decrease the flux of air pollutants inside leaves and thus the uptake of air pollutants by leaf tissues (Kiyomizu et al. 2019). Leaf trichomes and grooves appear to have a role in protecting plants from PM exposure (Li et al. 2019). The higher groove proportion and presence of trichomes on the leaf surface absorbs some PM and buffers its negative effect on stomata (Li et al. 2019). Air pollutants accumulated on plant foliage may also be mitigated by phyllosphere microbes (Wei et al. 2017). To counteract the oxidative stress induced by PM, plants increase the activity of the antioxidant system, including enzymes such as peroxidase and catalase (Ghorbanli et al. 2007; Mudway et al. 2020).
As mentioned above, atmospheric PM often contains heavy metals (Ghasemi et al. 2020). A considerable quantity of atmospheric heavy metals is absorbed via the foliar organs of plants after the wet or dry deposition of atmospheric fallouts on the plant canopy (; Liu et al. 2019; Przybysz et al. 2019; Shahid et al. 2017). Heavy metal uptake from the air greatly depends on a number of factors, including the physico-chemical characteristics of the cuticle and metals, the chemical and physical forms of the adsorbed metal, the morphology and surface area of the plant leaves, the surface texture of leaves (pubescence and roughness), exposure duration, environmental conditions, plant gas exchange, concentrations of atmospheric PM, and PM size, load and composition (Shahid et al. 2017; Sharma et al. 2020). Not all airborne heavy metals are immobilised on the foliage surface; some heavy metals linked to PM can enter plant leaf tissues and can be translocated to the stem below and roots through the vascular sap (Sharma et al. 2020; Uzu et al. 2010). The concentrations of heavy metals in the foliage of plants growing close to the emission source are usually high (Mori et al. 2015; Noh et al. 2019; Zhu et al. 2019). The considerable accumulation of heavy metals derived from PM is due to the direct transfer of contaminants from the atmosphere to foliar organs but also due to the atmosphere-soil-root transfer (Liu et al. 2019). Heavy metals accumulated by plants disturb most physiological, metabolic and biochemical processes (Shahid et al. 2017).
One of the enzymes involved in plant responses to abiotic stress (including salt, UV light, drought and particularly oxidative stress and heavy metals) is heme oxygenase (HO) (Hancock and Russell 2021; He and He 2014; Mahawar et al. 2021; Wegiel et al. 2014). In plants (Arabidopsis thaliana L.), the HO family comprises four members that fall into two subfamilies: the HO1 subfamily (HO-1, HO-3, HO-4) and the HO2 subfamily (HO-2) (Fang et al. 2021). The catalytic action of HO-1 is the breakdown of heme. This is an oxygen-dependent reaction that uses NADPH as a cofactor and generates biliverdin, carbon monoxide (CO) and iron (Hancock and Russell 2021;Wilks 2002). This reaction is essential in physiological processes as diverse as iron reutilisation and cellular signalling in mammals, synthesis of essential light harvesting pigments (e.g. phytochrome chromophore formation) in cyanobacteria and higher plants, and the acquisition of iron by bacterial pathogens (Lecube et al. 2014; Wilks 2002). In plants, HO-1 is also associated with root development and crosstalk between NO, CO and hydrogen peroxide (Lecube et al. 2014). According to Lawal et al. (2015), in a human HO-1 protects endothelial cells from the toxicity of air pollutant chemicals.
Until now, city planners have selected plants for urbanised areas primarily on the basis of their decorative value and tolerance to urban abiotic stresses. Recent findings have led to consideration starting to be given to the ability of plants to purify ambient air from PM. Research on the phytoremediation properties of urban plants is being conducted worldwide. However, to date there is no universal formula for assessing whether a given species is useful for air phytoremediation and thus experiments should cover the widest possible number of species occurring under different climatic conditions. Therefore, the aim of this study was to examine 10 tree and shrub species recommended for planting in the Indian city of Jodhpur (Rajasthan) on the edge of the Thar Desert and determine: (1) the accumulation of surface and in-wax PM (both in three different size fractions), (2) the amount of epicuticular waxes on foliage, (3) the concentrations of heavy metals (Cd and Cu) on/in the leaves of the examined species, and (4) the level of heme oxygenase enzyme in leaves that accumulate PM and heavy metals.