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Zhao, Y.; Wang, J.; Huang, W.; Zhang, D.; Wu, J.; Li, B.; Li, M.; Liu, L.; Yan, M. ABA-Mediated Regulation of Cd-Responsive Genes in Plants. Encyclopedia. Available online: https://encyclopedia.pub/entry/42128 (accessed on 03 July 2024).
Zhao Y, Wang J, Huang W, Zhang D, Wu J, Li B, et al. ABA-Mediated Regulation of Cd-Responsive Genes in Plants. Encyclopedia. Available at: https://encyclopedia.pub/entry/42128. Accessed July 03, 2024.
Zhao, Yuquan, Jiaqi Wang, Wei Huang, Dawei Zhang, Jinfeng Wu, Bao Li, Mei Li, Lili Liu, Mingli Yan. "ABA-Mediated Regulation of Cd-Responsive Genes in Plants" Encyclopedia, https://encyclopedia.pub/entry/42128 (accessed July 03, 2024).
Zhao, Y., Wang, J., Huang, W., Zhang, D., Wu, J., Li, B., Li, M., Liu, L., & Yan, M. (2023, March 13). ABA-Mediated Regulation of Cd-Responsive Genes in Plants. In Encyclopedia. https://encyclopedia.pub/entry/42128
Zhao, Yuquan, et al. "ABA-Mediated Regulation of Cd-Responsive Genes in Plants." Encyclopedia. Web. 13 March, 2023.
ABA-Mediated Regulation of Cd-Responsive Genes in Plants
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This entry is adapted from the peer-reviewed paper 10.3390/plants12051023

Cadmium (Cd) is a highly toxic heavy metal that has no biological function and can persist in organisms for a long time (biological half-life: 10–30 years). Cadmium exposure can cause metabolic disorders in plant leaves, leading to excessive accumulation of reactive oxygen species (ROS) such as H2O2, further causing oxidative stress, cell death, and even plant death. Abscisic acid (ABA) is a sesquiterpene phytohormone that plays important roles in plant growth and development, e.g., in inducing dormancy in buds and seeds, causing stomatal closure, and promoting abscission of flowers and fruits.

Cd abscisic acid plants

1. Regulation of Transpiration by Abscisic Acid in Plants

In higher plants, the accumulation of heavy metals in leaves affects the function of stomata, which in turn affects transpiration. Studies have reported that transpiration rate is related to the xylem loading of cadmium (Cd) and is the main driver of Cd transport from roots to shoots [1][2][3][4]. The Cd content in Pingyi sweet tea roots increased with increasing leaf transpiration rate and decreased with decreasing transpiration rate [5]. Transpiration inhibitors such as paraffin and CaCl2 could reduce Cd content in tobacco (Nicotiana tabacum L.) leaves, and the reduction in Cd content was linearly correlated with the transpiration rate of tobacco leaves [1]. Consistent with the above findings, previous related studies in maize (Zea mays), mustard (Brassica juncea L.), rice, and wheat (Triticum aestivum) reported that higher transpiration rates were associated with higher Cd levels in shoots [6].
Stomata regulate the parallel diffusion pathways of water and CO2 between leaves and atmosphere, thus playing a regulatory role in transpiration and photosynthesis [7]. Studies have reported that abscisic acid (ABA) regulates transpiration by modulating stomatal aperture [3][6][8][9]. Abscisic acid treatment reduced transpiration rate by 72% and 64% in Habataki and Sasanishiki (two rice cultivars), respectively, resulting in the reduction in Cd accumulation in rice shoots [10]. After spraying ABA, the transpiration rate of Pingyi sweet tea leaves and Cd2+ uptake and accumulation in the root system reduced, mitigating damage to the root system due to Cd [5]. Under Cd stress, endogenous ABA levels of non-hyperaccumulation ecotype Sedum alfredii increased, which reduced the size and density of stomata in the leaves and also reduced the transport of Cd2+ to the shoots [6]. In contrast, under Cd stress, endogenous ABA contents in hyperaccumulation ecotype S. alfredii were maintained only at low levels, and they could not limit transpiration rate, thus exhibiting higher Cd accumulation [6]. The above findings suggested that the reduction in Cd content caused by ABA is closely related to the inhibition of transpiration.

2. Regulation of Metal Ion Transport by Abscisic Acid in Plants

In the inter-root environment of rice, heavy metal ions are transported to rice roots by specific transporter proteins through the plasma membrane and then to the xylem or phloem via the plastid extracellular pathway or symplast pathway [4][11]; further, they are transported to various organs in shoots [4][11]. However, Cd does not have its own transporter, and it enters the plant body through the transporter of essential elements (e.g., Zn, Fe, and Ca) [12][13]. A study reported that Cd can enter the rice root system through OsIRT1 [13], and similarly, Arabidopsis irt1 mutants have lower Cd levels than wild-type plants [14].
Abscisic acid reduced the transcript levels of IRT1 in cucumber (Cucumis sativus L.) and Arabidopsis roots [15]. Similarly, exogenous ABA could significantly reduce the Cd levels in the shoots of wild-type Arabidopsis [16]. However, its effect on Arabidopsis irt1 mutants was not significant, and the addition of iron-regulated transporter 1 (IRT1) inhibitors eliminated the difference between Cd levels in shoots and roots in wild-type Arabidopsis with and without the addition of ABA [16]. Fan, et al. [17] reported that the application of 0.5 µM ABA under 10 µM Cd stress led to reduction in IRT1 transcript levels by 90% in Arabidopsis roots; however, in ABA-insensitive double mutant snrk2.2/2.3, the repression of IRT1 by ABA was not as pronounced as in wild-type Arabidopsis [17]. Consistent with the above findings, inoculation of ABA-producing bacteria in soil under Cd stress significantly downregulated the expression of root IRT1, which in turn inhibited Cd uptake by Arabidopsis [18]. However, inoculation of ABA-producing bacteria had little effect on Cd levels in Arabidopsis irt1 knockout mutant [18]. These results suggested that the decrease in plant Cd levels induced by ABA application is mainly achieved through the regulation of IRT1.
Notably, a recent study by reported that the regulation of Cd accumulation in plants by ABA was related to the concentration of Fe2+ in the external environment [19]. Under the condition of sufficient Fe2+, ABA significantly inhibited the IRT1 expression and reduced Cd accumulation [19]. Under Fe2+-deficient conditions, ABA may regulate Cd accumulation by promoting the redirection of Fe in the ectoplasm [19]. This suggested that ABA-mediated regulation of Cd accumulation is a complex process.
Heavy metal ATPase 3 (HMA3) is a protein localized on the vesicle membrane and is responsible for the transport of Cd and Zn into the vesicles [20]. In rice, OsHMA3 is responsible for the segregation of Cd into the root vesicles [21]. Plants possessing nonfunctional OsHMA3 exhibited increased transport of Cd from the roots to shoots [12]. Conversely, overexpression of OsHMA3 enhanced Cd segregation and thus reduced Cd transport from the roots to shoots [12]. Unlike HMA3, the function of its homologous protein, HMA2, is not clear enough. Heavy metal ATPase 2 and ATPase 4 (HMA2 and HMA4) are present on the plasma membrane of thin-walled cells of vascular bundles and mediate the transport of Cd and Zn from the roots to shoots [12][20][22]. The functional deficiency of HMA2 and HMA4 in Arabidopsis resulted in the almost complete loss of Cd transport from the roots to shoots [22]. Rice HMA2 mutants exhibited reduced Cd and Zn translocation rates from roots to shoots [23][24]. Similarly, knockout of HMA2 lowered Cd and Zn content in in the reproductive organs of rice [12]. In addition, Ectopic expression of BrpHMA2 enhanced Cd accumulation in transgenic Arabidopsis and yeast [25]. Contradictorily, OsHMA2 overexpression plants showed reduced seed Cd concentration [24]. Therefore, further studies are necessary. In a study related to Cd accumulation in S. alfredii, researchers indicated that ABA increased Cd resistance and Cd transport from roots to shoots in S. alfredii through the induction of HMA3 and HMA4 transcripts [26]. However, HMA2 expression was negatively correlated with endogenous ABA content [26], which implied that ABA may inhibit HMA2 expression. Similarly, ectopic expression of MhNCED3 in Arabidopsis reduced AtHMA2 expression [27]. These results suggested that ABA may mediate the expression of some genes of the HMA family to affect Cd transport and accumulation.
Natural resistance-associated macrophage protein (NRAMP) family genes are involved in transmembrane transport of divalent heavy metal ions (including Cd2+) and play an important role in response to heavy metal stress [28][29]. Under Cd stress, soybean NRAMP genes were significantly upregulated [29]. Similarly, the expression of potato NRAMP genes (NRAMP1–5) significantly increased under Cd stress [28]. In rice, OsNRAMP5 was thought as the main Cd transporter [12][21]. A recent study reported that high expression of OsNRAMP5 reduced Cd accumulation in rice seeds [21]. Natural resistance-associated macrophage protein family genes have been reported to be regulated mainly by phytohormones and transcription factors under abiotic stress [28]. A study indicated that increased ABA synthesis suppresses NRAMPs expression [27]. However, Zhou and Yang [30] reported that ABA downregulated the expression of OsNRAMP1 but upregulated OsNRAMP2 and OsNRAMP3. No evidence is available regarding the regulation of NRAMP5 by ABA. Therefore, further research is necessary.
The aforementioned metal transporters are often involved in the transport of essential elements. For example, IRT1 is involved in Fe2+ transport [12]; OsHMA2 is required for Zn transport, and OsNRAMP5 is the main protein for Mn uptake and transport [12][21]. However, knockdown or overexpression of these genes often affect crop yield, which limits their application in breeding. Notably, overexpression of OsHMA3 did not affect rice yield [21]. Therefore, HMA3 has exhibited potential for the application in crop breeding.

3. Regulation of Metal Ion Sequestration by Abscisic Acid in Plants

Despite entering the root cells, most Cd still cannot reach the shoots [12]. Metal ions can be chelated by reduced glutathione (GSH), phytochelatins (PCs), and nicotianamine (NA) [26][31][32]. These three share a common precursor: cysteine (Cys) [31][33]. Metal ions are segregated into vesicles via transport proteins after chelation, effectively ensuring that free metals are at low levels in the cytosol [31]. Arabidopsis synthesizes GSH via γ-glutamylcysteine synthase 1 (GSH1) and glutathione synthase 2 (GSH2) [34]. In plants, algae, and some fungi or worms [35][36], phytochelatin synthase (PCS) may catalyzes glutathione tripeptide γ-Glu-Cys-Gly (GSH) to synthesize PCs ((γ-Glu-Cys)n-Gly, n = 2–11) [32][37]. Studies show that Cd, As, and Pb in the cytoplasm can be coupled by GSH or PCs and then segregated into vesicles to alleviate the toxicity of heavy metals to cells [34]. A study reported that the formation of PC–Cd complexes is the main mechanism of Cd detoxification in Arabidopsis [22]. Consistent with these results, the accumulation of PCs in the root system is responsible for the higher Cd tolerance in wheat and higher Cu, Zn, and Cd tolerance in aquatic plants [31].
Studies have reported that the activity of PCS is the main cause of sequestration of heavy metals, such as Cd, As, and Hg, in plants [35][38][39][40]. Abscisic acid can alleviate metal stress by regulating the transcript level of PCS. In ramie (Boehmeria nivea), Cd and ABA could significantly induce BnPCS1 [41]. In grey poplar (Populus × canescens), the application of exogenous ABA increased the transcript levels of PCS [15]. Consistent with these results, Cd or ABA treatment increased the transcript levels of StPCS1 and PCS activity in potato (Solanum tuberosum) roots, whereas the addition of Flu decreased the transcript levels of StPCS1 and PCS activity [42]. These results may indicate that ABA plays an important role in the metal ion chelation process.

4. Regulation of the Antioxidant System by Abscisic Acid in Plants

Under normal physiological conditions, a balance exists between the production and clearance of oxygen species (ROS) in all intercellular compartments. However, this balance may be disturbed by some adverse environmental factors. One of the main consequences of the action of heavy metals, including Cd, is enhanced ROS production, which leads to damage to membranes, nucleic acids, and proteins and impairment of normal cellular functions [43]. In turn, plants mitigate the damage caused by ROS through antioxidant systems [44]. For example, in land cotton, the expression of superoxide dismutase (SOD), ascorbate peroxidase (APX), and GSH is increased in response to Cd stress [45].
In poplar, ABA significantly increased the activities of antioxidant enzymes such as SOD, catalase (CAT), and APX, which scavenged Cd-induced ROS [46]. Similarly, ABA pretreatment alleviated Cd toxicity in roots by modulating the antioxidant defense system in mung bean seedling [47]. Exogenous ABA significantly increased the activities of antioxidant enzymes (SOD, CAT, and APX), which in turn scavenged excess ROS and protected cell membranes from oxidative damage by ROS [48]. Meanwhile, in purple flowering stalk (Brassica campestris L. ssp. chinensis var. purpurea Hort.), ABA alleviated the toxicity of Cd by activating the antioxidant enzyme system to reduce ROS [49]. In addition, exogenous ABA addition can lead to increases in non-enzymatic antioxidants such as ascorbic acid, GSH, carotenoids, and α-tocopherol [8]. Among them, GSH is a major antioxidant that scavenges excess ROS, maintains cellular redox homeostasis, and regulates protein function [44]; therefore, it plays an important role in plant survival under adverse conditions [44]. In addition, GSH can induce the expression of many downstream Cd-tolerance-related genes through the ABA signaling pathway [50]. Interestingly, ABA pretreatment can restore the level of GSH reduced by Cd stress and indirectly regulate oxidative stress caused by ROS accumulation under Cd stress [47]. These results suggested that ABA can alleviate Cd stress by regulating the antioxidant system in plants.

5. Other Regulatory Effects of Abscisic Acid

In Arabidopsis, under the effect of proton pumps, more NO3− and Cd2+ accumulate in the vesicles of root cells of Arabidopsis, thus reducing the toxicity of Cd2+ to the cells [51]. Nitrate transporter 1.5 (NRT 1.5) is a long-distance transporter of NO3− [51]. Arabidopsis NRT 1.5 is expressed mainly in the mid-column sheath cells in roots and is involved in loading NO3− into the xylem [51][52]. By inhibiting NRT 1.5 expression, ABA affects NO3− partitioning in the root system, allowing more NO3− to accumulate in the root system and thereby increasing Cd tolerance in plants [51][52].

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Subjects: Biochemistry & Molecular Biology
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Yuquan Zhao
,
Jiaqi Wang
,
Wei Huang
,
Dawei Zhang
,
Jinfeng Wu
,
Bao Li
,
Mei Li
,
Lili Liu
,
Mingli Yan
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Update Date: 14 Mar 2023
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