Pollution, 6(4): 827-848, Autumn 2020 DOI: 10.22059/poll.2020.303151.821 Print ISSN: 2383-451X Online ISSN: 2383-4501 Web Page: https://jpoll.ut.ac.ir, Email: [email protected]

Physiological and Growth Responses to Pollutant-Induced Biochemical Changes in Plants: A Review

Mulenga, C.1,3*, Clarke, C.2, Meincken, M.1

1. Department of Forest and Wood Science, Stellenbosch University, Bag X1 Matieland 7602, Stellenbosch, South Africa 2. Department of Soil Science, Stellenbosch University, Bag X1 Matieland 7602, Stellenbosch, South Africa 3. Department of Biomaterials Science and Technology, Copperbelt University, P. O. Box 21692, Kitwe, Zambia

Received: 19.05.2020 Accepted: 01.07.2020

ABSTRACT: Industrial activities compromise the ambient air quality at a local, regional and global level through gaseous and dust emissions. This study reviews uptake mechanisms and the associated phytotoxicity of pollutants in plants, focusing on heavy metals and SO2. It further describes detoxification mechanisms and the resultant biochemical and physiological changes in plants. Finally, the morpho-physiological and growth responses to stress-induced biochemical changes are discussed. Heavy metals and SO2 enter the plant tissue through the stomata, cuticular layers, lenticels and root hairs. In 2- 2- the plant cells, SO2 converts to SO3 or SO4 ions upon reacting with water molecules, 2- which in excess are toxic to plants. However, the detoxification process of SO3 increases the production of reactive oxygen species (ROS). ROS are toxic to plants and damages biomolecules such as lipids, proteins, carbohydrates and DNA. On the other hand, heavy metals, such as Cu and Fe catalyse the Fenton/Haber-Weiss reactions, breaking down H2O2 into OH•. Additionally, Pb and Zn inhibit the activities of ROS-detoxifying enzymes, while other heavy metals bind to cellular layers making them rigid, thereby reducing cell division. Therefore, pollutant toxicity in plants affects biochemical parameters damaging organic molecules and limiting cambial activity. Damaged biomolecules inhibit the plant's capacity to carry out physiological functions, such as photosynthesis, stomatal functions, transpiration and respiration while impaired cambial activity reduces cell division and elongation resulting in reduced plant growth and productivity.

Keywords: Heavy metals, SO2, biomolecule damage, physiological functions, cambial activity.

INTRODUCTION oxides (NOx), Carbon dioxide (CO2) and Industrial pollution sources produce a wide Carbon monoxide (CO). Comparatively, the range of pollutants in a combined form composition of dust emissions may include including gases and dust emissions heavy metals, such as Zinc (Zn), Manganese depending on the industrial processes of a (Mn), Copper (Cu), Iron (Fe), Nickel (Ni), particular site. Gaseous pollutants may Mercury (Hg), Cadmium (Cd), Chromium account for Sulphur dioxide (SO2), Nitric (Cr), Lead (Pb) and Aluminium (Al). Most pollutants emanating from industrial * Corresponding Author, Email: [email protected] processes are aerodynamic (Ncube et al.,

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2014) and are therefore dispersed by wind polluted environments. Seyyednejad & and the constituents deposited across the Koochak (2013) argued that plant response nearby landscape. Gaseous pollutants and to environmental toxicities depends on particulate matter become available for factors, such as plant species and age, the uptake by plants via the leaf stomata and pollutant type and exposure conditions, such cuticles, bark lenticels and root hair. as duration, levels and season. The observed Heavy metals, such as Mn, B, Fe, Mo, changes in morphological and physiological Ni, Cu and Zn are required in trace amounts characteristics suggest the activation of as plant micronutrients (Etienne et al., 2018; strategic adaptation mechanisms in Tripathi et al., 2015), while non-essential mitigating the detrimental effects of toxicants elements like Pb, Hg, Al, Cr, and Cd are in a stressful environment (Leghari & Zaidi, toxic to plant life even in traces 2013). (Emamverdian et al., 2015). Conversely, The phytotoxicity of SO2 and heavy research has shown that even those required metals in plants can be traced from in traces may become toxic to plants at biochemical reactions at the cellular level. elevated levels (Emamverdian et al., 2015; However, most reviews focus on the growth Kulshrestha & Saxena, 2016). According to and yield changes as a response to pollution Tripathi et al. (2015), Fe in excess of 2000 stress. This manuscript delineates the plant mg/kg in plants is considered toxic, while morpho-physiological and growth alterations Cu, Zn, Mn and B toxicity threshold stands in response to pollutant-induced biochemical at 25 mg/kg, 120 mg/kg, 200 mg/kg and 80 stress. It first reviews uptake mechanisms mg/kg, respectively. Further, non-essential and the associated phytotoxicity of pollutants elements exhibit phytotoxicity at such low in plants focusing on heavy metals and SO2. concentrations as 3 mg/kg (Al), 10 mg/kg Subsequently, enzymatic and non-enzymatic (Cd), 28 mg/kg (Pb) and 100 µg/kg (Cr) attempts at pollutant detoxification and the (Amari et al., 2017; Shanker et al., 2005). resultant changes in biochemical and Similarly, at low concentration SO2 physiological reactions are described and stimulates physiological processes and finally, the morpho-physiological and growth growth of plants growing in sulphur (S) responses to stress-induced biochemical deficient soil where sulphate is metabolised changes are discussed. to meet the demand for S as a nutrient (Khan & Khan, 2011). On the other hand, Uptake Mechanisms and Phytotoxicity 2- 2- of Sulphur Dioxide and Heavy Metals excess sulphite (SO3 ) or sulphate (SO4 ) ions resulting from increased uptake of SO2 Sources and Dispersion of by plants are toxic and affect plant growth Environmental Pollutants and productivity (Brychkova et al., 2007). There are two primary sources of Studies show that exposure to air pollutants in the environment, namely pollution alters the biochemical natural and anthropogenic sources. (Seyyednejad et al., 2013; Wang et al., 2009; Putrefying organic matter, volcanic Woodward & Bennett, 2005), morphological eruptions and solar action on seawater (Ahmed et al., 2016; Leghari & Zaidi, 2013; constitute the natural sources (Cullis & Pourkhabbaz et al., 2010; Salam et al., 2016; Hirschler, 1980; Singh et al., 2012), while Saleem et al., 2019) and physiological processes, such as smelting, refining and (Gupta & Sarkar, 2016; Sen et al., 2017; fossil fuel combustion account for human- Thakar & Mishra, 2010; Pourrut et al., 2011) induced sources (Gheorghe & Ion, 2011). characteristics of plants. Ultimately, the Figure 1 shows the most common sources pollutant-induced changes affect the growth of environmental pollutants, such as SO2, and productivity of plants growing in air NOX, VOCs, heavy metals, CO and CO2.

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Fig. 1. Common sources of natural and anthropogenically-induced environmental pollutants

1 Environmental pollutants such as SO2 singlet oxygen atoms- O2 (Das & and heavy metals emanating from Roychoudhury, 2014) another family industrial activities are aerodynamic and member of the toxic ROS, which also dispersed by the wind across a given includes hydroxyl radicals (OH•). Singlet landscape (Ncube et al., 2014). Therefore, oxygen causes severe damage to proteins, weather conditions and topography play an lipids, pigments and nucleic acids (Dogra essential role in dispersing these pollutants & Kim, 2020) putting photosystems and across landscapes around fixed pollutant photosynthetic machinery into jeopardy sources (Cassiani et al., 2013). (Das & Roychoudhury, 2014). On the other •– hand, O2 transforms into the more toxic 1 • Uptake and Toxicity of Sulphur Dioxide and reactive O2 and OH , which causes in Plants lipid peroxidation (Halliwell, 2006). SO2 enters the plant tissue either through H2O2 has two roles, depending on its leaves or roots (Lee et al., 2017). In leaves, intercellular concentration. It regulates the it penetrates through the stomata regulated signal for physiological processes such as by the guard cells. It further diffuses into 2- photorespiration, photosynthesis and the mesophyll cells and converts to SO3 2- senescence (Das & Roychoudhury, 2014; or SO4 ions upon reacting with water Tanou et al. 2009) at low concentration. At molecules (Khan & Khan, 2011). The high intercellular concentration, H2O2 internal (mesophyll) resistance to SO2 is oxidises methionine (-SCH3) and cysteine low, because it is highly soluble and (-SH) residues and inactivated Calvin cycle dissolves rapidly in the cell sap. Slow 2- enzymes iron superoxide dismutase (Fe- conversion of SO2 to SO3 leads to their 2- SOD) and Cu/Zn-SOD by oxidising their oxidation to SO4 and consequently thiol groups. Bienert et al. (2007) noted utilisation by plants (Brychkova et al., that the longer half-life of H2O2 enables it 2007; Friend, 1973; Khan & Khan, 2011). 2- 2- to traverse long distances and across cell Excess SO 4 or SO 3 is toxic to plant life, membranes through aquaporins covering although the latter is about 30 times more significant lengths within the cell and toxic (Thomas et al., 1943). cause oxidative damage. They further According to Omasa et al. (2008), the 2- 2- argued that H2O2 is responsible for detoxification process of SO3 to SO4 programmed cell death and 50% loss of increases the production of toxic reactive enzymatic activities at a high cellular oxygen species (ROS), hydrogen peroxide •– concentration. (H2O2) and superoxide radicals (O2 ). Additionally, OH• is generated by the Furthermore, stomatal closure triggers an Fenton and Haber-Weiss-type reactions insufficient concentration of intercellular and is the most toxic and reactive among CO2, which instigates the formation of the members of the ROS family (Barceló &

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Gómez Ros, 2009). According to Das & include the family members of the natural Roychoudhury (2014), OH• destroys resistance-associated macrophage protein cellular compartments through protein (NRAMP), zinc-iron permease (ZIP) and destruction, lipid peroxidation and heavy metal ATPases (adenosine) (HMA) membrane damage. localised in different parts of the root Furthermore, Pinto et al. (2003) compartments. Studies on Arabidopsis observed that the lack of enzymatic thaliana and Noccaea caerulescens show mechanisms to scavenge OH• triggers its that each family member from the three excess accumulation in plant tissues and main categories of transporters is involved cause cellular death. in the transportation of different ions depending on its affinity (Milner et al., Uptake and Translocation of Heavy 2013, 2014). For example, AtZIP2 is Metal in Plants localised in the plasma membrane and is Heavy metals penetrate the foliar surfaces involved in the uptake and transport of through the stomata, lenticels, ectodesmata Mn2+/Zn2+ into the root stellar cells while and cuticular cracks (Fernández & Brown, AtZIP1 acts as a vacuolar exporter. 2013; Shahid et al. 2016). Therefore, According to Lin et al. (2016), NcZNT1, a particle size plays an essential role in the homolog of AtZIP4 is a plasma membrane- adsorption of heavy metals into the leaves. localised transporter of Zn2+ and Cd2+ Smaller particles penetrate the plant leaves while (IRT1) absorbs Fe2+, Fe3+, Cd2+ and more quickly compared to the larger ones Zn2+ in the same plant species (Lombi et remaining stuck on the surface wax. al., 2002). NcZNT1’s promoter is mainly Eichert et al. (2008) reported the active in the cells of the cortex, endodermis penetration of small size nanoparticles (43 and pericycle of Noccaea caerulescens nm) of Cu into Vicia faba leaves, while the roots. larger sized particles (1.1 µm) failed to Additionally, the NRAMP family penetrate through the stomata. members specialise in transporting bivalent Heavy metals exist in the soil solution metal ions into the root cells (Milner et al., as ions where plant roots can access them. 2014). On the other hand, HMAs transports Heavy metals together with micronutrients both monovalent and divalent heavy metal are then absorbed by the root hair and ions in plants. Localised in the chloroplast transported via the symplastic and (AtHMA1) and plasma membranes apoplastic pathways and loaded onto the (AtHMA2 and AtHMA4), these HMAs xylem for upward translocation along the family members export ions from the transpiration stream (Luo et al., 2016; Page chloroplast across the cytosol into the et al., 2006). The transpiration stream vascular cylinder facilitating their movement transports heavy metals through the xylem from roots to shoots (Cun et al., 2014). from root tissues to different parts of the Further, some toxic metal ions form plant (Page & Feller, 2015). The rate and complexes with phytochelatins, which extent of translocation are dependent on include malate, citrate and histidine many factors, including the tree age and (Kozhevnikova et al., 2014; Kozlov et al., species as well as metal speciation 1999). According to Richau et al. (2009) (chemical form-free ion or complexed to a and Fourcroy et al. (2014), heavy metal ligand) (Adriano, 2001; Roberts et al., ions in the complex form are then absorbed 2005). Therefore, transporters - mainly into the root cells by oligopeptide and proteins - of essential micronutrients in the ATP-binding cassette transporters (ABC). soil solution facilitate the uptake of toxic Luo et al. (2016) argued that there is scant metals into the plant roots. Shi et al. (2019) information on the mechanisms governing noted that transporters of trace elements

830 Pollution, 6(4): 827-848, Autumn 2020 the uptake of heavy metals by woody biomolecules, especially lipids, proteins plants. They noted that scientific and nucleic acids. information suggests that the influx of In addition to their influence on the toxic metals into woody plant roots is generation of the ROS, heavy metals are higher than into herbaceous plants. For capable of singularly or in combination example, He et al. (2011) reported a 100 causing adverse effects on the cell times higher Cd2+ influx into the roots of compartments. Pourrut et al. (2011) woody Populus tremula x Populus alba observed that Pb induces its phytotoxicity than the herbaceous Triticum aestivum. through binding the Pb2+ to cell membranes and cell wall producing rigidity Phytotoxicity of Heavy Metals and in these cellular components leading to a Biochemical Responses in Plants reduction in cell division. It further The bioactivity of heavy metals partly promotes the production of abnormal cells depends on their physicochemical at the colchicine-mitosis stage through the properties grouped as redox-active and induction of disturbances in the cell non-redox active (Emamverdian et al., division stages M and G2. Further, Baran 2015; Jozefczak et al., 2012). Bielen et al. (2013) deduced that the phytotoxicity of (2013) explained that non-redox active Zn depends on the bioavailability factors, heavy metals have an indirect action on the plants species and plant development stage. toxification of plant life as compared to the Zn reduces the photosynthetic pigments direct role redox-active heavy metals plays. including total chlorophyll by disturbing Non-redox active metals cause oxidative Mg and Fe absorption and translocation stress by inducing ROS-producing into the chloroplasts (Emamverdian et al., enzymes, glutathione depletion, 2015). The disturbance affects the antioxidative enzymes inhibition and efficiency and functionality of the entire binding to sulfhydryl groups of proteins. photosynthetic machinery. In addition, the On the other hand, redox-active metals toxicity of Cu reduces total chlorophyll and generate oxidative injury by undergoing carotenoid content compromising the plant Fenton reactions, thereby producing ROS photosynthetic competence and reduce cell toxic to plant macromolecules. elongation (Li et al., 2018; Nicholls & Mal, Excess heavy metal concentrations 2003). Ni creates an artificial deficiency of trigger the formation of ROS toxic to plant Zn2+ and Fe2+ by outcompeting them cells injuring the macromolecules required during plant uptake resulting in chlorosis for healthy plant functioning. Upon expression in plants (Aydinalp & interacting with cytoplasmic proteins, Marinova, 2009; Emamverdian et al., heavy metals reduce the concentration of 2015). Fe and Zn deficiency affects plant the protein pool in plants (Gupta et al., growth parameters leading to poor 2010; Pourrut et al., 2013, 2011). Pourrut nodulation and reduced yield. et al. (2013) and Gupta et al. (2010) Further, studies have shown that Mn observed that a protein pool reduction toxicity reduces CO2 assimilation, total causes ROS-induced acute oxidative stress, chlorophyll content, root and shoot growth protease activity stimulation, gene depending on plant species and levels of expression modification and free amino light (Li et al. 2010). Other metals, such as acid reduction. Yadav (2010) noted the Al3+ binds to DNA and hinders cell generation of ROS is a well-known division in roots due to improved rigidity attribute of heavy metal toxicity in plants. of double helix in cells walls and DNA He argued that ROS targets cellular (Steiner et al., 2012). In the process, it antioxidants reserves, and upon exhaustion, leads to perturbations in the absorption and they quickly attack and oxidise all types of

831 Mulenga, C. et al. translocation of Ca, Mg, P and K nutrients. Pathway and Detoxification of Reactive It further causes necrosis and chlorosis in Oxygen Species in Plants young and older leaves, respectively and Heavy Metal-Induced Generation of ROS decreases stomatal regions and ROS are produced under natural and photosynthetic activity (Batista et al., 2013; pollutant-induced conditions in various Trevizan et al., 2018). locations, including the plasma Additionally, the phytotoxicity of Arsenic membranes, chloroplasts, peroxisomes, (As) depends on its bioavailability and mitochondria and the cell wall (Gurda et speciation (Mohan & Pittman, 2007). In the al., 2012; Pucciariello et al., 2012). Under 3- oxidation state, Arsenate (AsO4 ) and natural conditions, incomplete reduction of 3- Arsenite (AsO3 ) also referred to as As(V) oxygen (O2) lead to the generation of ROS and As(III), respectively, are the main as unavoidable byproducts of aerobic species of As in the environment (Joseph et metabolism (Asada, 2006). The reduction al., 2015). In plant tissues, As(V) is of O2 to water (H2O) during the healthy •– converted to mobile, soluble and toxic cellular metabolism produces O , H2O2 As(III); a process leading to the production and OH• through energy or electron of ROS through the utilization of O2 as the transfer reactions (Shahid et al., 2014). final receptor of electrons (Talukdar, 2013). Several studies (Kumar et al., 2012; Sharma (2012) added that electron leakage Achary et al., 2012; Sheng et al., 2015; Sun and enzyme inhibition during the conversion et al., 2010; Valko et al., 2005) reports of As(V) to As(III) create pathways for ROS increased production of ROS in plants production in plants. Furthermore, As(V) exposed to heavy metal-induced stress. The conversion is followed by the biomethylation reported increase in ROS under pollutant- of As generating methylated forms of As induced conditions is attributed to the such as tetramethylarsonium ions, imbalance between its generation and monomethylarsonic and arsenobetaine, elimination (Kováčik et al., 2010). which are more reactive with O2 favouring Furthermore, Pourrut et al. (2011) observed the formation of ROS (Abbas et al., 2018). In that heavy metals deplete ROS scavenging addition to ROS generation, As(III) toxicity glutathione (GSH) and many other disrupts plant metabolism by reacting with antioxidants, thereby disrupting the ROS sulfhydryl groups of proteins and enzymes, balance through its enhanced production thereby causing detrimental effects on plant and accumulation in plant tissues. cells (Akter et al., 2006). On the other hand, Specifically, the metal-induced remnant As(V) interferes with the ATP generation of ROS in plants is dependent molecule by generating unstable ADP-As on the nature of the metals involved. which affects energy flow in cells and causes Redox-active heavy metals, e.g. Cu and Fe, cell death (Manzano et al., 2015). catalyse the Fenton and Haber-Weiss Several studies have demonstrated that reactions, respectively (Barceló & Gómez As exposure in plants inhibit root extension Ros, 2009). On the other hand, redox- and promote stunted growth (Nel et al., nonactive metals, e.g. Pb and Zn, inhibit 2006), reduces gaseous exchange and the activities of enzymes (Opdenakker et damage chloroplast membranes (Anjum et al., 2012). For example, Pourrut et al. al., 2011; Debona et al., 2017) and damage (2011) and Shahid et al. (2014) noted that cellular membranes leading to reduced Fe and Cu catalyse the Fenton reaction at • stomatal conductance, photosynthesis, neutral pH breaking down H2O2 into OH , transpiration, water transport and nutrient whereas Pb and Zn have a high affinity for uptake (Gill & Tuteja, 2010; Sharma et al. -SH groups, affecting the healthy 2012). functioning of enzymes.

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In the initial stages, ROS are unable to Das & Roychoudhury (2014), ROS causes cause damage, because different extensive damage to proteins, DNA, lipids antioxidant mechanisms scavenge them. and carbohydrates. Pourrut et al. (2011) However, the balance between ROS argued that the indirect effect of heavy production and elimination is easily metals on plants via organic molecules- disturbed by factors ranging from abiotic to damaging ROS generation are rapid and biotic stresses. Abiotic stress factors toxic than their direct effect. include: gaseous pollutants, drought (water Lipids provide energy for cellular deficiency conditions), high light intensity metabolism, cell membrane building and and temperature, soil salinity (excess Na+, organelle maintenance, among other K+ and Cl- ions) and heavy metals, while functions (Møller et al., 2007; Xiao & pests and diseases cause biotic stress. Chye, 2011). However, through the According to Choudhury et al. (2013), production of excess ROS, heavy metals peroxisomes and chloroplasts are the leading trigger lipid peroxidation (LPO). LPO is producers of ROS in the presence of light the worst form of heavy metal and mitochondria take charge under dark phytotoxicity, because it deteriorates cell reactions. In the chloroplast, ROS are membranes. Das & Roychoudhury (2014) produced by the core light-harvesting system noted that lipid radicals initiated by the composed of photosystems, PSI and PSII. As LPO chain reaction and oxidative stress a consequence, water stress, low CO2 and causes damage to DNA and proteins. The excess light necessitates the formation of polyunsaturated fatty acids (PUFA) are the •– O2 at the PS through a Mehler reaction (Das hotspots for ROS-induced damage. PUFAs •– 1 & Roychoudhury, 2014) and O2 then are prone to ROS attack, especially O2 and converts into the more toxic OH• via the OH•, but the latter is more destructive as it Fenton reaction. Furthermore, Das & triggers cyclic chain reactions causing Roychoudhury (2014) noted that further peroxidation of several PUFAs. mitochondrial ETC (mtETC) houses Additionally, heavy metal-induced ROS electrons with sufficient energy to reduce affects the structure and synthesis of oxygen and generate ROS. Complex III and proteins in plants by changing the protein Complex I are the primary components of quality and quantity through several mtETC responsible for ROS production mechanisms. The mechanisms include: 1) (Noctor et al., 2007). Mitochondria generally binding metal ions to free protein produce ROS in normal conditions, but are functional groups and 2) replacing significantly boosted under stressful micronutrients in metal-dependent proteins conditions (Pastore et al., 2007). with free heavy metal ions (Shahid et al., Peroxisomes are the main production sites of 2014). Ultimately, heavy metal-induced intercellular H2O2 hydrogen peroxide ROS quantitatively reduces the total generation, because of their integral protein content in cells. The quantitative oxidative metabolism ( o & Puppo, 2009). reduction of proteins results from the Wrzaczek et al. (2011) further noted that like modification of gene expression, reduced mitochondria and chloroplast peroxisomes amino acid content, consumption of ROS- •– produce O2 during various metabolic scavenging amino acids and increased processes. ribonuclease activity (Gupta et al., 2010). Although the mechanisms governing the The ROS-Induced Destruction of heavy metal-induced genotoxicity is not fully Organic Molecules understood, research has shown that ROS The three significant biomolecules at the instigates the propagation of heavy metal- receiving end of ROS attack in plants are: induced DNA damage in plant cells (Barbosa DNA, proteins and lipids. According to

833 Mulenga, C. et al. et al., 2010; Shen et al., 2012). According to agent. The AA cellular pool is replenished Das & Roychoudhury (2014), ROS severely by MDHAR and DHA using NADPH and attacks mitochondria and chloroplast DNA DHAR as reducing agents, respectively due to a lack of histones and associated (Shi et al., 2019). proteins and the proximity to the ROS generation machinery. The OH• is the most Detoxification of ROS through Non- reactive member of the ROS family and Enzymatic Antioxidants damages all components of DNA molecules Non-enzymatic antioxidants are other plant upon interaction (Hirata et al., 2011). For defense mechanisms utilised to detoxify example, the interactions between DNA and the stress-induced ROS. These include: α- ROS lead to the destruction of DNA-protein tocopherol, proline, ascorbic acid, cross-links, base modifications and deletions, flavonoids, carotenoids and GSH. Shi et al. as well as pyrimidine dimers damage and (2019) and Das & Roychoudhury (2014) strand breaks (Pourrut et al., 2013). Barbosa argued that ascorbic acid is the most et al. (2010) and Pourrut et al. (2011) abundant antioxidant capable of donating reported DNA damage in response to heavy electrons to a range of both non-enzymatic metal stress. and enzymatic reactions. The substantial accumulation of ascorbic acid in the Detoxification of ROS through cytosol and apoplast places it first in the Enzymatic Antioxidants defense line against ROS attack (Omasa et The ubiquitous superoxide dismutase (SOD) al., 2002; Smirnoff & Wheeler, 2000). It forms the first line of defense against ROS- protects cell membranes from ROS- induced phytotoxicity. As a catalyst, SOD induced damage by reacting with OH•, •– •– promotes the breakdown of O2 into H2O2 H2O2, and O2 to regenerate α-tocopherol and O2 avoiding the formation of the more from tocopheroxyl radical. At a cellular toxic and reactive OH• (Hossain et al., level, ascorbic acid plays a role in cell 2015). SOD are common ROS-scavenging division, cell wall synthesis and protection antioxidants found in different cellular (Seyyednejad & Koochak, 2013). Studies components and are classified based on the have shown that in air polluted ions binding them. Examples are manganese- environments, the content of AA is higher SOD in the mitochondria, iron-SOD in the for tolerant plants than sensitive species chloroplast and copper/zinc-SOD found in (Sen et al., 2017; Seyyednjad et al., 2011). the peroxisomes, chloroplasts and cytosol As a free radical scavenger, proline (Das & Roychoudhury, 2014; Kim et al., protects plants from ROS-induced damage 2009). Other known ROS-eliminating (Seyyednejad et al., 2011) by scavenging • 1 antioxidant enzymes include guaiacol OH , and O2 and inhibits the damages peroxide (GPX) catalase (CAT), glutathione caused by LPO. Studies have reported reductase (GR), dehydroascorbate reductase elevated concentration of proline in plants (DHAR), monodehydro- ascorbate reductase exposed to pollution stress. The (MDHAR) and ascorbate peroxidase (APX). accumulation of proline in stressful Das & Roychoudhury (2014) argued environments is attributed to either its that CAT has a high affinity for H2O2 reduced degradation or enhanced catalysing the dismutation of 6x106 production (Das & Roychoudhury, 2014). molecules of H2O2 to O2 and H2O under a Kameswaran et al. (2019) argued that its minute. They further noted that APX ability to accumulate in plants during eliminates H2O2 in the chloroplast and pollutant stress is beneficial to plants for cytosol reducing it to H2O and the role it plays in ROS elimination than dehydroascorbate (DHA). In this process, the other more effective amino acids, e.g. ascorbic acid (AA) is used as a reducing tyrosine, tryptophan and histidine.

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Seyyednejad et al. (2009) and Wang et GSH is involved in cell division, al. (2009) report that because of the positive differentiation, growth, senescence and correlation between proline content and SO2 death (Shahid et al., 2014). It is found in concentration in some species, there is need most plant cellular compartments and to re-designate SO2 toxicity threshold for performs multiple functions, such as particular species. For example, significant regulating sulphate transport, enzymatic accumulation of soluble sugar and proline activities and synthesising proteins, have been reported in Eucalyptus nucleotides, phytochelatins, detoxifying camaldulensis in a polluted site compared to xenobiotics and protection against abiotic reference samples (Seyyednejad & stress (Mullineaux & Rausch, 2005). They Koochak, 2011). Furthermore, Wang et al. noted that GSH participates in both (2009) explained that there is a positive enzymatic and non-enzymatic activities and correlation between lipid peroxidation and scavenges on all types of ROS to protect proline accumulation in plants exposed to different organic molecules. Furthermore, air pollutants. Earlier studies (Tankha & GSH is involved in the regeneration of AA, Gupta, 1992; Woodward & Bennett, 2005), which is a ROS scavenger. reported increased proline accumulation in the leaves of plants subjected to SO2, heavy Morpho-Physiological Responses to metals and salt stresses. Therefore, proline Stress-Induced Biochemical Changes accumulation plays a vital role in inhibiting Photosynthesis pollutant-induced toxification in plants. There is overwhelming evidence According to Das & Roychoudhury documenting the changes in the (2014), carotenoids are localised in both non- photosynthetic activity of plants grown in photosynthetic and photosynthetic plant polluted environments. The decrease in the tissues. Carotenoids are natural fat-soluble photosynthetic processes results from the pigments and play a role in the plant’s damage caused by biochemical reactions in photosynthetic processes (Seyyednejad et al., plant leaves (Enete et al., 2013; Joshi & 2011). Like chlorophyll, carotenoids gather Swami, 2007; Sen et al., 2017). Thakar & light energy in chloroplasts and protect Mishra (2010) and Joshi et al. (2009) chlorophyll from photooxidative destruction reported a correlation between (Seyyednjad et al., 2011). Furthermore, photosynthesis rate and specific carotenoids protect the photosynthetic biochemical parameters. They reported 1 machinery by scavenging O2 and generating reduced chlorophyll, water content, heat energy as a byproduct (Shahid et al., ascorbic acid and leaf extract pH with 2014). They also react with LPO products, decreasing photosynthetic activity in thereby ending the chain reaction and plants. Similarly, Ali et al. (2015) and transferring energy to chlorophyll molecules Ahmad et al. (2015) cited heavy metal (Das & Roychoudhury, 2014). Some interference with chloroplast replication researchers (Kováčik et al., 2012; Prajapati and cell division. They noted that Cd, Cu & Tripathi, 2008; Seyyednejad et al., 2011) and Pb reduce the number of chloroplasts have reported a reduction in the content of per cell, resulting in inhibition of carotenoid pigments in leaves in response to chlorophyll biosynthesis or impairment in pollution stress. For example, Kováčik et al. the supply of essential micronutrients. (2012) reported reduced water content, Therefore, the inhibition of chlorophyll sugar, chlorophylla, chlorophyllb and biosynthesis deprives leaves of carotenoids in Tillandsia albida exposed to photoreceptors required during Cd and Ni stress. photosynthesis.

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Respiration and Transpiration Therefore, alterations in the stomatal Prolonged exposure of plants to excessive function reduce plant growth by changing SO2 and heavy metals leads to the the production and translocation of development of symptomatically visible photosynthates. The reported decrease in injury to tissues and hidden physiological stomatal frequency is an adaptive measure disturbances. According to Koziol & aimed at preventing SO2 entry into the Whatley (1984), respiration taking place in leaves (Lee et al., 2017). In addition, the several sites of the cell (mitochondria, erosion of epicuticle wax structures around cytoplasm and peroxisomes) is either the stomata facilitates SO2 entry into stimulated or inhibited depending on the internal leaf spaces causing tissue damage degree of tissue injury. Notably, the repair and plant death (Lee et al., 2017; Taylor, process uses energy from the non-damaged 1978). adjacent tissues to the necrotic ones, According to Gupta & Sarkar (2016), thereby increasing the rate of transpiration most pollutants can upset the water balance in different cell sites (Gupta & Sarkar, in leaves, because they interfere with the 2016). In the process, energy and function of the stomatal aperture. They carbohydrates required for cell division and argued that although the cuticle acts as a growth are wasted through enhanced barrier to the exchange of gases and water respiration in response to pollution. Plant between the atmosphere and plant leaves, exposure to higher SO2 concentration gaseous pollutants and acidic water reduces the net photosynthesis, while molecules reduce the integrity of the increasing the respiration rate (Addison et cuticular layers. Loss of cuticular integrity al., 1984; Gheorghe & Ion, 2011; Koziol & leads to a considerable flux of ions Whatley, 1984). The trade-off affects the between cytoplasmic solutions and plant carbon balance and causes acute depositions on the leaf surfaces and visible damage and reduces growth rates cytoplasmic solutions (Winner & Atkinson, (Ashraf & Harris, 2013). According to 1986). The cuticular layer of leaf and Miller (1988), the balance between CO2 needle surfaces consists of waxes and required for respiration and photosynthesis cutin, offering the plant protection against expresses the net CO2 exchange during the air pollutants, insect attack, pathogen light period. He further argued that this infection and hostile environmental measurement singularly does not account conditions, such as frost and wind (Weigel for respiratory processes during the dark et al., 1989). These surfaces present the period nor help identify the complete initial contact and point of attack between physiological basis of the effect of air pollutants and plants. The reaction between pollution stress on plants. oxygen radicals and aromatic compounds destroys the wax layer, thereby Stomatal Function and Erosion of the compromising its ability to protect plants Cuticular Layer (Dhanyalakshmi et al., 2019; Shepherd & Exposure to air pollutants undermines the Wynne, 2006). Studies in on fir and spruce ability of guard cells to close and open due trees show that the early signs of plant to accumulating sulphur, heavy metals and exposure to gaseous pollutants are the suspended particulate matter on the leaf erosion of wax layers on stomatal regions surface (Lee et al., 2017). Consequently, (Harrington & Carlson, 2015). excess accumulation of pollutants on leaf surfaces affects gas exchange and reduces Foliar Dimensions and Injury biochemical activities, inhibits Leaf morphology has been used over the photosynthesis and impairs reproductive years to study the effects of environmental processes in plants (Chaurasia et al., 2013).

836 Pollution, 6(4): 827-848, Autumn 2020 pollution on plant growth. Changes in leaf symptomatic damage may range from a length, breadth and petiole length are change in leaf colour to leaf injury. Studies indicative of biochemical and physiological have reported brown or white spots as the disturbances caused by air pollution primary symptoms further adding yellow (Seyyednejad et al., 2009). Several studies spots, discolouration and necrotic report significant reductions on leaf appearance of leaf surfaces (Ahmed et al., dimensions and the number of leaves on 2016; Lee et al., 2017). trees growing in polluted sites (Assadi et al., 2011; Chukwuka & Uka, 2014; Leghari & Effect of Stress-Induced Physiological Zaidi, 2013; Pourkhabbaz et al., 2010; Sen and Morphological Changes on Plants et al., 2017; Seyyednejad et al., 2009; Plant Growth and Yield Seyyednejad & Koochak, 2013). Thompson (1981) studied the impact of Seyyednjad et al. (2011) attributed the copper smelting activities on the growth of reduction in leaf size and frequency to Pinus monophyla. He established three reduced leaf production and enhanced distinctive periods, i.e. a low copper premature senescence. Leaf area reduction production period between 1840 and 1908, leads to reduced absorbed radiation higher production from 1910 to 1930 and culminating in decreased photosynthesis low mining activity from 1935 until 1970. (Seyyednjad et al., 2011; Tiwari et al., Before the intermediate period, radial 2006). growth recorded on polluted and control The decline in plant foliar characteristics sites were not significantly different. is an adaptive measure providing reduced However, lower mean ring widths were leaf contact area with air pollutants, thereby observed at the pollutant-stressed site. The improving the plant resistance against growth rate reduced significantly during pollutant-induced stress. Besides, reduced the period of increased mining activities, leaf area balances the leaf tissue water yielding hardly reconstructable small rings content and increases the leaf tolerance in some trees at polluted sites. The growth levels under stressful conditions (Kuddus et patterns of P. monophyla during this period al., 2011; Leghari & Zaidi, 2013). were attributed to increased pollution Furthermore, research has shown that emanating from enhanced mining significant morphological changes caused by activities. However, significant increases in environmental pollutants - including heavy tree ring widths were observed after the metals and SO2 - in woody plants are high production period from 1935 until reductions in the growth of aerial parts and 1970. The accumulative deposition of leaf size, stomatal damage and leaf injury, mineral nutrients, which could have been necrosis and chlorosis (Dumčius et al., 2011; inadequate before the pollution peak period Salam et al., 2016; Seyyednjad et al., 2011). may have contributed to this unexplained Further to foliar dimensions, other growth pattern between 1935 and 1970. symptoms, such as necrotic spots and Unfortunately, there was no follow-up defoliation appear on leaves and tree study undertaken to confirm the results and branches following exposure to air establish factors, which contributed to contaminants at different concentrations increased tree growth in the aftermath of and duration of exposure (Ncube et al., excessive mining pollution. 2014). These symptoms are indicative of Battipaglia et al. (2010) studied the changes to plant biochemical reactions effects of exhaust pollution on the growth damaging the leaf pigments (Lee et al., of Pinus pinea along a high traffic road. 2017). Depending on the exposure They evaluated the correlations between conditions and plant species, significant the concentration of C and N stable

837 Mulenga, C. et al. isotopes and ring widths between 1955 and the formation of false rings around the 2005. The period between 1955 and 1979 latewood. before the road construction was marked as Fox et al. (1986) reported significantly unpolluted and the polluted period lower growth rates for periods characterised the time after the road corresponding to peaks in SO2 emissions. construction between 1980 and 2005. A Furthermore, the resumption of the average positive correlation was detected, showing growth in Larix occidentalis was observed significant differences between 13C mean immediately after a reduction in the values and tree radial growth before road emission levels. Other studies have construction. Furthermore, the 13C reported similar growth patterns of increased with decreased tree ring width Quercus pubescens and Pinus sylvestris after 1980, post road construction period. exposed to stressful environmental Safdari et al. (2012) assessed the growth conditions (Kincaid & Nash, 1988; Perone response of Pinus elderica to air pollution. et al., 2018; Seftigen et al., 2013; Singh et For the three sites studied (non-polluted, al., 2017). Seftigen et al. (2013) noted semi-polluted and polluted), the average adverse growth effects in Pinus sylvestris highest and lowest ring widths were than Picea abies after nitrogen deposition. reported at the pollutant-stressed and non- They argued that the reduction in nitrogen polluted sites, respectively. They further and other acidifying compounds resulted in observed the presence of false rings in improved pine growth without significant samples extracted from polluted and semi- impact on the growth of spruce. The results polluted sites. The transition from suggest that Pinus sylvestris is more earlywood to latewood was abrupt at the susceptible to changes in the acidification polluted and semi-polluted sites, while and nitrogen levels of forest ecosystems control samples recorded a gradual than Picea abies. Table 1 shows observed transition. The reported abrupt transition in growth adjustments on selected species on pollutant-stressed locations was affected by exposure to certain stress conditions. Table 1. Species-specific observed growth and yield alterations after exposure to different environmental stresses Stress and source Plant species Observed changes Author(s) *root elongation and biomass production Dose-response experiment Fagus sylvatica *root hair formation (Breckle & Kahle, 1992) (Pb, Cd) **root branching system **root secondary and primary laterals *ring width during higher Cu Copper smelter production Pinus monophyla (Thompson, 1981) (SO2, NOx, HM, PM) ** ring width during low Cu production after the higher Cu mining period *tree ring width after the road Pinus pinea (Battipaglia et al., 2010) construction Vehicular exhausts (Pb, **ring widths Hg, CO , NO , PM, VOCs, 2 x **false rings CO, SO ) Pinus elderica (Safdari et al., 2012) 2 **abrupt transition from earlywood to latewood Lead-Zinc smelter (SO2) Larix occidentalis *radial growth (Fox et al., 1986) Steel factory (HM) Quercus pubescens *radial growth (Perone et al., 2018) *radial growth in Pinus Sylvestris Sulphate, Nitrate and Picea abies without significant effects on Picea (Seftigen et al., 2013) Ammonium Pinus sylvestris abies *Reduced **Increased

838 Pollution, 6(4): 827-848, Autumn 2020

Table 1 illustrates that plant species formation and characteristics. The impact respond differently to varying of gaseous and heavy metal stresses on environmental stresses. Tolerant species cambial activity and characteristics of are capable of withstanding more extreme wood cells both under laboratory and field exposure conditions compared to sensitive conditions were evaluated. Iqbal et al. ones. Generally, plant growth and yield are (2010) and Rajput et al. (2008) observed profoundly affected by biochemical and confluent vasicentric axial parenchyma morpho-physiological alterations caused by cells, tri-to multi-seriate ray and multiple pollutant-induced stress. The vessels in Prosopis spicigera and Ailanthus photosynthetic activity is affected by excelsa exposed to stressful conditions. damaged biomolecules (Chaurasia et al., Other studies reported significant increases 2013; Thakar & Mishra, 2010), increased in vessel width and frequency, fibre length, transpiration and respiration (Gupta & tangential tracheid and lumen diameter in Sarkar, 2016; Koziol & Whatley, 1984; Cassia occidentalis, Abutilon indicum, Lee et al., 2017) and reduced foliar Abies religiosa, Calendula officinalis and dimensions (Tiwari et al., 2011). Reduced Croton sparsiflorus growing in SO2, NOx photosynthetic activity affects the cambial and particulate matter environment activity leading to reduced cell division, (Bernal-Salazar et al., 2004; Sukumaran, elongation and differentiation (Ahmad et 2014; Wali et al., 2007). al., 2015). Furthermore, the affinity of On the other hand, research on Pinus some heavy metals for binding to cell sylvestris, Mangifera indica, Prosopis membranes and cell walls compromises the cineraria and Syzygium cumini exposed to ability of wood cells to divide and expand heavy metals, SO2, particulate matter, NOx (Steiner et al., 2012; Pourrut et al., 2011). and CO2 reported reductions in fibre and The reduction in cambial activity limits vessel diameter, length and lumen ring widths and plant growth, resulting in (Dmuchowski et al., 1997; Gupta & Iqbal, reduced biomass production and plant 2005; Iqbal et al., 2010; Mahmooduzzafar productivity. et al., 2010). Reduced fusiform and ray On the other hand, the reported (Safdari initials, tracheid cell walls, diameter and et al., 2012; Thompson, 1981) increase in increased tracheid length and lumen, as growth and false rings, as well as the well as resin ducts, were observed in abrupt transition from earlywood to Juglans regia and Pinus elderica growing latewood can be attributed to an in an air polluted environment (Ahmad et unexpected increase in the growth rate of al., 2015; Safdari et al., 2012; Wani & plants. In nutrient deficient soil, SO2 and Khan, 2010). Another laboratory-based selected heavy metals can be utilized as study reported reduced vessel length, area, sulphate and micronutrient ions width and frequency in the stems and roots respectively to meet the demand of the of Trigonella foenum graecum Linn treated required nutrients (Khan & Khan, 2011; with Cd and Pb separately at different Tripathi et al., 2015). The availability of stages of plant growth (Ahmad et al., the initially lacking nutrients may improve 2005). The reductions were noted with the soil nutrition value, thereby enhancing increased concentration of individual or exacerbating the growth rate of plants. heavy metals applied. Table 2 shows pollutant-induced changes in the anatomic Wood Formation and Characteristics characteristics of selected plants species Studies on woody plants suggest air under field and laboratory conditions. pollution has devasting effects on wood

839 Mulenga, C. et al.

Table 2. Field and laboratory-based observed pollutant-induced changes in wood characteristics of selected herbaceous and woody plants. Stress and source Plant species Observed changes Author(s) Industrial plant (PM, N, *fibre length and width NOX, CO2, CO and Mangifera indica * vessel diameter, length and width (Gupta & Iqbal, 2005) 2 SO2) **vessel frequency per mm *vessel length and diameter *fibre length Prosopis cineraria **vessel frequency (Iqbal et al., 2010) **vasicentric axial parenchyma **tri-to multi-seriate rays *vessel length and width *fibre length and width (Mahmooduzzafar et Syzygium cumini *vessel and axial parenchyma al., 2010) frequency **fibre and ray frequency *vessel lumen diameter Ailanthus excelsa *vessel frequency (Rajput & Rao, 2005) **multiple vessel elements

*tangential tracheid cell walls and diameter. **ray and resin duct frequency per Pinus elderica 2 (Safdari et al., 2012) mm **tracheid fibre length and lumen diameter Cement dust Juglans regia *fusiform and ray initials (Wani & Khan, 2010) Dose-response Calendula *vessel diameter (Wali et al. 2007) experiment (SO2) officinalis **fibre and vessel length *vessel element length, width, area Dose-response Trigonella foenum and frequency (Ahmad et al., 2005) experiment (Cd, Pb) graecum Linn *fibre length and width *Reduced **Increased

Table 2 demonstrates that pollution- stressful environments is considered as the induced stress affects wood cells plant response/strategy to mitigate high dimensions and distribution patterns. negative tension in the transpiration stream According to Mahmooduzzafar et al. caused by pollutant induced stresses (2010) and Wali et al. (2007), wood fibres (Rajput et al., 2008). occupy a larger transectional area of wood in stressful environments. Attributed to the Forest Productivity and Sustainability in mechanical function of fibres, woody Polluted Landscapes plants require more fibres as an adaptive Over the years, studies on the effects of mechanism against the extreme growing heavy metals and SO2 on plant growth conditions. Furthermore, the production of focused mainly on herbaceous plants. shorter and narrower vessels offers Herbaceous plants account for the majority resistance against collapse and deformation of hyperaccumulators and crops. Increased required for plant safety (Gupta & Iqbal, interest in hyperaccumulators is aimed at 2005; Zimmermann, 1983). On the other identifying plants for phytoremediation hand, narrower vessels assure a smooth and purposes to restore massively polluted facilitated flow of sap throughout the plant landscapes through phytoextraction of (Husen & Iqbal, 1999). Increased pollutants using plants (Singh et al., 2016; frequency of vessels in plants growing in Tangahu et al., 2011). Studies on

840 Pollution, 6(4): 827-848, Autumn 2020 agricultural crops facilitate strategic transported into the transpiration stream measures to improve the productivity and through symplastic and apoplastic yield of farm produce in polluted pathways. In the plant tissue, pollutants are environments. On the other hand, studies then translocated and redistributed on woody plants are mostly concentrated throughout the plant by hydrostatic on the impact of climate change-induced pressure and transpiration. stresses, such as temperature, CO2, O3 and In plant cells, SO2 and heavy metals water availability on plant growth and participate in several biochemical reactions yield at the macroscale. producing ROS and inhibiting the normal However, there is limited information on functioning of enzymes involved in the the effect of SO2 and heavy metal stress on detoxification of ROS. ROS are destructive the growth and characteristics of woody to plants as they cause damage to organic plants. As discussed earlier, heavy metals molecules such as proteins, DNA, lipids and SO2 cause direct or indirect damage at and carbohydrates. In addition, some heavy plant molecular level, thereby instigating metals bind the cell membranes and cell changes in biochemical and physiological walls, making them rigid, thereby reducing parameters of plants. Additionally, there is a cell division and elongation. generalised understanding that pollution Increased production of ROS in stressful reduces forest growth and productivity. environments is attributed to the pollutant- Therefore, there is a need for studies to induced stress on the biochemical reactions establish the pollutant and species-specific instigated by the imbalance between the effects in woody plants growing in stressful generation and elimination of ROS in plant environments. In this regard, priority tissues. Therefore, the imbalance triggers research areas may include spatial and physiological and morphological alterations. temporal distribution of pollutants from Pollutant-induced phytotoxicity emitting sources, effects on tree growth and compromises the functionality and efficiency wood quality attributes, such as chemical of photosynthetic systems, stomatal composition, anatomical characteristics, functions and cambial activity. mechanics and machinability. Such studies Finally, pollution-induced stresses in would lead to the generation of scientific plants affect biochemical parameters information required for management plans inhibiting the plants capacity to carry out its to assure sustainable utilisation of both physiological functions, such as exotic and natural forests around polluted photosynthesis, transpiration and respiration. environments. The effects could be severe depending on plant species and exposure conditions, such CONCLUSIONS as pollutant type, concentration level, Increased industrial operations account for duration and season. Ultimately, pollutant- the emission of a wide range of pollutants induced toxification may result in visible including heavy metals, CO2, SO2, NOx plant injuries, reduced growth and yield, and CO into the atmosphere. The emitted thereby affecting the productivity of plants. pollutants are available for uptake by plants through different organs. For GRANT SUPPORT DETAILS example, heavy metals and SO2 enter the The present research has been financially plant tissue through the leaves penetrating supported by the Department of Forest and the stomata and cracked cuticular layers Wood Science, Stellenbosch University. and finally diffuse into the mesophyll cells. Further, heavy metals accumulated in the CONFLICT OF INTEREST soil solution are absorbed by root hairs and The authors declare that there is no conflict of interests regarding the publication of

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