The Accumulation and Physiological Responses of Camellia sinensis to Heavy Metals

Abstract

Heavy metals refer to metal elements with a density greater than 4.5 g/cm³. In recent years, human activities have increasingly exacerbated heavy metal pollution, and people are increasingly paying attention to the harm of heavy metal pollution to agricultural products. Tea is a common food, and the accumulation and physiological response of its parent Camellia sinensis to heavy metals have received increasing attention from scholars. Studies have shown that heavy metals can enter and accumulate in Camellia sinensis in various ways, and their toxicological effects on Camellia sinensis mainly include inhibiting growth and development, disrupting physiological and metabolic balance, and reducing the concentration of various chemicals in the body. This article summarizes the pathways by which heavy metals enter Camellia sinensis; the accumulation, physiological response, and tolerance effects of heavy metals in Camellia sinensis; and the underlying mechanisms involved. Finally, suggestions and prospects are made for the shortcomings of current research and future research directions.

1. Introduction

Heavy metal refers to metal elements with a density greater than 4.5 g/cm³. There are approximately 40 types, mainly including gold (Au), silver (Ag), copper (Cu), iron (Fe), zinc (Zn), manganese (Mn), mercury (Hg), lead (Pb), cadmium (Cd), chromium (Cr), and tin (Sn). Arsenic (As) is a nonmetallic substance; however, its source and harmful effects are similar to those of heavy metals, so it is often studied together with heavy metals and is called a metalloid [1]. In recent years, with the rapid development of agriculture and industry, many wastes have not been treated in a timely and effective manner, increasing heavy metal pollution in China.

Heavy metal pollutants are mainly generated by human activities. For example, industrial wastewater is used for irrigation in agriculture, resulting in a large number of heavy metals entering the soil, rivers, and other environments. In addition, large quantities of pesticides and fertilizers used to increase grain production are major sources of heavy metal pollution. Heavy metal pollution in the soil is the most serious. According to the 2014 National Soil Pollution Survey Bulletin, the excessive rate of heavy metals sites in China’s soil is 19.4%, with cadmium, copper, arsenic, lead, and other heavy metal pollution being the most prominent [2]. Additionally, heavy metal pollution in water bodies cannot be ignored. There are eight types of heavy metal pollution in the sediments at the edge of Poyang Lake, mainly from human production and living, industries and agriculture. The severity order is Cu > Cd > Pb > Cr > Zn > Hg > Ni > As and point source pollution can be converted into multiple sources [3].

Heavy metals in the environment can enter and accumulate in the human body through direct contact or through the food chain (a process known as bioconcentration). Once these metals exceed certain concentrations, they can cause acute or chronic poisoning, damage organs such as the kidney and liver, and disrupt the normal metabolism of the human body [4]. For example, studies have shown that Cd exposure can cause kidney toxicity, bone damage, neurovirulence, cardiovascular damage, diabetes, cancer, and other multiple organ system damage [5]. Another example is that when exposed to high doses of Pb, the human body may experience severe symptoms such as abdominal colic, anemia, wrist drop, and encephalopathy, while when exposed to low doses, Pb mainly affects physical development and intelligence and causes behavioral changes in infants and young children [6]. In brief, excessive heavy metals can seriously endanger human health and even cause death.

Economic plants are closely related to human production and life. As an increasing number of heavy metals are discharged into the environment, economic plants are becoming increasingly polluted. Therefore, the problem of heavy metal pollution in economic plants has received increasing attention. Some heavy metal elements, such as plant micronutrients (e.g., Cu, Zn, Ni), are essential for plants growth, but others (e.g., Cd, Pb) can cause serious negative impacts and even hormesis on plant growth. Plants suffering from heavy metal stress exhibit slow growth, stunted growth, inhibition of root elongation, and even death in severe cases [7]. Currently, research on the effects of heavy metals on economic plants has focused mainly on crops such as rice, corn, and soybeans, while research on tea plants is rare.

Camellia sinensis is a shrub, small tree, or tree of the genus Camellia that belongs to the family of Theaceae Mirb. It is mainly distributed in warm and humid areas. The optimal growth temperature is 20 to 25 °C, and the annual precipitation is greater than 1000 mm. It grows on sandy loam soil free of limestone and has good drainage [8,9,10,11]. Additionally, it exhibits light and shade tolerance. Its tender leaves can be used to make tea, and its seeds can be pressed for oil. It is a very common economic plant. As one of the world’s three largest non-alcoholic beverages, tea has an annual output of more than 4 million tons, and more than 200 million people worldwide drink tea [12,13]. Tea not only has a unique flavor, but also has health benefits for the human body. Catechins and other substances can play important roles in preventing and treating diseases such as cancer and coronary heart disease [14]. Tea can be drunk after soaking in water or can be made into vegetables for consumption, which is a food that directly or indirectly enters the mouth. With improvements in living standards, people are paying increasing attention to tea garden pollution and food safety issues [15]. Previous studies have shown that pollutants present in the soil can migrate into the body of Camellia sinensis, leading to health risks when drinking tea [16]. Liu et al.’s research indicates that tender leaf tea does not pose a health risk to the human body, but when using old leaf tea as a daily beverage, adult women and children need to pay attention to the intake of Mn [17]. Therefore, studying the impact of pollutants on Camellia sinensis is extremely important for human life and health.

Heavy metals in tea mainly originate from the soil, atmosphere, water, and production and processing processes, among which soil is the most direct and major pollution source. Under certain conditions, soil acidification may be related to an increase in metal concentration, while a decrease in soil pH typically increases the availability of metals for plants to absorb. Because the soil in tea gardens is mostly acidic and has a low adsorption capacity for heavy metal ions, the availability and bioavailability of heavy metals in the soil are greatly enhanced, increasing the potential safety risks of tea. Research shows that with the gradual decrease in soil pH, the availability of elements such as Pb, Cd, Cu, and Al in the soil significantly increases [18,19]. A study conducted in 2004 collected a large number of tea samples, measured the concentrations of two heavy metals, and compared them with 1997 data. The results showed that the average Cd concentration was 0.10 mg/kg, an increase of 66.7% compared to 0.06 mg/kg in 1997. The average concentration of As was 0.65 mg/kg, an increase of 117% compared to 0.30 mg/kg in 1997 [20]. Although both are significantly below the national limit standards, this rapid upward trend has attracted increased amounts of attention. In recent years, many achievements have been made in research on the response of Camellia sinensis to heavy metal stress.

2. Sources of Heavy Metals in Camellia sinensis

As shown in Figure 1, heavy metals can enter the Camellia sinensis body through various pathways from the external environment and accumulate [21].

2.1. Soil

Like other plants, Camellia sinensis needs to extract nutrients necessary for growth from the soil, so soil conditions largely determine the concentration of heavy metals in Camellia sinensis. Particles containing heavy metals are prone to accumulate in tea gardens under the transport action of natural external forces such as precipitation and wind. For example, during the spring and winter seasons in China, there are many sandstorms and haze weather events, and gases containing heavy metal particles are discharged into the atmosphere; under the action of the wind, these gases diffuse into tea gardens through atmospheric circulation and flow [22]. The root system, as the site in direct contact with soil, plays an important role in the plant response to heavy metal stress. The accumulation of heavy metals in Camellia sinensis mainly comes from the absorption of heavy metals by roots. When Camellia sinensis plants are contaminated with heavy metals, their roots, especially their taproots and absorbing roots, play important buffering and barrier roles in preventing the transfer of heavy metals from the soil to Camellia sinensis. This is because the cell walls of roots can fix most heavy metals, thereby reducing the amount of transport to the aboveground portion [23]. Pectic substances, carboxyl groups, and amino groups in the root cell wall play important roles in adsorbing heavy metals [24]. However, there are still many heavy metals that can be absorbed into the body of Camellia sinensis and transported through the xylem to the aboveground portion. The enrichment amount in each organ is generally the highest in the roots, greater in the stems than in the old leaves, and the lowest in the new shoots [25]. For example, one study showed that under normal conditions, the distribution order of Pb in Camellia sinensis from high to low was absorption root > stem > old leaf > main root > new shoot [26].

2.2. Water

Heavy metals can be transported through flowing water, and surface and underground runoff are important pathways for heavy metal migration. Industrial and agricultural wastewater containing heavy metals, if not properly treated, can leak into the ground and mix with groundwater, which can be widely spread and diffused under the action of flowing water transport. The concentration of heavy metals in surface runoff is influenced by various factors. Under different rainfall intensities, the concentration of heavy metals fluctuates and decreases over time. When the slope of the ground varies, the concentration of heavy metals increases with the increasing slope. In addition, under different slopes, as the slope increases, the Cd concentration in the soil first increases rapidly and then decreases slowly, and the overall concentration is much lower than that in the surface runoff [27]. The growth of Camellia sinensis cannot be separated from water sources. If Camellia sinensis plants are watered with water containing heavy metals, they will absorb heavy metals into the body. Although water can be continuously absorbed and discharged through transpiration, heavy metals cannot be discharged and can only be retained in plants, resulting in a concentration effect.

2.3. Human Factors

Human activities produce amounts of wastewater and gas, which include heavy metals and may influence Camellia sinensis. For example, exhaust gas from automobiles contains a large number of heavy metals, such as Pb and As, and under the effect of atmospheric circulation, plants in cities are significantly affected by toxic gases. Researchers have studied the accumulation of heavy metals by urban greening trees along urban trunk roads, and the results show that the comprehensive ranking of the accumulation of different heavy metals by most urban greening trees is basically the same, with almost all being Fe > Zn > Mn > Cd > Cu > Pb. Mn and Pb mainly come from natural sources, while Fe and Cd mainly come from human sources [28]. Similarly, during the gas exchange process of Camellia sinensis in cities, these heavy metals are also incorporated into the body, resulting in the enrichment of heavy metals.

3. Differences in the Enrichment Abilities of Camellia sinensis for Heavy Metals

3.1. Different Parts (Organs) Have Different Enrichment Abilities for Heavy Metals

A large amount of research has reported the ability of different parts of Camellia sinensis to accumulate heavy metals (Figure 2). Many studies have shown that the underground parts of Camellia sinensis, such as rhizome, are the main organs that accumulate most heavy metals, while the concentration of the aboveground parts is relatively low. Generally, the overall order is root > stem > old leaves > tender leaves > buds because most of the heavy metals are fixed by the roots, and the roots play a significant buffering and barrier role [29,30,31]. A study by Kang Mengli and Luo Yao et al. revealed that the distribution of Pb concentration in Camellia sinensis decreased in the following order: fine roots > coarse roots/stems > young buds > old leaves > buds. When the Pb concentration in the culture medium was 0–200 mg/L, the Pb concentration in the aboveground parts did not change significantly. After the concentration increased from 200 mg/L to 400 mg/L, the Pb concentration in the aboveground part increased significantly, and there was a significant positive correlation with the Pb concentration in the culture medium. In the aboveground part, there was a highly significant positive correlation between the change in Pb concentration in the buds and the change in Pb concentration in the culture medium [32]. In summary, when the degree of heavy metal pollution in tea garden soil is relatively low, a developed root system can deal with it and reduce economic losses.

The ability of different parts of Camellia sinensis to enrich different heavy metals also varies. Wang Xiaoping et al. used atomic fluorescence spectroscopy to study the distribution characteristics of As, Se, Hg, and Bi in different parts of young Camellia sinensis. The results showed that As, Se, and Hg mainly accumulated in the bark, roots, and old leaves, while it was difficult for Se to accumulate in Camellia sinensis [33]. Fang Yunshan et al. measured the concentrations of five heavy metals in the rhizosphere soil, young leaves, and old leaves of tea gardens in three different regions using graphite furnace atomic absorption spectrometry and reported that the concentrations of Cd, Pb, and Cu in young leaves were greater than those in old leaves, while the contents of Zn and Cr in old leaves were greater than those in young leaves [34]. Therefore, the specific distribution of different types of heavy metals, especially several heavy metals that have been less studied at present, in Camellia sinensis needs to be further explored.

3.2. Different Breeds Have Different Enrichment Abilities for Heavy Metals

Many studies have shown that there are differences in the absorption capacity, enrichment capacity, conversion mode, and transfer coefficient of heavy metals among different breeds of Camellia sinensis. Dai [35] conducted a study on the ability of nine breeds of Camellia sinensis to enrich heavy metals Cd, Pb, As, and Hg and reported that Bixiangzao, Xiangbolv, and Taoyuandaye have lower enrichment abilities. Qin et al. [36] studied the enrichment characteristics of Se, As, and Hg in 10 breeds, and the results showed that Fudingdahao, Xiangbolv, and Bixiangzao had moderate or greater Se enrichment abilities but weak Hg and As enrichment abilities. When studying the absorption and accumulation of heavy metals in Camellia sinensis, Liu et al. [37] analyzed the concentrations of Pb, Cd, and Cu in the rhizosphere soil, lateral roots, old leaves, and young leaves of five tea breeds in the same tea garden, as well as the enrichment and transfer coefficients. The results showed that even among breeds in the same habitat, there were certain differences, with the concentration distribution order being lateral roots, old leaves, and young leaves, with significant differences in the enrichment and transfer coefficients of old and young leaves. This finding indicates that different breeds of Camellia sinensis have different enrichment capacities for heavy metals, and the transfer coefficients of heavy metals in various organs are also different. This phenomenon may be related to genotype, or the interactions of genotype and environment. Different tea-producing regions or tea gardens often cultivate different breeds of Camellia sinensis. Therefore, studying the differences between breeds in terms of heavy metal enrichment is highly important for accurately and effectively reducing economic losses in tea gardens and preventing heavy metal pollution in tea.

3.3. Different Seasons Have Different Enrichment Abilities for Heavy Metals

In regions with large changes in the four seasons (spring, summer, autumn, and winter), the atmosphere, soil, light, precipitation, temperature, and other tea garden environments are also different due to different seasons, which affects the growth of Camellia sinensis and further affects the concentration of heavy metals absorbed and enriched by Camellia sinensis from the soil. Dai Sijia studied the differences in the concentrations of the heavy metals Cd, Pb, As, and Hg in Camellia sinensis in spring, summer, and autumn and found that the concentrations of Cd and As increased slightly with seasonal changes, while the concentrations of Hg and Pb did not change significantly in the three seasons, and the concentration of Hg decreased significantly [35]. Cui et al. [38] used the microwave digestion method to analyze the concentrations of the heavy metals As, Cd, Co, Cr, Cu, Fe, Mn, Pb, Sb, Sn, Sr, Ti, and Zn in large-leaf tea. The concentrations of As, Cd, Fe, Mn, and Pb in winter tea were 2.01, 3.07, 2.00, 4.16, and 2.73 times greater than those in summer tea, respectively, while the concentration of Cr was as much as six times greater than that in summer tea, but the concentrations of Cu and Zn were only 75% and 46% of spring tea, respectively. In general, the concentration of heavy metals in summer tea is the lowest, while the content in winter tea is the highest, and summer tea is rich in toxic and harmful elements such as As, Cd, and Cr. He et al. [39] used microwave digestion flame atomic absorption spectrometry to detect the difference in the concentration of Mn in the leaves of Kudingcha in spring, summer, and autumn, and the results were autumn > summer > spring. Therefore, taking corresponding control measures for Camellia sinensis in different seasons can help reduce the economic cost of tea production.

4. Physiological Effects of Heavy Metal Stress on Camellia sinensis

4.1. Effects of Heavy Metal Stress on Growth and Development

Heavy metal stress can have a serious impact on the growth and development of Camellia sinensis. Heavy metals can destroy the structure of chloroplasts and photosynthetic pigments, causing yellowing or brown spots on leaves and thereby inhibiting photosynthesis in Camellia sinensis, ultimately resulting in stunted plant growth and reduced biomass. Studies have shown that Cd stress significantly reduces the concentration of chlorophyll a, chlorophyll b, and carotenoids in Camellia sinensis. This may be because after entering the cell, Cd binds to the sulfhydryl group of chloroplast proteins, replacing the binding sites of Fe²⁺, Zn²⁺, and Mg²⁺ and thereby affecting the synthesis of chloroplasts [40]. Cr stress inhibits the accumulation of dry matter in the vegetative organs of Camellia sinensis and reduces chlorophyll concentration and stomatal conductance, thereby inhibiting photosynthesis and affecting growth [41]. A pot experiment revealed that the leaves of Camellia sinensis plants subjected to Pb stress turned yellow and wilted, their buds decreased, their germination ability decreased, their growth significantly decreased, and their biomass decreased [42]. Xia et al. [43] reported that different concentrations of Pb had a dose-dependent effect on the growth of Camellia sinensis. Low concentrations of Pb promote the growth of Camellia sinensis, mainly manifested by a strong green leaf color, long leaf spacing, and the presence of more new leaves. Plants subjected to high concentrations of Pb exhibited less germination, yellow leaves, and wilting.

Heavy metals can also cause morphological changes in the cells, tissues, and organs of Camellia sinensis. Research has shown that the central pillar and epidermis of the root system, the xylem and cambium of tender stems, and the phloem and cambium of leaves are the main accumulation sites of lead in various tissues of Camellia sinensis [44]. Pb stress leads to the dissolution and disappearance of root nuclei, partial expansion of mitochondrial cristae, invagination of cell membranes, and thickening of cell walls in Longjing and Yingshuang, resulting in the deformation of stem cell chloroplasts, disappearance of grana lamellae layers, disruption of thylakoids, and the appearance of large lipid particles, leading to a significant deterioration of leaf cell chloroplasts, rupture of chloroplast bilayer membranes, disordered arrangement of grana lamellae structures, and swelling of matrix thylakoids. FTIP studies have shown that Pb mainly binds to the carboxylic functional groups of cellulose, hemicellulose, and lignin in the cell wall, while proteins and pectins on the root cell wall may also participate in the binding of Pb [45].

4.2. Effects of Heavy Metal Stress on the Antioxidant System

Heavy metals can affect physiological processes such as photosynthesis, causing a large amount of active oxygen species in Camellia sinensis and disrupting the original redox balance, leading to a large accumulation of oxygen free radicals and ultimately causing oxidative stress. A study revealed that under Cd stress, the concentration of malondialdehyde and hydrogen peroxide in the leaves of Camellia sinensis significantly increased, strongly affecting the normal growth of Camellia sinensis [40]. Stress can also increase the accumulation of reactive oxygen species and the degree of lipid peroxidation in leaves, leading to a severe oxidative stress response [46].

In addition to directly causing the accumulation of reactive oxygen species, heavy metals can also indirectly cause oxidative stress in Camellia sinensis by disrupting its defense mechanisms. There are systems that scavenge reactive oxygen species in plant cells to alleviate oxidative stress, including antioxidant enzymes such as superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), glutathione peroxidase (GPX), and ascorbate peroxidase (APX). After Cd stress treatment, the activities of CAT, APX, and GPX in the leaves of Camellia sinensis decreased significantly, the accumulation of active oxygen species increased, and membrane lipid peroxidation was induced [40]. Another study also revealed that with an increasing Cr concentration, the activities of SOD, POD, and CAT in leaves decreased significantly, indicating that high concentrations of Cr can damage the antioxidant enzyme system of Camellia sinensis, thereby affecting the structure and function of cell membranes [41]. Ye et al. [47] reported that the activities of SOD, POD, and CAT in Cinnamomum cassia and Tieguanyin decreased with an increasing Pb concentration. Low concentrations of Pb did not produce significant differences in the physiological indicators of the two breeds of Camellia sinensis, while high concentrations of Pb produced differences. A study of Al stress in Camellia sinensis by Luo Liang and Xie Zhonglei showed that 10 mg/L Al decreased the concentration of malondialdehyde in Camellia sinensis, enhanced the activities of POD and CAT in Camellia sinensis, and increased the concentration of free co-amylase; however, 100 mg/L Al decreased the activity of these two enzymes and increased the concentration of malondialdehyde [48].

4.3. Effects of Heavy Metal Stress on Physiological Metabolism

Camellia sinensis contains various metabolic products, such as theanine, catechins, and caffeine. Their metabolic pathways are closely related to the growth and development of Camellia sinensis and their response to stress. One study revealed that under different concentrations of Pb, the concentrations of caffeine and free amino acids in leaves significantly decreased, but the concentration of catechins increased with increasing Pb concentration, possibly because Pb weakened nitrogen metabolism and enhanced carbon metabolism [42]. Shi et al. [26] also reported that after Cd stress treatment, the caffeine and amino acid concentrations in the shoots of Camellia sinensis significantly decreased, and the phenol–ammonia ratio increased. In addition, Cd stress can also lead to an increase in lignin concentration in the callus of roots and stems [39].

Tea polyphenols are not only products of carbon metabolism but also important endogenous antioxidant substances that can enhance the antioxidant capacity of Camellia sinensis and participate in defense reactions. Heavy metal stress can alter the biosynthesis and metabolism of tea polyphenols, thereby affecting the physiological metabolism of Camellia sinensis. Research has shown that 100 μmol/L Cd promoted the synthesis of phenolic substances, increased the accumulation of tea polyphenols, and thus alleviated oxidative stress. At the same time, the concentration of proline in leaves increased, which improved the maintenance of cell osmotic pressure. However, with an increasing Cd concentration, the synthesis of polyphenols was strongly affected and the concentration rapidly decreased [40]. In addition, the physiological and metabolic processes of phenolic compounds in different parts of Camellia sinensis respond differently to heavy metal stress. A study revealed that Cd stress treatment could affect the ability of Camellia sinensis calli to synthesize soluble phenolic compounds to varying degrees. The concentration of polyphenols in the roots and stem calli increased compared to that in the control group, while the concentration in the leaf calli decreased slightly [49].

In Camellia sinensis, heavy metals also chelate with amino acids, proteins, etc., reducing the supply of these substances and thereby affecting the physiological activities of Camellia sinensis [50]. The combined pollution of the heavy metals Cr, As, Cd, and Pb significantly affects the synthesis of chlorophyll a and b in Camellia sinensis, thereby affecting photosynthesis. Combined pollution also affects the net photosynthetic rate, stomatal conductance, intercellular CO₂ concentration, transpiration rate, and relative electrical conductivity, as well as the activities of SOD, POD, CAT, and the concentrations of proline and malondialdehyde in Camellia sinensis [51]. Some studies have shown that under a single treatment, Cd and As have a significant negative impact on the photosynthetic rate, transpiration rate, and stomatal conductance of Camellia sinensis, but the impact of As on chlorophyll synthesis is not significant [52]. When the concentration of bioavailable Hg in the soil was 25–150 mg/kg, Camellia sinensis did not exhibit apparent pathological symptoms. When the Hg concentration was 150–200 mg/kg, its growth and photosynthesis indicators were greater than those of the control group, showing a positive effect. When the Hg concentration was >200 mg/kg, it significantly inhibited the growth and photosynthesis of Camellia sinensis. The activities of SOD, POD, and CAT in Camellia sinensis generally increase and then decrease with increasing Hg concentration, reaching a maximum at 300 mg/kg Hg [53]. In a study of Cr stress, the growth of Camellia sinensis increased when the Cr concentration in the soil was ≤50 mg/kg and decreased when the Cr concentration was ≥75 mg/kg. The SOD activity decreased with the increasing Cr concentration but was greater than that in the control group. The POD and CAT activities first increased and then decreased with the increasing Cr concentration and reached a maximum value at approximately 150 mg/kg [52,53].

5. Tolerance of Camellia sinensis to Heavy Metals and Its Adaptive Mechanisms to Heavy Metal Stress

Plants have a certain resistance to heavy metals and can survive in environments containing lower concentrations of heavy metals without toxic phenomena such as decreased growth rates or death. Phragmites australis has a high resistance to heavy metals. In environments where many other plants cannot grow, they can grow normally and even complete their life cycle [54]. In 1963, a study divided plants into two categories based on their growth environment: metallophytes and facultative metallophytes. Metallophytes refer to plants that can grow normally only in metal-contaminated environments, while pseudometallophytes refer to plants that can grow normally in both metal-contaminated and nonmetal-contaminated environments [55]. Camellia sinensis is a typical non-metallophyte, meaning that specific adaptations to excess levels of particular heavy metals are probably absent, although there might well be variation between breeds in the tolerance and accumulation capacities of many heavy metals.

In general, plant resistance to heavy metals can be achieved through two pathways, avoidance and tolerance, and both pathways can play a role simultaneously. Avoidance refers to the ability of some plants to limit the absorption of heavy metals in the environment through certain in vitro protective mechanisms to maintain a low concentration of heavy metals in the body, thereby preventing toxicity. For example, the roots of some plants can secrete substances to reduce the concentration of available heavy metal ions in the surrounding environment. The mechanism mainly includes changing the pH value of the rhizosphere, competing with heavy metal ions for adsorption sites in the soil, forming chelates to affect the adsorption and desorption processes of heavy metals in the soil, etc. [56,57,58,59]. Tolerance refers to the specific physiological mechanisms within plants that enable them to survive in environments with high concentrations of heavy metals without harm. These plants generally contain high concentrations of heavy metals but can be detoxified through various pathways in a timely manner. For example, some plants have the ability to actively expel metal ions from their protoplasm membranes [60,61,62], while others shed leaves that can enrich heavy metals to expel them from the body [63,64,65,66,67,68]. LMA is the leaf mass per unit area, which is one of the important leaf trait indicators of plants. It is the reciprocal of the specific leaf area (SLA) and mainly characterizes the utilization efficiency of plant resources. Some plants mainly concentrate heavy metals on the roots and stems to reduce their impact on the leaves of photosynthetic organs by regulating the distribution of biomass, such as increasing the root and stem ratio, thickening the leaves, increasing the LMA content, and improving the antioxidant scavenging capacity [69].

Some scholars have observed that tea yield does not decrease after the soil in tea gardens becomes slightly polluted, indicating that under heavy metal stress, Camellia sinensis initiates a physiological emergency response to stress. Han et al. [70] reported that an appropriate amount of Zn can promote the growth and germination of Camellia sinensis; increase the concentration of chlorophyll in leaves, amino acids in shoots, and soluble sugars; and enhance the activities of polyphenol oxidase and nitrate reductase, which ultimately improves the yield and quality of tea. Excessive Zn inhibits the growth of Camellia sinensis, causing a decrease in yield and quality. A study revealed that Pb stress treatment had a negative effect on the growth and development of Camellia sinensis; however, Camellia sinensis was strongly tolerant to Pb, and even under 2100 mg/kg Pb stress, it could complete its normal life cycle, with only a small number of pathological manifestations, but no lethal manifestations [37]. This indicates that Camellia sinensis has a certain resistance to heavy metals, which may be related to certain specific metabolic pathways or enzymes in its body. A study investigated the tolerance mechanism of Camellia sinensis. The author believes that the increase or decrease in the concentration of free amino acid components is related to changes in nitrogen metabolism. Low concentrations of Pb can promote the synthesis of amino acids and proteins in Camellia sinensis, thereby enhancing tolerance. However, when the concentration exceeds a certain level, nitrogen metabolism is inhibited and toxic phenomena occur [71].

In addition to its own physiological response mechanism, the external environment of Camellia sinensis can also affect tolerance to heavy metals. The rhizosphere is where the interaction between soil and plants is most active because there are a large number of rhizosphere growth-promoting bacteria that have important impacts on plant growth and metabolism in the soil. Heavy metals can have a significant direct or indirect impact on the rhizosphere environment. Under heavy metal stress, plants can modify the rhizosphere environment by adjusting the composition of root exudates to alleviate toxicity and adapt to stress conditions. For example, in the presence of Al, the accumulation of organic acids in the rhizosphere of Camellia sinensis increases, and rhizosphere growth-promoting bacteria can also indirectly affect the growth of Camellia sinensis by affecting its absorption of Al, thereby exhibiting certain physiological and biochemical indicators and changes in Al concentration in the body [72].

6. Discussion and Outlook

With the development of the social economy, the problem of heavy metal pollution has become a hot topic of attention, and the prevention and control of heavy metal pollution in Camellia sinensis has also received increasing attention. An excessive concentration of one or more heavy metals in the soil of tea gardens can affect the growth and development of Camellia sinensis and cause poisoning for human consumption. In response, there are clear indicator requirements in China’s “Soil Environmental Quality Standard for Soil Pollution Risk Management and Control of Agricultural Land (Trial)” [73].

Currently, a large number of studies have shown that heavy metals can enter the body of Camellia sinensis through the soil, water sources, and human factors. Moreover, the degree of heavy metal enrichment in Camellia sinensis depends on the organs of enrichment, the affected breeds, or the seasons. Heavy metals enriched in the plant body have multiple toxic effects on Camellia sinensis, mainly manifested as inhibiting growth and development, interfering with photosynthesis, disrupting physiological and metabolic processes, and reducing the concentration of certain chemicals in the body. Although Camellia sinensis can overcome some stress and even utilize small amounts of heavy metals through certain tolerance mechanisms, heavy metals still objectively exist in their bodies. If they are used for food production, this can also pose a threat to human health. However, there are still many gaps in current research, so the following research directions should be strengthened in the future:

(1) Atmospheric deposition is also one of the important sources of heavy metals and the impact of atmospheric pollutants containing heavy metals such as PM2.5 on agricultural plants has always been a concern [74]. Especially PM2.5, it refers to particulate matter with a diameter less than or equal to 2.5 μm in the atmosphere, also known as pulmonary particulate matter, which is rich in a large number of toxic and harmful substances, and has a long residence time and long transportation distance in the atmosphere; it also has a serious impact on human health and atmospheric environmental quality. Camellia sinensis may also accumulate heavy metals in the atmosphere through gas exchange [75]. Wan et al. [76] have shown that heavy metals were absorbed via the stomata and stratum corneum on the leaf surface of plants, and then transported to the phloem through the pathways of exosomes or endosomes. Finally, they are transported to organs such as leaves, fruits, and roots in the same way as photosynthetic products. However, there is currently limited knowledge on how atmospheric heavy metals enter the body of Camellia sinensis and their potential impacts. Therefore, future research can treat Camellia sinensis with heavy metal aerosols to determine the pathways and specific effects of atmospheric heavy metals entering the tea tree body, in order to prevent and control the damage of air pollution to Camellia sinensis during agricultural cultivation.

(2) As affected by environmental factors such as climate and pH, heavy metals have different dissolution rates in different soils [77,78]. At the same time, different breeds of Camellia sinensis have different physiological responses to heavy metal stress due to their different genetic characteristics. Therefore, the study of heavy metal pollution in tea garden soil requires comprehensive consideration of multiple factors, and more attention should be given to the combined effects of multiple factors in the future.

(3) The chemical composition of the soil is very complex, and there are differences in the types and concentrations of pollutants in tea garden soil. Heavy metals usually do not exist alone with a single element but with multiple coexisting elements. Moreover, the growth and development of Camellia sinensis are affected not only by heavy metals but also by other chemicals, and there may be antagonistic or synergistic effects between them. In fact, combined pollution is more common [79]. The impact of complex pollution on the physiological characteristics of Camellia sinensis is comprehensive, and the specific extent of the impact depends on the concentration and combination of various substances. However, most of the existing studies have focused on single heavy metal pollution, while there are few reports on multiple heavy metals and their combined pollution with other pollutants. Therefore, research on heavy metal combined pollution and its toxicity mechanism needs to be increased.

(4) Research on tea Camellia sinensis has mostly focused on heavy metals, drought, low temperature freezing damage, selenium fertilizer, nitrogen and phosphorus elements, CO₂, etc. There are also many studies that combine heavy metals with other factors [80,81,82,83]. However, current research mainly focuses on combining heavy metals with drought, while other common stress factors are relatively rare. Therefore, future research can combine heavy metals with other factors such as selenium fertilizer to observe whether another factor can aggravate or slow down the damage of heavy metals to Camellia sinensis, providing feasible solutions for mitigating the harm of heavy metals in tea gardens.

(5) The resistance mechanism of plants to heavy metals is very complex, possibly controlled by multiple genes, and is a comprehensive response to multiple physiological processes [84,85]. Therefore, further research on the mechanism of heavy metal resistance in Camellia sinensis and further exploration of the key factors controlling heavy metal resistance are highly important for reducing the harm of heavy metals to Camellia sinensis and improving its stress resistance.